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Sex Chromosomes in Land Plants

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Sex Chromosomes in Land Plants PP62CH20-Ming ARI 15 April 2011 10:7 Sex Chromosomes in Land Plants Ray Ming,1 Abdelhafid Bendahmane,2,3 and Susanne S. Renner4 1Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana-Champaign, Illinois 61801; email: [email protected] 2INRA-CNRS, UMR1165, UnitedeRechercheenG´ enomique´ Veg´ etale,´ F-91057 Evry, France; email: abdelhafi[email protected] 3Department of Plant Production, College of Food and Agricultural Sciences, King Saud University, Riyadh 11451, Saudi Arabia 4Department of Biology, University of Munich, D-80638 Munich, Germany; email: [email protected] Annu. Rev. Plant Biol. 2011. 62:485–514 Keywords The Annual Review of Plant Biology is online at plant.annualreviews.org land plants, pseudoautosomal region, sex determination, sex chromosomes, suppression of recombination This article’s doi: 10.1146/annurev-arplant-042110-103914 Abstract Copyright c 2011 by Annual Reviews. All rights reserved Sex chromosomes in land plants can evolve as a consequence of close linkage between the two sex determination genes with complementary 1543-5008/11/0602-0485$20.00 dominance required to establish stable dioecious populations, and they by Washington University, Medical Library on 06/25/11. For personal use only. Annu. Rev. Plant Biol. 2011.62:485-514. Downloaded from www.annualreviews.org are found in at least 48 species across 20 families. The sex chromosomes in hepatics, mosses, and gymnosperms are morphologically heteromor- phic. In angiosperms, heteromorphic sex chromosomes are found in at least 19 species from 4 families, while homomorphic sex chromosomes occur in 20 species from 13 families. The prevalence of the XY sys- tem found in 44 out of 48 species may reflect the predominance of the evolutionary pathway from gynodioecy towards dioecy. All dioecious species have the potential to evolve sex chromosomes, and reversions back from dioecy to various forms of monoecy, gynodioecy, or andro- dioecy have also occurred. Such reversals may occur especially during the early stages of sex chromosome evolution before the lethality of the YY (or WW) genotype is established. 485 PP62CH20-Ming ARI 15 April 2011 10:7 are dioecious (129). Although the circum- Contents scription of angiosperm families has changed dramatically since 1995, the numbers of recog- INTRODUCTION.................. 486 nized dioecious genera and species have hardly MECHANISMS OF SEX changed. The patchy phylogenetic distribution DETERMINATION.............. 486 of dioecy, which is the precondition for the THERISEOFSEX evolution of sex chromosomes, has long been CHROMOSOMES................ 488 taken to indicate that sex chromosomes in EVOLUTION OF SEX plants have evolved many times independently CHROMOSOMES................ 489 (24, 30, 57, 58, 77, 92, 100, 156, 166). SEX CHROMOSOMES IN LAND Here we review the occurrence of sex chro- PLANTS.......................... 492 mosomes in land plants, focusing on the molec- Bryophytes........................ 492 ular data regarding their evolution and func- Gymnosperms..................... 493 tion. Although sex chromosomes are currently Angiosperms. 498 known only from a limited number of species, PHYLOGENETIC PERSPECTIVE progress in model systems, mainly Silene and AND AGES OF PLANT SEX Carica, has been rapid and molecular data are CHROMOSOMES................ 503 permitting the testing of classic predictions of WHY THE XY SYSTEM IS the steps expected to lead to the origin of sex PREVALENT.................... 505 chromosomes. To set the stage, we begin with WHY SEX CHROMOSOMES ARE the mechanisms of sex determination. The- RAREINPLANTS............... 506 ory predicts that sex chromosomes (gonosomes) CONCLUSIONS.................... 506 evolve from autosomes and that heteromorphy of sex chromosomes is one step in their evo- lution, occurring well after the differentiation INTRODUCTION into XY or WZ functionality (13, 99, 171). As Sexual systems in plants are almost over- the sex chromosomes diverge from their au- whelmingly diverse, and understanding their tosomal ancestor and from each other, they origin and evolution requires data from many can increase or decrease in size. Our review different fields, including ecology, develop- summarizes the evidence for this happening in mental biology, and genetics. Sexual system groups with sex chromosomes of different evo- here refers to the distribution and function of lutionary ages (cf. Evolution of Sex Chromo- gamete-producing morphological structures somes section below). We also bring in phy- (136). The open architecture and modular logenetic and molecular clock–based evidence. growth of plants have resulted in numerous Our review ends by considering reasons for by Washington University, Medical Library on 06/25/11. For personal use only. Annu. Rev. Plant Biol. 2011.62:485-514. Downloaded from www.annualreviews.org gamete production patterns, which in turn are why sex chromosomes in plants are rare and, reflected in the large number of sexual systems where they have evolved, XY systems appear to (9, 36, 180). The sexual system that predomi- predominate. nates in animals, namely the restriction of male Dioecy: plant species and female function onto different individuals that form unisexual (gonochory), is strikingly rare among plants: MECHANISMS OF flowers on two types of SEX DETERMINATION individuals, staminate Among land plants, strict separation of the flowers on males and sexes (dioecy) occurs in only 9–10%, i.e., Hermaphroditism is the norm in land plants, pistillate flowers on 29,000 out of the 300,000 species with an un- and the separation of sexual function into dif- females. The word even distribution (for details, see Phylogenetic ferent individuals evolved independently many dioecious is from Perspective section below). Of the flowering times from a hermaphroditic ancestral state Greek and means “two households” plants (angiosperms), approximately 6% or (156). The arisal of genes determining the pres- 14,600 species in 960 genera and 200 families ence of male and female structures therefore 486 Ming · Bendahmane · Renner PP62CH20-Ming ARI 15 April 2011 10:7 sets the stage for the evolution of sex chromo- in melon, acts as a stamen suppressor in buds somes. The first step toward sex chromosome determined to develop a carpel (178). evolution is the occurrence of male and female In both Cucumis species, sex expression pat- sterile mutations, leading to the development terns can be modified by hormonal and envi- of unisexual reproductive structures. Such ronmental factors, with ethylene playing a ma- mutations occur frequently and repeatedly in jor role (20, 183). For example, treatment of plant species, as demonstrated by the presence monoecious melon plants with ethylene leads of unisexual species in 75% of angiosperm to plants with only female flowers. In con- families and numerous male sterile mutants in trast, treatment of gynoecious melon plants domesticated crop plants (129). Stamen and with ethylene inhibitors leads to hermaphrodite carpel development involve large numbers of flowers. Consistent with ethylene being a fem- specialized genetic functions that are required inizing agent, the A gene in melon and the M at various developmental stages, and mutations gene in cucumber are orthologs and code for in any of the many regulatory genes could trig- the rate-limiting step in ethylene biosynthe- ger abortion or loss of function of male and/or sis, the 1-aminocyclopropane-1-carboxylic acid female organs (170, 189). Growth hormones synthase (ACS) gene. In both plants, the ACS affect sex expression in some species, but not genes, referred to as CmACS-7 in melon (17) others. The recently cloned sex determination and CsACS-2 in cucumber (18), are expressed genes in the Cucurbitaceae family provide a in carpel primordia, and loss of enzymatic activ- good example of the underlying genetics. ity leads to stamen development. The observa- Several species in the Cucurbitaceae, in- tion that the ethylene signal required to inhibit cluding cucumber (Cucumis sativus) and honey the stamens is generated in a different tissue, melon or cantaloupe (Cucumis melo), show in- the carpel primordium, and must be translo- traspecific polymorphism in their sexual sys- cated to the target tissue, is puzzling. Ethy- tems. In these species, floral primordia are ini- lene has a dual role and is also required at the tially bisexual with sex determination occurring same time for carpel development; applying ex- by the selective developmental arrest of either ogenous hormone, or engineering melons to the stamen or the carpel, resulting in unisex- overexpress ACS, results in increased female- ual flowers (2, 61). In melon, sex determina- ness (118). The F gene in cucumber is likely tion is governed by the genes andromonoecious to encode an ACS enzyme (161). Nevertheless, (a)andgynoecious ( g), and the interactions of melon and cucumber plants expressing inactive their different alleles can result in a range of sex- CmACS-7 and CsACS-2 isoforms develop nor- ual phenotypes (63, 126). Monoecious (A-G-) mal carpels, suggesting that other ACS isoforms and andromonoecious (aaG-) individuals bear provide the carpel-promoting function. male flowers on the main stem and female or The isolation of the gynoecy gene in melon by Washington University, Medical Library on 06/25/11. For personal use only. Annu. Rev. Plant Biol. 2011.62:485-514. Downloaded from www.annualreviews.org hermaphrodite flowers, respectively, on axil- has solved another piece in the puzzle, ex-
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