Research Article

Evolution and Development of Inflorescence Architectures

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Science  08 Jun 2007:
Vol. 316, Issue 5830, pp. 1452-1456
DOI: 10.1126/science.1140429

Abstract

To understand the constraints on biological diversity, we analyzed how selection and development interact to control the evolution of inflorescences, the branching structures that bear flowers. We show that a single developmental model accounts for the restricted range of inflorescence types observed in nature and that this model is supported by molecular genetic studies. The model predicts associations between inflorescence architecture, climate, and life history, which we validated empirically. Paths, or evolutionary wormholes, link different architectures in a multidimensional fitness space, but the rate of evolution along these paths is constrained by genetic and environmental factors, which explains why some evolutionary transitions are rare between closely related plant taxa.

Organisms display great diversity in shape and architecture, but the range of observed forms represents only a small fraction of what is theoretically possible (1, 2). For example, when patterns of shell coiling are considered within a mathematically defined space of possible forms (morphospace), the observed forms are restricted to only a subregion of this space (3). One explanation for such restrictions is selection (4). However, it is likely that developmental and genetic mechanisms also play a role. For example, the absence of vertebrates with more than four limbs is thought to reflect an interplay between both developmental and selective constraints (5, 6). Developmental mechanisms restrict the range of genetic and phenotypic variation available for selection, whereas selection influences the evolution of developmental processes. Such two-way interactions can be unravelled using morphospaces based on developmental genetic mechanisms. We take this approach for the evolution of inflorescences, which has a history of both theoretical 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 plastochron (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 theoretically possible structures increases rapidly (8). However, only a small subset of these structures corresponds to inflorescences observed in nature (Fig. 1). They are grouped into three broad architectural types: (i) panicles, which comprise a branching series of axes that terminate in flowers; (ii) racemes, which comprise axes bearing flowers in lateral positions or lateral axes that reiterate this pattern; and (iii) cymes, which comprise axes that terminate in flowers and lateral axes that reiterate this pattern (911) (Fig. 1, D to I). The appearance of each inflorescence type varies according to the arrangement of lateral meristems around the stem (phyllotaxy), the pattern of internode lengths, and additional variations on the three architectural themes. Although panicles, racemes, and cymes are all found among flowering plants, a restricted range of types is evident at local taxonomic levels: Genera seldom include species with both racemes and cymes.

Fig. 1.

Hypothetical and observed inflorescence structures. Arrows, meristems; circles, flowers. (A to C) Inflorescence structures not observed in nature. (D to F) Three main classes of inflorescence architectures: panicle (D), raceme (E), and cyme (F). (G to I) Species illustrating inflorescence types: (G) fruiting panicle of Sorbus aucuparia, (H) flowering raceme of Antirrhinum majus, (I) flowering cyme of Myosotis arvensis.

These observations raise two related questions. First, what determines the extent of morphospace occupied by inflorescences in nature: Why do we find these three main architectural types and not more or fewer? Second, what constrains evolution within the occupied morphospace, imposing a local barrier between racemes and cymes?

A unifying inflorescence model. Previously, distinct developmental models have been postulated for different inflorescence types (12, 13), leading to a fractured view of phenotypic space. From an evolutionary perspective, however, inflorescence types should be related to each other through genetic changes. A developmental model that encompasses different architectural types within a single parameter space is thus needed. To construct it, we considered meristems giving rise to shoots or flowers as two extremes of a continuum. The variable that characterizes this continuum is called vegetativeness (veg), with high levels of veg corresponding to shoot meristem identity and low levels to flower meristem identity. The veg level may be related to many factors such as plant age, meristem position, internal state of a meristem, and the environment (1417). For simplicity, we identify the factors influencing veg as plant age t, measured from the beginning of inflorescence development, and/or the internal state of the meristem.

If veg is high and does not change with time, an indeterminate vegetative branching structure is generated (Fig. 2A). For the plant to produce flowers, veg must decline in some or all meristems during growth. The simplest assumption is that veg decreases in all meristems equally. The resulting architecture is a panicle of flowers, which form at time T when low levels of veg are reached (Fig. 2B).

Fig. 2.

Architectures and time course of veg decline for various inflorescence models. Small filled circles, meristems; white circles, flowers. Colors highlight paths of representative meristems: main meristem, blue; lowest lateral meristem, orange; third lateral meristem from bottom, red. Plots show the time course of veg decline in selected meristems after their initiation. (A) Level of veg does not change with time; an indeterminate vegetative branching structure results. (B) Veg declines at a similar rate in all meristems and yields flowers upon reaching threshold VK at time T; a panicle results. (C) Veg in apical meristems (state A) reaches threshold VK at time TA > TB for lateral meristems (state B). The resulting structure is a compound raceme, with lower branches terminating in flowers. (D) Transient model in which lateral meristems are initially in state B but revert to state A if veg does not reach the threshold VK; a raceme with indeterminate branches is produced for TB < TA. (E) Transient model in which TB > TA yields a cyme.

To generate further architectural types, we assume that meristems can be in one of two internal states, A and B, such that meristems in these states attain low levels of veg at different times, TA and TB. Suppose that the apical meristem of the main axis is in state A, whereas all lateral meristems are in state B. If TB < TA, lateral meristems will attain floral identity more quickly than does the apical meristem, yielding a raceme in the upper part of the plant (red path in Fig. 2C). However, lateral apices in the lower part of the inflorescence will also rapidly progress toward floral identity, producing a graded series of panicles (orange path in Fig. 2C). This result is inconsistent with the structure of lateral branches of compound racemes, which typically do not terminate in flowers (Fig. 1E).

To resolve this discrepancy, we postulate that state B is transient. All lateral meristems are formed in state B, but they have two possible fates afterwards. If veg is sufficiently low, the meristem becomes a flower (red path, Fig. 2D). Otherwise, the meristem reverts to state A and produces a branch (orange path, Fig. 2D). The rationale for this reversion is that a newly created meristem (state B) changes its identity once it becomes the terminal meristem of the next-order branch (state A). Biologically, state B represents the stage when a meristem is newly formed (immature), whereas state A represents a more advanced stage of meristem development (mature). We call the resulting model the transient model.

A key feature of the transient model is that it 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 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 only be generated with more complex mechanisms. The transient mechanism may therefore account for the restriction of observed inflorescence types to a small region of morphospace. Potentially adaptive architectures may not be attained in nature because they cannot be produced by developmental processes captured by the transient mechanism.

Fig. 3.

Morphospace for the transient model. Different phenotypes are generated by varying the times TA and TB at which flowers begin to form. Values along each axis range from 0 to 10 plastochrons. Black arrows, pointing away from the wild-type architecture of Arabidopsis, indicate the effect of tfl1 and lfy mutations [under inductive conditions (20)]. Inflorescences are shown at six plastochrons.

Integration of models with developmental and molecular genetics. To assess the plausibility of the transient model, we related it to underlying genetic mechanisms. We focused on two architectural genes from Arabidopsis, TERMINAL FLOWER 1 (TFL1) and LEAFY (LFY) (1823), as they produce phenotypes that displace the wild-type plant in orthogonal directions in morphospace (Fig. 3). Compared to wild-type Arabidopsis, which produces branched racemes, mutants lacking TFL1 activity produce inflorescences with short axes that terminate in flowers, whereas mutants lacking LFY produce highly branched inflorescences bearing shootlike flowers.

We incorporated genes into the transient model by postulating that TFL1 increases veg and LFY reduces veg in meristems (Fig. 4A). The wild-type Arabidopsis architecture results from high TFL1 and low LFY activity in state A meristems (yielding high veg) and high LFY and low TFL1 activity in state B meristems (yielding low veg). This pattern of gene expression is produced by assuming that: (i) LFY and TFL1 inhibit each other (18, 20, 22), (ii) TFL1 expression is inhibited in state B, (iii) LFY is less sensitive to TFL1 inhibition in state B [this enhances LFY in B meristems and allows LFY to attain high activity even in plants overexpressing TFL1 (24)], and (iv) the levels of TFL1 and LFY increase with plant age (21, 25). The shootlike flowers observed in lfy mutants (20) and plants overexpressing TFL1 (22, 24) are captured by assuming that they correspond to intermediate veg levels, lying between the levels for normal shoots and flowers.

Fig. 4.

Incorporating LFY and TFL1 genes into the transient model for Arabidopsis. (A) Interactions between genes, time, veg, and growth underlying the model. Growth increases the number of modules and hence influences the spatial pattern of gene expression. Gene activity affects veg and hence influences whether a meristem will continue to generate more modules or whether it will cease growing. Arrowheads indicate up-regulation; bars, down-regulation. Growth promotes production of meristems in state A or B, with state B reverting to A unless the floral threshold is reached. (B to H) Wild-type, mutant, and transgenic phenotypes generated by the model with the interactions shown in (A), assuming inductive conditions (20). Circles indicate flowers, color-coded according to veg levels. White, normal flower; yellow/green, shootlike flower). Arrows indicate branches. (For detailed explanation, see SOM.)

With these assumptions, the transient model largely accounts for mutant and overexpression phenotypes of Arabidopsis (Fig. 4, B to H, and SOM text) and for observed patterns of gene expression. According to the model, a lateral meristem that gives rise to a branch is initially in state B, which corresponds to relatively low TFL1 and high LFY. This pattern reverses when the meristem switches back to state A. These features agree with experimental data: TFL1 expression is low in newly formed lateral primordia and only increases later (22). Furthermore, LFY is expressed early in primordia that will give rise to lateral branches but is absent from mature lateral shoot meristems (25, 26). The transient model thus provides a functional explanation for observed expression patterns.

Evolutionary origins and implications of the transient mechanism. Both the range of architectural types observed in flowering plants and molecular genetic data lend support to the transient mechanism, but the evolutionary origin of this mechanism is unclear. To elucidate it, we considered the fitness of different architectures in the region of morphospace generated by the transient model (SOM text).

With unlimited pollination and a growing season of fixed length, the optimal inflorescence architecture is a panicle. This is because the plant can delay flowering by keeping its meristems in a vegetative state until the latest time needed for fruit production, thus maximizing branching and the number of fruits (Fig. 5, A and B). However, if the length of the growth seasons varies from year to year, a plant that delays flowering too long may fail to produce any fruits by the end of a short season. This would reduce fitness, particularly if annual seed production is essential for genotype survival. The best strategy may thus be for a plant to “hedge its bets” (2732) and generate flowers sequentially during a season, so that some flowers are produced early if the season is short but more flowers can still be produced later if the season is long. Racemes and cymes, in which only a fraction of meristems switch to floral identity at any time, may then have higher fitness values than panicles. This is illustrated in Fig. 5, C and D, in which racemes and cymes form separate adaptive peaks in the fitness landscape for annual plants, with the positions of the peaks depending on the standard deviation of growth duration.

Fig. 5.

(A to E) Two-dimensional fitness landscapes. Fitness levels are indicated by height and color. For each genotype, fitness is calculated over seasons with an average duration Td and standard deviation σ, assuming that fraction θ of mature plants survives from one season to the next. Plants illustrate the architecture generated at time Td. (A) For annuals with fixed growth duration, the optimal inflorescence is a panicle, represented by a single adaptive peak. (B) If Td is reduced, the optimal architecture is a less highly branched panicle. (C) When σ is increased, two peaks arise corresponding to compound racemes and cymes. (D) With a further increase in σ, the peaks diverge. Optimal architectures are simple racemes and cymes. (E) Increased longevity θ shifts the peaks toward panicles. (F and G) Regions of high fitness in 3D fitness spaces. Horizontal sections correspond to the high-fitness regions in 2D fitness landscapes. (F) Path capturing the relation between architecture and σ. Colored sections correspond to figures (C) (top) and (D) (bottom). (G) Wormhole capturing the relation between architectures and longevity θ. Colored sections correspond to figures (D) (bottom) and (E) (top).

To the extent that the impact of variable season length increases from tropical to more temperate conditions, our model predicts higher frequencies of racemes and cymes in temperate compared with tropical climates, and the opposite trend for panicles. To test these predictions, we extracted the incidence of each architectural type in different climatic zones from the Watson and Dallwitz database of angiosperm families (33) (fig. S1A). Although this database is not ideal for our purposes, as it aggregates characters for all species in the same family, it reveals significant trends. Consistent with our predictions, cymes are relatively more frequent in more temperate conditions (P < 0.01), whereas panicles show the opposite trend (P < 0.001). Racemes are also more frequent in temperate than tropical conditions, but not significantly (P> 0.2).

In addition to the environmental influences, positions of peaks in the theoretical fitness landscapes depend on factors under genetic control, such as plant longevity. If a plant is perennial (i.e., lives more than 1 year), the negative impact of short seasons in an uncertain environment is reduced by spreading the risk over multiple years (Fig. 5E). We found no significant associations of raceme or panicle architectures with longevity, but cymes are significantly less common in families with only woody perennials and more common in families with annuals, as predicted (fig. S1B) (P < 0.05). Furthermore, this trend is observed in temperate but not tropical families. Although we have focused on the effects of environmental uncertainty, similar theoretical fitness landscapes involving interactions between internal and external factors could also be generated by considering the effects of limitations on pollination rate.

Although these results provide a rationale for sequential patterns of flower production, they do not explain why the transient mechanism evolved rather than other developmental mechanisms. One possibility is that the transient mechanism arose more readily because it built on the preexisting developmental process of meristem establishment. Establishing a new lateral meristem requires a period of time during which genes needed for meristem maintenance become activated (34). The transient mechanism could have arisen by coupling veg levels to this basic transition of meristems from a newly initiated (immature) to an established (mature) state. Thus, the evolution of the transient mechanism may reflect an earlier developmental genetic constraint that biased the variants available for selection toward this mechanism (6).

Evolution between racemes and cymes. In uncertain or pollinator-limited environments, racemes and cymes can represent equivalent adaptive solutions separated by a valley in the fitness landscape (Fig. 5, C to E). Such low-fitness valleys may have been circumvented in various ways during evolution. One is through changes in the environment. Figure 5F shows fitness landscapes that have been calculated for different degrees of environmental uncertainty and combined to form a three-dimensional (3D) fitness space, with the vertical axis representing the standard deviation in growth duration. An inverted U-shaped high-fitness region connects racemes, panicles, and cymes. Connecting paths may also occur through variation in genetically controlled factors. For example, a path emerges when plant longevity is varied along the vertical axis (Fig. 5G). Connecting paths of this type are common features of higher dimensional genotypic spaces (35, 36). We propose the general term “evolutionary wormhole” for such high-dimensional connections.

Movement along evolutionary wormholes that connect racemes and cymes appears limited, as individual genera seldom include both architectures. This constraint may arise because moving along wormholes requires coordinated changes of several parameters, involving multiple genetic steps. Large jumps between regions of high fitness are thus unlikely; moreover, gene segregation would generate low-fitness phenotypes. In addition, mutations required to move along some stretches of a wormhole, such as crossing between racemes and cymes, involve changes in regulatory interactions rather than simple loss or reduction of function. For example, creating a cyme in Arabidopsis would require changing the LFY and TFL1 promoters or other genes that interact with LFY, TFL1 or veg, such that veg becomes high in state B and low in state A (the reverse of wild type). Such mutations are likely to be rare. Thus, evolution of inflorescences is constrained by the nature of the developmental genetic mechanism, as well as by the interaction between organism and environment.

Conclusion. The diversity of inflorescence architectures reflects an interplay between development and selection at several levels. We propose that a relatively simple developmental mechanism—the transient model—underlies the restriction of inflorescence types to a small region of morphospace. This mechanism offers a selective advantage in dealing with environmental limitations and uncertainty over a simpler mechanism that can generate only panicles. Although similar advantages might also be achieved through other developmental mechanisms, the transient mechanism may have evolved because it co-opted a previously available developmental transition from the immature to mature state of apices. Within the confines of the morphospace spanned by the transient model, inflorescence architectures cannot evolve freely but are restricted to following paths of high fitness or evolutionary wormholes. The combination of theoretical and experimental approaches described here shows how development and selection can interact during evolution to carve out biological forms from the vast space of theoretical possibilities.

Supporting Online Material

www.sciencemag.org/cgi/content/full/1140429/DC1

Materials and Methods

SOM Text

Fig. S1

References

SOM Programs

References and Notes

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