Trends in Genetics
Volume 27, Issue 9, September 2011, Pages 368-376
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Review
Multiple developmental processes underlie sex differentiation in angiosperms

https://doi.org/10.1016/j.tig.2011.05.003Get rights and content

The production of unisexual flowers has evolved numerous times in dioecious and monoecious plant taxa. Based on repeated evolutionary origins, a great variety of developmental and genetic mechanisms underlying unisexual flower development is predicted. Here, we comprehensively review the modes of development of unisexual flowers, test potential correlations with sexual system, and end with a synthesis of the genetics and hormonal regulation of plant sex determination. We find that the stage of organ abortion in male and female flowers is temporally correlated within species and also confirm that the arrest of development does not tend to occur preferentially at a particular stage, or via a common process.

Section snippets

Pattern and process of unisexual flower development

Historically, two broad categories of unisexual flowers have been recognized 1, 2. In one type (‘type I’ [3]; see Glossary), flowers are bisexual at initiation and become unisexual by termination of the development of the androecium (the male reproductive organs) or gynoecium (the female reproductive organs). In a second type (‘type II’), sex differentiation occurs before initiation of stamens and carpels. The ‘type I’ category includes flowers that are unisexual by abortion of reproductive

Developmental stages of flower sex differentiation

Unisexual flowers are borne by both monoecious (including andro- and gynomonoecious) and dioecious (including andro- and gynodioecious) taxa. Of the flowering plants (angiosperms), ca 6% are dioecious and 7% are monoecious 5, 6. To summarize the literature on unisexual flower development, we recognize four stages of sexual organ abortion: before the initiation of stamen or carpel primordia (stage 0); early in stamen or carpel development (stage 1); pre-meiosis (stage 2); and post-meiosis (stage

Ecological and evolutionary considerations in the evolution of unisexual flower development

The stage of organ arrest that characterizes extant taxa is not necessarily the stage of arrest associated with the evolutionary origin of flower unisexuality for that lineage. Following an initial loss of sexual function, subsequent mutations that result in earlier termination of development might accumulate and be selected for. Resources that are not used in the development of the aborted organs could be allocated to the alternative reproductive function, thereby increasing fertility [13]. If

Developmental processes associated with loss of organ function

Nonfunctional organs of unisexual flowers are usually described merely as ‘aborted’ or as staminodes and pistillodes. As such, analyses of the developmental processes involved in the loss of organ function were available for only 21 of the 292 taxa surveyed. We recognize eight stages of androecium and gynoecium development (Table S3 in the supplementary material online) [19], and distinguish six processes that lead to the loss of reproductive organ function (Box 1). None of the six

Genetic basis of unisexual flower development

Genes that regulate the development of unisexual flowers might be either differentially expressed within a uniform genetic background, as in monoecious species, or segregated as different functional alleles among individuals, as in dioecious species. To distinguish clearly the genetics of unisexual flower development, we adopt the following usage. Sex differentiation genes determine sexual function and lead to the production of differentiated gametes. In plants, these might be differentially

Hormonal regulation of unisexual flower development

A variety of plant hormones is likely to be involved in the regulation of sex-determining genes and developmental pathways in both type I and type II unisexual flowers. These same growth regulators also are critical to the differentiation and function of vegetative organs at various stages throughout plant development 73, 74. This consistent redeployment of regulatory molecules reflects the indeterminate and modular nature of plant growth, with both vegetative and reproductive organs developing

Phenotypic plasticity and the development of unisexual flowers

Phenotypic plasticity in general, and sexual plasticity or lability of individual plants over time, are a common occurrence [79]. Typically, when external environmental cues can alter the sexual development of an individual, the developmental system is termed ‘environmental sex determination’ (ESD) in contrast to genetic sex determination (GSD) [80]. However, in light of growing understanding of the roles of plant hormones and epigenetic chromatin remodeling in induction of flowering 81, 82 and

Concluding remarks

Future research should expand beyond the identification of sex-differentiating genes to target genetic pathways, hormonal and other regulatory pathways, and integrate these studies with detailed analyses of the specific cell-, tissue- and organ-level developmental processes that result in loss of reproductive function. In contrast to analogous systems in animals, one should not be searching for universal sex-differentiating genes or processes. Unisexual flowers have evolved independently in

Acknowledgments

This work was conducted as part of the ‘Emergence of gender and sex chromosomes: Evolutionary insights from a diversity of taxa’ catalysis meeting supported by the National Evolutionary Synthesis Center (NESCent), NSF# EF0423641.

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