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The Interplay Between Inflorescence Development and Function As the Crucible of Architectural Diversity

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The Interplay Between Inflorescence Development and Function As the Crucible of Architectural Diversity Annals of Botany Page 1 of 17 doi:10.1093/aob/mcs252, available online at www.aob.oxfordjournals.org REVIEW: PART OF A SPECIAL ISSUE ON INFLORESCENCES The interplay between inflorescence development and function as the crucible of architectural diversity Lawrence D. Harder1,* and Przemyslaw Prusinkiewicz2 1Department of Biological Sciences, University of Calgary, Calgary, Alberta, Canada T2N 1N4 and 2Department of Computer Science, University of Calgary, Calgary, Alberta, Canada T2N 1N4 * For correspondence. Email [email protected] Received: 27 July 2012 Returned for revision: 13 September 2012 Accepted: 17 October 2012 † Background Most angiosperms present flowers in inflorescences, which play roles in reproduction, primarily Downloaded from related to pollination, beyond those served by individual flowers alone. An inflorescence’s overall reproductive contribution depends primarily on the three-dimensional arrangement of the floral canopy and its dynamics during its flowering period. These features depend in turn on characteristics of the underlying branching structure (scaffold) that supports and supplies water and nutrients to the floral canopy. This scaffold is produced by devel- opmental algorithms that are genetically specified and hormonally mediated. Thus, the extensive inflorescence diversity evident among angiosperms evolves through changes in the developmental programmes that specify http://aob.oxfordjournals.org/ scaffold characteristics, which in turn modify canopy features that promote reproductive performance in a par- ticular pollination and mating environment. Nevertheless, developmental and ecological aspects of inflorescences have typically been studied independently, limiting comprehensive understanding of the relations between inflor- escence form, reproductive function, and evolution. † Scope This review fosters an integrated perspective on inflorescences by summarizing aspects of their devel- opment and pollination function that enable and guide inflorescence evolution and diversification. † Conclusions The architecture of flowering inflorescences comprises three related components: topology (branching patterns, flower number), geometry (phyllotaxis, internode and pedicel lengths, three-dimensional flower arrangement) and phenology (flower opening rate and longevity, dichogamy). Genetic and developmental at The Univesity of Calgary on January 16, 2013 evidence reveals that these components are largely subject to quantitative control. Consequently, inflorescence evolution proceeds along a multidimensional continuum. Nevertheless, some combinations of topology, geom- etry and phenology are represented more commonly than others, because they serve reproductive function par- ticularly effectively. For wind-pollinated species, these combinations often represent compromise solutions to the conflicting physical influences on pollen removal, transport and deposition. For animal-pollinated species, dominant selective influences include the conflicting benefits of large displays for attracting pollinators and of small displays for limiting among-flower self-pollination. The variety of architectural components that comprise inflorescences enable diverse resolutions of these conflicts. Key words: Inflorescence, angiosperm, form and function, evolution, development, architecture, floral display, pollination, geitonogamy, heterochrony. INTRODUCTION in pollen export (pollen discounting) and siring success (Harder and Barrett, 1995; Karron and Mitchell, 2012). Such The diversity of floral morphology and inflorescence architec- collective effects probably shape the evolution of the extensive ture within angiosperms illustrates the extreme evolutionary inflorescence diversity that is evident within and among angio- plasticity of reproductive structures. Strangely, although sperm clades (e.g. Fig. 1; Stebbins, 1974; Weberling, 1992; floral diversity has stimulated functional interpretations for Claßen-Bockhoff, 2000; Bradford and Barnes, 2001; Doust over two centuries (Baker, 1983) and has featured as evidence and Kellogg, 2002; Evans et al., 2003; Weller et al., 2006; of adaptation since Darwin (1862, 1877), inflorescence diver- Tripp, 2007; Pozner et al., 2012). sity has received much less attention from this perspective (al- As for all aspects of morphology, inflorescence adaptation though see Wyatt, 1982; Harder et al., 2004; Prusinkiewicz and diversification depend on both the functional conse- et al., 2007). This disparity is surprising, as plants typically quences of alternative characteristics, and the evolutionary produce and display flowers aggregated in inflorescences in options and limits established by the generating developmental which flowers seldom act independently during development, processes (cf. Brakefield, 2006; Breuker et al., 2006). pollination, fruit development and seed dispersal. For Nevertheless, the bodies of literature that address inflorescence example, plants that display many flowers simultaneously development and function rarely intersect: ontogenetic studies attract more pollinators than those with small displays seldom consider consequences for plant performance, and (Ohashi and Yahara, 2001), but are also more likely to experi- adaptive hypotheses commonly ignore developmental possi- ence among-flower self-pollination (geitonogamy: Barrett bilities and constraints. Here, we review this disparate litera- et al., 1994; Karron et al., 2004) and an associated reduction ture in search of a unified perspective that recognizes the # The Author 2012. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected] Page 2 of 17 Harder and Prusinkiewicz — Inflorescence development and function A BC Downloaded from DE H F http://aob.oxfordjournals.org/ B D G E C A FG H at The Univesity of Calgary on January 16, 2013 F IG. 1. Examples of architectural diversity caused by interspecific variation in branching geometry on an underlying cymose topology within South African Iridaceae, including: (A) Moraea tripetala, (B) Chasmanthe floribunda, (C) Crocosmia paniculata, (D) Dierama latifolium, (E) Freesia occidentalis, (F) Babiana villosa, (G) Hesperantha coccinea (with Prosoeca ganglbaueri) and (H) Babiana ringens. The inset phylogeny in (D) illustrates the relationships between the species as inferred by Goldblatt et al. (2008). reciprocal relations through which inflorescence structure both Nevertheless, new perspectives emerge, which may serve to influences and is evolutionarily influenced by reproductive motivate more integrated future studies. function. After providing an ontogenetic definition of an in- florescence and identifying the essential components of its architecture, we review current understanding of the develop- INFLORESCENCES AND THEIR mental controls on those components, with emphasis on archi- ARCHITECTURAL COMPONENTS tectural effects with identifiable ecological implications. We Flowering plants are modular organisms that develop as shoot then examine the consequences of inflorescence architecture apical meristems repeatedly produce metamers, each of which for reproduction, focusing on pollination, which is the essen- comprises a stem segment (internode), distal node, attached tial function of inflorescences. Given the largely independent leaf and axillary bud(s) (Bell, 2008). Consequently, a plant’s progress of studies of inflorescence development and function, architecture grows as metamers are added, internodes elongate our synthesis is unavoidably incomplete. In particular, we do (or not) and axillary buds create branches (or not). This iter- not consider biomechanics, the flow of water, hormones and ated pattern continues after a shoot apical meristem switches nutrients, or the developmental progression of inflorescences from vegetative mode to become an inflorescence meristem. into infructescences and their role in seed dispersal. In this reproductive mode, apical and lateral meristems may Harder and Prusinkiewicz — Inflorescence development and function Page 3 of 17 switch from producing inflorescence axes (shoot identity) to aspects, such as the lengths of internodes and branching producing flowers (floral identity) (Bennett and Leyser, angles (branching geometry) (see, for example, Reinheimer 2006). As a flower is a specialized, highly condensed repro- et al., 2009; Prusinkiewicz and Runions, 2012). Likewise, ductive branch, each axillary flower is subtended by a leaf, the floral canopy can be viewed topologically or geometrically, which may not develop, be rudimentary (bract) or be indistin- by focusing respectively on the numbers of flowers, perhaps of guishable from the leaves that subtend vegetative buds. An in- different types and/or developmental stages, or on their spatial florescence is thus recognized by the transition along an axis arrangement. From a functional perspective, scaffold structure from the production of vegetative branches to flower produc- provides physical support and a conduit for the flow of water, tion, not by the presence or absence of leaves (see Hempel nutrients and hormones to flowers and fruits (Wyatt, 1982), and Feldman, 1994). whereas canopy structure determines interactions with pollen The form (architecture) of inflorescences can be considered vectors, fruit/seed dispersers, floral herbivores and seed preda- from several intersecting perspectives. Within an inflorescence tors (see below). Thus, both structurally and functionally, the one can distinguish the branching scaffold (Fig. 2J) and the scaffold and
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