Agricultural Systems 97 (2008) 99–107

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Agricultural Systems
journal homepage: www.elsevier.com/locate/agsy

Review

Integrated agricultural research and crop breeding: Allelopathic weed control

in cereals and long-term productivity in perennial biomass crops
M. Weih a,*, U.M.E. Didon a, A.-C. Rönnberg-Wästljung b, C. Björkman c
a
Swedish University of Agricultural Sciences, Department of Crop Production Ecology, P.O. Box 7043, SE-750 07 Uppsala, Sweden
b
Swedish University of Agricultural Sciences, Department of Plant Biology and Forest Genetics, P.O. Box 7080, SE-750 07 Uppsala, Sweden
c
Swedish University of Agricultural Sciences, Department of Ecology, P.O. Box 7044, SE-750 07 Uppsala, Sweden

a r t i c l e i n f o a b s t r a c t

Article history: Future agricultural research will need to increasingly integrate ecological, physiological and molecular
Received 13 September 2007 methods, in order to understand agricultural crops in situ and their interaction with the environment
Received in revised form 23 January 2008 as well as organisms impacting on their long-term health and productivity (‘agricultural eco-genomics’).
Accepted 21 February 2008
The need for integration will increasingly implicate on crop breeding strategies for most agricultural sys-
tems. In this paper, implications are highlighted for two contrasting areas of agricultural research related
to sustainable crop production: first, the possibilities to utilize crop allelopathic activity to suppress
weeds as an alternative to chemical weed control; and second the increasing interest to environmentally
Keywords:
Allelopathy
friendly and sustainable produce perennial energy crops on agricultural land. ‘Sustainability’ in agricul-
Crop breeding ture is difficult to define unequivocally, but frequently implies the increased utilization of ecological pro-
Energy crops cesses. Breeding strategies towards increased utilization of allelopathic crops require initially the
Quantitative trait loci (QTL) integration and verification of allelopathic processes in various agricultural contexts, because there is
Weed control currently great uncertainty about the predictable operation of allelopathic activity in different ecological
Biological control contexts. Breeding programs for future biomass crops, most promising are perennials such as Salix, would
Salix greatly benefit from the integration of ecological information affecting long-term productivity, e.g., eco-
Insect pests
physiological growth determinants at stand level and the biological control of pests. Agricultural eco-
genomics could facilitate a compromise between intensive agriculture and the frequently expressed
demand for greater sustainability in agriculture.
Ó 2008 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 100
2. Integration of agricultural research at several levels . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 100
2.1. Integration of molecular and genetic approaches . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101
2.2. Integration of physiological processes at the whole-plant level . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101
2.3. Integration of ecological information . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101
2.4. Integration of management strategies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101
3. Crop breeding of cereals: can allelopathic crop functions become powerful selection criteria?. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102
3.1. Allelopathic germplasm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102
3.2. Allelochemicals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102
3.3. Genetic background of allelopathic activity. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102
3.4. Implications for breeding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103
4. Crop breeding of agricultural crops grown for energy. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103
4.1. Perennial energy crops . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 104
4.2. Current achievements in Salix breeding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 104
4.3. Implications for future breeding of perennial crops . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 104
4.4. Implementation of ecological information into Salix breeding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 104

* Corresponding author. Tel.: +46 18 672543; fax: +46 18 673440.

E-mail address: martin.weih@vpe.slu.se (M. Weih).

0308-521X/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.agsy.2008.02.009
100
5. ‘Agro-eco-genomics’ – do we need a new approach? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105
1. Introduction
Crop yield is often defined as the outcome of crop growth and
development processes occurring during the growing season (Sla-
fer, 2003), but includes also the non-growth period during winter
in the case of perennial crops. Growth and development are deter-
mined by the genetic constitution of the crop (genotype) and var-
ious ecological factors affecting the phenotype, including the
abiotic and biotic environment (climate, herbivores, diseases, weed
flora, etc.) and management actions. There is often a large gap be-
tween actual crop yields achieved by farmers and potential crop
yield. The reasons are that crops grown experimentally experience
environments with no limitation of nutrients and water at the
same time as pests, diseases, weeds and other stresses are effec-
tively controlled by specific management actions that are not fea-
sible in the agricultural practice (Evans, 1993; Cassman, 1999). The
yield gap is determined partly by climatic factors and/or crop and
soil management practices reducing the expression of the genetic
potential, and partly by genetic factors conferring adaptation to a
given set of relevant ecological factors (e.g., phenological adjust-
ment, tolerance/resistance to pests and diseases). Crop breeding
programs usually target simple phenotypic traits most often re-
lated to yield parameters of economic interest and measured in a
sample of environments in a region of economic interest. In addi-
tion, the breeding goals most often build on the frequent applica-
tion of chemicals for weed and pest control. The breeding tools
have frequently been very successful, but their application is time
consuming and expensive, especially for new perennial crops with
short breeding histories. Crop breeding is today increasingly as-
sisted by molecular biological methods, for example by using
quantitative trait loci (QTL) analysis to elucidate the genetic archi-
tecture of yield traits (Asíns, 2002; Holland, 2007) and marker-as-
sisted selection (MAS) (Francia et al., 2005) to support breeding.
QTL analysis is a suitable approach to investigate the genetic basis
of phenotypic traits and the method has been used extensively in
agricultural crop breeding (e.g., MAS) to detect interesting genomic
areas for quantitative trait variation (e.g., Hirel et al., 2001;
Varshney et al., 2006; Manneh et al., 2007). Despite the great
achievements in molecular breeding methods, we are far from
understanding crop yield through gene mapping (Tardieu et al.,
2005; Fischer, 2007; Holland, 2007). The arrival of new breeding
tools in the genomics era offers a single- to multiple-gene focus,
in which the point of departure for breeding improvements is at
the gene level (Morgante and Salamini, 2003; Borevitz and Chory,
2004; Boerjan, 2005). The implementation of the new tools into
practical breeding therefore requires bridging effectively the
apparent gap between genes and crop response (Edmeades et al.,
2004), by integrating research in genetics/genomics, physiology
and ecology.
The integration of physiology and crop breeding has been dis-
cussed extensively in the literature (e.g., Shorter et al., 1991; Jack-
son et al., 1996; Snape, 2001), but most studies have adopted a
largely physiological perspective on breeding, focusing mostly on
the regulation of genes that might be relevant for the expression
of particular physiological characters and mechanisms. Moreover,
much of this research seems to be executed outside a relevant
agro-ecological context and without a serious attempt to integrate
single physiological processes into a whole-plant or systems ap-
proach (Sinclair and Purcell, 2005).
M. Weih et al. / Agricultural Systems 97 (2008) 99–107
Crop management implies the controlled modification of spe-
cific ecological factors in order to minimize the gap between po-
tential and realized crop performance. Thus, ecological research
on crop performance in relation to, e.g., potential pests and weeds,
should be an important component of a breeding approach inte-
grating crop management. Techniques and approaches originating
from genomics research are increasingly also incorporated into
ecological research and focus on the function and variation of
genes in an ecological context (‘eco-genomics’, Feder and Mitch-
ell-Olds, 2003). Also here, a major criticism has been that gene
function is often not measured in ecologically relevant environ-
ments (Ouborg and Vriezen, 2007).
Crop breeding currently faces two major challenges: first, the
shift in focus from traditional yield- and quality-related parame-
ters towards crop traits particularly relevant in more sustainable
forms of agriculture (Bruinsma, 2003), and second the increasing
importance of new energy crops grown agriculturally instead of
traditional food crops (Jordan et al., 2007). ‘Sustainability’ in agri-
culture is difficult to define unequivocally, but may often employ
agronomic practices minimizing highly processed chemical inputs,
stressing soil building programs, and long-term environmental
sustainability (Bruinsma, 2003). On one hand, the increasing
importance of sustainability issues in agriculture suggests that fu-
ture breeding programs need to focus more on crop characters rel-
evant in the context of sustainable agriculture methods (Murphy
et al., 2005; Mason and Spaner, 2006; Sagar and Kartha, 2007 for
biomass crops). Suggested methods include the utilization of alle-
lopathic crop properties for weed control (Lovett, 1991; Bond and
Grundy, 2001; Belz, 2007) and the use of natural arthropod preda-
tors instead of pesticides (e.g., Carcamo et al., 1995; Letourneau
and Goldstein, 2001; Schmidt et al., 2005). On the other hand,
the anticipated future shift from traditional food crops towards en-
ergy crops involves particular challenges for crop breeding, be-
cause many of the most promising energy crops are perennial
(e.g., short rotation willow, miscanthus), as opposed to the annual
character of most traditional agricultural crops, and have a rela-
tively short breeding history (Gullberg, 1993; Clifton-Brown
et al., 2001).
The point of departure for this paper is the accumulated evi-
dence indicating that agricultural research will need to strongly
integrate ecological, physiological and molecular methods. In the
following chapter, several levels of integration are briefly high-
lighted, providing the basis for a critical discussion of the implica-
tions that the need for increased integration will have for future
crop breeding. Two major issues are discussed in detail to illustrate
the implications for breeding: the potential for breeding towards
specific allelopathic properties to reduce herbicide rates in the
agricultural production of especially cereals (chapter 3), and the
specific challenges associated with the implementation of new
tools into breeding programs for a perennial biomass crop (Salix
spp.) grown for energy purpose on agricultural land in boreo-tem-
perate regions (chapter 4).
2. Integration of agricultural research at several levels
A key task in agricultural research is to study the biological
mechanisms that influence or underlie important crop traits. The
mechanisms of each trait of interest are usually manifested at rela-
tively low levels of biological organization (genes within individu-
 M. Weih et al. / Agricultural Systems 97 (2008) 99–107
als, individual organisms within ecosystems), while the significance
and relevance of a trait often is only apparent at higher levels (e.g.,
Feder and Mitchell-Olds, 2003). It is therefore necessary to investi-
gate the genetic control of important crop traits, how the traits affect
short- and long-term crop productivity in a given agricultural envi-
ronment, and how this environment (e.g., climate, weeds and insect
pests) interacts with the expression of the crop traits at different
time scales. This is an enormous task, which will require a very high
degree of integration of molecular, genetic, physiological and eco-
logical disciplines. Major needs for integration appear at various lev-
els, of which mainly four are discussed here.
2.1. Integration of molecular and genetic approaches
When molecular biologists have tried to introduce genes for
specific physiological processes into plants in order to improve
complex traits, many have been unable to show significant effects
on the final trait, although clear effects on the single physiological
processes were demonstrated (for nutrient use efficiency, see re-
view by Good et al., 2004). Thus, the use of molecular biological
methods alone appears to be rather ineffective with regard to the
improvement of complex crop traits at a whole-plant perspective.
However, some successful applications have been demonstrated,
e.g., marker-assisted selection (MAS) has been used to improve
resistance towards pests and pathogens in various crops (Varshney
et al., 2006). Areas in the genome of importance for trait variation,
i.e., quantitative trait loci (QTL) for complex traits, such as water
and nutrient use efficiency, have been identified in mapping popu-
lations of major agricultural crops and potential energy crops (e.g.,
Hirel et al., 2001; Rönnberg-Wästljung et al., 2005; Manneh et al.,
2007). Thus, the identification of candidate genes and analysis of
their expression pattern is a powerful tool to focus rapidly on
genes that can improve complex traits. If operational genetic trans-
formation systems are available for crops, transgenics have a great
potential for the test and verification of gene functions identified
by classical breeding and MAS.
2.2. Integration of physiological processes at the whole-plant level
Breeding and selection for improved genotypes requires the
screening of many growth-related traits in large numbers of geno-
types. The collection of sufficient amounts of data on relevant com-
plex traits and the physiological processes behind can be difficult
or even impossible. We therefore will need to shift focus from the
genetic control of single physiological processes towards a whole-
plant approach (Sinclair and Purcell, 2005) and towards consi-
deration of the relevant agro-ecological context. This implies the
establishment of links between single crop functions (e.g., allelo-
pathic activity) and whole-plant functions (e.g., crop productivity)
under various environmental conditions, as well as the development
of high-throughput methods for the rapid assessment of complex
crop traits (e.g., long-term productivity) on large quantities of
field-grown plants (cf. Weih and Rönnberg-Wästljung, 2007).
2.3. Integration of ecological information
A general problem in agriculture is that many processes that, in
natural systems, provide essential services, such as fertilization,
mineralization, pollination, predation, etc., need to be artificially
boosted to get an adequate yield, for example, by using herbicides
and pesticides. Herbicides constitute an increasing proportion of
crop protection chemicals relative to pesticides, because the use
of pesticides is decreasing due to pest-resistant crops being devel-
oped either through conventional breeding or the incorporation of
transgenes imparting pest resistance traits (Duke et al., 2001). In
contrast to pest-resistant crops, the introduction of herbicide-
101
resistant crops will make farming increasingly dependent on herbi-
cides and thus enhance herbicide use in agriculture.
An essential difference between annual and perennial crops is
that many potentially important ecological processes (e.g., compe-
tition and predation) operate at a time scale longer than 1 year.
Thus, in perennial crop systems, the need for boosting actions
may be lower because many of the processes are operating natu-
rally and there is increasing evidence that perennial systems can
utilize ecological processes more efficiently than annual systems
(Jordan et al., 2007). The active management of agricultural sys-
tems relying on the utilization of ecological processes will only
be possible if we understand the mechanisms behind the relevant
ecological processes and at what temporal scales these processes
operate (Jordan, 1993). For example, the consideration of mecha-
nisms related to the biological control of pests and weeds (e.g.,
allelopathy) requires ecological information on complex processes
beyond single genes and even single plants, and the involved pro-
cesses often act at delayed time scales compared to the more or
less rapid effects on crop yield envisaged in traditional genetic
and molecular biological work. Thus, breeding strategies need to
integrate the relatively short-term events studied by geneticists
and molecular biologists with the longer-term ecological informa-
tion investigated by ecologists.
2.4. Integration of management strategies
Crop growth, development and yield are determined by com-
plex interactions between genotype, physiology and environment,
the latter is often heavily influenced by management actions (e.g.,
crop harvest). Therefore, crop breeding relying on ecological pro-
cesses needs to be done in concert with matching management
strategies that enhance the processes of interest (Jordan, 1993).
Important management actions, such as crop harvests, often
imply major disturbance factors in all agricultural systems. The ef-
fects are often negative on ecological processes that otherwise may
stabilize the systems. For example, biological control by natural
enemies of insect pests is disrupted by harvesting in perennial wil-
low coppice systems (see chapter 4.4; Björkman et al., 2004). The
disturbance effect is likely to increase with the frequency of har-
vest actions. Thus, in perennial compared with annual systems,
there is a greater probability that ecological processes act at a rate
close to the corresponding natural systems. In general, if the effect
of artificial weed or pest control (e.g., herbicides or pesticides)
should be accomplished by utilization of ecological processes, it
is necessary to allow the action of several (or multiple) biological
control processes for longer time periods in a cultivation system
(Fig. 1). Particularly perennial systems may lack the weed control
Sum of control processes
Natural control
(Need for)
artificial control
(to achieve same effect)
Time
Fig. 1. Relationship between time and the sum of ecological (biological) control
processes (e.g., predation, allelopathy, etc.) and the mirror image, indicating the
need for the same artificial control (e.g., pesticides) to achieve the same controlling
effect on pests or weeds. The hatched area indicates observed responses of mirid
bugs (predators of leaf beetles) in short rotation coppice willows (cf. Fig. 3).
102 M. Weih et al. / Agricultural Systems 97 (2008) 99–107

effect accomplished by soil management practices after harvesting erally explained 34% of the weed suppressive effect, and in 4% of
in annual cropping systems. However, weed problems in perennial the rice cultivars the weed suppressive effect was largely explained
systems are usually greatest during the stand establishment phase by allelopathy (Olofsdotter et al., 2002). Wheat (Triticum spp.) cul-
and negligible later on (cf. Nordh, 2005 for short rotation willow). tivars screened in the laboratory also showed large variation in
allelopathic potential (Spruell, 1984; Wu et al., 2000), but only a
small proportion (0–21%) of the competitive ability in wheat was
3. Crop breeding of cereals: can allelopathic crop functions
explained by allelopathic activity (Bertholdsson, 2005). Consider-
become powerful selection criteria?
able variation in the allelopathic potential of barley (Hordeum
vulgare L.) has been demonstrated by Bertholdsson, 2004, 2005,
Since the 1950s, agriculture depended on the use of herbicides
and 7–58% of the weed suppressive effect examined in the field
and pesticides to suppress weeds and ensure high yields. The traits
could be assigned to the allelopathic activity of the cultivars inves-
important for weed competition were not among the major foci of
tigated in the laboratory (Bertholdsson, 2005). Great variation in
breeders, because herbicides took care of the weeds in practical
allelopathic activity has also been demonstrated in the laboratory
farming. Therefore, the specific characteristics enhancing compet-
for oats (Avena sativa L.) and rye (Secale cereale L.) (Fay and Duke,
itive ability of cereal crops against weeds have been considered
1977; Belz and Hurle, 2005).
very little in crop breeding programs. The application of weed
and pest controlling chemical agents has therefore steadily in-
3.2. Allelochemicals
creased, although a number of pesticides have had well-docu-
mented negative consequences on the environment and on
Great progress has been made in identifying potential allelo-
human health. Biological control offers a number of alternative ap-
pathic compounds, and a number of highly active compounds have
proaches for pest, disease and weed control in agriculture (Jordan,
been found in particular in root exudates (Weidenhamer, 1996;
1993; Bond and Grundy, 2001; Mason and Spaner, 2006), but the
Field et al., 2006 and references therein). In rice, various phenolic
application of biological weed control has often proved difficult
acids have shown allelopathic activity in laboratory bioassays,
in practice (Müller-Schärer et al., 2000). Allelopathy is regarded
but other substances were identified as more important allelo-
as a promising component of biological control measures (Lovett,
chemicals (Chung et al., 2001, 2006; Dong et al., 2005; Field
1991) and is defined as any direct or indirect effect of one plant
et al., 2006). The main groups of allelochemicals in wheat and
(or microorganism) on another mediated through the production
rye include phenolic and hydroxamic acids (Barnes and Putnam,
of chemical compounds that escape into the environment (Rice,
1987; Pérez and Ormeño-Núñez, 1991; Wu et al., 2001). Scopole-
1974; Macías et al., 2007). In general, the role of allelopathy in
tin, various phenolic acids and an amino acid are discussed as pos-
plant–plant interactions and especially its potential for weed con-
sible allelochemicals in oats (Fay and Duke, 1977; Sánchez-
trol in agriculture are controversial, because evidence for direct
Moreiras et al., 2004). The phytotoxic effect of sorghum has been
allelopathic effects and ecological relevance is often difficult to
attributed to the exudation of sorgoleone, a group of benzoquinon-
prove (Blum et al., 1999; Inderjit and Weston, 2000; Inderjit and
es for which biosynthesis and exudation characteristics are under
Weiner, 2001; Inderjit, 2006). Nevertheless, crop plants with supe-
way to be thoroughly described (Czarnota et al., 2001; Yang
rior weed suppressive ability under field conditions would be
et al., 2004; Dayan, 2006; Field et al., 2006).
highly desirable in agriculture (Olofsdotter, 2001). A number of
studies have shown that there are large differences between crop
3.3. Genetic background of allelopathic activity
cultivars in their ability to suppress weeds and these differences
have been explained in part by means of variable capacity to se-
Quantitative trait loci (QTL) associated with allelopathic effects
crete chemical substances affecting weed growth, i.e., allelopathy
have been identified in rice (Jensen et al., 2001; Okuno and Ebana,
(Wu et al., 2000; Olofsdotter et al., 2002). Allelopathic activity
2003; Dong et al., 2005). Genetic and molecular biological work on
has been suggested to be particularly high in cereals (Sánchez-
wheat allelopathy or allelochemicals includes the identification of
Moreiras et al., 2004), and Olofsdotter et al. (2002) concluded that
QTL and initial studies on gene functions (Niemeyer and Jerez,
allelopathy was the dominant factor determining enhanced com-
1997; Wu et al., 2003; Macías et al., 2007). In barley, oats, rye
petitive ability in some rice cultivars. These results may indicate
and maize little genetic (e.g., QTL) or molecular biological informa-
a potential of allelopathy traits for use as effective selection criteria
tion is available on quantitative differences in allelochemical pro-
in breeding programs of cereals in particular. In general, the weed
duction of cultivars with different allelopathic activity (Belz,
competitiveness of the cultivars produced during the history of
2007). The identification of QTL for allelopathic functions in rice
crop breeding is poorly known (Murphy et al., 2005; Mason and
and wheat indicates a possibility to enhance allelopathic activity
Spaner, 2006). In particular, the influence of crop breeding since
in crops using MAS (Olofsdotter et al., 2002). However, as Belz
the 1950s on crop competitive ability is unknown and it is unclear
(2007) pointed out, direct links between QTL and allelopathic
whether the crop’s own defence system has been affected during
activity or allelochemicals have yet not been demonstrated. Molec-
the history of breeding. For example, certain allelochemicals (e.g.,
ular biological work on Sorghum includes the identification of
hydroxyamic acids, see chapter 3.2) appear to be absent in culti-
genes associated with the sorgoleone pathway and indicates the
vated barley, but have been found in wild Hordeum species (Barria
possibility to enhance the gene expression of allelochemicals
et al., 1992). A handbook on testing methodology of cereal varieties
through gene engineering (Duke, 2003). Moreover, the genes con-
regarding their weed competitiveness has been recently prepared
trolling allelochemical pathways in maize, oats and rice, appear to
(Donner and Osman, 2007), but gives no specific recommendations
operate as functional gene clusters, in contrast to other well-
for variety testing with regard to allelopathic traits.
known secondary metabolite pathways such as the anthocyanin
biosynthesis, in which the involved genes are unlinked (Field
3.1. Allelopathic germplasm et al., 2006). The existence of functional gene clusters implies that
the involved biochemical pathways can be inherited as a functional
In both laboratory and field screening, thousands of rice (Oryza entity (Qi et al., 2004), which might be an advantage in the molec-
sativa L) cultivars have been examined for allelopathic potential ular breeding of cereal cultivars with enhanced weed suppressive
and partly showed great variation in allelopathic activity (Olofsd- ability. Major obstacles for the development of efficient breeding
otter, 2001; Olofsdotter et al., 2002). The allelopathic activity gen- programs towards enhanced allelopathic activity include the com-
 M. Weih et al. / Agricultural Systems 97 (2008) 99–107
plexity of the ecological, physiological, biochemical and molecular
biological processes involved in the phenomenon of allelopathy
(e.g., autotoxicity, environmental influence on allelopathy effects,
multiple-gene functions; Duke et al., 2001; Fitter, 2003; Belz,
2007) and thereby the difficulty to identify clear breeding objec-
tives and reliable traits that can be rapidly assessed in large quan-
tities of field-grown crop individuals.
3.4. Implications for breeding
Weed management in agriculture aimed at the reduction of her-
bicide use needs to comprise multiple strategies, among them the
use of cultivars with improved competitive traits, such as superior
early-season growth, increased leaf area and enhanced allelopathic
activity (Jordan, 1993; Christensen, 1995; Didon and Hansson,
2002; Mason and Spaner, 2006). The improvement of allelopathic
traits of crops through modern breeding is frequently discussed
as a most promising option, with strong potential for the develop-
ment of highly weed suppressive cultivars (Duke, 2003; Belz, 2007;
Macías et al., 2007). Nevertheless, predicting that allelopathy will
occur in a given field situation will be a formidable task, because
results from allelopathic studies are often inconsistent and do
not allow the clear separation of allelopathic effects from other
plant–plant or plant–environment interactions (Qasem and Hill,
1989; Wardle et al., 1992; Inderjit et al., 2001; Kobayashi, 2004).
In addition, allelopathic activity is influenced by plant develop-
mental stage (Burgos et al., 1999; Ben-Hammouda et al., 2001),
as well as interaction with the biotic and abiotic environment (Sei-
gler, 1996; Blum et al., 1999; Thelen et al., 2005; Dayan, 2006). All
these complications clearly indicate that breeding strategies for the
development of highly allelopathic and weed suppressive cultivars
must verify all the necessary steps in the breeding process (cf.
Fig. 2) in situ, at a whole-plant perspective and within a relevant
agro-ecological context. Crop breeding will therefore require
strong multidisciplinary collaboration including physiologists,
ecologists and molecular biologists (Olofsdotter, 2001; Murphy
et al., 2005). Due to the long time scales and great importance of
environmental interactions in the ecological processes utilized,
Fig. 2. Scheme for the different steps involved in a breeding strategy for sustainable crop improvement. QTL = quantitative trait loci, MAS = marker-assisted selection, and
SNP = single nucleotide polymorphism.
103
crop modelers will play a crucial role in supporting the breeding
process (Fig. 2; Shorter et al., 1991; An et al., 2003; Yin et al.,
2004). Furthermore, breeding to enhance crop allelopathic activity
needs to be done in concert with development of management
strategies that effectively take advantage of the enhanced allelo-
pathic activity (Ransom et al., 2007). For example, the application
of crop rotations is often a successful weed management strategy
(e.g., Bond and Grundy, 2001). The introduction of crops or culti-
vars with enhanced allelopathic effects against weeds into the crop
rotation could be an effective way to maximize the weed control
effect. The allelopathic effects might include direct influences of
root exudates actively excreted in the rhizosphere (i.e., increased
competitive ability), and/or pre-crop influences, where allelopathic
compounds are released during the decomposition of plant resi-
dues; many cereals indeed incorporate both functions (Sánchez-
Moreiras et al., 2004).
Current research achievements thus indicate that allelopathic
crop functions could possibly become powerful selection criteria
within cereal breeding. However, the prerequisite for the success-
ful utilization of allelopathic activity in terms of breeding is that
allelopathy is confirmed in various ecological contexts and that
the integration of ecological information becomes an essential part
of breeding strategies.
4. Crop breeding of agricultural crops grown for energy
The production of biomass for energy purposes on agricultural
land is an important way to generate renewable energy and a sig-
nificant and increasing fraction of agricultural land in Europe and
world-wide is likely to be dedicated to the culture of energy crops
in the near future (Hoogwijk et al., 2003; Johansson and Azar,
2007). Regarding the transport sector, so-called first-generation
bio-fuels such as bio-diesel and bio-ethanol (mainly produced
from oilseed rape and cereals) dominate the bio-fuel sector today
(EUBIA, 2006). Compared to traditional breeding for food purposes,
future breeding of these annual crops for use as biofuel will require
new breeding goals such as reduced harvest index (i.e., decreased
grain fraction and increased straw fraction) in cereals (Jørgensen
104 M. Weih et al. / Agricultural Systems 97 (2008) 99–107
et al., 2007), but can largely rely on the existing breeding programs
for annual crops. However, a shift towards second-generation bio-
fuels, produced from mainly lignocellulosic biomass (i.e., perenni-
als such as miscanthus, fibre hemp and short rotation willow), is
expected for the future (Jordan et al., 2007). These developments
will greatly increase the incentives to grow perennial crops on
agricultural land.
4.1. Perennial energy crops
Several perennials are currently discussed as potential energy
crops on agricultural land, among them rhizomatous grasses such
as miscanthus (Clifton-Brown et al., 2001; Lewandowski et al.,
2003) and fibre hemp (Ranalli, 2004), but for most of these crops
no breeding programs are established so far and only little experi-
ence is available on the breeding and practical agriculture of these
crops under commercial conditions. Willow (Salix) coppice grown
in short rotation on agricultural land is an exception in this re-
spect: breeding programs to improve yield and resistance as well
as management systems for the agriculture of this perennial crop
have been developed in Europe and North-America during the last
decades (Christersson et al., 1993; Gullberg, 1993; Smart et al.,
2005; Kuzovkina et al., 2008).
4.2. Current achievements in Salix breeding
A major challenge in breeding of a perennial crop such as Salix is
the production of plant material with high productivity over many
years. The cyclic nature of Salix cultivation, with harvests every 3–5
years for a period of up to 25 years, also stresses the need for spe-
cific breeding goals compared to breeding of an annual agricultural
crop. Durable resistance towards pathogens and insects, tolerance
towards abiotic factors such as frost and drought, and nutrient re-
source economy are especially important, because plants are sup-
posed to grow for many years.
Yield and resistance traits often interact with environmental
factors in perennial crops such as Salix (e.g. Weih, 2001; Nordh,
2005; Weih and Nordh, 2005). Moreover, the interaction may vary
over time, which can have important implications for breeding
especially in long-lived perennial systems. For example, in a soil
contrast with clay and sand the G  E interaction was of greatest
importance in the first years after establishment, while in a nutri-
ent contrast with high and low nutrient availability the G  E inter-
action increased with time (Rönnberg-Wästljung et al., 1994).
Quantitative trait loci (QTL) analysis has been used to study the
genetic control of complex growth traits as well as to elucidate the
genetics behind G  E interactions (Rönnberg-Wästljung et al.,
2005; Weih et al., 2006). A part of this analysis is to develop genet-
ic linkage maps, which have been made for various Salix species
and hybrids (Hanley et al., 2002; Barcaccia et al., 2003; Rönn-
berg-Wästljung et al., 2003). The QTL have been identified and
mapped with significant effects on Salix frost resistance and phe-
nology (Tsarouhas et al., 2003, 2004), growth, water-use efficiency
and drought tolerance (Rönnberg-Wästljung et al., 2005; Weih
et al., 2006). Common QTL across various field and controlled envi-
ronments were found, but also QTL specific for particular environ-
ments. Some QTL were stable across different environments and
could be useful selection tools in MAS (Francia et al., 2005), but
even the QTL specific for particular environments could be used
for MAS in the selection of genotypes adapted to specific environ-
ments (Rönnberg-Wästljung et al., 2005).
Association mapping is another technique increasingly consid-
ered in the breeding of perennial crops, for which functional map-
ping populations take long time to establish (Neale and Savolainen,
2004; Boerjan, 2005). Here, associations between markers and
phenotypes of individuals in natural populations are utilized and
the method allows greater mapping resolution compared to the
QTL approach. Association mapping requires large allelic variation,
but has been applied successfully. The broad knowledge base on
QTL for yield and resistance traits in Populus (e.g., Bradshaw and
Stettler, 1995; Wullschleger et al., 2005; Jorge et al., 2005; Rae
et al., 2007) and the sequencing and annotation of genes in the
Populus genome (Tuskan et al., 2006) make new approaches avail-
able for the identification of genes behind QTL in Populus. The close
taxonomic relationship between Populus and Salix renders the Pop-
ulus genome sequence a valuable tool also in Salix breeding. Thus,
Hanley et al. (2006) concluded that it should be possible to isolate
functional candidate genes from willow using the public poplar
genome resources as a basis, and thereby pinpoint the specific
genes underlying the corresponding QTL. These possibilities indi-
cate a great potential to gain maximized benefit in the breeding
of complex traits through the integration of molecular and genetic
approaches.
4.3. Implications for future breeding of perennial crops
The above mentioned techniques have a great potential to re-
duce the gap between genotype and crop response, and to move
breeding closer to the gene(s) causing phenotypic variation. For
Salix, large-scale breeding based on MAS appears fully realistic
and the corresponding research activities are under way (e.g., in
Sweden and UK; Fig. 2). The MAS approach is particularly powerful
for traits which are difficult and time consuming to measure, and
for traits which, for natural reasons, cannot be phenotyped every
year, but can have dramatic impacts on crop yield (e.g., resistance
against pests with cyclic appearance; Francia et al., 2005). The typ-
ical characteristics of long-lived systems such as perennial cultures
imply particular challenges also for phenotyping. Especially for
perennial crops, growth and crop optimization models are valuable
tools to identify relevant traits for phenotyping and screening
across large quantities of genotypes. Here, the knowledge from
growth optimization models could be implemented into breeding
by the model-based development of non-destructive high-
throughput methods for the rapid estimation of relevant crop traits
(Fig. 2; Weih and Rönnberg-Wästljung, 2007). The development of
high-throughput phenotyping, in combination with the introduc-
tion of MAS at an early breeding stage, will both make phenotyping
more effective and reduce the number of individuals required for
phenotyping, which ultimately could make breeding more cost
effective.
4.4. Implementation of ecological information into Salix breeding
In ecology, there has been an intense debate about the relative
role of bottom-up (plants) and top-down (natural enemies) forces
in affecting the density of herbivorous organisms (Hairston et al.,
1960; Walker and Jones, 2001; Denno et al., 2002). Most interest-
ingly, the mechanisms discussed in this debate are identical with
those used in the biological control of many plant-feeding pests,
e.g., plant quality and predation pressure (Walter, 2003). This
raises the question whether ecological information on herbivore–
plant interactions could be used in the breeding of perennial crops
owing properties that minimize the risk for pest attacks. For exam-
ple, it has been suggested that the frequent harvest events in short
rotation willow plantations, i.e., every 3rd to 5th year, constantly
provide leaf beetles with high-quality, nutritious food (Price and
Martinsen, 1994). The often observed high densities of leaf beetles
in willow plantations, resulting in a reduced biomass production of
up to 40% (Björkman et al., 2000a), appear thus as a consequence of
improved plant quality, which would be in support for an impor-
tant role of bottom-up forces in affecting herbivore densities. How-
ever, attempts to verify this hypothesis revealed inconsistent
 M. Weih et al. / Agricultural Systems 97 (2008) 99–107
6 searcher and require systematic collaborations among research
5 proaches thus have been developed within different disciplines.
Log density per ha
4 application of genomic tools to study agriculture-related questions
3 neously studying all or most of its genes’ (Koltai and Volpin, 2003).
2 ics puts much stronger focus on the study of organisms in situ
1 Herbivore
Natural enemy
0 tempt to take increased advantage of ecological processes, agricul-
Years after harvest
Fig. 3. Simplified drawing of observed changes in the density of a willow herbiv-
orous leaf beetle and its main natural enemy, a mirid bug, with time after harve-
sting. Redrawn from Björkman et al. (2004).
results (Kelly and Curry, 1991; Björkman et al., 2000b; C. Björk-
man, unpubl.). In fact, most evidence suggests that top-down
forces are more important and that harvest events disrupt the
build-up of biological control through natural enemies (Björkman
et al., 2000b, 2004; Fig. 3).
A combination of various methods is probably needed to effec-
tively protect perennial crops from pests: the establishment of
moderately resistant or tolerant plants in combination with man-
agement methods to support natural enemies appears to be a gen-
erally attractive alternative (Walter, 2003). Plant resistance traits
(e.g., leaf hairs) induced by pest activities are especially interesting
here, partly because these are often associated with lower resource
costs for the plant in the long-term, compared to constitutive
traits, and partly because inducible resistance traits involve a lower
risk for the evolution of counter-adaptations in the herbivore. For
example in willows, there is evidence for induced increase in leaf
trichome density in response to leaf beetle grazing (Dalin and
Björkman, 2003; Dalin et al., 2004). The induction coincides in time
with the main feeding period of the larval offspring of the beetles,
and increased leaf trichome density affects the leaf beetle larvae
negatively (Dalin and Björkman, 2003). Although induced plant re-
sponses have been reported to impact not only on the herbivores,
but also their natural enemies (Agrawal et al., 2002; Ode, 2006),
the main natural enemies in the willow system are not negatively
affected by leaf trichome density (Björkman and Ahrné, 2005).
Thus, by learning more about the genetics behind the induced in-
crease in willow leaf trichome density, it might be possible to pro-
duce genotypes that, in concert with a proper management
strategy, effectively decrease the risk of reduced long-term bio-
mass productivity by willow leaf beetles.
A major challenge in an attempt to utilize biological control
mechanisms for breeding is thus the identification of ecologically
relevant resistance traits that can be used in the development of
molecular markers for early selection. A first attempt to identify
genetic causes behind herbivory resistance in a willow system re-
vealed a number of QTL for several damage types, but only few of
them were reliable by means of common QTL across different envi-
ronments (Rönnberg-Wästljung et al., 2006).
5. ‘Agro-eco-genomics’ – do we need a new approach?
The two examples discussed above, i.e., allelopathy and biomass
crop breeding, were from very different areas of agricultural re-
search, but revealed a common insight: the molecular tools and
much of the functional understanding required to achieve the goal
of more integrated agriculture are often available, but effective
integration may frequently be beyond the capacity of a single re-
105
communities with differing research cultures. Integrative ap-
For example, agricultural functional genomics was defined as the
and focuses on ‘understanding of a crop or a pathogen by simulta-
In contrast to agricultural genomics, ecological functional genom-
and the longer time scales required for the investigation of ecolog-
ical processes (Feder and Mitchell-Olds, 2003). Considering the
ecological time scales to be applied in agricultural systems that at-
tural research could greatly benefit from development towards
increased integration. The major goal for such an integrated ‘agri-
cultural eco-genomics’ approach would be the understanding of
agricultural crops in situ and their interaction with environment
as well as organisms impacting on their long-term health and
productivity.
A focus on maximizing the utilization of ecological interaction
effects faces the challenge of utilizing ecological processes in a suf-
ficiently controlled way, such that the long-term benefits, com-
pared to intensive agriculture (cf. Cassman, 1999), exceed the
great costs and risks associated with the development and imple-
mentation of the adequate methods. Agricultural eco-genomics,
with its integrated approach, offers an interesting approach for
the search of a sound compromise between intensive agriculture
and the frequently expressed demand for greater sustainability in
agriculture. Agriculture in general will probably gain a lot from
an increased use of perennial crops and a greater focus on sustain-
ability, as these provide possibilities for enhanced utilization of
ecological processes (cf. Jordan et al., 2007) and possibly also great-
er resilience against disturbances in the context of climate change.
Climate change, especially an increase in temperature, will most
likely affect the ecological interactions of importance in crop
breeding to management. For example, crop genotypes and differ-
ent species of weeds and herbivores may respond differently to
changes in temperature (i.e., genotype  temperature interactions;
e.g., Slafer and Rawson, 1995; Weih, 2001; Dahlhoff and Rank,
2007). Genotype  environment (G  E) interaction effects are par-
ticularly important in perennial systems, where crops accumulate
environmental effects across several years, as well as in an agricul-
tural practice, which would greatly rely on the utilization of eco-
logical processes sensitive to G  E interaction effects (see Fig. 1).
Therefore, considering G  E interaction effects is of primary
importance in future plant breeding aimed at the increased utiliza-
tion of ecological processes.
Acknowledgements
We would like to thank various colleagues for inspiring discus-
sions before and during the preparation of the manuscript, and also
two anonymous referees and the journal editor for valuable com-
ments to a previous version of the manuscript. MW, CB and ACRW
received funding from the Swedish Energy Agency. UMED would
like to acknowledge the financial support from the Swedish Re-
search Council for Environment, Agricultural Sciences and Spatial
Planning (Formas).
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