Floral Induction in Roses☆

Andrew V Roberts, University of East London, London, United Kingdom

Patrick S Blake, Horticulture Research International, Kent, United Kingdom
r 2017 Elsevier Inc. All rights reserved.

Introduction

Most wild roses are described as seasonal flowering because they produce flowers only during a short flowering season in late
spring/early summer. Recurrent-flowering cultivars produce flowers continuously throughout the growing season. They possess a
mutant gene that is recessive to its wild-type allele. Recurrent-flowering roses often mutate into climbing roses with a second
flowering late in the growing season. The inflorescence terminates the growth of a shoot, therefore, the flowering characteristics of a
rose is an important determinant of its growth habit. The main focus of this article is on genetic and hormonal factors involved in
the expression of seasonal-flowering, recurrent-flowering and the type of flowering in climbing roses derived by mutation from
recurrent-flowering roses.

Patterns of Vegetative Growth and Floral Initiation

A delay between seed germination and flowering is common in woody species. A plant is described as juvenile until it is competent
to produce flowers and is described as mature thereafter. The transition between the juvenile and mature phases is often
accompanied by changes in the vegetative characters. In many woody plants, including seasonal-flowering roses, changes occur in
growth rates, the shape of leaves and the ability of cuttings to form roots. Shoots that are formed at the base of mature woody
plants are typically juvenile and it has been postulated that mature shoots are only formed when there has been a “physiological
distancing” of the shoot apical meristem from the root system.
In their first growing season, seedlings of seasonal-flowering roses produce no flowers and can be regarded as juvenile. In their
second or, sometimes, third growing season they produce flowers and can be regarded as mature.
Seedlings of recurrent-flowering roses produce flowers soon after germination. In most recurrent-flowering roses, the flowers
appear on shoots with only six to seven compound leaves. Seedlings of climbing roses derived from recurrent-flowering roses by
mutation form flowers on shoots with approximately 14 compound leaves. The juvenile period of these roses can be regarded as
absent or of very short duration.
In temperate climates, most seasonal and recurrent-flowering field roses shed their leaves in late autumn and enter a dormant
period. However, within the vegetative buds on the dormant, leafless stems of mature shoots, cells of the terminal meristem
continue to divide slowly and form new leaf primordia. This slow increase in the number of leaf primordia is accompanied
by a gradual increase in the length of the bud. At bud-break in spring, the bud elongates and the leaves are sequentially
exposed (Fig. 1). The first leaves to be exposed are scale leaves at the base of the new shoot. These increase in number with the
period of dormancy to which the buds were subjected. They are followed by compound leaves. The shoot apical meristem then
undergoes a physiological change. It stops producing leaves and starts to initiate an inflorescence of one or more flowers. The
switch from vegetative to reproductive growth is accompanied by a flattening of the meristematic dome. Several weeks later, in late
spring or early summer, the flowers eventually emerge. The growth of the primary axis is terminated by the inflorescence and no
new leaves are formed. Further growth occurs from secondary shoots, which originate from buds in the axils of leaves on the
primary shoots.
In most seasonal-flowering roses, the secondary shoots elongate forming new leaves continuously throughout the remainder of
the growing season but are restrained from forming new flowers. Resources are not wasted on production of new flowers that
would be unlikely to form ripe hips in the same growing season. Recurrent-flowering cultivars possess a mutant gene that
overcomes this restraint and each secondary shoot, after producing a certain number of leaves, produces an inflorescence. The
number of compound leaves below the inflorescence on secondary shoots is approximately the same as those on the primary
shoots. If recurrent-flowering plants are maintained in a warm greenhouse, the development of axillary buds, each with a certain
number of leaves then a terminal inflorescence, occurs indefinitely in a repeating cycle of events. The determinate growth pattern of
recurrent-flowering roses, in which the growth of each shoot is terminated by an inflorescence, contrasts with the indeterminate
growth of the secondary shoots of seasonal roses (Fig. 1).
Comparisons between recurrent-flowering bush roses and their climbing mutants show that the climbing roses differ only in
producing more compound leaves before the inflorescence is initiated. Their longer shoots result from a greater number of
internodes, rather than from a greater length of internodes.

☆
Change History: January 2017. Andrew V. Roberts updated the text. Consequently the section “Mutations That Affect Floral Initiation” was replaced by “The
Genes for Seasonal Flowering, Recurrent-flowering and Climbing Roses” and the Section “Mechanisms for Floral Induction” was replaced by the more specific
heading “Control of Floral Induction by Gibberellins”. In the revised version, the order of these revised sections was reversed. A “references” section was also
added.

Reference Module in Life Sciences doi:10.1016/B978-0-12-809633-8.05057-3 1

2 Floral Induction in Roses

Fig. 1 A scheme illustrating the development of primary and secondary shoots in seasonal- and recurrent-flowering roses. In both types of rose,
floral initiation occurs at bud-break and terminates vegetative growth of the primary shoot. The development of secondary shoots in recurrent-
flowering roses is terminated by an inflorescence but vegetative growth continues indefinitely in seasonal-flowering roses.

Control of Floral Induction by Gibberellins

In seasonal-flowering roses, a period of dormancy is required before flowers can be initiated. Thus, for example, plants of Rosa
canina that have overwintered in a warm greenhouse do not flower in spring. After dormancy, young shoots that form in spring
first form the number of compound leaves that is typical of the species then floral initiation occurs.
In recurrent-flowering roses, the only factor that limits the initiation of flowers on new shoots is the requirement that a certain
number of leaves must first be initiated. As these roses have no specific environmental requirements for floral initiation (such as
long or short days, or a cold spell), they are described as self-inductive.
The class of plant hormones known as gibberellins are able to repress flowering in several woody Rosaceae, including apple,
cherry and rose. Evidence for the influence of gibberellins in roses comes from experiments involving the seasonal-flowering
climber “Félicité et Perpétue” and its recurrent-flowering sport “Little White Pet” (Roberts et al., 1999; Randoux et al., 2012). These
two cultivars are closely similar except for the seasonal versus recurrent-flowering character and the consequential effect of these
flowering patterns on their respective climbing and bush habits. Therefore, any physiological differences between them can be
attributed to the effect of the recurrent-flowering mutation.
The gibberellins in these roses were identified and quantified by gas chromatography–mass spectrometry (Roberts et al., 1999).
They were investigated at bud-break in March, in April just before the preformed flowers emerged and in September towards the
end of the growing season (Table 1). The gibberellins that showed most variability were GA1 and GA3. In “Félicité et Perpétue”,
their concentrations were low in March, increased substantially by April but by September had fallen again to similar levels to
those found in March. In “Little White Pet” these hormones were present in much lower concentrations than in “Félicité et
Perpétue”, particularly in April, when they were, respectively, 17-fold and 12-fold lower than in “Félicité et Perpétue”. To interpret
floral initiation in these roses, a model was proposed in which floral initiation proceeds if the combined concentration of
gibberellins stays below a certain threshold level but is prevented if they rise above that threshold. Thus at bud-break in “Félicité et
Perpétue”, floral initiation proceeds because the concentration of gibberellins is below the threshold. A second flowering is
prevented because, by April, the threshold has been exceeded. In “Little White Pet” the concentration of gibberellins remains below
the threshold throughout the growing season and flowering is unrestrained. Supporting evidence came from experiments in which
solutions of GA1 or GA3 in 70% ethanol (2 mg mL 1) were repeatedly applied, in 2 mL quantities, to growing shoots at bud-break.
In treated shoots of “Félicité et Perpétue”, the transition from vegetative to floral development was almost completely suppressed
by both of these gibberellins and branches of the inflorescence developed as vegetative shoots, whereas in “Little White Pet”
flowering proceeded normally (Table 2; Fig. 2).
The applications of gibberellins did not significantly affect the number of nodes formed before floral initiation but, in
accordance with the known properties of these gibberellins, they increased internode length. According to the proposed model,
the combined concentrations of endogenous and exogenously applied gibberellins exceeded the threshold in “Félicité et Perpétue”
in March and prevented the first flowering. However, in “Little White Pet”, as the concentration of endogenous gibberellins was
 Floral Induction in Roses 3

Table 1 Concentrations of gibberellins A1 and A3 at bud-break (March), prior to flowering

(April) and late season (September)
1
Concentration of gibberellins (ng g fresh weight7SE)

March April September

“Félicité et Perpétue” GA1 0.770.30 36.871.73 2.270.07

GA3 13.770.09 285.7727.00 12.570.42
“Little White Pet” GA1 0.270.05 2.270.03 2.670.02
GA3 7.370.50 22.970.62 12.570.28

Source: Based on the data of Roberts, A.V., Blake, P.S., Lewis, R., Taylor, J.M., Dunstan, D.I., 1999. The effect of
gibberellins on flowering in roses. Journal of Plant Growth Regulators 18, 113–119.

Table 2 Response at flowering of “Félicité et Perpétue” and “Little White Pet” to applications of GA3 at
bud-break

No. of flowers Mean internode No. of nodes below

per inflorescence length the inflorescence

“Félicité et Perpétue” Control 15.672.83 31.671.73 6.370.37

GA3 0.370.25 52.272.21 6.970.59
“Little White Pet” Control 11.471.94 34.472.39 6.070.38
GA3 12.073.77 54.673.10 6.070.38

Source: Based on the data of Roberts, A.V., Blake, P.S., Lewis, R., Taylor, J.M. Dunstan, D.I., 1999. The effect of gibberellins on
flowering in roses. Journal of Plant Growth Regulators 18, 113–119.

Fig. 2 Control shoot of “Félicité et Perpétue” (left) and an equivalent shoot that was treated with GA3 at bud-break (right). Note that, in the
treated shoot, flowers have been replaced by vegetative shoots.
4 Floral Induction in Roses

lower, the combined concentrations did not exceed the threshold and floral initiation was not inhibited. More recent data relating
to gene action, described in the following section, has increased our understanding of the role of gibberellins.

Genes for Seasonal-Flowering, Recurrent-Flowering and Climbing Roses

Recurrent-flowering sports of Rosa chinensis were found, cultivated and bred in China about 1000 years ago (Guoliang, 2003).
Modern-day recurrent-flowering cultivars were bred from these sports. The gene responsible for this characteristic is a mutant gene
that is recessive to its wild-type allele and F1 hybrids between recurrent-flowering cultivars and wild roses are seasonal-flowering. It
is generally the case that a recessive mutant gene is a damaged gene that is unable to function normally. In the case of the recurrent-
flowering gene the ability that has been lost is the restraint of flowering. Recently information has emerged at the molecular level,
on how this happens.
The wild-type homologue of the recessive gene for seasonal flowering in roses has been named RoKSN, where Ro stands for rose
and KSN for “Koushin”, the ancient Japanese name for recurrent-flowering Rosa chinensis (Iwata et al., 2012). RoKSN encodes a
protein called RoKSN (written without italics). RoKSN is activated (transcribed into mRNA) when gibberellins are present in shoot
apices in a sufficiently high concentration. RoKSN is then produced which prevents the initiation of flowers (Randoux et al., 2012;
Remay et al., 2009). The role of wild-type RoKSN is to repress the transition from vegetative growth to flowering. The effect of the
recurrent-flowering mutation is to render RoKSN impotent and unable to repress this transition. Evidence for the role of the wild-
type RoKSN and the effect of the mutation includes comparisons between the previously mentioned roses “Félicité et Perpétue”
and “Little White Pet” (Iwata et al., 2012; Randoux et al., 2012) with regard to the amounts of transcripts of RoKSN and the protein
RoKSN present in their shoot tips. In both of these roses, flowers are initiated soon after bud break at the start of the growing
season when endogenous concentrations of gibberellins are low (as in March, Table 1). At this stage neither the RoKSN transcript
nor the protein RoKSN is detectable (Iwata et al., 2012). In “Félicité et Perpétue”, when concentrations of gibberellins rise in April
(Table 1), RoKSN is transcribed, RoKSN accumulates and initiation of flowers is blocked until the following spring. In “Little White
Pet”, RoKSN has been disabled and neither the RoKSN transcript nor RoKSN were detectable at any stage of development. In the
absence of RoKSN and its inhibitory effects, flowering proceeds unabated through to the end of the growing season. It has not yet
been resolved how the mutation to recurrent flowering in the RoKSN gene interacts with the gibberellin pathway.
In its origins “Félicité et Perpétue” is a diploid hybrid between a recurrent-flowering rose, probably a Noisette rose, and
R. sempervirens which is seasonal flowering. From the Noisette rose it inherited the disabled form of RoKSN and from
R. sempervirens it inherited wild-type RoKSN. Both forms of RoKSN can be detected in shoot apices of “Félicité et Perpétue” but only
the disabled RoKSN can be detected in “Little White Pet” (Iwata et al., 2012). This indicates that the mutation from “Félicité et
Perpétue” to “Little White Pet” resulted from a deletion of wild type RoKSN.
Very specific information is now available about the mutational event that gave rise to recurrent flowering. It resulted from the
insertion of a 9-kbp transposon into the second intron of the RoKSN gene (Iwata et al., 2012). Transposons, also known by
the descriptive terms “mobile genetic elements” and “jumping genes” are composed of DNA that can replicate and move (jump),
to new locations in the genome, often disrupting genes into which they are inserted. The transposon disabled RoKSN to the extent
that no transcript is detectable and RoKSN is not produced.
In an interesting experiment which further demonstrates the ability of RoKSN to inhibit flowering, a recurrent-flowering
tetraploid cultivar of Rosa hybrida was transformed with a construct containing wild-type RoKSN (Randoux et al., 2013). Five
transgenic plantlets were regenerated from in vitro culture. They did not produce flowers within 12 months of transfer from
in vitro culture to a greenhouse, which is what would be expected of seasonal-flowering roses. In contrast, controls consisting of
non-transformed plants and plants transformed with an empty vector flowered within 70 days which is typical of recurrent-
flowering roses.
Recurrent-flowering roses frequently mutate to a climbing habit in which the first flush of flowers in spring is followed by a
second flowering late in the growing season. The climbing mutants differ from the original cultivar in producing more nodes
before the inflorescence is initiated, not by an increase in the length of internodes. They arise from a mutation that occurs within
the transposon that disabled RoKSN and involves a reduction of 9-kbp transposon to a 1-kbp fragment of DNA (Iwata et al., 2012).
This reduction results in a partial reversion to seasonal flowering. In the diploid climbing rose “Old Blush Cl.” the only form of
RoKSN present is that with the 1-kbp fragment. In five cultivars including the tetraploid climbing rose “Peace Cl.” both the 9-kbp
transposon and the 1-kbp forms of RoKSN are present (Iwata et al., 2012). This shows that the gene containing the 1-kbp fragment
is dominant over the gene containing the original 9-kbp fragment.

Future Prospects
Recurrent flowering has been a crucial factor in the popularity of roses as cultivated plants. The advanced techniques now available
for investigating this phenomenon may lead to new developments in rose breeding. For example, Rosa rugosa is an unusual wild
rose in that it produces flowers throughout the growing season. It would be interesting to know if the control of flowering in this
species differs from that in recurrent flowering cultivars derived from R. chinensis and if this might lead to opportunities for
introducing novel patterns of flowering.
Recent developments in the understanding of the control of flowering in roses have been assisted by similarities with control
mechanisms in other plant genera, including the ephemeral weed Arabidopsis thaliana. Similarities are particularly close between
 Floral Induction in Roses 5

roses and other genera of the family Rosaceae. For example, the strawberry, Fragaria vesca, has a recurrent-flowering variant known
as the woodland strawberry. This arose from a frameshift mutation that disabled FvKSN, the strawberry’s homologue of RoKSN.
It is quite likely that work on roses as model species might assist in the study of the control of flowering in other commercially
important Rosaceae, including Malus (apple) which has a longer juvenile period than roses and is consequently a less convenient
subject for genetic studies.

References

Guoliang, W., 2003. Ancient Chinese roses. In: Roberts, A.V., Debener, T., Gudin, S. (Eds.), Encyclopedia of Rose Science. Oxford and San Diego: Elsevier Ltd, pp. 387–395.
Iwata, H., Amèlia, G., Arnaud, R., et al., 2012. The TFL1 homologue KSN is a regulator of continuous flowering in rose and strawberry. The Plant Journal 69, 116–125.
Randoux, M., Davière, J.-M., Jeauffre, J., et al., 2013. RoKSN, a floral repressor, forms protein complexes with RoFD and RoFT to regulate vegetative and reproductive
development in rose. New Phytologist 202, 161–173.
Randoux, M., Jeauffre, J., Thouroude, T., et al., 2012. Journal of Experimental Botany 63, 6543–6554.
Remay, A., Lalanne, D., Thouroude, T., et al., 2009. A survey of flowering genes reveals the role of gibberellins in floral control in rose. Theoretical and Applied Genetics 119,
767–781.
Roberts, A.V., Blake, P.S., Lewis, R., Taylor, J.M., Dunstan, D.I., 1999. The effect of gibberellins on flowering in roses. Journal of Plant Growth Regulation 18, 113–119.

Further Reading

Cockshull, K.E., Horridge, J.S., 1977. Apical dominance and flower initiation in the rose. Journal of Horticultural Science 42, 421–427.
De Vries, D.P., 1976. Juvenility in hybrid tea roses. Euphytica 25, 273–284.
Hackett, W.P., 1987. Juvenility, maturation and rejuvenation in woody plants. Horticultural Reviews 7, 109–155.
Horridge, J.S., Cockshull, K.E., 1974. Flower initiation and development in the glasshouse rose. Scientia Horticulturae 2, 273–284.
Wickland, D.P., Hanzawa, Y., 2015. The Flowering Locus T/Terminal Flower 1 gene family: Functional evolution and molecular mechanisms. Molecular Plant 8, 983–997.