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

Abstract

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

Chromosome-scale assembly of the genome ofSalix dunniireveals a male-heterogametic sex determination system on chromosome 7

“…These data support the view (Yang et al 2020) that sex-determining loci have probably evolved independently within the genus Salix, as well as separately in poplars. This is consistent with evidence that, despite dioecy being found in almost all willows, the W-linked sequences of some species began diverging within the genus (Pucholt et al 2017;Zhou et al 2020).…”

“…Such a gene has been suggested to be the sex determining gene of all Salicaceae (Yang et al 2020), based on the finding of ARR17-like genes in the W-linked regions of S. viminalis and S.…”

“…tremula (Müller et al 2020;Xue et al 2020). In two species of the Salix Chamaetia-Vetrix clade (S. purpurea and S. viminalis), a similar gene has been detected in the W-linked region of chromosome 15, and a partial and non-functional copy was found in the Z-linked region of the S. purpurea chromosome 15 (Almeida et al 2020;Yang et al 2020;Zhou et al 2020).…”

Sex determination through X-Y heterogamety inSalix nigra

“…We identified a new sex-linked region (SLR) in willows that exhibits XY heterogamety on chromosome 7 in Salix nigra. This result establishes that sex chromosomes in Salix have undergone changes in the genomic location as well as (Geraldes et al, 2015;Pakull et al, 2011;Pakull et al, 2009) and P. alba exhibiting ZW sex determination (Paolucci et al, 2010) and a third SLR on chromosome 14 with XY heterogamety in P. euphratica (Yang et al, 2020). (Zhou et al, 2020) and the 100kb SLR in P. trichocarpa (Geraldes et al, 2015).…”

“…This set of 16 genes included a homolog to cytokinin oxidase (AT5G56970.1), a possible candidate for presence in the metabolic pathway controlling sex determination (Feng et al, 2020). (Charlesworth, 2016b;Yang et al, 2020;Zhou et al, 2020) suggests caution when interpreting too much from homology across this entire interval.…”