Sex-Determining Mechanisms in Land Plants - Barley World

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S68The Plant CellThe Dioecious AngiospermsSilene latifolia is a dioecious species with individual plantsproducing either all female or all male flowers. As it is by far thebest characterized dioecious species to date, our review of sexdeterminingmechanisms in dioecious plants will focus on thisspecies. In male and female S. latifolia flowers, the gynoeciumand androecium initiate but arrest development prematurely,leading to functionally unisexual flowers (Grant et al., 1994). Thesexual phenotype of individuals is determined by sex chromosomes;males are heterogametic (XY) and females are homogametic(XX). Early cytogenetic studies of sex-determining mutantsin S. latifolia led Westergaard (1946, 1958) to conclude that theY chromosome is divided into three regions relevant to sexexpression: one required for the suppression of female developmentand two required for the promotion of male development.None of these regions would be necessary for thedevelopment of female reproductive organs, because thesefunctions would reside on the X or autosomal chromosomes.Additional sex-determining mutants have been generated recentlyby x-ray mutagenesis of pollen and selecting bothhermaphrodites and asexual F1 progeny (Farbos et al., 1999;Lardon et al., 1999; Lebel-Hardenack et al., 2002). Thesemutants verify the earlier work of Westergaard (1946, 1958; hislines were apparently lost) and have resulted in the identificationof two additional classes of mutants, those that are not Y linkedand hermaphroditic and those that are Y linked and asexual. Thehermaphroditic deletion mutants are likely to contain a gene(s)necessary for the female-suppressing function, whereas theasexual deletion mutants likely contain the male-promotinggene(s). Genetic screens to identify mutant XX hermaphroditesor asexuals have not been reported. Although these sexdetermininggenes have not been cloned, the construction ofan amplified fragment length polymorphism map of the Ychromosome using lines deleted for overlapping regions of theY chromosome will be useful for genetic and physical mapping ofthe sex-determining mutants (Lebel-Hardenack et al., 2002) andmay ultimately lead to their cloning.Another approach to identify sex-determining genes in S.latifolia has been to clone genes that are expressed specifically inthe male flowers and determine their linkage to the Y chromosome(reviewed by Charlesworth, 2002). Of the >50 isolatedgenes that have been correlated with sex expression in S. latifoliato date, only the four listed in Table 1 have been shown to belinked to the Y chromosome. Genes linked exclusively to the Ychromosome have not been found, because all of the Y-linkedgenes have X or autosomal homologs. These data indicatethat the S. latifolia Y chromosome most closely resembles theX-degenerate class of sequences of the human Y chromosome.Genes within this class have an X homolog, the X andY homologs encode similar but nonidentical isoforms, many ofthem are ubiquitously expressed, and all are present in low copynumber in the genome (Skaletsky et al., 2003). As shown in Table1, many of these features are shared with the Y-linked genes ofS. latifolia.Although molecular approaches have not yet succeeded inidentifying the major regulatory sex-determining genes in S.latifolia, this work has and will continue to test theories of how Ychromosomes evolved from an ancestral pair of autosomes inplants (Charlesworth, 1996, 2002; Negrutiu et al., 2001). Thesetheories state that once mutations that result in geneticallydetermined males (where female genes are repressed) andfemales (where male genes are repressed) occur, recombinationbetween the sex-determining genes must be suppressed toavoid recombinant asexual or hermaphroditic offspring. Anotherconsequence of nonrecombination is the certainty that unisexualmale and female offspring will be produced in equal ratios.Recombination between homologous chromosomes often issuppressed by the accumulation of chromosomal inversions onone homolog (in this case, the Y). The lack of X-Y recombinationwould eventually lead to degeneracy and loss of gene function onthe Y chromosome, with the exception of genes required for malefertility and those necessary to suppress female fertility. The S.latifolia Y chromosome appears not to fit this paradigm forseveral reasons. First, the Y chromosome is 1.4 times larger thanthe X chromosome and is largely euchromatic, indicating that itmay not be degenerate (Ciupercescu et al., 1990; Grabowska-Joachimiak and Joachimiak, 2002). Second, measurements ofDNA polymorphism in sex-linked gene pairs have revealed thatalthough the DNA polymorphism of S4Y-1 is greater than that ofS4X-1, the DNA polymorphism of SlY-1 is 20-fold lower than thatof SlX-1 (Filatov et al., 2000, 2001; Filatov and Charlesworth2002). Given that the S. latifolia sex chromosomes diverged lessthan 20 million years ago (Desfeux et al., 1996; Charlesworth,2002), which is much less than the 240- to 320-million-yeartimeline for human sex chromosome evolution (Lahn and Page,1999), it is likely that the S. latifolia Y chromosome is at a relativelyyoung stage of evolution (Charlesworth, 2002). Comparativesequencing of the S. latifolia sex chromosomes will be importantin understanding the evolution of the Y chromosome in plants,especially compared with the Y chromosome of Marchantia andthe sex-determining chromosome region of papaya.Table 1. Sex Chromosome–Linked Genes in S. latifoliaY-Linked Gene X-Linked Gene Male-Specific Expression Function ReferenceSlY-1 SlX-1 SlY-1 yes, SlX-1 no WD-repeat protein Delichere et al., 1999SlY-4 SlX-4 No Fructose-2,6-bisphosphatase Atanassov et al., 2001MRO3-Y a MRO3-X a Yes Unknown Matsunaga et al., 1996; Guttman andCharlesworth 1998DD44Y DD44X No Oligomycin sensitivity–conferringproteinMoore et al., 2003a The Y homolog is inactive and the X homolog is active.
Sex DeterminationS69FUTURE DIRECTIONSSex determination in plants is a fundamental developmentalprocess that is particularly important for economic reasons,because the sexual phenotypes of commercially important cropsdictate how they are bred and cultivated. Although most cropplants are not considered model systems—and sex determinationis not a problem that can be addressed in the modelangiosperm Arabidopsis—the economic value in manipulatingthe sexual phenotypes of crop plants should continue todrive interest in this area of research. Recent studies of sexdeterminingmechanisms have demonstrated clearly that angiosperms,including crop plants, have evolved a variety ofsex-determining mechanisms that involve a number of differentgenetic and epigenetic factors, from sex chromosomes to planthormones. Although the determinants of sexual phenotype arediverse, determining whether the downstream master sexregulatorygenes that specify male or female development areheld in common or not will require cloning the sex-determininggenes from a variety of plant species.Choosing to study sex determination in plants representingother major land plant lineages will allow several broaderdevelopmental and evolutionary questions to be addressed.One unresolved question is how heterospory evolved fromhomospory. By identifying the sex-determining genes in homosporousplants such as Ceratopteris and examining theexpression of possible homologous genes in closely relatedheterosporous species, one can test the hypothesis that theswitch from homospory to heterospory involved a heterochronicshift in the timing of expression of these genes from thegametophyte to the sporophyte generation. Other questions tobe resolved are how sex chromosomes evolved in plants andwhether similar processes led to distinct sex chromosomes inplants and animals. Comparing the Y chromosome sequences ofMarchantia and S. latifolia, for example, will be invaluable inunderstanding how male-promoting genes and female-suppressinggenes became localized to a Y chromosome and howrecombination between the Y and its homolog was and continuesto be suppressed.ACKNOWLEDGMENTSSupport was provided by the National Science Foundation (MCB-9723154). This is journal paper 17271 of the Purdue UniversityAgricultural Experiment Station.Received August 25, 2003; accepted January 19, 2004.REFERENCESAinsworth, C., ed (1999). Sex Determination in Plants. (Oxford, UK:BIOS Scientific Publishers).Ainsworth, C. (2000). Boys and girls come out to play: The molecularbiology of dioecious plants. Ann. Bot. 86, 211–221.Ainsworth, C., Crossley, S., Buchanan-Wollaston, V., Thangavelu,M., and Parker, J. (1995). Male and female flowers of the dioeciousplant sorrel show different patterns of MADS box gene expression.Plant Cell 7, 1583–1598.Arumuganathan, K., and Earle, E.D. (1991). Nuclear DNA content ofsome important plant species. Plant Mol. Biol. Rep. 9, 208–218.Atanassov, I., Delichere, C., Filatov, D., Charlesworth, D., Negrutiu,I., and Moneger, F. (2001). Analysis and evolution of two functionalY-linked loci in a plant sex chromosome system. Mol. Biol. Evol.18, 2126–2168.Baker, B.S., and Ridge, K.A. (1980). Sex and the single cell. I. On theaction of major loci affecting sex determination in Drosophilamelanogaster. Genetics 94, 383–423.Banks, J. (1998). Sex determination in the fern Ceratopteris. TrendsPlant Sci. 2, 175–180.Banks, J., Hickok, L., and Webb, M.A. (1993). The programming ofsexual phenotype in the homosporous fern, Ceratopteris richardii. Int.J. Plant Sci. 154, 522–534.Barrett, S. (2002). The evolution of plant sexual diversity. Nat. Rev. 3,274–284.Bensen, R., Johal, J., Crane, V.C., Tossberg, J.T., Schnable, P.S.,Meeley, R.B., and Briggs, S.P. (1995). Cloning and characterizationof the maize An1 gene. Plant Cell 7, 75–84.Calderon-Urrea, A., and Dellaporta, S.L. (1999). Cell death and cellprotection genes determine the fate of pistils in maize. Development126, 435–441.Charlesworth, D. (1996). The evolution of chromosomal sex determinationand dosage compensation. Curr. Biol. 6, 149–162.Charlesworth, D. (2002). Plant sex determination and sex chromosomes.Heredity 88, 94–101.Ciupercescu, D., Veuskens, J., Mouras, A., Ye, D., Briquet, M., andNegrutiu, I. (1990). Karyotyping Melandrium album, a dioecious plantwith heteromorphic sex chromosomes. Genome 33, 556–562.Cline, T.W. (1983). The interaction between daughterless and sex-lethalin triploids: A lethal sex-transforming maternal effect linking sexdetermination and dosage compensation in Drosophila melanogaster.Dev. 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Eine die Antheridienbildung bei farnen forderndeSubstanz in den Prothallien von Pteridium aquilinum L. Kuhn. Ber.Dtsch. Bot. Ges. 63, 139–147.Elo, A., Lemmetyinen, J., Turunen, M., Tikka, L., and Sopanen, T.(2001). Three MADS-box genes similar to APETALA1 and FRUITFULLfrom silver birch (Betula pendula). Physiol. Plant. 112, 95–103.Farbos, I., Veuskens, J., Vyskot, B., Oliveira, M., Hinnisdaels, S.,Aghmir, A., Mouras, A., and Negrutiu, I. (1999). Sexual dimorphismin white campion: Deletion of the Y chromosome results in a floralasexual phenotype. Genetics 151, 1187–1196.Filatov, D., and Charlesworth, D. (2002). Substitution rates in theX- and Y-linked genes of the plants Silene latifolia and S. dioica. Mol.Biol. Evol. 19, 898–907.
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