SEX and SILENE

Red and White campion (Silene dioica and S. latifolia) light up our roadsides in May and June with splashes of magenta and white flowers. A special feature of both plants is they are dioecious, i.e. individuals are either male or female. Only about 6% of plants are dioecious, and of these only 178 possess sex chromosomes, defined as chromosomes with regions that carry the genes controlling the sexes of individuals, and which do not recombine. The two campions are members of this select group of plants, with males being XY and females XX – just as in humans.

Red campions flowering in a hedgerow by St Andrews, Fife, in late May, 2020. Inset: Cross-sections of male (left) and female (right) flowers. (Photo: R. J Abbott)

In an article just out in the New Phytologist, Baránková et al. advertise a database (http://www.sexchrom.csic.es) listing all 178 species together with their chromosome numbers, genome sizes, ploidy levels, sex determination mechanisms, and presence of homomorphic or heteromorphic sex chromosomes. For ten taxa, including Silene latifolia, more detailed information is provided on sex-linked genes within the sex chromosomes.


Left: White campion (Photo: R. J. Abbott).  Right: Chromosomes of female and male individuals of White campion with sex chromosomes marked (Photo: B. Vyskot and M. Soukupová, in Baránková et al. 2020).

A major contribution to our current understanding of the evolution of sex determination and sex chromosomes in White campion has been made by Deborah Charlesworth and her colleagues at Edinburgh University, together with former members of her research group, and researchers elsewhere.  Based on their combined efforts, 15 sex-linked genes, i.e. genes present in either one of the sex chromosomes, have been identified in S. latifolia, some of which have degenerated or have no copy on the Y chromosome. In addition, 19 genes have been discovered that exhibit sex-biased expression, i.e. are expressed differentially in males and females. These can be sex-linked or located on other chromosomes. By comparing differences in DNA sequences of homologous sex-linked genes, it is estimated that the X and Y chromosomes of S. latifolia originated between 6-11 million years ago. This means they are remarkably young compared with their counterparts in mammals (~160 million years old) and birds (~100 million years old) and, therefore, ideal for studying sex chromosome evolution. It also means they originated in Silene before S. dioica and S. latifolia diverged from each other, ~0.25-0.5 million years ago.


Mixed stand of Red and White campions and hybrids along a road verge at Leuchars, Fife.
(Photo: R. J. Abbott, 2 June, 2020)

In addition to dioecious species, there are hermaphrodite and gynodioecious species (species composed of females and hermaphrodite individuals) of Silene, and it is thought that gynodioecy represents an intermediate step in the evolution of dioecy from hermaphroditism. Surprisingly, dioecy has evolved twice in the genus. In the lineage containing Red and White campions, the sex chromosomes are heteromorphic, Y being larger than X, whereas in a second lineage, in which dioecy originated independently, the sex chromosomes are homomorphic (identical in size). 

Another interesting feature of Silene dioica and S. latifolia is that they hybridize wherever they come into contact (usually in disturbed sites), but this does not lead to extensive gene exchange away from where they hybridize. Sophie Karrenberg, Alex Widmer and colleagues have established that in Switzerland a number of barriers exist between the species to prevent gene exchange, of which ecological divergence is of prime importance. Red campions like colder and wetter habitats, while White campions prefer warmer and more disturbed habitats. Hybrids tend not to do well in either type of habitat, while migrants of one species do poorly in the habitat of the other species.

References

Baránková S, Pascual-Díaz JP, Sultana N, Alonso-Lifante MP, Balant M, Barros K, D’Ambrosio U, Malinská H, Peska V, Lorenzo IP, Kovarik A, Vyskot B, Janousek B, Garcia S. (2020). Sex-chrom, a database on plant sex chromosomes. New Phytologist (Early view). (https://nph.onlinelibrary.wiley.com/doi/epdf/10.1111/nph.16635)

Bernasconi, G, Antonovics J, Biere A, Charlesworth D, Delph LF, Filatov D, Giraud T, Hood ME, Marais GAB, McCauley D, Pannell JR, Shykoff JA, Vyskot B, Wolfe LM, Widmer A. (2009). Silene as a model system in ecology and evolution. Heredity 103: 5-14.  (https://www.nature.com/articles/hdy200934)

Charlesworth D. (2016). Plant sex chromosomes. Annual Review of Plant Biology 67: 397-420.

(https://www.annualreviews.org/doi/pdf/10.1146/annurev-arplant-043015-111911)

Charlesworth D (2019) Young sex chromosomes in plants and animals. New Phytologist 224: 1095-1107.

Favre A, Widmer A, Karrenberg S. (2017). Differential adaptation drives ecological speciation in campions (Silene): evidence from a multi-site transplant experiment. New Phytologist 213: 1487-1499.  (https://nph.onlinelibrary.wiley.com/doi/epdf/10.1111/nph.14202)

Karrenberg S, Liu X, Hallander E, Favre A, Herforth-Rahmé J, Widmer A. (2019). Ecological divergence plays and important role in strong but complex reproductive isolation in campions (Silene). Evolution 73: 245-261.

Richard Abbott

University of St Andrews

rja ‘at’ st-andrews.ac.uk 

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