One Hundred Ways to Invent the Sexes: Theoretical and Observed Paths to Dioecy in Plants

Henry, Isabelle; Akagi, Takashi; Tao, Ryutaro; Comai, Luca

doi:10.1146/annurev-arplant-042817-040615

Cited by 84 publications

(96 citation statements)

References 97 publications

(134 reference statements)

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“…The authors identified a Type C response regulator ( Shy Girl, SyGI ) on the Y chromosome that was associated with maleness. Overexpression of this gene in Arabidopsis and Nicotiana tabacum caused suppression of carpel development, supporting its potential role as a suppressor of female function [14]. This work has some interesting parallels with the results reported here for Salix and Populus .…”

Section: Discussionsupporting

confidence: 83%

“…However, RR9 and SyGI are clearly not orthologous and likely perform different roles in cytokinin signal transduction. This supports the view that there are numerous ways to achieve separate sexes in plants, and it is likely that a myriad of mechanisms underlie the hundreds of independent occurrences of dioecy in the angiosperms [51], even if a relatively small number of pathways are involved [11, 14].…”

Section: Discussionmentioning

confidence: 54%

“…In plants, male-specific Ys (MSYs) have been studied in papaya and persimmon. Both of these contain a female suppressor on the Y chromosome [12–14]. Recently, a female suppressing gene in asparagus has been identified on the Y chromosome using long-read sequencing technology with optical mapping [15].…”

Section: Introductionmentioning

confidence: 99%

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A Willow Sex Chromosome Reveals Convergent Evolution of Complex Palindromic Repeats

Zhou

Macaya‐Sanz

Carlson

et al. 2019

Preprint

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1 Background 2 Sex chromosomes in a wide variety of species share common characteristics, including the 3 presence of suppressed recombination surrounding sex determination loci. They have arisen 4 independently in numerous lineages, providing a conclusive example of convergent evolution. 5Mammalian sex chromosomes contain multiple palindromic repeats across the non-recombining 6 region that facilitate sequence conservation through gene conversion, and contain genes that are 7 crucial for sexual reproduction. Plant sex chromosomes are less well understood, and in 8 particular it is not clear how coding sequence conservation is maintained in the absence of 9 homologous recombination. 10 Results 11 Here we present the first evidence of large palindromic structures in a plant sex chromosome, 12 based on a highly contiguous assembly of the W chromosome of the dioecious shrub Salix 13 purpurea. Two consecutive palindromes span over a region of 200 kb, with conspicuous 20 kb 14 stretches of highly conserved sequences among the four arms. The closely-related species S. 15 suchowensis also has two copies of a portion of the palindrome arm and provides strong 16 evidence for gene conversion. Four genes in the palindrome are homologous to genes in the SDR 17 of the closely-related genus Populus, which is located on a different chromosome. These genes 18 show distinct, floral-biased expression patterns compared to paralogous copies on autosomes.19 Conclusion 20The presence of palindromic structures in sex chromosomes of mammals and plants highlights 21 the intrinsic importance of these features in adaptive evolution in the absence of recombination. 22Convergent evolution is driving both the independent establishment of sex chromosomes as well 23 as their fine-scale sequence structure. 24 26 103 297 kb in length lacked mapped markers and could not be placed unambiguously. 104Location of the SDR 105 We repeated sex association analysis with our new assembly with Chr15Z removed. 106Among 54,959 tested SNPs, all 105 significantly sex-associated SNPs were present only on 107 Chr15W (Fig. 1a; Additional File 2: Figure S2a-c), and markers from PARs and other scaffolds 108 in the main genome did not show any sex association (Additional File 2: Figure S2a). The eight 109 top-ranking sex-associated markers were distributed from 7.66 Mb to 8.66 Mb. Sex-associated 110 markers were primarily heterozygous in females and homozygous in males, confirming our 111 previously-reported observation of ZW sex determination in S. purpurea [18].

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Section: Discussionsupporting

confidence: 83%

Section: Discussionmentioning

confidence: 54%

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A Willow Sex Chromosome Reveals Convergent Evolution of Complex Palindromic Repeats

Zhou

Macaya‐Sanz

Carlson

et al. 2019

Preprint

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“…The origin and evolution of dioecy (separate sexes) has long been one of the most fascinating topics for biologists (Henry et al, 2018; Feng et al , 2020). The presence of dioecy ensures outcrossing and optimal allocation of reproductive resources for male and female sexual function, thereby providing them with certain advantages in fertility, survival and evolution (Bawa, 1980).…”

Section: Introductionmentioning

confidence: 99%

A general model to explain repeated turnovers of sex determination in the Salicaceae

Yang

Zhang

Wang

et al. 2020

Preprint

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0Dioecy, the presence of separate sexes on distinct individuals, has evolved repeatedly 3 1 in multiple plant lineages. However, the specific mechanisms through which sex 3 2 systems evolve and their commonalities among plant species remain poorly 3 3 understood. With both XY and ZW sex systems, the family Salicaceae provides a 3 4 system to uncover the evolutionary forces driving sex chromosome turnovers. In this 3 5 study, we performed a genome-wide association study to characterize sex 3 6 determination in two Populus species, P. euphratica and P. alba. Our results reveal an 3 7XY system of sex determination on chromosome 14 of P. euphratica, and a ZW 3 8 system on chromosome 19 of P. alba. We further assembled the corresponding sex 3 9 determination regions, and found that their sex chromosome turnovers may be driven 4 0 by the repeated translocations of a Helitron-like transposon. During the translocation, 4 1 this factor may have captured partial or intact sequences that are orthologous to a 4 2 type-A cytokinin response regulator gene. Based on results from this and other 4 3recently published studies, we hypothesize that this gene may act as a master regulator 4 4 of sex determination for the entire family. We propose a general model to explain how 4 5 the XY and ZW sex systems in this family can be determined by the same RR gene. 6Our study provides new insights into the diversification of incipient sex chromosome 4 7 in flowering plants by showing how transposition and rearrangement of a single gene 4 8 can control sex in both XY and ZW systems. 4 9 5 0

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“…Evidence todate supports several models, including a two-locus model (Westergaard, 1958) in Fragaria virginiana (Spigler et al, 2008), Silene latifolia (Fujita et al, 2011) and Actinidia spp. (Akagi et al, 2019), a single switch gene in Diospyros lotus (Akagi et al, 2014) and others (Renner, 2016;Pannell, 2017;Henry et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

The genetic basis of sex determination in grapevines (Vitis spp.)

Massonnet

Cochetel

Minio

et al. 2019

Preprint

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Sex determination in grapevine evolved through a complex succession of switches in sexual systems. Phased genomes built with single molecule real-time sequencing reads were assembled for eleven accessions of cultivated hermaphrodite grapevines and dioecious males and females, including the ancestor of domesticated grapevine and other related wild species. By comparing the phased sex haplotypes, we defined the sex locus of the Vitis genus and identified polymorphisms spanning regulatory and coding sequences that are in perfect association with each sex-type throughout the genus. These findings identified a novel male-fertility candidate gene, INP1, and significantly refined the model of sex determination in Vitis and its evolution.Whole-sequence alignments of male (M) (a), female (F) (b), and hermaphrodite (H) (c) sex haplotypes on Vv vinifera Cabernet Sauvignon chromosome 2 Alt1 (H). d, From top to bottom, schematic representations of the sex locus in hermaphrodite Vv vinifera Cabernet Sauvignon (HF), male Vv sylvestris DVIT3351.27 (MF) and female Vv sylvestris DVIT3603.07 (FF), male V. arizonica (MF), and male M. rotundifolia (MF). A triangle along chromosome 2 marks the position of VVIB23, the genetic marker closely linked to the sex locus (Riaz et al., 2006). Genes affected by nonsense mutations are indicated with an "X". Sex-linked polymorphisms affect protein sequencesComparison of the Vitis sex haplotypes also allowed the identification of SNPs and small INDELs (≤ 50 bp) perfectly associated with sex. All sex-related polymorphisms were on chromosome 2 of Cabernet Sauvignon from positions 4,801,876 to 5,061,548 ( Fig. 3a; Supplementary Table 2), further confirming and delimiting the sex locus (Fechter et al., 2012;Picq et al., 2014). In total, 1,275 SNPs were shared by all F haplotypes versus H and M haplotypes and 539 SNPs were shared by all M haplotypes versus F and H haplotypes. A small number of SNPs (127) were linked to the H haplotype. Interestingly, the highest density of M-associated SNPs was in the first 8 kbp of the sex locus (176 SNPs,4,801,876 to 4,809,592), and the first F-associated SNP was 40 kbp downstream (4,842,196). Sex-specific SNP distributions were also similar when including M. rotundifolia haplotypes in the comparison, but the number of clear sexassociated SNPs decreased because of the divergence of the two genera (Extended Data Fig. 2). Many of the sex-linked SNPs we identified impact predicted protein sequences (Fig. 3b). In total, 89 nonsynonymous F-specific SNPs were detected in ten genes. These included one in a gene encoding a trehalose-6-phosphate phosphatase (TPP), one in INAPERTURE POLLEN1 (INP1), seven in a exostosincoding gene, three in a 3-ketoacyl-acyl carrier protein synthase III gene (KASIII), seven in a PLATZ transcription factor-coding gene (PLATZ), eighteen in the first FMO, twenty six in the second FMO, eleven in the third FMO, eleven in the hypothetical protein (VviFSEX), and four in the adenine phosphoribosyltransferase 3 (APT3) (Supplementary Table 2). Three of t...

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One Hundred Ways to Invent the Sexes: Theoretical and Observed Paths to Dioecy in Plants

Cited by 84 publications

References 97 publications

A Willow Sex Chromosome Reveals Convergent Evolution of Complex Palindromic Repeats

A Willow Sex Chromosome Reveals Convergent Evolution of Complex Palindromic Repeats

A general model to explain repeated turnovers of sex determination in the Salicaceae

The genetic basis of sex determination in grapevines (Vitis spp.)

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