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Evolution and Development of Inflorescence Architectures Przemyslaw Prusinkiewicz, Yvette Erasmus, Brendan Lane, Lawrence D

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Evolution and Development of Inflorescence Architectures Przemyslaw Prusinkiewicz, Yvette Erasmus, Brendan Lane, Lawrence D RESEARCH ARTICLES These observations raise two related questions. First, what determines the extent of morphospace occupied by inflorescences in nature: Why do we Evolution and Development of find these three main architectural types and not more or fewer? Second, what constrains evolution within the occupied morphospace, imposing a Inflorescence Architectures local barrier between racemes and cymes? A unifying inflorescence model. Previously, Przemyslaw Prusinkiewicz,1 Yvette Erasmus,2* Brendan Lane,1 distinct developmental models have been postu- Lawrence D. Harder,3 Enrico Coen2† lated for different inflorescence types (12, 13), leading to a fractured view of phenotypic space. To understand the constraints on biological diversity, we analyzed how selection and development From an evolutionary perspective, however, in- interact to control the evolution of inflorescences, the branching structures that bear flowers. We florescence types should be related to each other show that a single developmental model accounts for the restricted range of inflorescence types through genetic changes. A developmental mod- observed in nature and that this model is supported by molecular genetic studies. The model el that encompasses different architectural types predicts associations between inflorescence architecture, climate, and life history, which we within a single parameter space is thus needed. validated empirically. Paths, or evolutionary wormholes, link different architectures in a To construct it, we considered meristems giving multidimensional fitness space, but the rate of evolution along these paths is constrained by rise to shoots or flowers as two extremes of a genetic and environmental factors, which explains why some evolutionary transitions are rare continuum. The variable that characterizes this between closely related plant taxa. continuum is called vegetativeness (veg), with high levels of veg corresponding to shoot meri- Downloaded from rganisms display great diversity in shape oretically possible structures increases rapidly stem identity and low levels to flower meristem and architecture, but the range of ob- (8). However, only a small subset of these struc- identity. The veg level may be related to many Oserved forms represents only a small tures corresponds to inflorescences observed in factors such as plant age, meristem position, in- fraction of what is theoretically possible (1, 2). nature (Fig. 1). They are grouped into three broad ternal state of a meristem, and the environment For example, when patterns of shell coiling are architectural types: (i) panicles, which com- (14–17). For simplicity, we identify the factors considered within a mathematically defined prise a branching series of axes that terminate in influencing veg as plant age t, measured from the http://science.sciencemag.org/ space of possible forms (morphospace), the ob- flowers; (ii) racemes, which comprise axes beginning of inflorescence development, and/or served forms are restricted to only a subregion bearing flowers in lateral positions or lateral the internal state of the meristem. of this space (3). One explanation for such re- axes that reiterate this pattern; and (iii) cymes, If veg is high and does not change with time, strictions is selection (4). However, it is likely which comprise axes that terminate in flowers an indeterminate vegetative branching structure that developmental and genetic mechanisms also and lateral axes that reiterate this pattern (9–11) is generated (Fig. 2A). For the plant to produce play a role. For example, the absence of ver- (Fig. 1, D to I). The appearance of each flowers, veg mustdeclineinsomeorallmeri- tebrates with more than four limbs is thought to inflorescence type varies according to the stems during growth. The simplest assumption reflect an interplay between both developmental arrangement of lateral meristems around the is that veg decreases in all meristems equally. and selective constraints (5, 6). Developmental stem (phyllotaxy), the pattern of internode The resulting architecture is a panicle of flowers, mechanisms restrict the range of genetic and lengths, and additional variations on the three which form at time T when low levels of veg phenotypic variation available for selection, architectural themes. Although panicles, race- are reached (Fig. 2B). on May 8, 2018 whereas selection influences the evolution of mes, and cymes are all found among flowering To generate further architectural types, we developmental processes. Such two-way inter- plants, a restricted range of types is evident at assume that meristems can be in one of two actions can be unravelled using morphospaces local taxonomic levels: Genera seldom include internal states, A and B, such that meristems in based on developmental genetic mechanisms. species with both racemes and cymes. these states attain low levels of veg at different We take this approach for the evolution of in- florescences, which has a history of both theo- retical and molecular genetic analysis. The arrangement of flowers on a plant reflects an iterative pattern of developmental decisions at the growing tips, or meristems. Each iteration occurs over a time interval known as a plasto- chron (7), during which a meristem may either switch to floral identity or continue to produce further meristems and, hence, branches. As the number of iterations rises, the number of the- 1Department of Computer Science, University of Calgary, 2500 University Drive N.W. Calgary, Alberta T2N 1N4, Ca- nada. 2Department of Cell and Developmental Biology, John Innes Centre, Colney Lane, Norwich NR4 7UH, UK. 3Department of Biological Sciences, University of Calgary, 2500 University Drive N.W. Calgary, Alberta T2N 1N4, Canada. Fig. 1. Hypothetical and observed inflorescence structures. Arrows, meristems; circles, flowers. (A *Present address: Institute of Molecular Plant Science, Daniel to C) Inflorescence structures not observed in nature. (D to F) Three main classes of inflorescence Rutherford Building, Kings Buildings, Mayfield Road, Edin- burgh, EH9 3JR, UK. architectures: panicle (D), raceme (E), and cyme (F). (G to I) Species illustrating inflorescence types: †To whom correspondence should be addressed. Email: (G) fruiting panicle of Sorbus aucuparia, (H) flowering raceme of Antirrhinum majus, (I) flowering [email protected] cyme of Myosotis arvensis. 1452 8 JUNE 2007 VOL 316 SCIENCE www.sciencemag.org RESEARCH ARTICLES times, TA and TB. Suppose that the apical result is inconsistent with the structure of lateral rationale for this reversion is that a newly created meristem of the main axis is in state A, whereas branches of compound racemes, which typically meristem (state B) changes its identity once it all lateral meristems are in state B. If TB < TA, do not terminate in flowers (Fig. 1E). becomes the terminal meristem of the next-order lateral meristems will attain floral identity more To resolve this discrepancy, we postulate that branch (state A). Biologically, state B represents quickly than does the apical meristem, yielding a state B is transient. All lateral meristems are the stage when a meristem is newly formed (im- raceme in the upper part of the plant (red path in formed in state B, but they have two possible mature), whereas state A represents a more ad- Fig. 2C). However, lateral apices in the lower fates afterwards. If veg is sufficiently low, the vanced stage of meristem development (mature). part of the inflorescence will also rapidly pro- meristem becomes a flower (red path, Fig. 2D). We call the resulting model the transient model. gress toward floral identity, producing a graded Otherwise, the meristem reverts to state A and A key feature of the transient model is that it series of panicles (orange path in Fig. 2C). This produces a branch (orange path, Fig. 2D). The can generate cymes as well as racemes and panicles, thus accounting for these inflorescence types within a single framework. In cymes, lateral meristems repetitively create meristems in two different states: a terminal meristem giving rise to a flower, and a lateral meristem giving rise to a branch (Fig. 1F). This can be captured with the transient model by setting TA < TB. Immature lateral meristems then take longer to attain floral identity than do mature meristems, creating the reverse of the situation for racemes (Fig. 2E). The region of morphospace generated by the transient model is illustrated in Fig. 3. The main Downloaded from diagonal (TA = TB) corresponds to panicles, flanked by racemes on one side (TA > TB)and cymes on the other (TA < TB). This planar region represents only a slice of the entire morphospace. For example, the hypothetical forms shown in Fig. 1, A to C, do not lie in this region and could http://science.sciencemag.org/ only be generated with more complex mecha- nisms. The transient mechanism may therefore account for the restriction of observed inflores- Fig. 2. Architectures and time course of veg decline for various inflorescence models. Small filled cence types to a small region of morphospace. circles, meristems; white circles, flowers. Colors highlight paths of representative meristems: main Potentially adaptive architectures may not be at- meristem, blue; lowest lateral meristem, orange; third lateral meristem from bottom, red. Plots tained in nature because they cannot be produced show the time course of veg decline in selected meristems after their initiation. (A) Level of veg by developmental processes captured by the tran- does not change with
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