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Analysis of the Plant Architecture via Tree-structured Statistical Models - The Hidden Markov Tree Models

Analysis of the Plant Architecture via Tree-structured Statistical Models - The Hidden Markov Tree Models

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Analysis of the plant architecture via tree-structured

statistical models: the hidden Markov tree models

J.-B. Durand

1

, Y. Guédon

2

, Y. Caraglio

2

and E. Costes

3

1

Institut National Polytechnique de Grenoble, Laboratoire de Modélisation et Calcul/IMAG, BP 53, 38041 Grenoble cedex 9, France;

2

Unité Mixte de
Recherche CIRAD/CNRS/INRA/IRD/Université de Montpellier II, Botanique et Bioinformatique de l’Architecture des Plantes TA40/PS2, 34398 Montpellier
cedex 5, France;

3

Unité Mixte de Recherche INRA/Agro.M/CIRAD/IRD BDPPC, Equipe ‘Architecture et Fonctionnement des Espèces Fruitières’, 2 place
Pierre Viala, 34060 Montpellier cedex 1, France

Summary

• Plant architecture is the result of repetitions that occur through growth and
branching processes. During plant ontogeny, changes in the morphological
characteristics of plant entities are interpreted as the indirect translation of different
physiological states of the meristems. Thus connected entities can exhibit either
similar or very contrasted characteristics.
• We propose a statistical model to reveal and characterize homogeneous zones
and transitions between zones within tree-structured data: the hidden Markov tree
(HMT) model. This model leads to a clustering of the entities into classes sharing the
same ‘hidden state’.
• The application of the HMT model to two plant sets (apple trees and bush
willows), measured at annual shoot scale, highlights ordered states defined by
different morphological characteristics. The model provides a synthetic overview
of state locations, pointing out homogeneous zones or ruptures. It also illustrates
where within branching structures, and when during plant ontogeny, morphological
changes occur.
• However, the labelling exhibits some patterns that cannot be described by the
model parameters. Some of these limitations are addressed by two alternative HMT
families.

Key words:

apple tree, bush willow, clustering of tree-structured entities,
differentiation of meristems, hidden Markov tree models, plant architecture modelling,
tree segmentation.

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New Phytologist

(2005)

doi

: 10.1111/j.1469-8137.2005.01405.x

Author for correspondence:

Jean-Baptiste Durand
Tel: +33 4 76 63 57 09
Fax: +33 4 76 63 12 63
Email: Jean-Baptiste.Durand@imag.fr

Received:

30 September 2004

Accepted:

14 December 2004

Introduction

For many years, plant architecture has been viewed as the
result of repetitions (Barlow, 1994), which occur at different
levels of organization (metamers, growth units, axes and
branching systems; Barthélémy, 1991) through growth and
branching processes. In addition, the plant components have
been shown to be distributed within individuals according to
precise rules (Barthélémy

et al

., 1997). The changes that occur
during plant ontogeny have been described along axes for
successive annual shoots, and according to their position
for lateral shoots. These changes reflect the impact of plant
topology on the potentiality of annual growth. The differences
between entities were interpreted as different stages of
differentiation of the meristems, which are ordered in time and
correspond to the notion of physiological age (Nozeran

et al

.,
1971; Gatsuk

et al

., 1980; Barthélémy

et al

., 1997). In the
present study, we assume that the physiological age of meristems
can be assessed retrospectively, that is, deduced from the
morphological characteristics of the plant entities within the
tree structure. We aim to characterize these changes by diverse
morphological variables attached to a given entity, such as
number of nodes, length, and presence/absence of flowering.
These variables are called entity attributes. Connected entities
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that have similar attributes can be interpreted as homogeneous
zones, as opposed to transitions between zones, corresponding
to abrupt changes in the values of the attributes. For example,
flowering is a factor of rupture in the plant architecture when
meristem differentiation leads to sympodial branching. The
discrimination between dominating and dominated axes, in
sympodial plants with different degrees of hierarchy, can also
be formulated as the search for ruptures and continuities.
Indeed, the architectural concept of reiteration (Barthélémy,
1991) corresponds to axes or branching systems with a same
degree of hierarchy. More generally, it makes sense to identify
zones where the entities, at a given scale, can be classified
clearly into a small number of classes defined by different
morphological and functional characteristics. Such classifica-
tion can lead biologists to identify when during plant ontogeny,
or where in branching systems, morphological changes are
significant enough to be discriminated by statistical studies.
This can provide objective criteria for the design of sampling
procedures within tree crowns, especially for physiological
investigations that need to target tissues or organs in specific
states (e.g. flowered vs not flowered).
A statistical approach is relevant for the analysis of archi-
tectural data, both for exploratory analysis, and for inferring
some embedded structures that are not directly apparent in
the data. Statistical models are intended to make explicit some
regularity, patterns or levels of organization from attributes,
for instance tree-structured zones. The statistical analysis of
sequential data from plant architecture, illustrated by Guédon

et al

. (2001), is mainly based on Markovian models, for
instance hidden semi-Markov chains for modelling homoge-
neous zones. These models, although accurately accounting
for the structure contained along remarkable paths in the plant
(e.g. a tree trunk), are not relevant for identifying tree-structured
zones, as the dependencies between entities of disjoint sequences
are eluded. The complete topology has somehow to be included
in the model for the existence of multiple dependent successors
(or descendants) to be considered in the distribution of
zones.
We propose to use the statistical framework of the hidden
Markov tree (HMT) model, introduced by Crouse

et al

.
(1998) in the signal-processing context, to model homo-
geneous zones efficiently within a tree structure whose
topology is fixed in the data. These models are based on
hidden states whose persistence, which leads to homogeneous
zones, is obtained by defining local dependencies between the
states attached to adjacent entities. The HMT modelling is
complementary to the plant-comparison method of Ferraro
& Godin (2000, 2003), based on an edit distance between
tree-structured data. This edit distance integrates the com-
parison of topology and that of the attributes. Instead, our
method determines zones with common attribute distribu-
tion, the plant topology being taken into account locally by
the dependencies between one entity and the adjacent ones.
Markovian models for tree-structured data, as well as the edit
distance between tree-structured data, have been integrated in
the

axai

mod software (Godin

et al

., 1997).
The labelling of the tree entities using the model states,
the ‘state tree restoration’, provides a synthetic overview of the
state locations. The plant is automatically segmented into
comparable parts, whereas state changes highlight where
the ruptures are. Moreover, the labelling procedure visually
reveals some features that cannot be described explicitly by
the model parameters (macroscopic tree-structured patterns,
influence of branching on state succession, etc.). These
features can be analysed,

a posteriori

, from the restored state
tree (extraction of counts, frequencies of occurrences, etc.).
Following the presentation of tree-structured representa-
tions of plants, the statistical modelling of architectural data
by HMT models is developed in this paper, relying on the
aforementioned botanical concepts and hypotheses. Some
practical aspects of the application of the HMT model to
botanical data are addressed. The importance of HMT
modelling is illustrated through applications in agronomy and
ecology. Finally, different families of HMT models and other
potential extensions of the model are presented, and perspec-
tives of other applications are outlined.

Materials and Methods

Tree-structured representation of plants

As discussed by Godin & Caraglio (1998), plant topology can
be described formally through rooted multiscale tree graphs,
the vertices of which correspond to their constituent botanical
entities, and the edges of which represent the physical con-
nections between them. Each scale corresponds to a more-or-
less macroscopic viewpoint on the plant. As only single-scaled
tree graphs can be analysed using HMT models, it is necessary
to choose a scale for the plant description. Part of the topol-
ogical information contained at a higher scale can, nevertheless,
be taken into account in attributes, for example by counting
the number of short shoots borne by a given axis. Such a
balance between topological information within the tree-
structured data and its representation at the attribute level
relies on modelling choices. This is why the plant is typically
represented at a macroscopic level, lower than the internode
scale (growth unit, annual shoot or axis). Moreover, the
changes that occur during plant ontogeny, which are those of
interest in the present study, should be (or are assumed to be)
more easily revealed at macroscopic scales, such as the annual
shoot scale, than at finer scales. More generally, these changes
are directly related to the level of organization at which
growth periodicity is expressed.
For each vertex

u

of the tree graph, the attribute vector is
denoted by

X

u

and can mix qualitative and quantitative
variables. The parent of

u

is denoted by

ρ

(

u

) (except if

u

is the
root vertex), and the set of children of

u

is denoted by

c

(

u

). If
this set is empty,

u

is called a leaf vertex. The different types
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of connection of the plant entities are represented by typed
edges: < for succession; + for branching. These notations are
illustrated in Fig. 1.

Modelling homogeneous zones in plants with HMT
models

The plant architecture is modelled by assigning one state to
each entity. This state represents the class of the entity. Each
class contains entities that have similar attributes. The states
are ordered (at least partially), and take a small number of
values. As each entity corresponds to a vertex

u

of the tree
graph, this is equivalent to associating the tree representation
of the plant with a state tree. The states determine the dis-
tribution of the morphological and functional characteristics
of the entities measured by the attributes

X

u

. A set of connected
vertices assigned to a given state defines a homogeneous zone,
whereas connected vertices assigned to different states induce
ruptures in the plant architecture. The propagation of the
states within the plant is related to its topological organization.
This can be modelled in a probabilistic framework by the
HMT models.
The HMT models were introduced by Crouse

et al

. (1998)
for modelling the dependencies and heterogeneity into a tree-
structured process. The principle is to associate each vertex

u

with a hidden state

S

u

taking values in a finite set, such that
the distribution of the attributes

X

u

depends on the value of

S

u

only. The dependencies between the states (

S

u

)

u

ensure
their propagation from one vertex to its children. They deter-
mine how the states, and hence the zones, are distributed. The
notion of order induced by physiological age mostly applies
at the state level. This is ensured by particular structures of
the transition probability matrix

P

= (

p

ij

)

i

,

j

, where

p

ij



= P

(

S

u

=

j

|

S

ρ

(

u

) =

i

) represents the probability of switching from state

i

in the parent vertex

ρ

(

u

) to state

j

in vertex

u

. The dependen-
cies between hidden states are essentially local; in the basic
HMT model proposed by Crouse

et al

. (1998), the state of
vertex

u

depends on the state of its parent vertex only. This
local dependency assumption gives its name to the Markov
property for trees. The HMT model is quite close to the
hidden Markov chains used for sequence or time-series
analysis (Ephraim & Merhav, 2002). Both have the same
parameter set and are based on local dependency assumptions
between hidden states. These dependencies reproduce the
structure of the observed process at the state level.

Practical issues with HMT models

The application of the HMT model to botanical data is
broken down into two successive steps, as discussed by
Durand

et al

. (2004). The first is parameter estimation from
the measured entities; the second is state tree restoration. Let

n

denote the number of entities and

K

the number of states.
Parameter estimation is based on an iterative method (instance
of the EM algorithm). Following parameter estimation, state
tree restoration is used for model interpretation and validation.
Its purpose is the search for the most likely state tree correspond-
ing to the entities. The restoration procedure takes into
account the dependencies between connected vertices, as the
model does. During this procedure, one of the

K

classes is
assigned to each entity, based on the estimated model and the
measurements for the entity.
The state tree restoration makes the underlying zones
directly apparent. Their actual meaning depends on the
application and particularly on the nature of the attributes.
For example, when searching for dominating paths in plants,
Fig. 1 Tree-structured representation of a plant. (a) Plant represented at growth unit scale. (b) Tree-structured formal representation of the plant.
Part of the topological information is represented at the attribute level only (e.g. the three shoots borne by u
1
).
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these can be identified by extracting from the tree sequences
of consecutive states associated with large values of the entity
length and of the number of internodes. Generally, different
zones in a same state have equivalent attribute distributions,
by definition of the HMT model. Thus the plant is automat-
ically segmented into comparable parts, whereas state changes
highlight where the ruptures are (e.g. see Fig. 3a,c)
Moreover, the model can be assessed and interpreted by
considering the fit between the marginal distribution of one
variable and the corresponding empirical distribution (histo-
gram of the data for this variable), as illustrated in Fig. 5.
The restored state tree can be used for visualization of the fit
between the observation distribution for each state

j

, and
the histogram of all entities in state

j

(see Fig. 2).
The HMT model of Crouse

et al

. (1998) also has the follow-
ing remarkable properties, deduced from the assumptions above.
(1) The privileged orientation is from the root to the leaf
vertices. Thus the propagation of one hidden state

S

u

to its
children

c

(

u

) can be seen as state-splitting.
(2) The children states are independent, given

S

u

.
We call this model the independent-children hidden Markov
out-tree (HMOT) model.
Because of the strong assumptions above, complex tree-
structured patterns and long-range dependencies cannot
be captured explicitly by this HMT model. In this case,
the restoration procedure may reveal such features, which can
be characterized quantitatively by the analysis,

a posteriori

, of
the restored state tree (computation of counts, frequencies
of occurrences, etc.).
Other practical aspects of the HMT methodology include
selecting the number of hidden states. The actual number of
states is determined using statistical criteria. The chosen
criterion depends on the aim of the analysis. The Bayesian
information criterion (BIC) is used frequently to determine
the number of hidden states (Geiger

et al

., 2001), although its
properties have not been established in this context. This
criterion is intended to assess the compromise between model
fit to the data and parsimony. Alternatively, one may favour an
easy interpretation of the model in the selection stage. This
leads us to select the model that maximizes a compromise
between state separation and model fit. This is the purpose of
the integrated classification likelihood criterion proposed by
Biernacki

et al

. (2000).

Applications to botanical data

The following applications are considered in both an agronomic/
genetic and a forestry/ecological context. Both species studied
(apple tree and bush willow) exhibit a sympodial branching
which occurs, respectively, after terminal meristem flowering
and death. Thus the main biological question addressed here
concerns the impact of sympodial development on sub-
sequent growth, and its role in the organization of the whole
tree. A secondary aim is to address issues of synchronism within
entire branching systems. In apple tree, there is a particular
focus on flowering occurrences and their alternation with
vegetative growth. In bush willow, the aim is to test the assump-
tion of ordered morphological changes in a whole sympodial
branching system, and to analyse the impact of climatic
conditions on this order.

Apple tree – Context and aim of the analysis

In fruit trees,
one objective is to describe the intraspecies diversity of tree
forms and branching patterns, which interact with product-
ivity, regularity and ease of training in the orchard (Lauri

et al

., 1997). Previous modelling approaches have described
the early stages of development of a set of cultivars of apple
tree (

Malus domestica

Borkh.,

Rosaceae

), exploring branching
patterns along 1-yr-old trunks (Costes & Guédon, 2002).
Further exploration into the architectural development over
6 yr was carried out for two genotypes, using basic statistical
methods (Costes

et al

., 2003). Although similar growth and
flowering behaviours were demonstrated for all the branches
within the tree crown, whatever their location, these studies
did not consider the patterns of flowering occurrence at
the tree scale. The method presented here aims to improve
the approach to modelling plant structure by extending the
previous models, which were carried out at local scales and
focused on the branching process, towards characterization of
the whole plant structure.

Plant material

Two trees per scion cv. Fuji, grafted on Lancep
Pajam 1 (type M9), were described in 1999 at Melgueil INRA
experimental station (south-east France), when the trees
were 6 yr old. In short, each tree was broken down into three
scales of organization corresponding to the axes; growth units
(GU); and metamers (as defined by White, 1979). Four GU
types were considered: long GU (labelled U) >20 cm long;
medium GU (W)



20 cm but >5 cm long; short GU (D)



5 cm long; and a fourth GU type corresponding to the floral
GU or ‘bourse’ (I), which results from floral differentiation
of the apical meristem. Bourse shoots can develop into short,
medium or long GU, and were categorized in the same
manner as the other vegetative GUs. Thus in springtime the
three vegetative GUs (long, medium and short) can develop
either from the terminal bud, if this has not differentiated
into a bourse, or as a bourse shoot. Metamers were counted
on the long and medium GUs only, while the short GUs were
not broken down at metamer scale in order to simplify the
observations.
Spatial coordinates and diameters were collected at the
metamer scale, each five leaves along the long GU, and at
the top of the axis for short axes. Coordinates were collected
using 3

siaciiasriacx

(Polhemus Inc.) and 3A software
(Adam

et al

., 1999). From the database, which combined
both topological and geometrical observations, 3D reconstruc-
tions of the trees were obtained using the

axai

mod software
(see Fig. 3).
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Choice of scale and extraction of attributes

In the follow-
ing analysis the apple tree was considered at the GU scale in
order to investigate the alternation between flowering and
vegetative GU. The GUs whose growth stopped in 1998 (or
before) were removed from the analysis. The selected attributes,
at this scale, were the number of metamers per GU, and the
presence or absence of a flower on the GU. This choice of GU
scale was also motivated by a compromise between the number
of vertices, the complexity of the tree topology, and the
diversity of the attributes.

Statistical modelling We considered bivariate HMT models
with parametric observation distributions for the number
of metamers. These are discrete distributions, appropriate for
count data, chosen among the binomial, negative binomial
and Poisson distributions. Bernoulli distributions were chosen
for the presence/absence of flowers. Both variables were assumed
to be independent, given the hidden state.
Bush willows – Aims of the analysis This study aimed to
demonstrate structured growth expression within bush willows
submitted to various growth conditions. In order to reach
this goal, we wanted to reveal dominating paths or branching
systems, as opposed to equivalent ones.
Bush willow grows according to sympodial branching:
terminal flowering is expressed on growth units (referred to as
modules; Bell, 1991). Lateral axes (one or more) relay the pre-
vious module, and each one develops a new growth unit and
flowers terminally. This phenomenon is repeated each growth
season, thus the extension of plant structure is essentially due
to the branching process (flowering axes or succession of
modules). Some of these modules become stronger than others,
and as time goes by a ‘trunk’ can be identified (dominating
path). At any moment of the tree’s life, the upper part of the
tree (crown) is constituted of many modules which are more-
or-less equivalent. In this part of the tree, entities were sampled
and our modelling approach applied in order to obtain
automatic labelling of the entities. Based on this labelling,
we aimed to compare different populations, characterized by
their growth conditions, and to propose a classification of
entire individuals.
Plant material The data were collected in Mali by Bonnet
(2002), in the Bamako area, on 111 individuals of Combretum
adenogonium Steud. ex. A. Rich. (Combretaceae). The trees were
sampled under various natural conditions and in different
places. Each tree was characterized by diameter breast height;
total height; type of stress or injury (fire, cutting, pruning);
and some ecological descriptors (competition index, number
of lianas).
On each tree, one 4-yr-old crownlet was sampled, and
after cutting all the modules of the branching system were
described. For this description, two levels of organization were
considered: module (labelled A) and metamer (E). As a
consequence of the modular development, only the link + was
used at the module scale to describe the branching system. On
each module, quite simple and directly available parameters
were measured: total length, basal diameter, number of inter-
nodes, number of photosynthetic leaves, phyllotaxis, number
of flowers, and bark colour.
Choice of scale and extraction of attributes The module,
which is the level of expression of growth periodicity, was
chosen in order to investigate the changes in meristematic
activity according to successive branching. The attributes
considered were number of leaves and length of the module.
Diameter was not considered, as this attribute reflects
both the age of the entity and the global functioning of the
branching system rooted at this entity. For some modules the
number of leaves, or the length, was not available: in this case
all the branching system that originated from the module
was omitted from the analysis. For 12 individuals of our
data set, such missing measurements occurred at the base of
the trunk. Consequently, these individuals were removed
from the data set, and only 99 individuals were considered for
the analysis.
Statistical modelling The maximal number of states con-
sidered in the model building was fixed at six. The observation
distributions were assumed to belong to the same parametric
families as for apple tree. The actual number of states was
determined using the BIC, which focuses on the model fit.
Results
Apple tree
The model selected by the integrated classification likelihood
criterion has four states, while the BIC selected a five-state
model, interpretation of which is far more difficult. Both
criteria show that a model with more than six states is not
relevant, and the interpretation of the six-state model is rather
tedious. Thus the results of the five-state model are not detailed
here. State 0 (denoted L) is characterized by a high value of the
number of metamers per GU (Fig. 2; observation distribution
for state L is represented by a solid line). State 1 (M, dashed
line) is characterized by a medium value; state 2 (S, dotted
and dashed line) corresponds to GUs with a single metamer.
The probability of flowering, given these states, is very close to
zero. Hence these first three states, which correspond to vege-
tative GUs, are clearly ordered by the mean (and, incidentally,
the variance) of their observation distributions. In contrast,
state 3 (F, dotted line) is characterized by the systematic
presence of flowers, and by a very low number of metamers
per GU (fewer than six and generally fewer than three
metamers; Fig. 2).
The state tree restoration algorithm was applied to obtain
an automatic segmentation of the two apple trees, and also to
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assess and interpret the model by matching, for each state j,
the theoretical observation distribution for state j (deduced
from model parameters) with the empirical one (Fig. 2). The
empirical distribution is extracted from the data assigned to
state j by the state tree restoration stage. In the restoration
step, one of the four classes is assigned to each GU, based on
the estimated model and the measurements for the GU (number
of metamers and flowering). The restoration procedure, as
well as the model, takes into account the dependencies between
connected GUs.
Moreover, the state tree restoration provides a synthetic
view of the states’ locations. This is shown in Fig. 3a. For the
sake of clarity, only the trunk and one of the branches are
represented. State L (green) is mostly located at the base
of the trunk and of the main branches. State M (red) typically
corresponds to the distal part of the trunk and of the main
branches. States S (dark blue) and F (light blue) follow states
L and M, respectively, and then tend to alternate. The empirical
and predicted distributions of the number of metamers
per GU for each state are represented in Fig. 2. State L is
represented by a solid line in Fig. 2 and is green in Fig. 3a;
state M by a dashed line in Fig. 2 and red Fig. 3a, etc.
Information concerning the succession of states within the
tree is summed up quantitatively in the transition probability
matrix (Table 1). The initial state is state L. The selected
model has a single recurrent class, although the transition
probability matrix has a particular structure (Fig. 4).
The transition probabilities do not consider both types of
edge (succession and branching) separately in the independent-
children HMOT model. However, the restoration of the
state trees offers the possibility of estimating the transition
probabilities, given the type of edge. Subsequent to the state
restoration, the frequency of each possible transition from a
vertex to a successor vertex (<) has been computed, as well as
the number of parents (of successor descendants) whose restored
state is j (for each state j ). The estimated transition probability
matrix is represented in Table 2. Then the frequency of each
possible transition from a vertex to a branching vertex (+) has
been computed. The estimated transition probability matrix
Fig. 2 Definition of the four states in the hidden Markov out-tree model for apple tree cv. Fuji. Each state is characterized by one observation
distribution for the number of internodes per growth unit (GU). Binomial distributions, B; negative binomial distributions, NB. The type of
distribution is followed by the values of the estimated parameters. Each observation distribution for state j is compared with the histogram
extracted from the data assigned to state j (by the state tree restoration).
Table 1 Transition probability matrix

ρ(u)
u
L M S F
L 0.05 0.15 0.63 0.16
M 0.02 0.06 0.30 0.62
S 0.01 0.05 0.27 0.66
F 0.04 0.35 0.60 0.00
The value at line i and column j represents the probability of a
transition from state i − 1 to state j − 1. States L, M and S are
characterized by a high, medium and low number of metamers per
GU, respectively; F by presence of flowers.
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Research 819
Fig. 3 (a) Restored state tree for the apple tree data set. For the sake of clarity, only the trunk and one of the branches are represented. Each
growth unit (GU) is coloured according to its state. The green state (L) is characterized by a high number of metamers per GU; the red state
(M) by an intermediate number of metamers; the dark blue state (S) corresponds to GUs with a single metamer. Flowering does not occur in
any of these three states. In contrast, the light blue state (F) is characterized by the systematic presence of flowers, and by a very low number
of metamers. (b) Apple tree data set: alternation between short flowering shoots (light blue) and short vegetative shoots (dark blue). (c) Restored
state trees for the bush willow data set. Individuals from classes 1–3 (from left to right, respectively). State L, green (high length and number
of leaves); state M, red (intermediate length and number of leaves); state S, blue (low length and number of leaves). Arrows, extremities of
dominating paths starting from the base of the tree.
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is represented in Table 3, together with the number of parents
(of descendants borne) in each state.
When both matrices are compared, the results (Fig. 4)
highlight certain under/over-represented transitions accord-
ing to edge type. Homogeneous zones of GUs in state L or M
tend to follow each other, while a transition to state S is related
to branching. The separation between states L and M is not
so clear from this viewpoint. Furthermore, state F tends to
follow state S by succession, whereas state S systematically
follows state F by branching. This is related to the sympodial
development of the apple trees. Some extensions (see Discus-
sion) allow the distinction between < and + to be voluntarily
included in the model.
Bush willow
The best compromise between fit and parsimony is achieved
by an HMT with three recurrent states. State 0 (L) is char-
acterized by a high value of the length and number of leaves
per module (Fig. 5, state L represented by a dotted line). State
1 (M, dashed line) is characterized by intermediate values,
and state 2 (S, dotted and dashed line) by low values for both
Fig. 4 Transition graph with information on
succession or branching between successive
states. The dotted arrows correspond to
transition probabilities <0.3. Only the
transitions with probability >0.05 are
represented. Over-represented transitions
are denoted by < for succession; + for
branching; </+ denotes the absence of over-
representation. Codes for states are as in
Figs 2, 3a: state L, solid line, green; state M,
dashed line, red, etc.
Fig. 5 Definition of the three states for the Combretum HMOT. State L, dotted line; state M, dashed line; and state S, dotted-dashed line are
characterized by their observation distributions. Marginal distributions of the number of leaves and module length are a mixture of the three
observation distributions deduced from the model parameters (solid line). For both variables the marginal distribution is compared with the
empirical distribution (histogram).
Table 2 Transition probability matrix, conditional on the child entity
being a successor


Table 3 Transition probability matrix, conditional on the child entity
being a branching offspring


L M S F Count
L 0.09 0.44 0.01 0.46 167
M 0.03 0.12 0.02 0.84 554
S 0.01 0.05 0.27 0.67 1337
F 0
The last column represents the total number of parent entities <
(succession) in each state.
L M S F Count
L 0.05 0.11 0.75 0.09 1128
M 0.01 0.03 0.40 0.56 1365
S 0.27 0.00 0.63 0.09 11
F 0.04 0.35 0.61 0.00 2045
The last column represents the total number of parent entities +
(branching) in each state.
© New Phytologist (2005) www.newphytologist.org New Phytologist (2005) 166: 813–825
Research 821
variables. Thus the three states can be ordered from the mean
of their observation distributions.
One way of assessing the model is to consider the fit
between the marginal distribution of the variables, computed
from model parameters, and the corresponding empirical
distribution, extracted from the data. The marginal distribu-
tion is a mixture of the three observation distributions. The
weights of the mixture are estimated through the empirical
frequency of each state, based on the state restoration. This is
illustrated in Fig. 5, which shows the fit between the mixture
(distribution predicted from the model) and the histogram
(empirical distribution). It appears that, from a state-based
viewpoint, the information contained in both variables is
redundant. This is shown by the empirical correlation coeffi-
cient between number of leaves and length, which is 0.819.
Moreover, the states appear to be quite well separated.
The state tree restoration algorithm has been applied to
obtain an automatic segmentation of each bush willow (Fig. 3c).
Examination of the restoration shows that the three states
are roughly ordered spatially, as state M tends to follow state
L, and state S to follow state M, when progressing toward the
extremities. However, this remarkable succession, although
roughly valid at the scale of the whole plant, is not so clear at
a local scale. As 99 individuals have been used to estimate the
model parameters (the 12 remaining individuals had missing
data at the base of the trunk and were omitted), and as the
HMT model handles only local dependencies, the transition
matrix (Table 4) does not exhibit any left–right structure.
However, any return from state M or S to state L is quite rare.
The selected model is made up of a single recurrent class,
and state L is the initial state. Given the interindividual het-
erogeneity, which hides the expected succession of the states
in the trees, we performed a classification of the individuals
based on deterministic criteria of the transitions between the
restored states. The five following classes were considered:
(1) no transition to a lower state occurs;
(2) at least one S→M transition occurs, followed by an
M→L transition;
(3) at least one S→M transition and an M→L transition
occur, at no particular position;
(4) only S→M transitions or transitions to a higher state occur;
(5) only M→L transitions or transitions to a higher state occur.
Typical individuals belonging to the first three classes are
represented in Fig. 3c, jointly with the state tree restoration.
The analysis of dominating paths or branching systems, as
opposed to equivalent ones, is based on the state tree restora-
tion. As the states are ordered by means of conditional distri-
butions, we used a heuristic function to compute the cost of
each possible path in the plant, where the small values of the
states and the basal locations of these values are favoured.
The result of this algorithm is illustrated in Fig. 3c. If several
dominating paths exist, we obtain equivalent paths as a by-
product, as in the right-hand sample in Fig. 3c. For the deter-
mination of partially equivalent or subdominating paths, the
same process can be iterated after deleting the extremities of
the optimal paths.
In both applications the parameter estimation does not
take longer than 5 min on a computer with a Pentium IV
processor, and the state tree restoration is immediate.
Discussion
Interpretation of the model
In both applications considered, HMT modelling provides a
clustering of the plant entities that can easily be interpreted as
an index of vigour of the entities as the states are ordered: by
the means of distributions of length; number of leaves; or
number of internodes. In the case of apple trees, an a priori
classification of the type of growth unit was available with
the data, according to the length of the GUs. The aim is to
validate this a priori classification of GUs by comparing it
with the hidden states (which are based on the number of
internodes instead of length), as shown in Table 5. Class U is
expected to match with state L; class W with state M; class D
with state S; and class I with state F. A close match between
classes and states is achieved for classes D and I. However,
classes U and W, although in agreement with the states in
most cases, tend to be poorly separated; especially class U,
which is distributed equally between states L and M. This
mixing character of the model concerning the medium and
long shoots only is in accordance with the properties of the
HMT model illustrated in Fig. 2. On the one hand, the
variable ‘absence/presence of flower’ (vegetative/flowering)
allows the identification of flowering shoots; on the other
hand, the short shoots can be identified without ambiguity
with reference to medium or long shoots.
Table 4 Transition probability matrix for the bush willow data set


L M S
L 0.31 0.45 0.25
M 0.08 0.47 0.45
S 0.09 0.46 0.45
Table 5 Number of growth units of each class, given the hidden state

State
Class
U W D I
L 136 55 0 0
M 132 939 14 1
S 4 35 2902 0
F 0 0 0 2291
States L, M, S: high, medium and low number of metamers per GU,
respectively; state F: floral GU; classes U > 20 cm; 5 cm < W ≤ 20 cm;
D ≤ 5 cm; class I: bourse.
New Phytologist (2005) 166: 813–825 www.newphytologist.org © New Phytologist (2005)
Research 822
The succession of the hidden states can be studied through
the state tree restoration. A quantitative viewpoint on the
succession of states is achieved by the analysis of the transition
matrix. In the case of apple trees, the short flowering shoots
and the short vegetative shoots clearly tend to alternate
(Table 1). This is also striking through the state restoration
(Fig. 3b). This behaviour is typical of the development of
apple trees, where flowering occurs on terminal positions along
axes. The flowers are followed by a vegetative shoot, which is
sympodial, develops immediately, and is called a ‘bourse shoot’
(Crabbé & Escobedo, 1991). The following year flowering is
located on this bourse shoot, hence the alternation of flower-
ing and vegetative shoots.
However, the aspects of the hidden state succession that are
specific to a given type of edge are not correctly accounted for
in the HMT model. This is illustrated by Fig. 4: the edge type
associated with each possible transition (if any) is obtained
only indirectly from the model, through the state restoration.
This result is partly specific to the sympodial development of
apple trees after flowering. However, this is in accordance with
the modelling proposed in the Introduction: branching
corresponds to specific transitions (from any state to state S,
or from state F to any state), while succession is associated
with the repetition of entities or with transitions to a close
state, which creates homogeneous zones.
Furthermore, the underlying Markovian model assumes
that the child state is independent of its grandparents, given
the father state. From this viewpoint, this model is similar to
a first-order Markov chain. As a consequence, the remarkable
tree-structured patterns visible in Fig. 3b (the transition to a
‘short shoot’ state followed by the alternation of several vege-
tative or flowering shoots) cannot be modelled precisely. The
existence of such patterns could be accounted for only by
dependencies between consecutive ancestors within a fixed
range.
In both applications the HMT modelling emphasizes the
existence of ordered states, as each following state represents
a distribution with either lower vigour (number of leaves or
internodes) or an ultimate stage of development (flowering).
As stated in the Introduction, the different distributions can
be interpreted as an underlying stage of differentiation: the
physiological age of the meristems. Hence the states are a
natural way to quantify physiological age, and this quantification
now remains to be validated. In the bush willow data set the
states clearly represent ordered levels of meristem potentiality.
These levels still need to be crossed with the growth conditions,
and particularly the type of stress or injury, before validating
the notion of physiological age.
Given the above interpretation of the hidden states, we
would expect the presence of absorbing states within the
HMT models in both applications. These states would corre-
spond to an ultimate state in which the local characteristics of
the plant would not change any more. Models that include
such absorbing states have been estimated from the data sets,
but no statistical evidence in favour of these models has been
revealed from the model selection criteria. However, in the
case of apple trees the alternation between short vegetative
and flowering GUs, highlighted by the state tree restoration,
can be interpreted as an absorbing set of states (in a figurative
sense). This set is quite stable and is reached after only a few
transitions. The absence of any absorbing individual state
could then be related to the scale considered (GUs).
In the case of bush willow, a first important result is that
only three individuals among 99 do not exhibit any particular
arrangement of the three modelled states, despite the
very varied growth conditions of each tree. This reinforces
the assumption of ordered stages of meristem differentiation.
Moreover, some individuals that were struck by fire exhibit a
succession of states in reverse order (middle part of Fig. 3c).
This succession forbids the presence of an absorbing state,
and can be interpreted as an intermediate phase before the
resumption of plant development. In this study we can also
reveal and characterize equivalent paths in branching systems,
which correspond to the architectural concept of reiteration
(Barthélémy, 1991). Finally, this modelling approach could
provide a new framework for biological analysis of the climatic
conditions and/or events that lead to classification of individ-
uals on the basis of transitions between restored states.
Extensions to the proposed HMT model
Here we show that the HMT models allow homogeneous zones
and ruptures to be identified (based on measured morphological
characteristics of the entities), through hidden states that
represent different and ordered distributions of these local
characteristics. Although the efficiency of the modelling
approach is demonstrated for two independent data sets,
further investigations of different species and/or conditions
are required to assess the general nature of the present results,
and their interpretation via the concept of physiological age of
the meristems. The succession of the hidden states is roughly
modelled by a hypothesis of local dependency between parent
and child states (Markov property). This hypothesis captures
the basic characteristics of the hidden states’ succession.
Limitations of the basic HMT model and robustness of the
state tree restoration Considering the potential complexity
of dependencies within a tree structure, the HMT model
described above can be regarded as a rough model. This is the
simplest hidden Markovian model that can take the tree
structure into account. The main advantage of this rough
statistical model is its parsimony – for a given number of states
and a given modelling of the observation processes, its
parameterization is that of a simple hidden first-order Markov
chain. As a counterpart of such parsimony, some dependencies
cannot be modelled, particularly the dependencies between
child vertices of a given parent vertex, and those between a
vertex and its nonparent ancestors.
© New Phytologist (2005) www.newphytologist.org New Phytologist (2005) 166: 813–825
Research 823
In the examples studied, the states are markedly differenti-
ated by the attached observation distributions. For instance,
in the apple tree case, the potential ambiguity between states
that explains the ‘hidden’ nature of the model applies to the
medium and long shoots only. Hence the restoration of the
hidden state tree, which can be considered as robust relative
to a model misspecification, enables the structures that are
improperly represented in the model parameters to be
highlighted (see apple tree results).
As a consequence, in both applications considered in this
paper, the features that could not be captured explicitly by the
HMT model have been handled by the analysis of the restored
state tree (e.g. the frequencies of state transitions for each type
of edge, for apple tree). In the same direction, if several scales
are relevant for the analysis, an HMT model can be identified
for each scale separately and the restored state trees can be
computed for each scale. Then the interscale dependencies
can be analysed a posteriori.
Alternative families of HMT models However, some of the
aforementioned limitations can be addressed by specific
refinements of the model. The first is related to the absence
of distinction between succession and branching. This is a
consequence of the property of conditional independence
of the children states, given the parent state. It follows from
this property that the children’s conditional distribution is
invariant under any permutation of the children: assume that
vertex 1 has children set {2,3}. Then:
P(S
3
= k, S
2
= j | S
1
= i ) = P(S
3
= k | S
1
= i )P(S
2
= j | S
1
= i )
= P(S
2
= k | S
1
= i )P(S
3
= j | S
1
= i ) = P(S
3
= j, S
2
= k | S
1
= i ).
Consequently, the model cannot make the distinction between
succession and branching (see apple tree results; Fig. 4). As we
generally expect ruptures to be caused by branching (as opposed
to succession), the conditional independence assumption is
rather crippling.
Dependent-children hidden Markov out-tree model
To overcome this drawback, we propose a model where the
conditional independence assumption concerning the child
vertices is relaxed. We obtain the dependent-children HMOT
model, also oriented from the root to the leaf vertices, but
with dependent children states, given the parent state. This
model is parameterized by transition probabilities from the
parent state to the set of children states.
In the case of ordered children, this transition probability
corresponds to P(S
3
= k, S
2
= j | S
1
= i ) = p
i,jk
. The transition
probability P(S
3
= j, S
2
= k | S
1
= i ) = p
i,jk
is another para-
meter of the model that is a priori different from p
i,j
. The
number of parameters of a dependent-children HMOT model
is quite similar to that of a high-order or variable-order Markov
chain.
A way to reduce the number of parameters is to use the
information on the edge types (< and +) to partially order
the children. Practically, this means that the successor n(u) of the
parent entity is distinguished from the other offspring entities
b(u) deriving from the parent entity by branching. The set of
nonsuccessor entities is assumed to be unordered. In this case,
the transition probabilities at vertex u are P(S
n(u)
= j, S
b(u)
=
{k,m} | S
u
= i ) = p
i,j,km
. They are assumed to be invariant under
any permutation of the nonsuccessor entities. If the whole set
of children is assumed unordered, then the transition proba-
bilities at vertex u are P(S
c(u)
= {k,m} | S
u
= i ) = p
i,km
.
Hidden Markov in-tree model For some biological pheno-
mena (e.g. apical dominance, delayed branching), and for some
applications (when the attributes cannot be observed on
the innermost part of the plant due to cambial growth and
self-pruning), it seems more relevant to orient the tree from
the leaf vertices to the root. This leads to the hidden Markov
in-tree (HMIT) model, which is parameterized by transition
probabilities from the children states to the parent state. Thus
the propagation of the children states to the parent state can
be seen as state merging. As a consequence, the children states
are dependent given the parent state. Thus the transition
probability matrix is similar to that of a high-order or variable-
order Markov chain where, in the context of tree structures,
the variable number of child vertices plays the role of the order.
As for the dependent-children HMOT model, potential
assumptions on the order, partial order or absence of order on
the set of children determine the transition probabilities. In
the case of ordered children, the transition probability from
the children states of vertex 1 to the state at vertex 1 would be
P(S
1
= i | S
2
= j, S
3
= k) = p
jk,i
.
The three HMT models are illustrated in Fig. 6. These graphs
represent the conditional independence properties between
the random variables in the model, as described by Smyth
et al. (1997).
As a consequence, the next step towards modelling condi-
tional dependencies between children states, given the parent,
would be the implementation of the aforementioned families
of HMT models that are synthetically represented in Fig. 6.
Such dependencies would take into account the distinction
between succession and branching through the transition
matrix. They require additional assumptions of order, partial
order, or absence of order on the set of children.
Modelling the dependencies between ancestors A second
limitation of the independent-children HMOT is related
to the direct dependencies between a state and several of its
ancestors. For example, this would account for the existence
of tree-structured patterns. Such issues rely on building
variable-order HMT models, inspired by the variable-order
Markov chains in the case of sequence analysis (Bühlmann
& Wyner, 1999). However, the simultaneous modelling of
dependencies between children and ancestors does not seem
New Phytologist (2005) 166: 813–825 www.newphytologist.org © New Phytologist (2005)
Research 824
tractable. The application of this enhanced model to the apple
tree data set could illustrate its importance, and complete the
proposed analysis of the state succession (see apple tree results).
A further issue is the periodicity of flowering occurrence, which
remains to be analysed at a local scale as well as globally, for
example using the tree segmentation obtained by state restoration.
Perspectives on methodologies and applications
Analysis of the periodicity of flowering occurrence requires
computation of the distribution of empirical and theoretical
characteristics of trees, such as number of GUs between
flowering occurrences. This approach has been used for the
analysis of sequences, and the results are quite helpful for
model building and exploratory analysis, as well as for model
validation (Guédon et al., 2001). However, in the case of tree-
structured data, the loss of the notion of unique successor
makes the definition of such characteristics more difficult.
Concerning model building, the choice of the number of
states is based, ideally, on the exploratory analysis and on
statistical criteria, although in this paper greater importance is
given to these criteria. As a consequence, a high number of
hidden states cannot be statistically supported by small data
sets, thus discrimination by the HMT models of many mor-
phological changes requires large amounts of data. However,
the peripheral parts of individuals are numerous and tend to
have lower variability than the central parts, which have greater
variability. This should lead to an adaptive sampling in the
protocol of measurement. In the case of partial measurements,
the deletion of structural data (part of the tree topology) can
be handled by the HMIT model. Concerning the issue of
missing attributes for given entities, the pruning strategy
described in this paper for the bush willow data set can be avoided
by resorting to a dedicated algorithm, developed by Celeux &
Durand (2002) in the context of hidden Markov chains.
From the viewpoint of application, dominating or
equivalent paths have been handled here by HMT modelling
only. The approach is based on a heuristic cost function that
favours small values of the states at basal positions. However,
this ad hoc method can barely be extended to the determina-
tion of equivalent (or partially equivalent) branching systems.
Such a family of problems can be approached by dedicated
methods that rely on an edit distance between tree structures
(Ferraro & Godin, 2000, 2003). These algorithms implement
the comparison of branching systems on the basis of both
topology and variables – in our case, the state variable. Further-
more, the existence of an order on the state values would
provide a natural local cost function for this variable. As a result,
the combination of the state tree restoration provided by HMT
modelling, with tree comparison algorithms, is a promising
way of determining reiterated complexes or identifying some
hierarchical levels among branching systems.
As the HMT models provide a general framework for the
identification of homogeneous zones within a plant – for its
automatic segmentation into several parts of similar nature, or
for the extraction of remarkable paths – this approach proves
especially useful in the context of perennial plants. In this case
(or any other context of usually huge and complex crowns),
the amount of available entities per plant is large. Hence the
trees may need to be sampled. For this purpose, the homoge-
neous zones are expected to provide some guidelines for the
selection of branching systems for the reconstruction of
whole individuals. Lastly, a number of models (not necessarily
stochastic) are valid under the assumption that the local
characteristics of the plant do not vary abruptly. Conse-
quently, homogeneous data sets obtained by such a sampling
method could be analysed independently using different
models.
More generally, the segmentation of plants into a small
number of states will offer new possibilities for quantifying
Fig. 6 Families of hidden Markov tree models and their parameters.
© New Phytologist (2005) www.newphytologist.org New Phytologist (2005) 166: 813–825
Research 825
physiological age. As a perspective, this should lead to a
methodology for the validation of this notion.
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are not relevant for identifying tree-structured zones. Some practical aspects of the application of the HMT model to botanical data are addressed. annual shoot or axis). be taken into account in attributes. is obtained by defining local dependencies between the states attached to adjacent entities. We propose to use the statistical framework of the hidden Markov tree (HMT) model. This can provide objective criteria for the design of sampling procedures within tree crowns. have been integrated in the mod software (Godin et al. should be (or are assumed to be) more easily revealed at macroscopic scales. from the restored state tree (extraction of counts. 1991) corresponds to axes or branching systems with a same degree of hierarchy. nevertheless. and the set of children of u is denoted by c (u). or where in branching systems. The discrimination between dominating and dominated axes.g. the changes that occur during plant ontogeny. Finally. As only single-scaled tree graphs can be analysed using HMT models. Materials and Methods Tree-structured representation of plants As discussed by Godin & Caraglio (1998). Instead.. The HMT modelling is complementary to the plant-comparison method of Ferraro & Godin (2000. 1997). These models. Indeed. Moreover. The importance of HMT modelling is illustrated through applications in agronomy and ecology. a tree trunk). and for inferring some embedded structures that are not directly apparent in the data. it makes sense to identify zones where the entities. the plant topology being taken into account locally by the dependencies between one entity and the adjacent ones. for instance hidden semi-Markov chains for modelling homogeneous zones. frequencies of occurrences. 2003). For each vertex u of the tree graph. For example. in sympodial plants with different degrees of hierarchy. the vertices of which correspond to their constituent botanical entities. These features can be analysed. etc. the labelling procedure visually reveals some features that cannot be described explicitly by the model parameters (macroscopic tree-structured patterns. provides a synthetic overview of the state locations.). Statistical models are intended to make explicit some regularity. More generally. for instance tree-structured zones. (2001). as the dependencies between entities of disjoint sequences are eluded. These models are based on hidden states whose persistence. relying on the aforementioned botanical concepts and hypotheses. u is called a leaf vertex. a posteriori. whereas state changes highlight where the ruptures are. plant topology can be described formally through rooted multiscale tree graphs. it is necessary to choose a scale for the plant description. lower than the internode scale (growth unit. these changes are directly related to the level of organization at which growth periodicity is expressed. The complete topology has somehow to be included in the model for the existence of multiple dependent successors (or descendants) to be considered in the distribution of zones. This edit distance integrates the comparison of topology and that of the attributes. Moreover. Each scale corresponds to a more-orless macroscopic viewpoint on the plant. than at finer scales. More generally. Such a balance between topological information within the treestructured data and its representation at the attribute level relies on modelling choices. morphological changes are significant enough to be discriminated by statistical studies. is mainly based on Markovian models. A statistical approach is relevant for the analysis of architectural data. The statistical analysis of sequential data from plant architecture. the statistical modelling of architectural data by HMT models is developed in this paper. and the edges of which represent the physical connections between them. Part of the topological information contained at a higher scale can. Markovian models for tree-structured data. influence of branching on state succession. as well as the edit distance between tree-structured data. The plant is automatically segmented into comparable parts.newphytologist. such as the annual shoot scale. can also be formulated as the search for ruptures and continuities. illustrated by Guédon et al.g. The different types New Phytologist (2005) 166: 813– 825 www.org © New Phytologist (2005) . the architectural concept of reiteration (Barthélémy. (1998) in the signal-processing context. This is why the plant is typically represented at a macroscopic level. etc. The labelling of the tree entities using the model states. at a given scale. the attribute vector is denoted by Xu and can mix qualitative and quantitative variables. If this set is empty. corresponding to abrupt changes in the values of the attributes. especially for physiological investigations that need to target tissues or organs in specific states (e. and perspectives of other applications are outlined. as opposed to transitions between zones. introduced by Crouse et al. The parent of u is denoted by ρ(u) (except if u is the root vertex). Such classification can lead biologists to identify when during plant ontogeny. both for exploratory analysis. flowered vs not flowered). to model homogeneous zones efficiently within a tree structure whose topology is fixed in the data. for example by counting the number of short shoots borne by a given axis. patterns or levels of organization from attributes. can be classified clearly into a small number of classes defined by different morphological and functional characteristics. which leads to homogeneous zones. Following the presentation of tree-structured representations of plants. flowering is a factor of rupture in the plant architecture when meristem differentiation leads to sympodial branching. the ‘state tree restoration’. based on an edit distance between tree-structured data. our method determines zones with common attribute distribution.814 Research that have similar attributes can be interpreted as homogeneous zones. different families of HMT models and other potential extensions of the model are presented. although accurately accounting for the structure contained along remarkable paths in the plant (e.). which are those of interest in the present study.

As each entity corresponds to a vertex u of the tree graph. (a) Plant represented at growth unit scale. this is equivalent to associating the tree representation of the plant with a state tree. The states are ordered (at least partially). The restoration procedure takes into account the dependencies between connected vertices. This is ensured by particular structures of the transition probability matrix P = ( pij )i . Each class contains entities that have similar attributes. This local dependency assumption gives its name to the Markov property for trees.g. (1998). the second is state tree restoration. based on the estimated model and the measurements for the entity. These notations are illustrated in Fig. 1 Tree-structured representation of a plant. © New Phytologist (2005) www. when searching for dominating paths in plants. as discussed by Durand et al. Parameter estimation is based on an iterative method (instance of the EM algorithm). They determine how the states. The dependencies between the states (Su )u ensure their propagation from one vertex to its children. The dependencies between hidden states are essentially local. Its purpose is the search for the most likely state tree corresponding to the entities. Their actual meaning depends on the application and particularly on the nature of the attributes. 1. where pij = P (Su = j | Sρ(u) = i) represents the probability of switching from state i in the parent vertex ρ(u) to state j in vertex u. The HMT models were introduced by Crouse et al. These dependencies reproduce the structure of the observed process at the state level. Following parameter estimation. (2004).Research 815 Fig. Let n denote the number of entities and K the number of states. in the basic HMT model proposed by Crouse et al. are distributed. and take a small number of values. Part of the topological information is represented at the attribute level only (e. The first is parameter estimation from the measured entities. The states determine the distribution of the morphological and functional characteristics of the entities measured by the attributes Xu.org New Phytologist (2005) 166: 813–825 . Both have the same parameter set and are based on local dependency assumptions between hidden states. (1998) for modelling the dependencies and heterogeneity into a treestructured process. The principle is to associate each vertex u with a hidden state Su taking values in a finite set. Modelling homogeneous zones in plants with HMT models The plant architecture is modelled by assigning one state to each entity. the three shoots borne by u1). of connection of the plant entities are represented by typed edges: < for succession. 2002). During this procedure. The HMT model is quite close to the hidden Markov chains used for sequence or time-series analysis (Ephraim & Merhav. This can be modelled in a probabilistic framework by the HMT models. Practical issues with HMT models The application of the HMT model to botanical data is broken down into two successive steps. For example.newphytologist.j . one of the K classes is assigned to each entity. state tree restoration is used for model interpretation and validation. such that the distribution of the attributes Xu depends on the value of Su only. as the model does. the state of vertex u depends on the state of its parent vertex only. + for branching. and hence the zones. whereas connected vertices assigned to different states induce ruptures in the plant architecture. This state represents the class of the entity. The notion of order induced by physiological age mostly applies at the state level. The state tree restoration makes the underlying zones directly apparent. A set of connected vertices assigned to a given state defines a homogeneous zone. The propagation of the states within the plant is related to its topological organization. (b) Tree-structured formal representation of the plant.

Thus the plant is automatically segmented into comparable parts. medium GU (W) ≤20 cm but >5 cm long. Apple tree – Context and aim of the analysis In fruit trees. grafted on Lancep Pajam 1 (type M9). We call this model the independent-children hidden Markov out-tree (HMOT) model.. by definition of the HMT model. Bourse shoots can develop into short. In bush willow. deduced from the assumptions above. A secondary aim is to address issues of synchronism within entire branching systems. (1998) also has the following remarkable properties. Four GU types were considered: long GU (labelled U) >20 cm long. one may favour an easy interpretation of the model in the selection stage. and were categorized in the same manner as the other vegetative GUs. 3D reconstructions of the trees were obtained using the mod software (see Fig. these studies did not consider the patterns of flowering occurrence at the tree scale.. whereas state changes highlight where the ruptures are (e. given Su. (1) The privileged orientation is from the root to the leaf vertices. short GU (D) ≤5 cm long. and metamers (as defined by White. 1979). each tree was broken down into three scales of organization corresponding to the axes. Although similar growth and flowering behaviours were demonstrated for all the branches within the tree crown. Because of the strong assumptions above. of the restored state tree (computation of counts. the model can be assessed and interpreted by considering the fit between the marginal distribution of one variable and the corresponding empirical distribution (histogram of the data for this variable). Alternatively. Fuji.816 Research these can be identified by extracting from the tree sequences of consecutive states associated with large values of the entity length and of the number of internodes. and its role in the organization of the whole tree. 1999).). exploring branching patterns along 1-yr-old trunks (Costes & Guédon.c) Moreover. complex treestructured patterns and long-range dependencies cannot be captured explicitly by this HMT model. Further exploration into the architectural development over 6 yr was carried out for two genotypes. Thus in springtime the three vegetative GUs (long. Rosaceae). which were carried out at local scales and focused on the branching process. Spatial coordinates and diameters were collected at the metamer scale. 2). Metamers were counted on the long and medium GUs only.g. as illustrated in Fig.. The Bayesian information criterion (BIC) is used frequently to determine the number of hidden states (Geiger et al. and to analyse the impact of climatic conditions on this order. or as a bourse shoot. which can be characterized quantitatively by the analysis. Plant material Two trees per scion cv. when the trees were 6 yr old.org © New Phytologist (2005) . 3a. different zones in a same state have equivalent attribute distributions. each five leaves along the long GU. This is the purpose of the integrated classification likelihood criterion proposed by Biernacki et al. 2003). The restored state tree can be used for visualization of the fit between the observation distribution for each state j. were described in 1999 at Melgueil INRA experimental station (south-east France). 3). a posteriori. regularity and ease of training in the orchard (Lauri et al. one objective is to describe the intraspecies diversity of tree forms and branching patterns.newphytologist. the aim is to test the assumption of ordered morphological changes in a whole sympodial branching system. and a fourth GU type corresponding to the floral GU or ‘bourse’ (I). Previous modelling approaches have described the early stages of development of a set of cultivars of apple tree (Malus domestica Borkh.) and 3A software (Adam et al. there is a particular focus on flowering occurrences and their alternation with vegetative growth. whatever their location. although its properties have not been established in this context. This criterion is intended to assess the compromise between model fit to the data and parsimony. 2002). New Phytologist (2005) 166: 813– 825 www. 5.. and at the top of the axis for short axes. after terminal meristem flowering and death. Applications to botanical data The following applications are considered in both an agronomic/ genetic and a forestry/ecological context. if this has not differentiated into a bourse. 1997). which results from floral differentiation of the apical meristem. The chosen criterion depends on the aim of the analysis. which interact with productivity. In this case. medium and short) can develop either from the terminal bud. Thus the main biological question addressed here concerns the impact of sympodial development on subsequent growth. frequencies of occurrences. This leads us to select the model that maximizes a compromise between state separation and model fit. and the histogram of all entities in state j (see Fig. Both species studied (apple tree and bush willow) exhibit a sympodial branching which occurs. (2000). The method presented here aims to improve the approach to modelling plant structure by extending the previous models. growth units (GU). From the database. using basic statistical methods (Costes et al. 2001). see Fig. respectively. Generally. In apple tree. the restoration procedure may reveal such features. medium or long GU. The HMT model of Crouse et al. (2) The children states are independent. In short. etc. Thus the propagation of one hidden state Su to its children c (u) can be seen as state-splitting. while the short GUs were not broken down at metamer scale in order to simplify the observations. which combined both topological and geometrical observations. Coordinates were collected using 3 (Polhemus Inc. Other practical aspects of the HMT methodology include selecting the number of hidden states. towards characterization of the whole plant structure. The actual number of states is determined using statistical criteria..

ex. The GUs whose growth stopped in 1998 (or before) were removed from the analysis. appropriate for count data. Bush willows – Aims of the analysis This study aimed to demonstrate structured growth expression within bush willows submitted to various growth conditions. Based on this labelling. chosen among the binomial. In order to reach this goal. Plant material The data were collected in Mali by Bonnet (2002). and by a very low number of metamers per GU (fewer than six and generally fewer than three metamers. one 4-yr-old crownlet was sampled. Thus the results of the five-state model are not detailed here. these individuals were removed from the data set. 2. Bell. observation distribution for state L is represented by a solid line). the upper part of the tree (crown) is constituted of many modules which are moreor-less equivalent. which correspond to vegetative GUs. Fig. basal diameter. we aimed to compare different populations. Statistical modelling The maximal number of states considered in the model building was fixed at six. which is the level of expression of growth periodicity. Diameter was not considered. given these states. is very close to zero. This phenomenon is repeated each growth season. Each tree was characterized by diameter breast height. such missing measurements occurred at the base of the trunk. incidentally. Rich. Consequently. Hence these first three states. The attributes considered were number of leaves and length of the module. which focuses on the model fit. and each one develops a new growth unit and flowers terminally. and the interpretation of the six-state model is rather tedious. while the BIC selected a five-state model. thus the extension of plant structure is essentially due to the branching process (flowering axes or succession of modules). This choice of GU scale was also motivated by a compromise between the number of vertices. type of stress or injury (fire. were the number of metamers per GU. At any moment of the tree’s life. number of photosynthetic leaves. and only 99 individuals were considered for the analysis. number of lianas). state 2 (S. Lateral axes (one or more) relay the previous module. was chosen in order to investigate the changes in meristematic activity according to successive branching. Bernoulli distributions were chosen for the presence/absence of flowers. characterized by their growth conditions. On each module. Both variables were assumed to be independent. As a consequence of the modular development. or the length. and as time goes by a ‘trunk’ can be identified (dominating path). and some ecological descriptors (competition index. Some of these modules become stronger than others. and the presence or absence of a flower on the GU. as this attribute reflects both the age of the entity and the global functioning of the branching system rooted at this entity. two levels of organization were considered: module (labelled A) and metamer (E). and to propose a classification of entire individuals. we wanted to reveal dominating paths or branching systems. The state tree restoration algorithm was applied to obtain an automatic segmentation of the two apple trees. entities were sampled and our modelling approach applied in order to obtain automatic labelling of the entities. In this part of the tree. are clearly ordered by the mean (and. For some modules the number of leaves. only the link + was used at the module scale to describe the branching system.Research 817 Choice of scale and extraction of attributes In the following analysis the apple tree was considered at the GU scale in order to investigate the alternation between flowering and vegetative GU. The observation distributions were assumed to belong to the same parametric families as for apple tree. State 1 (M. state 3 (F. the variance) of their observation distributions. The actual number of states was determined using the BIC. These are discrete distributions. and bark colour. For this description. phyllotaxis. interpretation of which is far more difficult. Statistical modelling We considered bivariate HMT models with parametric observation distributions for the number of metamers. and after cutting all the modules of the branching system were described. quite simple and directly available parameters were measured: total length. given the hidden state. negative binomial and Poisson distributions. and the diversity of the attributes. In contrast.org New Phytologist (2005) 166: 813–825 . (Combretaceae). as opposed to equivalent ones. Choice of scale and extraction of attributes The module. total height. the complexity of the tree topology. number of internodes. 1991). Both criteria show that a model with more than six states is not relevant. The probability of flowering. and also to © New Phytologist (2005) www. dashed line) is characterized by a medium value. State 0 (denoted L) is characterized by a high value of the number of metamers per GU (Fig. Results Apple tree The model selected by the integrated classification likelihood criterion has four states.newphytologist. On each tree. For 12 individuals of our data set. 2). number of flowers. in the Bamako area. at this scale. Bush willow grows according to sympodial branching: terminal flowering is expressed on growth units (referred to as modules. was not available: in this case all the branching system that originated from the module was omitted from the analysis. cutting. The trees were sampled under various natural conditions and in different places. A. pruning). on 111 individuals of Combretum adenogonium Steud. The selected attributes. dotted line) is characterized by the systematic presence of flowers. dotted and dashed line) corresponds to GUs with a single metamer.

for each state j. The estimated transition probability matrix New Phytologist (2005) 166: 813– 825 www. 2 Definition of the four states in the hidden Markov out-tree model for apple tree cv. The restoration procedure.818 Research Fig. F by presence of flowers. However. NB. the restoration of the state trees offers the possibility of estimating the transition probabilities.60 F 0. States S (dark blue) and F (light blue) follow states L and M. The estimated transition probability matrix is represented in Table 2.66 0.15 0. This is shown in Fig. State L is represented by a solid line in Fig. The type of distribution is followed by the values of the estimated parameters. The empirical distribution is extracted from the data assigned to state j by the state tree restoration stage. 2 and red Fig. one of the four classes is assigned to each GU. Fuji. 2). the frequency of each possible transition from a vertex to a successor vertex (<) has been computed. For the sake of clarity. 4). States L. In the restoration step.06 0. etc.04 M 0.05 0. State M (red) typically corresponds to the distal part of the trunk and of the main branches. respectively. given the type of edge.02 0. The transition probabilities do not consider both types of edge (succession and branching) separately in the independentchildren HMOT model.62 0. Moreover. 2 and is green in Fig.05 0. 2. Information concerning the succession of states within the tree is summed up quantitatively in the transition probability matrix (Table 1). 3a. The empirical and predicted distributions of the number of metamers per GU for each state are represented in Fig.16 0. and then tend to alternate. the state tree restoration provides a synthetic view of the states’ locations.35 S 0.newphytologist. as well as the model. assess and interpret the model by matching. state M by a dashed line in Fig. respectively. Subsequent to the state restoration.01 0. although the transition probability matrix has a particular structure (Fig. M and S are characterized by a high.30 0. The initial state is state L. based on the estimated model and the measurements for the GU (number of metamers and flowering). State L (green) is mostly located at the base of the trunk and of the main branches. Table 1 Transition probability matrix u ρ (u) L M S F L 0. medium and low number of metamers per GU.63 0. takes into account the dependencies between connected GUs. negative binomial distributions. 3a. the theoretical observation distribution for state j (deduced from model parameters) with the empirical one (Fig. The selected model has a single recurrent class. as well as the number of parents (of successor descendants) whose restored state is j (for each state j). only the trunk and one of the branches are represented. Each state is characterized by one observation distribution for the number of internodes per growth unit (GU). 3a. B.org © New Phytologist (2005) .00 The value at line i and column j represents the probability of a transition from state i − 1 to state j − 1. Binomial distributions.27 0. Then the frequency of each possible transition from a vertex to a branching vertex (+) has been computed. Each observation distribution for state j is compared with the histogram extracted from the data assigned to state j (by the state tree restoration).

blue (low length and number of leaves). the dark blue state (S) corresponds to GUs with a single metamer.org New Phytologist (2005) 166: 813–825 . Arrows. the light blue state (F) is characterized by the systematic presence of flowers. Flowering does not occur in any of these three states. extremities of dominating paths starting from the base of the tree. state S. respectively). the red state (M) by an intermediate number of metamers. © New Phytologist (2005) www. Each growth unit (GU) is coloured according to its state. For the sake of clarity. The green state (L) is characterized by a high number of metamers per GU. 3 (a) Restored state tree for the apple tree data set. Individuals from classes 1–3 (from left to right. (c) Restored state trees for the bush willow data set. State L. In contrast. only the trunk and one of the branches are represented. green (high length and number of leaves).Research 819 Fig. and by a very low number of metamers. (b) Apple tree data set: alternation between short flowering shoots (light blue) and short vegetative shoots (dark blue).newphytologist. red (intermediate length and number of leaves). state M.

02 0. 5 Definition of the three states for the Combretum HMOT.61 F 0. Furthermore.01 M 0.01 0.00 0. Table 2 Transition probability matrix.newphytologist.56 0. the results (Fig.35 S 0. state F tends to follow state S by succession.40 0.09 0. </+ denotes the absence of overrepresentation. Codes for states are as in Figs 2. dotted-dashed line are characterized by their observation distributions. and state 2 (S. state L represented by a dotted line). and state S.46 0.75 0. Over-represented transitions are denoted by < for succession.12 0. Fig. When both matrices are compared. state M.09 0. 3a: state L. For both variables the marginal distribution is compared with the empirical distribution (histogram). etc. conditional on the child entity being a branching offspring L L M S F 0.org © New Phytologist (2005) . State 0 (L) is characterized by a high value of the length and number of leaves per module (Fig.09 0. The dotted arrows correspond to transition probabilities <0. Bush willow The best compromise between fit and parsimony is achieved by an HMT with three recurrent states. whereas state S systematically follows state F by branching.3. dashed line.03 0. together with the number of parents (of descendants borne) in each state. solid line. conditional on the child entity being a successor L L M S F 0. This is related to the sympodial development of the apple trees.04 M 0.05 are represented.63 0. dotted and dashed line) by low values for both The last column represents the total number of parent entities + (branching) in each state. while a transition to state S is related to branching.44 0. The separation between states L and M is not so clear from this viewpoint. 4 Transition graph with information on succession or branching between successive states. dashed line. New Phytologist (2005) 166: 813– 825 www. 5. State 1 (M.01 0. green.820 Research Fig.84 0. dashed line) is characterized by intermediate values.67 Count 167 554 1337 0 The last column represents the total number of parent entities < (succession) in each state.27 F 0. red. Marginal distributions of the number of leaves and module length are a mixture of the three observation distributions deduced from the model parameters (solid line).27 0.11 0. Some extensions (see Discussion) allow the distinction between < and + to be voluntarily included in the model.05 0. + for branching. dotted line. Table 3 Transition probability matrix. Homogeneous zones of GUs in state L or M tend to follow each other.05 S 0. state M.03 0. State L.00 Count 1128 1365 11 2045 is represented in Table 3. 4) highlight certain under/over-represented transitions according to edge type. Only the transitions with probability >0.

(5) only M→L transitions or transitions to a higher state occur. medium and low number of metamers per GU. Examination of the restoration shows that the three states are roughly ordered spatially. Table 5 Number of growth units of each class. jointly with the state tree restoration. class W with state M. computed from model parameters. © New Phytologist (2005) www. the variable ‘absence/presence of flower’ (vegetative/flowering) allows the identification of flowering shoots. is not so clear at a local scale. classes U and W. The weights of the mixture are estimated through the empirical frequency of each state. as in the right-hand sample in Fig. (3) at least one S→M transition and an M→L transition occur. or number of internodes. followed by an M→L transition. and the state tree restoration is immediate.819. we used a heuristic function to compute the cost of each possible path in the plant. (2) at least one S→M transition occurs. the information contained in both variables is redundant. on the other hand. and the corresponding empirical distribution. Class U is expected to match with state L. although roughly valid at the scale of the whole plant. especially class U. we obtain equivalent paths as a byproduct. any return from state M or S to state L is quite rare. As 99 individuals have been used to estimate the model parameters (the 12 remaining individuals had missing data at the base of the trunk and were omitted).08 0. and state S to follow state M. 3c). 3c.45 821 variables. from a state-based viewpoint. Thus the three states can be ordered from the mean of their observation distributions. The selected model is made up of a single recurrent class. Given the interindividual heterogeneity.47 0. and state L is the initial state. as opposed to equivalent ones. A close match between classes and states is achieved for classes D and I. which is distributed equally between states L and M.31 0. The marginal distribution is a mixture of the three observation distributions.25 0. The five following classes were considered: (1) no transition to a lower state occurs. at no particular position. is based on the state tree restora- tion. However.org New Phytologist (2005) 166: 813–825 . number of leaves. 5 cm < W ≤ 20 cm. 5. the states appear to be quite well separated. state F: floral GU. In the case of apple trees.Research Table 4 Transition probability matrix for the bush willow data set L L M S 0. It appears that. based on the state restoration. This mixing character of the model concerning the medium and long shoots only is in accordance with the properties of the HMT model illustrated in Fig. HMT modelling provides a clustering of the plant entities that can easily be interpreted as an index of vigour of the entities as the states are ordered: by the means of distributions of length. However. However.46 S 0. This is shown by the empirical correlation coefficient between number of leaves and length. although in agreement with the states in most cases. 2. which is 0. The aim is to validate this a priori classification of GUs by comparing it with the hidden states (which are based on the number of internodes instead of length). the same process can be iterated after deleting the extremities of the optimal paths. which hides the expected succession of the states in the trees. classes U > 20 cm. the short shoots can be identified without ambiguity with reference to medium or long shoots.45 0. This is illustrated in Fig. On the one hand.45 0. class D with state S. (4) only S→M transitions or transitions to a higher state occur. Typical individuals belonging to the first three classes are represented in Fig. this remarkable succession. where the small values of the states and the basal locations of these values are favoured. and as the HMT model handles only local dependencies. If several dominating paths exist. given the hidden state Class State L M S F U 136 132 4 0 W 55 939 35 0 D 0 14 2902 0 I 0 1 0 2291 States L. as state M tends to follow state L. As the states are ordered by means of conditional distributions.09 M 0. which shows the fit between the mixture (distribution predicted from the model) and the histogram (empirical distribution). an a priori classification of the type of growth unit was available with the data. S: high.newphytologist. M. Moreover. respectively. The result of this algorithm is illustrated in Fig. 3c. and class I with state F. as shown in Table 5. 3c. For the determination of partially equivalent or subdominating paths. The state tree restoration algorithm has been applied to obtain an automatic segmentation of each bush willow (Fig. The analysis of dominating paths or branching systems. Discussion Interpretation of the model In both applications considered. One way of assessing the model is to consider the fit between the marginal distribution of the variables. the transition matrix (Table 4) does not exhibit any left–right structure. we performed a classification of the individuals based on deterministic criteria of the transitions between the restored states. extracted from the data. class I: bourse. tend to be poorly separated. according to the length of the GUs. In both applications the parameter estimation does not take longer than 5 min on a computer with a Pentium IV processor. D ≤ 5 cm. when progressing toward the extremities.

This succession forbids the presence of an absorbing state. this model is similar to a first-order Markov chain. while succession is associated with the repetition of entities or with transitions to a close state. This is illustrated by Fig. and can be interpreted as an intermediate phase before the resumption of plant development. As stated in the Introduction.822 Research The succession of the hidden states can be studied through the state tree restoration. As a counterpart of such parsimony. As a consequence. the HMT model described above can be regarded as a rough model. The main advantage of this rough statistical model is its parsimony – for a given number of states and a given modelling of the observation processes. hence the alternation of flowering and vegetative shoots. In the case of bush willow. This is the simplest hidden Markovian model that can take the tree structure into account. In both applications the HMT modelling emphasizes the existence of ordered states. the remarkable tree-structured patterns visible in Fig. 1991). where flowering occurs on terminal positions along axes. and particularly the type of stress or injury. particularly the dependencies between child vertices of a given parent vertex. Furthermore. which is sympodial. and this quantification now remains to be validated.org © New Phytologist (2005) . Given the above interpretation of the hidden states. 3b). and their interpretation via the concept of physiological age of the meristems. 4: the edge type associated with each possible transition (if any) is obtained only indirectly from the model. The succession of the hidden states is roughly modelled by a hypothesis of local dependency between parent and child states (Markov property). a first important result is that only three individuals among 99 do not exhibit any particular arrangement of the three modelled states. the short flowering shoots and the short vegetative shoots clearly tend to alternate (Table 1). The flowers are followed by a vegetative shoot. Extensions to the proposed HMT model Here we show that the HMT models allow homogeneous zones and ruptures to be identified (based on measured morphological characteristics of the entities). this is in accordance with the modelling proposed in the Introduction: branching corresponds to specific transitions (from any state to state S. The absence of any absorbing individual state could then be related to the scale considered (GUs). develops immediately. This reinforces the assumption of ordered stages of meristem differentiation. given the father state. However. This behaviour is typical of the development of apple trees. The existence of such patterns could be accounted for only by dependencies between consecutive ancestors within a fixed range. its parameterization is that of a simple hidden first-order Markov chain. highlighted by the state tree restoration. This set is quite stable and is reached after only a few transitions. in the case of apple trees the alternation between short vegetative and flowering GUs. Although the efficiency of the modelling approach is demonstrated for two independent data sets. In the bush willow data set the states clearly represent ordered levels of meristem potentiality. Moreover. 1991). some individuals that were struck by fire exhibit a succession of states in reverse order (middle part of Fig. or from state F to any state). These levels still need to be crossed with the growth conditions. and those between a vertex and its nonparent ancestors. This hypothesis captures the basic characteristics of the hidden states’ succession. the different distributions can be interpreted as an underlying stage of differentiation: the physiological age of the meristems. through hidden states that represent different and ordered distributions of these local characteristics. In this study we can also reveal and characterize equivalent paths in branching systems. and is called a ‘bourse shoot’ (Crabbé & Escobedo. However. Finally. However. A quantitative viewpoint on the succession of states is achieved by the analysis of the transition matrix. which correspond to the architectural concept of reiteration (Barthélémy. Models that include such absorbing states have been estimated from the data sets. this modelling approach could provide a new framework for biological analysis of the climatic conditions and/or events that lead to classification of individuals on the basis of transitions between restored states. In the case of apple trees. New Phytologist (2005) 166: 813– 825 www. some dependencies cannot be modelled. Hence the states are a natural way to quantify physiological age. This is also striking through the state restoration (Fig. 3c). but no statistical evidence in favour of these models has been revealed from the model selection criteria. before validating the notion of physiological age. which creates homogeneous zones. From this viewpoint. as each following state represents a distribution with either lower vigour (number of leaves or internodes) or an ultimate stage of development (flowering). we would expect the presence of absorbing states within the HMT models in both applications. These states would correspond to an ultimate state in which the local characteristics of the plant would not change any more. This result is partly specific to the sympodial development of apple trees after flowering. through the state restoration. the underlying Markovian model assumes that the child state is independent of its grandparents. further investigations of different species and/or conditions are required to assess the general nature of the present results. The following year flowering is located on this bourse shoot. Limitations of the basic HMT model and robustness of the state tree restoration Considering the potential complexity of dependencies within a tree structure. the aspects of the hidden state succession that are specific to a given type of edge are not correctly accounted for in the HMT model. 3b (the transition to a ‘short shoot’ state followed by the alternation of several vegetative or flowering shoots) cannot be modelled precisely. can be interpreted as an absorbing set of states (in a figurative sense).newphytologist. despite the very varied growth conditions of each tree.

the variable number of child vertices plays the role of the order. we propose a model where the conditional independence assumption concerning the child vertices is relaxed. The transition probability P(S3 = j.m} | Su = i) = pi. potential assumptions on the order. S3 = k) = pjk. Thus the propagation of the children states to the parent state can be seen as state merging. As a consequence. The set of nonsuccessor entities is assumed to be unordered. some of the aforementioned limitations can be addressed by specific refinements of the model. or absence of order on the set of children.j. partial order or absence of order on the set of children determine the transition probabilities. 6. delayed branching). S2 = j | S1 = i) = pi.Research 823 In the examples studied. if several scales are relevant for the analysis. this means that the successor n(u) of the parent entity is distinguished from the other offspring entities b(u) deriving from the parent entity by branching. the transition probabilities at vertex u are P(Sn(u) = j. For instance. Then the interscale dependencies can be analysed a posteriori. For example. which is parameterized by transition probabilities from the children states to the parent state.jk. As we generally expect ruptures to be caused by branching (as opposed to succession). in the context of tree structures. We obtain the dependent-children HMOT model. If the whole set of children is assumed unordered. Sb(u) = {k. However. given the parent. the frequencies of state transitions for each type of edge. As a consequence.org New Phytologist (2005) 166: 813–825 . the children states are dependent given the parent state. the conditional independence assumption is rather crippling. As a consequence. This leads to the hidden Markov in-tree (HMIT) model. an HMT model can be identified for each scale separately and the restored state trees can be computed for each scale. this transition probability corresponds to P(S3 = k. This model is parameterized by transition probabilities from the parent state to the set of children states. Such dependencies would take into account the distinction between succession and branching through the transition matrix.j. Modelling the dependencies between ancestors A second limitation of the independent-children HMOT is related to the direct dependencies between a state and several of its ancestors. the features that could not be captured explicitly by the HMT model have been handled by the analysis of the restored state tree (e. also oriented from the root to the leaf vertices. the transition probability from the children states of vertex 1 to the state at vertex 1 would be P(S1 = i | S2 = j. (1997). the potential ambiguity between states that explains the ‘hidden’ nature of the model applies to the medium and long shoots only. Practically.3}. As for the dependent-children HMOT model. 6. S2 = j | S1 = i) = P(S3 = k | S1 = i)P(S2 = j | S1 = i) = P(S 2 = k | S1 = i)P(S3 = j | S1 = i) = P(S3 = j. then the transition probabilities at vertex u are P(Sc(u) = {k.newphytologist. Then: P(S3 = k. the states are markedly differentiated by the attached observation distributions. in the apple tree case. A way to reduce the number of parameters is to use the information on the edge types (< and +) to partially order the children. the model cannot make the distinction between succession and branching (see apple tree results. Such issues rely on building variable-order HMT models. it seems more relevant to orient the tree from the leaf vertices to the root. would be the implementation of the aforementioned families of HMT models that are synthetically represented in Fig. In the same direction. this would account for the existence of tree-structured patterns. 1999). They require additional assumptions of order.g. S2 = k | S1 = i) = pi. inspired by the variable-order Markov chains in the case of sequence analysis (Bühlmann & Wyner. S2 = k | S1 = i). and for some applications (when the attributes cannot be observed on the innermost part of the plant due to cambial growth and self-pruning). This is a consequence of the property of conditional independence of the children states. in both applications considered in this paper. The first is related to the absence of distinction between succession and branching. apical dominance. given the parent state.jk is another parameter of the model that is a priori different from pi. Alternative families of HMT models However. the simultaneous modelling of dependencies between children and ancestors does not seem © New Phytologist (2005) www. In the case of ordered children. enables the structures that are improperly represented in the model parameters to be highlighted (see apple tree results). Fig.km.g. Hidden Markov in-tree model For some biological phenomena (e. Hence the restoration of the hidden state tree. In this case. They are assumed to be invariant under any permutation of the nonsuccessor entities. The number of parameters of a dependent-children HMOT model is quite similar to that of a high-order or variable-order Markov chain.km. given the parent state. as described by Smyth et al. 4). The three HMT models are illustrated in Fig. the next step towards modelling conditional dependencies between children states. Dependent-children hidden Markov out-tree model To overcome this drawback. It follows from this property that the children’s conditional distribution is invariant under any permutation of the children: assume that vertex 1 has children set {2. Thus the transition probability matrix is similar to that of a high-order or variableorder Markov chain where. which can be considered as robust relative to a model misspecification.m} | Su = i) = pi. In the case of ordered children. These graphs represent the conditional independence properties between the random variables in the model. for apple tree). partial order. but with dependent children states.i. Consequently.

this ad hoc method can barely be extended to the determination of equivalent (or partially equivalent) branching systems. However. a number of models (not necessarily stochastic) are valid under the assumption that the local characteristics of the plant do not vary abruptly. the choice of the number of states is based. 6 Families of hidden Markov tree models and their parameters. the state variable. or for the extraction of remarkable paths – this approach proves especially useful in the context of perennial plants. In this case (or any other context of usually huge and complex crowns). tractable. This should lead to an adaptive sampling in the protocol of measurement. such as number of GUs between flowering occurrences. on the exploratory analysis and on statistical criteria. with tree comparison algorithms. which remains to be analysed at a local scale as well as globally. thus discrimination by the HMT models of many morphological changes requires large amounts of data. the existence of an order on the state values would provide a natural local cost function for this variable. However. 2000. Furthermore. developed by Celeux & Durand (2002) in the context of hidden Markov chains. These algorithms implement the comparison of branching systems on the basis of both topology and variables – in our case. for example using the tree segmentation obtained by state restoration. in the case of treestructured data. the segmentation of plants into a small number of states will offer new possibilities for quantifying New Phytologist (2005) 166: 813– 825 www. Perspectives on methodologies and applications Analysis of the periodicity of flowering occurrence requires computation of the distribution of empirical and theoretical characteristics of trees.. Consequently. Hence the trees may need to be sampled. and complete the proposed analysis of the state succession (see apple tree results). A further issue is the periodicity of flowering occurrence. More generally. As the HMT models provide a general framework for the identification of homogeneous zones within a plant – for its automatic segmentation into several parts of similar nature. although in this paper greater importance is given to these criteria. the amount of available entities per plant is large. 2001). the deletion of structural data (part of the tree topology) can be handled by the HMIT model. Concerning model building. The approach is based on a heuristic cost function that favours small values of the states at basal positions. From the viewpoint of application.newphytologist. As a result. is a promising way of determining reiterated complexes or identifying some hierarchical levels among branching systems.org © New Phytologist (2005) . 2003). the homogeneous zones are expected to provide some guidelines for the selection of branching systems for the reconstruction of whole individuals. dominating or equivalent paths have been handled here by HMT modelling only. Such a family of problems can be approached by dedicated methods that rely on an edit distance between tree structures (Ferraro & Godin. However. ideally. This approach has been used for the analysis of sequences. the loss of the notion of unique successor makes the definition of such characteristics more difficult.824 Research Fig. a high number of hidden states cannot be statistically supported by small data sets. As a consequence. the peripheral parts of individuals are numerous and tend to have lower variability than the central parts. In the case of partial measurements. which have greater variability. Concerning the issue of missing attributes for given entities. the combination of the state tree restoration provided by HMT modelling. the pruning strategy described in this paper for the bush willow data set can be avoided by resorting to a dedicated algorithm. For this purpose. The application of this enhanced model to the apple tree data set could illustrate its importance. homogeneous data sets obtained by such a sampling method could be analysed independently using different models. Lastly. and the results are quite helpful for model building and exploratory analysis. as well as for model validation (Guédon et al.

IEEE Transactions on Pattern Analysis and Machine Intelligence 22: 719 –725. Hidden Markov processes. Heckerman D. OR. 369–379. Wyner AJ. 1991. Gatsuk LE. 1997. Caraglio Y.newphytologist. 1979. facilitating projects from symposia to open access for our Tansley reviews. Sinoquet H. Godin C. Compstat 2002. Geiger D. In: Michalewicz MT. Celeux G. White J. Annals of Botany 89: 513 –524. Costes E. Annals of Forest Sciences 57: 445–461. Choosing the order of a hidden Markov chain through cross-validated likelihood. this should lead to a methodology for the validation of this notion. Ahrend P. Rapid reports and Methods papers are encouraged.Research 825 physiological age. Barthélémy D. 53–84.pdf Costes E. 1999. I. Stratified exponential families: graphical models and model selection. Algorithmica 36: 1–39. Lauri PÉ.ac. gradients morphogénétiques etâge physiologique chez les végétaux. Vorontzova LI. Smyth P. Godin C. Portland. 89 –136. Online-only colour is free. Ephraim Y.hu-berlin. 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You can take out a personal subscription to the journal for a fraction of the institutional price. ed. 1971. Baraniuk RG. 3A – A Software for the Acquisition of Plant Architecture. from online submission through to publication ‘as-ready’ via OnlineEarly – the 2003 average submission to decision time was just 35 days. Annals of Statistics 29: 505–529. IEEE Transactions on Information Theory 48: 1518–1569. Caraglio Y. L’Arbre: Biologie et Développement. the USA Office (newphytol@ornl.newphytologist. Naturalia Monspeliensia. Godin C.gov. A distance measure between plant architectures. Guédon Y. Version 2. 2001. Govaert G. From cell to system: repetitive units of growth in the development of roots and shoots. Acta Biotheoretica 39: 309 –323. 2002. © New Phytologist (2005) www.org New Phytologist (2005) 166: 813–825 . Golden Delicious). ed. Escobedo-Alvarez JA. Growth Patterns in Vascular Plants. Melbourne. Tokyo: Oxford University Press. Advances in Morphology 9: 1–66. Germany: Humboldt-Universität zu Berlin. 2000. Crouse MS. 2002. Godin C. Université Paris XII. We are committed to rapid processing. Research reviews. Zhukova LA.. DESS Gestion des Systèmes Agro-Sylvo-Pastoraux en Zone Tropicale. In: Klinke S. Rates start at £109 in Europe/$202 in the USA & Canada for the online edition (click on ‘Subscribe’ at the website). and essential print colour costs will be met if necessary. Ferraro P. Journal of Ecology 68: 675–696. 2003. do get in touch with Central Office (newphytol@lancaster. Age states of plants of various growth forms: a review. for a local contact in North America. King H. Barthélémy D. Journal of Theoretical Biology 191: 1–46. Neville P. http://ise.org. Biernacki C. As a perspective. eds. Pattern analysis in branching and axillary flowering sequences. Durand J-B. We also provide 25 offprints as well as a PDF for each article.wiwi. Mekk C. tel 865 576 5261). Modelling branching patterns on 1-year-old trunks of six apple cultivars. Gonçalvès P. Guédon Y. Heckerman D. tel +44 1524 592918) or. • If you have any questions. Clermont-Ferrand. Vol.de/~sigbert/compstat2002/paper/ short/C_02_celeux. Durand J-B. Probabilistic independence networks for hidden Markov probability models. Annals of Statistics 27: 480–513. IEEE Transactions on Signal Processing 52: 2551–2560. Nowak RD. Computational methods for hidden Markov trees – an application to wavelet trees.0. Neural Computation 9: 227–270. In: Bouchon J. Costes E. Relationship between the early development of apple fruiting branches and the regularity of bearing – an approach to the strategies of various cultivars. Costes E. eds. 2000. Exploring within-tree architectural development of two apple tree cultivars over 6 years. Annals of Botany 91: 91–104. • Regular papers. Measuring and analysing plants with the mod software. Sinoquet H. ex. Caraglio Y. 1998. 2002. Bell A. Guédon Y. Lespinasse JM. Jordan MI. Bühlmann P. Architecture. Godin C.uk. 1994. 1997. 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