Volume 4 Special Issue 1 2010
Plant Development and Evolution

How to reference: Erbar C (2010) Floral Organ Determination and Ontogenetical Patterns during Angiosperm Evolution. In: Fernando DD (Ed) Plant Development and Evolution. International Journal of Plant Developmental Biology 4 (Special Issue 1), 1-16

Guest Editor

Danilo D. Fernando

State University of New York, USA


www.esf.edu/EFB/

CONTENTS AND ABSTRACTS

Claudia Erbar (Germany) Floral Organ Determination and Ontogenetical Patterns during Angiosperm Evolution (pp 1-16)

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ABSTRACT

Invited Review: Since the late 1980’s/early 1990’s enormous progress had been made in understanding the genetic and molecular regulation of flower development. The genetic ABCDE model describes five classes of genes that are responsible for the specification of floral organ identity in a combinatorial manner. The molecular quartet model advances the genetic ABCDE model by describing the presumed interactions between floral MADS-domain proteins. Although the basic developmental program appears to be quite conserved, in non-core eudicots modifications such as “sliding-boundary” and “fading borders” models had to be established. The genetic models proposed as yet predict the organ quality, but do not explain how the number of organs or the spatial pattern in which organ primordia appear (e.g. spiral or whorled) is regulated. With Apiaceae and Brassicaceae two families are presented which contrary to their uniform flower construction show fairly diverse patterns in organ initiation. Cleomaceae, sister to Brassicaceae, are even more diverse as regards stamen number as well as initiation patterns. The other members of the core Brassicales add further diversity to the androecial initiation pattern. Multistaminate androecia stand for a further interesting aspect as the stamen primordia are initiated either spirally directly on the floral apex or on so-called primary androecial primordia (fascicle primordia) in centrifugal or centripetal succession. Since the identity of floral organs is strictly dependent on the activity of the MADS-box genes, duplication and diversification within these genes must have been key processes in flower evolution. Hence, insights into the phylogeny of the floral homeotic genes may help to better understand the evolution of flowers (“evo-devo”). The unique nectary organs of the Ranunculaceae are presented as example for duplication and new functions in the B class genes.

Jill C. Preston (USA) Evolutionary Genetics of Core Eudicot Inflorescence and Flower Development (pp 17-29)

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Invited Review: The genetic basis of flowering is best understood in the model core eudicot species Arabidopsis thaliana (Brassicaceae), and involves the genetic reprogramming of shoot apical meristems, ending in the production of flowers. Although inflorescences and flowers of core eudicots share a common ground plan, variation in architecture, shape and ornamentation suggests repeated modifications to this ancestral plan. Comparative studies, primarily in Brassicaceae and Leguminoseae (rosids), and Asteraceae, Plantaginaceae and Solanaceae (asterids), have revealed a common developmental framework for flowering across core eudicots. This serves as a basis for understanding genetic changes that underlie the diversification of inflorescence and floral form. Recent work is starting to reveal the relative importance of regulatory versus protein coding changes in genes involved in diversification of inflorescence and flower development across core eudicots. Furthermore, these studies highlight the importance of phylogenetic history for understanding functional conservation of duplicated genes.

Barbara A. Ambrose (USA) MADS-box Genes in Plant Evolution and Development (pp 30-37)

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Invited Review: Evolutionary developmental studies have shown that large transcription factor families underlie key morphological features. The duplication and diversification of these transcription factor families has been important to provide material for the generation of new interacting partners where duplicates could take on a new role or a sub-function of the original protein. Arguably one of the most important of these transcription factor families in plants is the MADS-box family of transcription factors. MADS-box genes are an ancient group found in animals, plants and fungi but have duplicated and diversified much more in plants than in animals and fungi. The plant MADS-box genes can be further sub-divided into Type I, Type II MIKCc and Type II MIKC* MADS-box-genes. The Type II MIKCc MADS-box genes are best known for their role in the ABC model of floral organ identity. MIKCc MADS-box genes are also important for flowering time, fruit, endosperm and seed development. There have been many Type II MIKCc studies performed across the land plants however, comparatively little is known about the Type II MIKC* and Type I MADS-box genes. Therefore, recent functional analyses of the previously uncharacterized MIKC* and Type I MADS-box genes are particularly exciting. Recent genome analyses have shown that MIKC* and Type I MADS-box genes can also be found in Physcomitrella patens and Selaginella moellendorffii. Phylogenetic, functional and expression analyses of MADS-box genes across the land plants will provide insight into the role of all types of MADS-box genes in the evolution and development of land plant body plans.

Florian Jabbour (Germany), Hélène L. Citerne (France) Modeling Flowers and Inflorescences (pp 38-46)

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Invited Mini-Review: Modeling approaches, using mathematical and computational tools for visualization and simulation, are gaining new interest in the field of developmental biology. These methods are providing new insights into molecular interactions, growth processes and morphological evolution. The distinctive reproductive structures of angiosperms, flowers and inflorescences, are of particular interest from both a developmental and evolutionary perspective. Here we review the diversity of studies which have used modeling approaches to investigate the structure and development of flowers and inflorescences. Models of architecture (branching and determinacy) and phyllotaxis (primordia arrangement) are described, focusing on different factors ranging from environmental pressures to physical constraints, chemical signaling, and genetic determination. Modeling has also been used to provide a description and framework for understanding growth at the level of single floral organs. In addition, we also consider models that explore the behaviour of gene regulatory networks involved in the development of plant reproductive structures. Models of flowers and inflorescences are still mostly disconnected, and integrating these will help explain the developmental processes underlying morphological diversity. Modeling is a useful tool for testing hypotheses and guiding empirical research and will undoubtedly become an increasingly important component of integrative studies of plant development and evolution.

Danilo D. Fernando, Christina R. Quinn, Eric D. Brenner (USA), John N. Owens (Thailand) Male Gametophyte Development and Evolution in Extant Gymnosperms (pp 47-63)

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Invited Review: The male gametophytes of gymnosperms are characterized by the diversities in pollen morphology, cellular composition and pattern of cell division, pollen tube morphology, sperm delivery, growth pattern through the ovule and nucellus, and pollen tube wall composition both within and among the four living orders, i.e., Cycadales, Ginkgoales, Coniferales, and Gnetales. At dehiscence, gymnosperm pollen grains contain a variable number of cells yet none have sperm at this stage. Pollen germination in the ovule usually occurs within a few hours or days in gnetophytes, about a week or so in conifers and Ginkgo, or after several months in cycads. Complete development of the male gametophytes typically involves two to five mitotic divisions. Evolution of the male gametophyte appears to have involved a reduction of its component cells with prothallial cells being among those reduced or eliminated. There is a shift in the site of sperm discharge from a proximal position in pollen grains of cycads and Ginkgo to distal in conifers and gnetophytes. Two methods of sperm delivery occur in gymnosperms: zooidogamy, defined by pollen tubes with motile sperm as exhibited in cycads and Ginkgo, and siphonogamy, defined by pollen tubes with non-motile sperm which are directly delivered into the egg as exhibited in conifers and gnetophytes. Different pollen tube morphologies occur in the nucellus, i.e., branched and haustorial in cycads and Ginkgo, and unbranched and non-haustorial in conifers and gnetophytes. Pollen tubes form heterotrophic relationships with the nucellus, but it is only in cycads that intracellular penetration results in significant destruction of the nucellus. Pollen tube walls of gymnosperms contain cellulose and arabinogalactan proteins; however, pectins are prevalent in cycads and mixed β-glucan in Ginkgo. A standard terminology to describe the cellular composition of the male gametophytes in gymnosperms is proposed.

Catherine Anne Kidner, Saima Umbreen (United Kingdom) Why is Leaf Shape so Variable? (pp 64-75)

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Invited Review: The genetic pathways which control leaf shape have been revealed through work in a range of model systems. We are now beginning to understand how plants produce leaves of different shapes. However, why leaves have different shapes is not so well-studied. Leaf shape is extremely variable between species. Shape also varies within species, within populations and as a plastic or developmentally programmed response, within individual plants, suggesting there is an adaptive role for leaf shape. Theoretical studies and modelling have suggested several roles that leaf shape could play due to its effects on affect light capture, water balance and temperature regulation. Clear trends in leaf shape variation are seen along environmental clines but the few studies that have been done on the adaptive role of leaf shape have produced equivocal results. Selection on leaf shape is weak and variable though there is some support for adaptive effects of leaf dissection. Other important factors could be microclimate, correlations with phyllotaxy or vascular patterning, and biotic interactions. Cooperation between ecologists, physiologists, anatomists, geneticists is required to determine the interactions between these factors. This will be aided by the application of large-scale sequencing, and techniques such as PCA and QTL to dissect the genetics involved.

Oriane Hidalgo, Stefan Gleissberg (USA) Evolution of Reproductive Morphology in the Papaveraceae s.l. (Papaveraceae and Fumariaceae, Ranunculales) (pp 76-85)

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Invited Mini-Review: 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 reproductive 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.

Alma Piñeyro-Nelson (Mexico), Eduardo Flores-Sandoval (Australia), Adriana Garay-Arroyo, Berenice García-Ponce, Elena R. Álvarez-Buylla (Mexico) Development and Evolution of the Unique Floral Organ Arrangement of Lacandonia schismatica (pp 86-97)

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Invited Review: 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.

Cheng-Jiang Ruan (China) Review and Advances in Style Curvature for the Malvaceae (pp 98-111)

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Invited Review: The flowers of the Malvaceae with varying levels of herkogamy via style curvature have long intrigued evolutionary botanists. This review covers the flower opening process, approach herkogamy, style curvature and character evolution based on molecular phenogenetic trees, adaptive significances of style curvature and the mating system in some portions of the genera in this family. Hermaphroditic flowers have showy petals and pollen and nectar rewards to pollinators. Approach herkogamy, in which stigmas are located on the top of a monadelphous stamen, has evolved as a mechanism to reduce the frequency of intra-floral self-pollination or the interference between male-female organs. Protandrous or monochogamous flowers in the fields open at about 5-7 days and 1-2 days respectively, and pollination is conducted by insects and birds. Interestingly, un-pollinated styles in some species curve when pollination fails. According to our observations and published or internet data, this curvature occurs in 23 species distributed in eight genera of four tribes (Malvavisceae, Ureneae, Hibisceae, Malveae) and appears to have evolved at least eight times. A shift to use style curvature is associated with a shift to annual or perennial herbs, and an unpredictable pollinator environment is likely an important trigger for this evolution. The adaptive significances of style curvature in the Malvaceae include delayed selfing, promotion of outcrossing or reduction in intrafloral male-female interference, sometimes two or three of which simultaneously occur in style curvature of one species (e.g., Kosteletzkya virginica). Delayed selfing via style curvature represents reproductive assurance and a mixed mating system, but the relationship between them is still an evolutionary enigma.

Joshua A. Banta, Massimo Pigliucci (USA) Genetic and Environmental Variation Affect the Ontogeny of Reproductive Traits in Arabidopsis thaliana (pp 112-121)

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Original Research Paper: Despite the wealth of molecular information about inflorescence development in the model plant Arabidopsis thaliana, we know much less about how traits involved in reproduction vary and covary at a phenotypic level, even though phenotypic variation and covariation are the substrates of natural selection and subsequent evolution. If we are to understand A. thaliana’s microevolutionary dynamics to the same extent that we understand its molecular genetics, then we must first flesh out and describe this (co)-variation. We characterized the covariation of reproductive traits in A. thaliana, utilizing multiple natural genotypes to assess whether such covariation is genetically variable. We subjected plants to naturally relevant variation in apical meristem damage and nutrient levels to explore the degree to which the relationships among traits are plastic. We found that inflorescence ontogeny (as inferred from the relationships among reproductive traits) is altered in apically damaged plants, and that variation in nutrient levels affects ontogeny as well. We also found that genetically clustered groups of plants qualitatively differ in the relationships among traits. These findings are discussed in terms of constraints on selection and of possible selection pressures for different inflorescence ontogenies in this species.