Edited by: Alexandra Jullien, AgroParisTech, France
Reviewed by: Leo Marcelis, Wageningen University and Research Centre, Netherlands; Theodore M. DeJong, University of California, Davis, USA
*Correspondence: Evelyne Costes, INRA, Unité Mixte de Recherche 1334, Amélioration Génétique et Adaptation des Plantes Méditerranéennes et Tropicales Centre de Coopération Internationale en Recherche Agronomique pour le Développement-INRA-Montpellier SupAgro, Architecture et Fonctionnement des Espèces Fruitières Team, Avenue Agropolis, TA A 96/03 34398 Montpellier, France e-mail:
This article was submitted to Plant Biophysics and Modeling, a section of the journal Frontiers in Plant Science.
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Branching in temperate plants is closely linked to bud fates, either floral or vegetative. Here, we review how the fate of meristematic tissues contained in buds and their position along a shoot imprint specific branching patterns which differ among species. Through examples chosen in closely related species in different genera of the Rosaceae family, a panorama of patterns is apparent. Patterns depend on whether vegetative and floral buds are borne individually or together in mixed buds, develop as the shoot grows or after a rest period, and are located in axillary or terminal positions along the parent shoot. The resulting branching patterns are conserved among varieties in a given species but progressively change with the parent shoot length during plant ontogeny. They can also be modulated by agronomic and environmental conditions. The existence of various organizations in the topology and fate of meristematic tissues and their appendages in closely related species questions the between-species conservation of physiological and molecular mechanisms leading to bud outgrowth vs. quiescence and to floral induction vs. vegetative development.
Polycarpic plants are characterized by the co-existence of multiple axes which result from the activity of different meristems. These axes can be similar or morphologically differentiated. In temperate species, axes have been classified depending on the presence vs. absence of neoformed organs, i.e., organs that were not included in the bud at an embryonic stage but formed during the morphogenesis and elongation period of the shoot (see also glossary in Supplementary Material). Typically, short axes are composed of preformed organs only whereas long shoots are composed of preformed organs followed by neoformed ones (see Costes et al.,
In parallel, the physiological and genetic mechanisms underlying meristem organogenesis and the control of axillary meristem outgrowth have been extensively studied. Apical dominance is considered to be a function of auxin (IAA) production in the apical meristem (Thiman and Skoog, 1933 in Cline,
In the present paper, we aim at extending the current debate to more complex plants with different timings and locations of meristem outgrowths. In particular, polycarpic perennial plants growing in temperate conditions are characterized by the formation of buds that are able to survive winter periods and resume growth at spring. Moreover, these plants can be viewed as a population of meristems, each of them having different stages of differentiation and passing from one stage to the next one through remarkable transitions during ontogeny (White,
We review branching organization in temperate Rosaceae species used for ornament or fruit production. The Rosaceae family constitutes an interesting case study since it includes many economically important species but also contains very diverse plant forms; trees (e.g.,
Separated in individual axillary buds located in distinct zones in a tall tree, with strong apical dominance and acrotony (cherry),
Separated in axillary buds that are distinct but can be produced together at the same node in trees, with apical dominance and acrotony (almond), a tendency toward basitony (peach), or a tendency toward sympodial branching,
Combined into mixed buds located in terminal positions, composed of leaf primordia and a terminal inflorescence, that develops after a vegetative period lasting one to several years (apple), 1 year (“non-recurrent” or “once flowering,” rose and strawberry), several weeks (“recurrent” or “perpetual flowering” rose and strawberry, respectively).
The different configurations in the topology and fate of meristematic tissues and their appendages described in closely related species questions the evolution within the Rosaceae family and the co-adaptation of plant forms with their environment. They also question the between-species conservation of physiological and molecular mechanisms leading to bud outgrowth vs. quiescence, and to floral induction vs. vegetative development.
In both species, axillary buds can be vegetative, floral, or blind. The floral buds enclose a single, terminal flower, and typical of
For recurrent-flowering roses which represent the majority of cultivated roses, the flowering is auto-inducible and systematic, i.e., not subject to environmental conditions, provided that a trophic minimum is reached, and usually corresponding to production of six to seven leaves (Roberts and Blake,
Compared to the other Rosaceae model plants described above, strawberry is an herbaceous perennial. In strawberry, cultivated or woody, the branching is sympodial, with floral initiation occurring terminally. Extension axes can develop in the uppermost axillary buds below the terminal inflorescence (Battey et al.,
Whatever the flowering type, stolons emerge in long days from basal axillary buds, elongate and produce new plants through the so-called runnering process (Savini et al.,
In this review we have shown that different species are characterized by a typical organization of branching and flowering traits. How these organizations are modulated depends on internal factors such as the ontogenetic stage of the parent shoot or the genotype (see Supplementary Material—Changes in branching pattern with plant ageing (ontogeny) and Variability of branching pattern depending on the genotype, respectively). Moreover, branching patterns exhibit plasticity depending on cultural management and climatic conditions, either in fields or in greenhouses. Examples of this plasticity are provided in Supplementary material, focusing on tree management in the case of fruit trees and on the effects 47 of climatic controlled conditions in rose and strawberry.
A limited number of species and genera of the Rosacea family were considered which belong to two distant sub-taxa,
The most forest-type morphotype, represented by the cherry example, combines a strong acrotony—at both tree and shoot level—with a systematic separation of floral and vegetative meristems. The location of flowering buds in preformed zones, far from the SAM, allows the end of the juvenile period without altering the vegetative growth capacity of the SAM. By maintaining a long organogenetic period in the SAM of orthotropic axes, especially in the main axis, a tall tree is constructed, that is able to compete for light with its neighbors in a forest habitat. In contrast, the closer the floral tissues are from the apex the higher SAM determinacy. Among
The proximity between floral induction and SAM is maximal in the case of terminal flowering leading to sympodial branching. This sympodial branching when associated to a basitonic branching, at least for reiteration, leads to more bushy and creeping morphotypes, as in rose and strawberry. The present review revealed that apple tree, rose, and strawberry share common characteristics due to the terminal position of flowering and mixed buds with vegetative organs (leaf and shoot primordia) and flowers or inflorescences. Strawberry represents an extreme case of reduction of the vegetative apparatus into a rosette with axillary shoots (morphologically equivalent to a bourse and bourse shoot in apple) and a strong reiteration process via runnering. The main differences between these species result from (i) the position of long shoots and reiteration, mainly acrotonic in apple, either acrotonic when branching sequentially or basitonic when reiterating in rose and strawberry; (ii) the time interval between two consecutive flowering occurrences, from pluri-annual in apple to annual in once-flowering genotypes or intra-annual in recurrent-flowering genotypes of rose and strawberry. Even though transgenic plants could be induced to perpetual flowering when
Common molecular mechanisms between these species may be involved in the SAM maintenance, determinacy and flowering on the one hand and in the monopodial/sympodial and acrotony/basitony branching on the other hand. Indeed, the role of
In most species considered in this review, buds are formed and their fate determined during a growing season whereas they grow after a dormant winter period, in the following spring. This is typical of perennial structures, aside from the notable exception of sylleptic branching. Among the population of buds developed during a growing season, only a portion differentiates into flowers, at specific positions. These positions can also be viewed as particular time steps during the annual shoot development. In the cherry tree case, floral induction occurs in buds located in the preformed part of the shoot only, thus in a small number of meristems formed early during the season. This could result from the temporary expression of key genes as previously shown in poplar, in which a peak of
In species characterized by terminal flowering, the shoot apical meristem is not able to maintain its organogenic activity during an indeterminate period and floral induction occurs when this acitivity ceases. Because floral induction occurs either on short or long shoots which stop growing at different periods, the conditions of floral induction must be maintained throughout the growing season. Several authors have suggested that the constitution of an embryonic shoot in terminal floral buds in apple requires that organogenic activity is maintained until the winter rest period (Fulford,
Examining the topology and fates of meristematic and floral tissues at more global scales shows that the differentiation of tissues issuing from meristems is not limited to leaf emergence and phyllotactic arrangement but complex and precise spatial and temporal regulation operate in the populations of meristems constituting polycarpic plants. The quantification and modeling of bud fates depending on their position makes possible the simulation of plant development over time (e.g., Lopez et al.,
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
We gratefully thank our reviewers for helpful comments and editing. Studies on strawberry were supported by Région Aquitaine and EU FP7-KBBE-2010-4 Project (Grant Agreement no. 265942).
The Supplementary Material for this article can be found online at: