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Development and Evolution of the Unique Floral Organ Arrangement of Lacandonia Schismatica

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Development and Evolution of the Unique Floral Organ Arrangement of Lacandonia Schismatica ® International Journal of Plant Developmental Biology ©2010 Global Science Books Development and Evolution of the Unique Floral Organ Arrangement of Lacandonia schismatica Alma Piñeyro-Nelson1 • Eduardo Flores-Sandoval2 • Adriana Garay-Arroyo1 • Berenice García-Ponce1 • Elena R. Álvarez-Buylla1* 1 Laboratorio de Genética Molecular, Desarrollo y Evolución de Plantas, Departamento de Ecología Funcional, Instituto de Ecología, Universidad Nacional Autónoma de México, Ciudad Universitaria, 3er circuito exterior junto al Jardín Botánico, Del. Coyoacán, México D.F. 04510, Mexico 2 School of Biological Sciences, Monash University, Clayton Campus, Wellington Road, Clayton, Victoria 3800, Australia Corresponding author : * [email protected] ABSTRACT Lacandonia schismatica (Triuridaceae) is the only known angiosperm species with flowers composed of central stamens surrounded by carpels. If the reproductive axes of this species are interpreted as heterotopic flowers, crucial questions on the evolution of morphological novelties arise, such as: a) is this phenotype fixed or whether intermediate floral variants within L. schismatica populations exist, and b) what is the nature and number of molecular alterations involved in such a morphological saltation. Furthermore, the temporal progression of floral organ formation in this taxon is unaltered with respect to the great majority of angiosperms (perianth, then stamens and finally carpels). This suggests that the regulatory mechanisms underlying the spatial and temporal morphogenetic patterns of flower development can be altered independently of each other. Through developmental genetic studies, the underlying molecular components involved in the unique position of sexual organs in L. schismatica have started to be unravelled. However, studies on floral meristem identity genes, including B-function genes and their regulators (LFY, UFO and SEP) will be important to address the molecular basis of any regulatory alterations. In this contribution we summarize the developmental, systematic and structural data that nurture the on going debate concerning the nature of the Triurid reproductive structures, considered either true flowers (euanthia) or compressed inflorescences (pseudanthia). Finally, we discuss the theoretical approaches that are helping us to understand developmental constraints of the ABC gene regulatory network, and how such theoretical analyses could help explain the arrangement of L. schismatica flowers. _____________________________________________________________________________________________________________ Keywords: ABC model, developmental genetics, homeosis, reproductive structures, Triuridaceae CONTENTS INTRODUCTION........................................................................................................................................................................................ 86 TAXONOMY OF LACANDONIA SCHISMATICA AND RELATED TRIURIDACEAE SPECIES ........................................................... 87 PECULIARITIES OF LACANDONIA SCHISMATICA ............................................................................................................................... 88 Reproductive and cell biology of Lacandonia schismatica ..................................................................................................................... 88 Peculiar nuclear architecture.................................................................................................................................................................... 88 PHYLOGENETIC POSITION OF LACANDONIA SCHISMATICA WITHIN PANDANALES................................................................. 88 CONTROVERSIES ON THE IDENTITY OF THE REPRODUCTIVE STRUCTURES OF TRIURIDACEAE....................................... 89 Euanthial vs Pseudanthial interpretation of the reproductive axes in Triuridaceae.................................................................................. 89 Is there an unclear floral/inflorescence meristem distinction in Triuridaceae? Morphology-based hypotheses....................................... 90 Developmental genetics hypotheses ........................................................................................................................................................ 91 THE HOMEOTIC FLOWERS OF LACANDONIA SCHISMATICA CONSTITUTE A MORPHOLOGICAL SALTATION: STUDIES AT THE POPULATION LEVEL....................................................................................................................................................................... 91 MOLECULAR GENETIC MECHANISMS UNDERLYING THE SINGULAR SPATIAL ORGAN ARRANGEMENT OF LACANDONIA SCHISMATICA FLOWERS................................................................................................................................................ 92 ABC model-based hypotheses to explain the inside-out flower of Lacandonia schismatica................................................................... 92 Molecular genetics data on Lacandonia schismatica floral development................................................................................................ 93 Alterations of cis versus trans factors in the regulation of B genes underlying the inside-out flower of Lacandonia schismatica ......... 93 DEVELOPMENTAL CONSTRAINTS NOT BROKEN DURING FLOWER EVOLUTION IN L. SCHISMATICA: THE TEMPORAL PATTERN OF FLORAL ORGAN FORMATION AND THE PRESENCE OF COMPOUND PRIMORDIA............................................ 94 CHANGES IN FLOWER MERISTEM IDENTITY GENES UNDERLYING COMMON PRIMORDIA AS AN ADDITIONAL EXPLANATION OF LACANDONIA SCHISMATICA ONTOGENY.......................................................................................................... 94 CONCLUSIONS.......................................................................................................................................................................................... 95 ACKNOWLEDGEMENTS ......................................................................................................................................................................... 95 REFERENCES............................................................................................................................................................................................. 96 _____________________________________________________________________________________________________________ INTRODUCTION phology-centered school of the 18th and 19th centuries was fundamental in describing plant sexual organs, which would The field of Evolutionary Developmental Biology or Evo- prove fundamental for taxonomic and comparative mor- Devo has profited from the data and conceptual inputs from phology studies (Smyth 2005). In the 20th century, biolo- a diverse set of scholars and fields of study. The mor- gists such as C.H. Waddington and D’Arcy Thompson Received: 9 July, 2009. Accepted: 25 May, 2010. Invited Review International Journal of Plant Developmental Biology 4 (Special Issue 1), 86-97 ©2010 Global Science Books among others, made important propositions regarding the role of interactions among genetic and non genetic elements during development, as well as the need to explicitly acknowledge the role of physical and mechanical con- straints affecting organismal form. More recently, Evo- Devo has benefited from the growing field of develop- mental genetics, which has utilized empirical data attained through the study of homeotic transformations in model systems, to propose developmental models such as the ABC model of plant floral organ formation (Bowman et al. 1989, 1991; Coen and Meyerowitz 1991; Smyth 2005). Such models have been instrumental to assess the role of home- otic genes in the development of the flower structure in both model and non-model plant species (Soltis et al. 2007). Experimental data attained from Arabidopsis thaliana has also enabled the development of computational models that address the role of Gene Regulatory Networks (GRN) Fig. 1 Lacandonia schismatica flower. Note semi-transparent tepals and in the emergence of evolutionarily stable genetic expression three central stamens (dark yellow) surrounded by numerous carpels patterns associated with organ development (Espinosa-Soto (photo by Esteban Martínez). et al. 2004; Álvarez-Buylla et al. 2008). These contempo- rary experimental and theoretical approaches have benefited particularly from ideas put forward by Waddington (1957) involving major changes in body plans in the case of who introduced the notion of epigenetic landscapes as a flowers, or limb number in arthropods (Bowman et al. metaphor to explain the dynamic nature of development. In 1991; Ford and Gottlieb 1992; Ronshaugen et al. 2002). such a metaphor, the landscape topology is a dynamic sys- Similar homeotic alterations seem to be involved in the case tem defined by complex interactions among genetic and of the remarkable inside-out flower of the Mexican mono- non-genetic factors, and basins correspond to stable deve- cot herb, Lacandonia schismatica. lopmental pathways. In the epigenetic landscape, once a As a contribution to this special issue of the IJPDB, we basin has been reached, the developmental process will be synthesize here the state of knowledge about the evolution buffered against external or internal interventions, thus and development of L. schismatica, a living example of a being canalized (Slack 2002). This and other concepts put natural heterotopic species (see
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