Evolution of Reproductive Morphology in the Papaveraceae S.L. (Papaveraceae and Fumariaceae, Ranunculales)
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® International Journal of Plant Developmental Biology ©2010 Global Science Books Evolution of Reproductive Morphology in the Papaveraceae s.l. (Papaveraceae and Fumariaceae, Ranunculales) Oriane Hidalgo • Stefan Gleissberg* Department of Environmental and Plant Biology, Ohio University, 500 Porter Hall, Athens, Ohio 45701, USA Corresponding author : * [email protected] ABSTRACT Flower bearing branching systems are of major importance for plant reproduction, and exhibit significant variation between and within lineages. A key goal in evolutionary biology is to discover and characterize changes in the genetic programming of development that drive the modification and diversification of morphology. Here we present a synopsis of reproductive architecture in Papaveraceae s.l., a lineage in which the evolution of inflorescence determinacy, flower structure and symmetry, and effloration sequence produced unique reproduc- tive syndromes. We discuss the potential of this group to study key issues on the evolution of reproductive structures, and refer to candidate gene families, choice of landmark species, and available tools for developmental genetic investigations. _____________________________________________________________________________________________________________ Keywords: effloration sequence, flower organ identity, flower symmetry, Fumariaceae, inflorescence determinacy Abbreviations: AP1, APETALA1; AP3, APETALA3; CEN, CENTRORADIALIS; CRC, CRABS CLAW; CYC, CYCLOIDEA; FLO, FLORICAULA; FUL, FRUITFULL; LFY, LEAFY; PI, PISTILLATA; TFL1, TERMINAL FLOWER1; VIGS, Virus-Induced Gene Silencing CONTENTS INTRODUCTION........................................................................................................................................................................................ 76 FLORAL AND INFLORESCENCE DIVERSITY IN PAPAVERACEAE S.L............................................................................................ 79 Floral diversity......................................................................................................................................................................................... 79 Inflorescence diversity............................................................................................................................................................................. 79 CANDIDATE GENE APPROACHES TO FLOWER AND INFLORESCENCE DIVERSITY IN PAPAVERACEAE S.L.: STATE-OF- THE-ART AND PROSPECTS..................................................................................................................................................................... 80 Floral organ identity genes ...................................................................................................................................................................... 80 Floral symmetry genes............................................................................................................................................................................. 82 Floral meristem identity genes................................................................................................................................................................. 82 Tools available for investigation.............................................................................................................................................................. 83 CONCLUDING REMARKS ....................................................................................................................................................................... 83 ACKNOWLEDGEMENTS ......................................................................................................................................................................... 83 REFERENCES............................................................................................................................................................................................. 83 _____________________________________________________________________________________________________________ INTRODUCTION A great diversity of flowers and inflorescences is seen early in angiosperm history, a morphological radiation The flower, the basic reproductive organ of angiosperms, is referred to as the “abominable mystery” by Darwin (Crepet incomparably more diverse than equivalent structures found 1998, 2000; Friedman 2009). In fact, principal trends such in any other group of organisms (Barrett 2002). This extra- as floral symmetry shifts and synorganization, are already ordinary reproductive variety is further increased by a wide found in the fossil record and in extant basal angiosperms, range of specialized branching systems clustering flowers, but further appear recurrently throughout angiosperm the inflorescences (Weberling 1992), which expose flowers phylogeny (Soltis et al. 2009). This makes it difficult to and then fruits with their seeds to ensure successful repro- infer ancestral character states in the reconstruction of the duction (Prusinkiewicz 2007). The evolution of flowers and “primitive” flower (for one of the most recent attempts, see inflorescences is logically tightly connected (Coen and Endress and Doyle 2009). The fundamental problem that Nugent 1994). The huge morphological diversity of flowers evolutionary developmental biology addresses is the and inflorescences raises the question of its evolutionary correspondence of morphological traits and their underlying origin through re-orchestration of genetic control elements. developmental processes in the comparison of different An integrated understanding of floral and inflorescence lineages. A common approach is to study the genetic regu- diversification constitutes a major task of plant evolutionary lation of specific morphological traits in isolation. However, biology, and can also be expected to have a tremendous and traits are often functionally linked and may exhibit coordi- economically relevant impact on plant breeding strategies. nate evolution. Understanding the genetic basis of the evo- However, available evolutionary developmental (evo-devo) lution of such morphological syndromes requires a tho- data on the topic remain so far mostly restricted to a few rough examination of multiple traits that show interdepen- model systems widely dispersed within flowering plant dency. A prime example is the coordinated evolution of lineages. flower and inflorescence morphology. So far, studies have Received: 15 May, 2009. Accepted: 21 April, 2010. Invited Review International Journal of Plant Developmental Biology 4 (Special Issue 1), 76-85 ©2010 Global Science Books Fig. 1 Summarized phylogeny of the Papaveraceae s.l. based on molecular inferences and traditional classifications (Hoot et al. 1997; Lidén et al. 1997; Wang et al. 2009, and references therein). Flower symmetry and determinate/indeterminate inflorescence states are indicated for all genera. Flower picture, flower diagram and inflorescence type scheme are given for some selected representatives of the family throughout its phylogeny. : Taxonomic groups of traditional classifications for which monophyly is not confirmed by current molecular data. revealed an astonishing degree of conservation of develop- lopmental studies in angiosperms (Kramer 2009). The pop- mental mechanisms across flowering plants. Therefore, for py relatives in the broad circumscription (Papaveraceae s.l.), non-model lineages, a candidate gene approach that uses the comprise around 760 species and 44 genera (Stevens 2001 evidence from established model systems remains a straight- onwards), and is constituted of two main groups, the Papa- forward and powerful strategy to address morphological veraceae (poppies in the narrower sense) on the one hand, evolution. Because the current major model systems are and the Fumariaceae on the other (the fumitory family; or representatives of either core eudicots (e.g. Antirrhinum L., Fumarioideae subfamily of Papaveraceae s.l.). An isolated Arabidopsis (DC.) Heynh.) or monocots (e.g. Oryza L.), taxon, Pteridophyllum racemosum Siebold & Zucc., often and efforts understandably concentrate on plants of econo- viewed as a separate family Pteridophyllaceae (or Pterido- mic importance, it has been realized that research in basal phylloideae subfamily of Papaveraceae s.l.), may be sister angiosperms and basal eudicots is especially needed, as it to Fumariaceae (Wang et al. 2009; Fig. 1). Papaveraceae s.l. will be instrumental in deciphering major evolutionary tran- has attracted researchers because various diversity patterns sitions in the regulation of development (Soltis et al. 2002). invite comparative studies. The family received much atten- Research in the Papaveraceae s.l. may be a very useful tion for its biochemical richness in alkaloids (Hesse 2002; response to this current need. This family belongs to the Ziegler et al. 2006). Diversity in leaf shape (Gleissberg and Ranunculales, the order which diverged first in the eudicot Kadereit 1999) and inflorescence morphology (Günther lineage (Soltis et al. 2007c; APG III 2009), and is early 1975a, 1975b) has also been studied. branched within the order (Kim et al. 2004a; Soltis et al. Therefore, Papaveraceae s.l. is a useful lineage to draw 2007c; Wang et al. 2009). The phylogenetic position of comparisons between major angiosperm clades such as eu- Ranunculales, between the core eudicot and grass model dicots and monocots, as well as to elucidate the emergence systems,