Sandra K. Floyd

Radial patterning of Arabidopsis Shoots by class III HD-ZIP and KANADI genes

BACKGROUND Shoots of all land plants have a radial pattern that can be considered to have an adaxial (central)-abaxial (peripheral) polarity. In Arabidopsis, gain-of-function alleles of PHAVOLUTA and PHABULOSA, members of the class III HD-ZIP gene family, result in adaxialization of lateral organs. Conversely, loss-of-function alleles of the KANADI genes cause an adaxialization of lateral organs. Thus, the class III HD-ZIP and KANADI genes comprise a genetic system that patterns abaxial-adaxial polarity in lateral organs produced from the apical meristem. RESULTS We show that gain-of-function alleles of REVOLUTA, another member of the class III HD-ZIP gene family, are characterized by adaxialized lateral organs and alterations in the radial patterning of vascular bundles in the stem. The gain-of-function phenotype can be obtained by changing only the REVOLUTA mRNA sequence and without changing the protein sequence; this finding indicates that this phenotype is likely mediated through an interference with microRNA binding. Loss of KANADI activity results in similar alterations in vascular patterning as compared to REVOLUTA gain-of-function alleles. Simultaneous loss-of-function of PHABULOSA, PHAVOLUTA, and REVOLUTA abaxializes cotyledons, abolishes the formation of the primary apical meristem, and in severe cases, eliminates bilateral symmetry; these phenotypes implicate these three genes in radial patterning of both embryonic and postembryonic growth. CONCLUSIONS Based on complementary vascular and leaf phenotypes of class III HD-ZIP and KANADI mutants, we propose that a common genetic program dependent upon miRNAs governs adaxial-abaxial patterning of leaves and radial patterning of stems in the angiosperm shoot. This finding implies that a common patterning mechanism is shared between apical and vascular meristems.

Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities

Asymmetric development of plant lateral organs is initiated by a partitioning of organ primordia into distinct domains along their adaxial/abaxial axis. Two primary determinants of abaxial cell fate are members of the KANADI and YABBY gene families. Progressive loss of KANADI activity in loss-of-function mutants results in progressive transformation of abaxial cell types into adaxial ones and a correlated loss of lamina formation. Novel, localized planes of blade expansion occur in some kanadi loss-of-function genotypes and these ectopic lamina outgrowths are YABBY dependent. We propose that the initial asymmetric leaf development is regulated primarily by mutual antagonism between KANADI and PHB-like genes, which is translated into polar YABBY expression. Subsequently, polar YABBY expression contributes both to abaxial cell fate and to abaxial/adaxial juxtaposition-mediated lamina expansion.

The Ancestral Developmental Tool Kit of Land Plants

The origin of land plants from aquatic ancestors and their subsequent evolutionary radiation was due to major modifications in an ancestral developmental program allowing for plants of increasing complexity and stature. By comparing the developmental programs in different kinds of plants, we can understand how developmental differences lead to morphological differences. The ability to dissect the developmental genetic pathways of model angiosperm taxa such as Arabidopsis and maize has revealed many important developmental gene families that comprise the tool kit for flowering plant growth, patterning, and differentiation. This knowledge has been used to a limited extent as the basis for candidate gene approaches to explore the distribution and expression/function of a few developmental gene families in other flowering plants, gymnosperms, and to some extent, more distantly related plants. With the addition of nearly complete sequenced genomes for the moss Physcomitrella and the lycophyte Selaginella, comparisons of many more gene families are becoming possible. We performed searches of the unassembled Physcomitrella and Selaginella genomic sequences for some key developmental families. We combine these new data with information available in the literature from candidate gene approaches and present a first estimate of a suite of developmental genes that may have comprised the ancestral patterning tool kit of land plants. We conclude that the genome of the earliest embryophytes encoded homologues of many of the important developmental genes that have been identified in model angiosperm taxa, but the roles of these were probably somewhat different than the roles attributed to them in Arabidopsis and maize. Developmental gene families have diversified during land plant evolution, and genome complexity may correlate well with phylogenetic position.

Green Genes—Comparative Genomics of the Green Branch of Life

As more plant genome sequences become available, researchers are increasingly using comparative genomics to address some of the major questions in plant biology. Such questions include the evolution of photosynthesis and multicellularity, the developmental genetic changes responsible for alterations in body plan, and the origin of important plant innovations such as roots, leaves, and vascular tissue.

Differentiating Arabidopsis Shoots from Leaves by Combined YABBY Activities

YABBY activity is required in seed plants for specification of leaves and the origin of the YABBY genes coincides with the origin of seed plant leaves. This work probes the role of YABBY genes in molding shoot programs into laminar organs by examining shoot and leaf development in plants mutant for four vegetative YABBY genes. In seed plants, leaves are born on radial shoots, but unlike shoots, they are determinate dorsiventral organs made of flat lamina. YABBY genes are found only in seed plants and in all cases studied are expressed primarily in lateral organs and in a polar manner. Despite their simple expression, Arabidopsis thaliana plants lacking all YABBY gene activities have a wide range of morphological defects in all lateral organs as well as the shoot apical meristem (SAM). Here, we show that leaves lacking all YABBY activities are initiated as dorsiventral appendages but fail to properly activate lamina programs. In particular, the activation of most CINCINNATA-class TCP genes does not commence, SAM-specific programs are reactivated, and a marginal leaf domain is not established. Altered distribution of auxin signaling and the auxin efflux carrier PIN1, highly reduced venation, initiation of multiple cotyledons, and gradual loss of the SAM accompany these defects. We suggest that YABBY functions were recruited to mold modified shoot systems into flat plant appendages by translating organ polarity into lamina-specific programs that include marginal auxin flow and activation of a maturation schedule directing determinate growth.

Evolution of class III homeodomain-leucine zipper genes in streptophytes.

Land plants underwent tremendous evolutionary change following the divergence of the ancestral lineage from algal relatives. Several important developmental innovations appeared as the embryophyte clade diversified, leading to the appearance of new organs and tissue types. To understand how these changes came about, we need to identify the fundamental genetic developmental programs that are responsible for growth, patterning, and differentiation and describe how these programs were modified and elaborated through time to produce novel morphologies. Class III homeodomain–leucine zipper (class III HD–Zip) genes, identified in the model plant Arabidopsis thaliana, provide good candidates for basic land plant patterning genes. We show that these genes may have evolved in a common ancestor of land plants and their algal sister group and that the gene family has diversified as land plant lineages have diversified. Phylogenetic analysis, expression data from nonflowering lineages, and evidence from Arabidopsis and other flowering plants indicate that class III HD–Zip genes acquired new functions in sporophyte apical growth, vascular patterning and differentiation, and leaf development. Modification of expression patterns that accompanied diversification of class III HD–Zip genes likely played an important role in the evolution of land plant form.

THE EVOLUTION OF EMBRYO SIZE IN ANGIOSPERMS AND OTHER SEED PLANTS: IMPLICATIONS FOR THE EVOLUTION OF SEED DORMANCY

Abstract.— Seed dormancy plays an important role in germination ecology and seed plant evolution. Morphological seed dormancy is caused by an underdeveloped embryo that must mature prior to germination. It has been suggested that the presence of an underdeveloped embryo is plesiomorphic among seed plants and that parallel directional change in embryo morphology has occurred separately in gymnosperms and in angiosperms. We test these hypotheses using original data on embryo morphology of key basal taxa, a published dataset, and the generalized least squares (GLS) method of ancestral character state reconstruction. Reconstructions for embryo to seed ratio (E:S) using family means for 179 families showed that E:S has increased between the ancestral angiosperm and almost all extant angiosperm taxa. Species in the rosid clade have particularly large embryos relative to the angiosperm ancestor. Results for the gymnosperms show a similar but smaller increase. There were no statistically significant differences in E:S between basal taxa and any derived group due to extremely large standard errors produced by GLS models. However, differences between reconstructed values for the angiosperm ancestor and more highly nested nodes are large and these results are robust to topological and branch‐length manipulations. Our analysis supports the idea that the underdeveloped embryo is primitive among seed plants and that there has been a directional change in E:S within both angiosperms and gymnosperms. Our analysis suggests that dormancy enforced by an underdeveloped embryo is plesiomorphic among angiosperms and that nondormancy and other dormancy types probably evolved within the angiosperms. The shift in E:S was likely a heterochronic change, and has important implications for the life history of seed plants.

Distinct Developmental Mechanisms Reflect the Independent Origins of Leaves in Vascular Plants

Vascular plants diverged more than 400 million years ago into two lineages, the lycophytes and the euphyllophytes . Leaf-like organs evolved independently in these two groups . Microphylls in lycophytes are hypothesized to have originated as lateral outgrowths of tissue that later became vascularized (the enation theory) or through the sterilization of sporangia (the sterilization hypothesis) . Megaphylls in euphyllophytes are thought to represent modified lateral branches . The fossil record also indicates that the seed plant megaphyll evolved uniquely in the ancestor of seed plants, independent of megaphylls in ferns, because seed plants evolved from leafless progymnosperm ancestors . Surprisingly, a recent study of KNOX and ARP gene expression in a lycophyte was reported to indicate recruitment of a similar mechanism for determinacy in both types of leaves . We examined the expression of Class III HD-Zip genes in the lycophyte Selaginella kraussiana and in two gymnosperms, Ginkgo and Pseudotsuga. Our data indicate that mechanisms promoting leaf initiation, vascularization, and polarity are quite different in lycophytes and seed plants, consistent with the hypotheses that megaphylls originated as lateral branches whereas microphylls originated as tissue outgrowths.

Evolution of Endosperm Developmental Patterns among Basal Flowering Plants

A phylogenetically based comparative investigation of endosperm development was undertaken in a sample of 13 basal angiosperm taxa. The specific goals were to (1) provide a full developmental analysis of all aspects of endosperm in each species, (2) compare patterns among taxa to determine phylogenetic character distribution, (3) reconstruct the ancestral developmental pattern for angiosperms, and (4) explore scenarios of ontogenetic evolution that occurred during the early radiation of flowering plants. Five taxa, Acorus calamus, Cabomba caroliniana, Ceratophyllum demersum, Drimys winteri, and Platanus racemosa, are described in detail. Data from an additional eight taxa were analyzed and compared with these five. Endosperm ontogeny can be conceived of as a series of stages (characters) during which differential patterns of development occur among taxa (character states). We discovered that differential developmental fate of chalazal and micropylar domains is a common pattern among the endosperms of all basal angiosperm taxa and suggest that this may be a feature of endosperm development in all angiosperms. Differential development of chalazal and micropylar domains in endosperm in basal angiosperms also bears a marked similarity to what occurs in angiosperm embryos. This may have implications for understanding the evolutionary origin of endosperm. Basal angiosperms also exhibit variable endosperm developmental characters, indicating that significant ontogenetic transformation occurred during the early radiation of the clade, although magnoliid taxa exhibit a high degree of conservation in endosperm characters. Identification of the roles of the division of the primary endosperm nucleus and subsequent development of the chalazal and micropylar domains provides the first insight into how different endosperm developmental patterns are evolutionarily and developmentally related.

Gene expression patterns in seed plant shoot meristems and leaves: homoplasy or homology?

The fossil record reveals that seed plant leaves evolved from ancestral lateral branch systems. Over time, the lateral branch systems evolved to become determinate, planar and eventually laminar. Considering their evolutionary histories, it is instructive to compare the developmental genetics of shoot apical meristems (SAMs) and leaves in extant seed plants. Genetic experiments in model angiosperm species have assigned functions of meristem maintenance, specification of stem cell identity, boundary formation, polarity establishment and primordium initiation to specific genes. Investigation of roles of the same or homologous genes during leaf development has revealed strikingly similar functions in leaves compared to SAMs. Specifically, the marginal blastozone that characterizes many angiosperm leaves appears to function in a manner mechanistically similar to the SAM. We argue here that the similarities may be homologous due to descent from ancestral roles in an ancestral shoot system. Molecular aspects of SAM and leaf development in gymnosperms is largely neglected and could provide insight into seed plant leaf evolution.