The origin and evolution of sex chromosomes, revealed by sequencing of the Silene latifolia female genome

Yue, Jingjing; Krasovec, Marc; Kazama, Yusuke; Zhang, Xingtan; Xie, Wei; Zhang, S.Z.; Xu, Xiuming; Kan, Baolin; Ming, Ray; Filatov, Dmitry A.

doi:10.1016/j.cub.2023.05.046

Cited by 21 publications

(46 citation statements)

References 96 publications

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“…Ten representative genes known to control seed size and shape in Arabidopsis and rice were uploaded into Geneious Prime 2023.2.1, from the NCBI nucleotide database ( Sayers et al., 2022 ). The X-chromosome sequence was downloaded and used for local BLAST ( Yue et al., 2023 ). The loci in A. thaliana and the genes found in the X chromosome of S. latifolia with low E- values are listed in Table 2 .…”

Section: Methodsmentioning

confidence: 99%

Seed shape and size of Silene latifolia, differences between sexes, and influence of the parental genome in hybrids with Silene dioica

Marcel,

Javier,

Emilio

et al. 2024

Front. Plant Sci.

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IntroductionPlants undergo various natural changes that dramatically modify their genomes. One is polyploidization and the second is hybridization. Both are regarded as key factors in plant evolution and result in phenotypic differences in different plant organs. In Silene, we can find both examples in nature, and this genus has a seed shape diversity that has long been recognized as a valuable source of information for infrageneric classification.MethodsMorphometric analysis is a statistical study of shape and size and their covariations with other variables. Traditionally, seed shape description was limited to an approximate comparison with geometric figures (rounded, globular, reniform, or heart-shaped). Seed shape quantification has been based on direct measurements, such as area, perimeter, length, and width, narrowing statistical analysis. We used seed images and processed them to obtain silhouettes. We performed geometric morphometric analyses, such as similarity to geometric models and elliptic Fourier analysis, to study the hybrid offspring of S. latifolia and S. dioica.ResultsWe generated synthetic tetraploids of Silene latifolia and performed controlled crosses between diploid S. latifolia and Silene dioica to analyze seed morphology. After imaging capture and post-processing, statistical analysis revealed differences in seed size, but not in shape, between S. latifolia diploids and tetraploids, as well as some differences in shape among the parentals and hybrids. A detailed inspection using fluorescence microscopy allowed for the identification of shape differences in the cells of the seed coat. In the case of hybrids, differences were found in circularity and solidity. Overal seed shape is maternally regulated for both species, whereas cell shape cannot be associated with any of the sexes.DiscussionOur results provide additional tools useful for the combination of morphology with genetics, ecology or taxonomy. Seed shape is a robust indicator that can be used as a complementary tool for the genetic and phylogenetic analyses of Silene hybrid populations.

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Section: Methodsmentioning

confidence: 99%

Seed shape and size of Silene latifolia, differences between sexes, and influence of the parental genome in hybrids with Silene dioica

Marcel,

Javier,

Emilio

et al. 2024

Front. Plant Sci.

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“…However, the Y-linked region may be small and carry only a few genes, or degeneration of Y-linked genes may mean that few gene pairs are available, resulting in uncertain estimates. Nevertheless, enough gametolog pairs have been found to demonstrate that synonymous site divergence can be as high as 25% (or even more for some genes) in plants with heteromorphic XY pairs, including S. latifolia ( Yue et al 2023 ), and species of Cannabis and hops ( Prentout et al 2021 ).…”

Section: How Old Are Nonrecombining Sex-determining Regions?mentioning

confidence: 99%

“…Importantly, however, suppressed recombination must have evolved in some organisms because separate events have been discovered, creating “evolutionary strata” of Y-X divergence. Plants with such evidence for creation of new nonrecombining regions include 3 of the heteromorphic systems in Table 1 , S. latifolia and its close relatives ( Campos et al 2016 ; Yue et al 2023 ), whose homologous chromosome recombines in Silene vulgaris ( Bergero et al 2013 ), papaya ( Wang et al 2012 ), and probably the Cannabaceae ( Prentout et al 2021 ). It remains unclear how many dioecious angiosperms have evolved strata.…”

Section: How Old Are Nonrecombining Sex-determining Regions?mentioning

confidence: 99%

Why should we study plant sex chromosomes?

Charlesworth,

Harkess

2024

The Plant Cell

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Understanding plant sex chromosomes involves studying interactions between developmental and physiological genetics, genome evolution, and evolutionary ecology. We focus on areas of overlap between these. Ideas about how species with separate sexes (dioecious species, in plant terminology) can evolve are even more relevant to plants than to most animal taxa because dioecy has evolved many times from ancestral functionally hermaphroditic populations, often recently. One aim of studying plant sex chromosomes is to discover how separate males and females evolved from ancestors with no such genetic sex-determining polymorphism, and the diversity in the genetic control of maleness vs femaleness. Different systems share some interesting features, and their differences help to understand why completely sex-linked regions may evolve. In some dioecious plants, the sex-determining genome regions are physically small. In others, regions without crossing over have evolved sometimes extensive regions with properties very similar to those of the familiar animal sex chromosomes. The differences also affect the evolutionary changes possible when the environment (or pollination environment, for angiosperms) changes, as dioecy is an ecologically risky strategy for sessile organisms. Dioecious plants have repeatedly reverted to cosexuality, and hermaphroditic strains of fruit crops such as papaya and grapes are desired by plant breeders. Sex-linked regions are predicted to become enriched in genes with sex differences in expression, especially when higher expression benefits one sex function but harms the other. Such trade-offs may be important for understanding other plant developmental and physiological processes and have direct applications in plant breeding.

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“…[32] As the ratio of the X chromosomes to the Y chromosome increased, hermaphroditic flowers were produced more frequently and in the case of XXXXY plant, almost all flowers were hermaphrodites. It is interesting that SlWUS1 is not dosage compensated (i.e., not upregulated in males) [28] despite the location in the oldest stratum 1 [33] where we may expect dosage compensation to be prevalent, particularly given the recent models predicting that dosage compensation is responsible for evolution of X-Y recombination repression. [34,35] This likely reflects the dosage sensitivity of SlWUS1 that should not be altered by evolving dosage compensation system.…”

Section: Evolution Of Gynoecium Suppression In S Latifolia Via Two Ge...mentioning

confidence: 99%

Evolution of sex‐determination in dioecious plants: From active Y to X/A balance?

Kazama,

Kobayashi,

Filatov

2023

BioEssays

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Sex chromosomes in plants have been known for a century, but only recently have we begun to understand the mechanisms behind sex determination in dioecious plants. Here, we discuss evolution of sex determination, focusing on Silene latifolia, where evolution of separate sexes is consistent with the classic “two mutations” model—a loss of function male sterility mutation and a gain of function gynoecium suppression mutation, which turned an ancestral hermaphroditic population into separate males and females. Interestingly, the gynoecium suppression function in S. latifolia evolved via loss of function in at least two sex‐linked genes and works via gene dosage balance between sex‐linked, and autosomal genes. This system resembles X/A‐ratio‐based sex determination systems in Drosophila and Rumex, and could represent a steppingstone in the evolution of X/A‐ratio‐based sex determination from an active Y system.

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The origin and evolution of sex chromosomes, revealed by sequencing of the Silene latifolia female genome

Cited by 21 publications

References 96 publications

Seed shape and size of Silene latifolia, differences between sexes, and influence of the parental genome in hybrids with Silene dioica

Seed shape and size of Silene latifolia, differences between sexes, and influence of the parental genome in hybrids with Silene dioica

Why should we study plant sex chromosomes?

Evolution of sex‐determination in dioecious plants: From active Y to X/A balance?

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