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NEWS & VIEWS A M E R I C A N J O U R N A L O F B O TA N Y O N T H E N AT U R E O F T H I N G S : E S S AY S New Ideas and Directions in Botany Pathways for making unisexual flowers and unisexual plants: Moving beyond the “two mutations linked on one chromosome” model1 Susanne S. Renner2,3 KEY WORDS developmental genetics; dioecy; monoecy; retrotransposon; sex determination genes; unisexual Sex determination in higher plants is of fundamental biological interest and has great practical significance for fruit yield and high-quality seed production. The last decades have witnessed an explosion in the genetic-developmental understanding of a typical hermaphroditic flower; however, the genes controlling dicliny (unisexual flowers) and dioecy (unisexual individuals) are only now being revealed (Akagi et al., 2014; Boualem et al., 2015). These genetic-developmental insights, from distantly related groups, now need to be brought together with the large body of empirical observations showing that dicliny and dioecy each evolved independently many thousands of times, but often in the same genera and families suggesting related evolutionary pathways (Darwin, 1877; Lloyd, 1972, 1975a, b, 1980; Renner and Ricklefs, 1995; Renner, 2014). Here I highlight how the recent insights may redirect our understanding of pathways to dioecy in flowering plants. The fundamental model for the evolution of dioecy in angiosperms has long been that “at least two gene mutations are necessary to transform an hermaphroditic or monoecious species into one with separate sexes; one mutation must affect ovule production, and the other the production of pollen” (Charlesworth and Charlesworth, 1978: p. 975), with the corollary that “different genes determining sex [are] grouped together in one region of one chromosome in most species” (p. 976). This model disregards that (1) in monoecious species, mutations suppressing male and female function do not need to arise since they already exist and that (2) there is little evidence that sex-determining genes in dioecious plants are grouped together on one chromosome. The developmental-genetic 1 Manuscript received 16 January 2016; revision accepted 11 February 2016. Systematic Botany and Mycology, University of Munich (LMU), Menzinger-Str. 67 80638 Munich, Germany 3 E-mail: [email protected] doi:10.3732/ajb.1600029 2 insights summarized in the next two sections now suggest it is time to abandon strict adherence to the “two major mutations linked on one chromosome” model of angiosperm dioecy. PATHWAYS TO UNISEXUAL FLOWERS AND INDIVIDUALS IN DIOSPYROS AND CUCUMIS The Ebenaceae genus Diospyros includes about 475 species of tropical or subtropical trees that as far as is known are dioecious, with the flowers having either fertile stamens and arrested carpels, or reduced stamens and normal carpels. The family has a crown age of ca. 54 Myr and four genera, with Diospyros diverging from Actinidia about 52 Ma (Akagi et al., 2014). Akagi et al. (2014) searched the genome of Diospyros lotus, a species with XY males and homomorphic sex chromosomes, for short completely sexlinked sequences and discovered a sex-determining gene that they named OGI for Oppressor of MeGI and Japanese for “male tree”. OGI is expressed only in male flower buds and controls an autosomal gene named MeGI (=Male Growth Inhibitor gene and Japanese for “female tree”). MeGI encodes male-suppressing regulatory RNA and has female-biased bud and flower-specific expression. The two genes result from gene duplication, with one MeGI copy having moved to the Y chromosome. Y-linked OGI sequences were also detected in other species of Ebenaceae, suggesting that the duplication happened a long time ago. Since the MeGI male-suppressing gene is autosomal it does not match the model of “two mutations becoming linked on the proto-sex-chromosome” (Charlesworth and Charlesworth, 1978). OGI could instead be an example of a single-locus sex-determining gene (Charlesworth, 2015), and Akagi et al. (2014: p. 649) suggested that perhaps it is, “a single master regulator of sex determination, such as SRY in humans.” SRY is the male-determining gene on the Y-chromosomes of mammals A M E R I C A N J O U R N A L O F B OTA N Y 103(4): 587–589, 2016; http://www.amjbot.org/ © 2016 Botanical Society of America • 587 O N T H E N AT U R E O F T H I N G S : E S S AY S (Foster and Graves, 1994). Put simply, autosomal MeGI makes RNA that suppresses anther function in female flowers and plants; its duplicate copy OGI, on the Y chromosome, makes RNA that suppresses MeGI in male flowers and plants. Cucurbitaceae may be a bit older than the Ebenaceae (Schaefer et al., 2009: ca. 63 Myr), and the suppression of either stamens or carpel in their flowers happens earlier during floral development, so that mature flowers are readily recognized as staminate or pistillate (Fig. 1). About 50% of the 950–980 species of Cucurbitaceae are monoecious and 50% dioecious; no wild species have only bisexual flowers, although a few have individuals with bisexual flowers and others with staminate flowers (Schaefer and Renner, 2011). Dioecy appears to be ancestral, with much back and forth between dioecy and monoecy (Zhang et al., 2006; Schaefer and Renner, 2010; Volz and Renner, 2008), and dioecy may even go back to the common ancestor of Begoniaceae, Cucurbitaceae, Datiscaceae, and Tetramelaceae, all of which have normally unisexual flowers (Zhang et al., 2006). Spontaneous mutations that modify flower sex phenotype are common and were favored by breeding targeted toward femaleness. In Cucumis, a genus of 66 species, most of them monoecious but a few dioecious (Sebastian et al., 2010), breeders have selected gynoecious or “all-female” cultivars of C. sativus because of their high fruit yield, with the plants in greenhouses then either parthenocarpic or else requiring a few androecious plants (with only male flowers) or monoecious plants with both types of flowers to ensure fertilization. Their sexual lability and economic importance have made cucurbits, which also include melon (Cucumis melo) and watermelon (Citrullus lanatus), an important system for the developmental genetics of sex determination. The laboratory group of Abdel Bendahmane, building on work by Tova Trebitsh and colleagues, has isolated the sex determining genes of C. melo and C. sativus (CmWIP1, CmACS11, CmACS7; CsWIP1, CsACS11, CsACS2) and has published a model that explains both the development of unisexual flowers and the transition from monoecy to gynoecy (the aforementioned all-female plants), androecy (the aforementioned all-male plants), and dioecy (two sexes in equal ratios). To show that a combination of alleles of these genes can lead to artificial dioecy, Boualem et al. (2015), in two rounds of crossing, mated female plants homozygous for the recessive alleles Cmwip1 and Cmacs11 and male plants of Cmwip1/CmWIP1 A M E R I C A N J O U R N A L O F B OTA N Y or Cmacs11/Cmacs11 genotypes. They found no significant deviation from a 1:1 sex ratio, demonstrating that the combination of alleles of genes controlling monoecy (repression of bisexual flowers) can lead to dioecy (repression of bisexual individuals). The sexdetermining genes G (WIP), A (ACS11), and M (ACS7) sit on three different chromosomes (A. Bendahame, Institute of Plant Sciences Paris-Saclary, Université Paris-Sud, personal communication, 6 February 2016), and the androecy gene, ACS11, controls the development of pistillate flowers by producing an enzyme that is rate‐ limiting for the biosynthesis of ethylene (Trebitsh et al., 1997; Boualem et al., 2008). When ACS11 is active and ethylene is produced at the correct location, pistillate flowers develop. When a mutation causes ACS11 to be inhibited, the result is a lower level of ethylene in the developing flower bud, resulting in staminate flowers. Gynoecy, by contrast, is due to suppression of a C2H2 zincfinger transcription factor of the WIP protein subfamily due to retrotransposon-mediated DNA methylation (Martin et al., 2009). This natural and heritable epigenetic change, caused by the insertion of a transposon, leads to the spread of DNA methylation to the WIP1 promoter. If WIP1 is not methylated, but instead expressed, carpels are aborted, and flowers become staminate (Martin et al., 2009). COMPARISON OF SEX DETERMINATION IN DIOECIOUS DIOSPYROS AND MONOECIOUS/DIOECIOUS CUCUMIS WITH THE TWO TRADITIONAL MODELS OF DIOECY EVOLUTION In Diospyros, the key steps to dioecy were the duplication of an autosomal gene encoding a regulatory small-RNA, with one copy becoming Y-linked and repressing function of the autosomal copy. The system apparently goes back to the ancestor of modern Diospyros, a genus with homomorphic sex chromosomes (Akagi et al., 2014), yet the OGI gene alone determines sex in persimmons. In Cucumis, monoecy and dioecy (the latter manmade in C. sativus but occurring naturally in other Cucumis species) are caused by differential ethylene sensitivity of male and female meristems and the insertion of a retrotransposon affecting a carpel promoter. The sex-determining genes appear conserved across the genus (Boualem et al., 2015), and there is no evidence of sex chromosomes. Dioecious cucurbits in related genera, such as Coccinia grandis, however have hugely FIGURE 1 Male (left) and female (right) flowers of Sicyos angulatus, the star-cucumber, an annual vine in the Cucurbitaceae native to eastern North America. Cucurbitaceae, with 950–980 species, have ancestrally unisexual flowers and roughly equal proportions of monoecious and dioecious species. Dioecy appears to be ancestral. Photographs by Anil Kumar Thakur. 588 • APRIL 2016, VOLUME 103 • RENNER—MAKING UNISEXUAL FLOWERS AND UNISEXUAL PLANTS A M E R I C A N J O U R N A L O F B OTA N Y O N T H E N AT U R E O F T H I N G S : E S S AY S heteromorphic sex chromosomes (Sousa et al., 2013). Neither the Diospyros nor the Cucumis system conforms to the “two mutations linked on one chromosome” model of the evolution of dioecy. The search for a dominant female-suppressing mutation, which in the standard model becomes tightly linked to recessive malesterility mutations on the proto-sex chromosome (Charlesworth and Charlesworth, 1978), of course continues in other systems. So does the search for support for the gynodioecy pathway (Charlesworth and Charlesworth, 1978), which involves the transition to nuclearcontrolled dioecy from normally cytoplasmically controlled gynodioecy, a sexual system named by Darwin (1877: p. 298) in which populations include individuals with only female flowers and others with bisexual flowers (e.g., Delph, 1990: Veronica section Hebe; McCauley and Bailey, 2009; Miller and Bruns, 2016). As considered by Darwin (1877: p. 298), species “which I have called gynodioecious are found in various widely distinct families, but are much more common in the Labiatæ. [These species] rarely show any tendency to be dioecious, as far as can be judged from their present condition and from the absence of species having separated sexes within the same groups.” In spite of the sparse genetic and phylogenetic evidence for transitions from gynodioecy to dioecy, this pathway has received vast attention. Determining whether some dioecious angiosperms perhaps do have male and female sex-determining genes linked in a recombination-suppressed region (i.e., follow the Charlesworth and Charlesworth (1978) model of plant sex chromosome evolution) is technically very difficult (Charlesworth, 2015). Even in dioecious Silene latifolia, with a distinct Y chromosome but no fully sequenced genome, current evidence suggests that the “Y is not heavily weighted with genes involved in male development and does not fit the criteria for functional coherency” (Moore et al., 2003: p. 332; Kazama et al., 2016: new map of the Silene Y). Many old and speciesrich dioecious clade, such as Baccharis (300 species, Asteraceae), Ilex (400–600 species, Aquifoliaceae), Litsea (400 species of trees, Lauraceae), Pandanus (600 species, Pandanaceae), or Smilax (210 species; Smilacaceae), however, have not yet been investigated in terms of the developmental genetics of their unisexual flowers and individuals, and given the thousands of times that dioecy has evolved and been lost in flowering plants, it is perhaps to be expected that the genetics of sex determination takes paths other than just the “two sequential mutations linked on a chromosome” model. Darwin, C. R. 1877. The different forms of flowers on plants of the same species. John Murray, London, UK. Delph, L. F. 1990. The evolution of gender dimorphism in New Zealand Hebe (Scrophulariaceae) species. Evolutionary Trends in Plants 4: 85–97. Foster, J. W., and J. A. M. Graves. 1994. 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Rajab, R. Fernandez, H. Morin, M. Pitrat, C. Dogimont, and A. Bendahmane. 2009. A transposon-induced epigenetic change leads to sex determination in melon. Nature 461: 1135–1138. McCauley, D. E., and M. F. Bailey. 2009. Recent advances in the study of gynodioecy: The interface of theory and empiricism. Annals of Botany 104: 611–620. Miller, I., and E. Bruns. 2016. The effect of disease on the evolution of females and the genetic basis of sex in populations with cytoplasmic male sterility. Proceedings of the Royal Society, B, Biological Sciences 283: 20153035. Moore, R. C., O. Kozyreva, S. Lebel-Hardenack, J. Siroky, R. Hobza, B. Vyskot, and S. R. Grant. 2003. Genetic and functional analysis of DD44, a sexlinked gene from the dioecious plant Silene latifolia, provides clues to early events in sex chromosome evolution. Genetics 163: 321–334. Renner, S. S. 2014. 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Telford, and S. S. Renner. 2010. Cucumber and melon have their wild progenitors in India, and the sister species of Cucumis melo is from Australia. Proceedings of the National Academy of Sciences, USA 107: 14269–14273. Sousa, A., J. Fuchs, and S. S. Renner. 2013. Molecular cytogenetics (FISH, GISH) of Coccinia grandis: A ca. 3 myr-old species of Cucurbitaceae with the largest Y/autosome divergence in flowering plants. Cytogenetic and Genome Research 139: 107–118. Trebitsh, T., J. E. Staub, and S. D. O’Neill. 1997. Identification of a 1-aminocyclopropane-1-carboxylic acid synthase gene linked to the Female (F) locus that enhances female sex expression in cucumber. Plant Physiology 113: 987–995. Volz, S. M., and S. S. Renner. 2008. Hybridization, polyploidy, and evolutionary transitions between monoecy and dioecy in Bryonia (Cucurbitaceae). American Journal of Botany 95: 1297–1306. Zhang, L.-B., M. P. Simmons, A. Kocyan, and S. S. Renner. 2006. Phylogeny of the Cucurbitales based on DNA sequences of nine loci from three genomes: Implications for morphological and sexual system evolution. Molecular Phylogenetics and Evolution 39: 305–322. ACKNOWLEDGEMENTS I thank Lynda Delph and two anonymous reviewers for critical comments. This work is supported by DFG grant RE 603/19-1. LITERATURE CITED Akagi, T., I. M. Henry, R. Tao, and L. Comai. 2014. A Y-chromosome–encoded small RNA acts as a sex determinant in persimmons. Science 346: 646–650. Boualem, A., M. Fergany, R. Fernandez, C. Troadec, A. Martin, H. Morin, M.-A. Sari, et al. 2008. A conserved mutation in an ethylene biosynthesis enzyme leads to andromonoecy in melons. Science 321: 836–838. Boualem, A., C. Troadec, C. Camps, A. Lemhemdi, H. Morin, M.-A. Sari, R. Fraenkel-Zagouri, et al. 2015. A cucurbit androecy gene reveals how unisexual flowers develop and dioecy emerges. Science 350: 688–691. Charlesworth, B., and D. Charlesworth. 1978. A model for the evolution of dioecy and gynodioecy. American Naturalist 112: 975–997. Charlesworth, D. 2015. Plant contributions to our understanding of sex chromosome evolution. New Phytologist 208: 52–65. APRIL 2016, VOLUME 103 • RENNER—MAKING UNISEXUAL FLOWERS AND UNISEXUAL PLANTS • 589