MYB transcription factor gene involved in sex determination in Asparagus officinalis

Abstract

Dioecy is a plant mating system in which individuals of a species are either male or female. Although many flowering plants evolved independently from hermaphroditism to dioecy, the molecular mechanism underlying this transition remains largely unknown. Sex determination in the dioecious plant Asparagus officinalis is controlled by X and Y chromosomes; the male and female karyotypes are XY and XX, respectively. Transcriptome analysis of A. officinalis buds showed that a MYB-like gene, Male Specific Expression 1 (MSE1), is specifically expressed in males. MSE1 exhibits tight linkage with the Y chromosome, specific expression in early anther development and loss of function on the X chromosome. Knockout of the MSE1 orthologue in Arabidopsis induces male sterility. Thus, MSE1 acts in sex determination in A. officinalis.

Sex Determination by Two Y-Linked Genes in Garden Asparagus

“…There is no evidence of repeated inversions leading to the formation of strata on the asparagus Y chromosome ( Figure 1E), as has been inferred for older and more degenerate plant sex chromosomes like Carica papaya (Wang et al, 2012) and Silene latifolia (Bergero et al, 2008;Kazama et al, 2016). However, the finding that aspTDF1 is not sex-linked in all dioecious Asparagus species (Harkess et al 2017, Murase et al, 2017Tsugama et al, 2017) indicates that gene content in the sexdetermination region, and indeed the molecular basis of sex determination, are evolving in the genus.…”

“…An additional spontaneous frameshift mutant verified SOFF as the female-suppressor. As predicted by the two-gene models for a dominant M-locus on the Y-chromosome (Westergaard, 1958;Charlesworth, 2018;Marks, 1973;Charlesworth and Charlesworth, 1978), a homolog of DEFECTIVE IN TAPETAL DEVELOPMENT AND FUNCTION1 (TDF1), encoding an R2R3 MYB transcription factor for which knockouts in Arabidopsis thaliana are male-sterile (Zhu et al, 2008), was identified in the non-recombining Y-specific region of the asparagus Y-chromosome (Harkess et al, 2017) and found to be male-specific across several, but not all, dioecious Asparagus species (Murase et al, 2017;Tsugama et al, 2017). The garden asparagus aspTDF1 was able to rescue the tdf1 mutation in Arabidopsis (Murase et al, 2017;Tsugama et al, 2017), but the function of aspTDF1 has not been validated in…”

“…Though long hypothesized in several species, we show functional evidence that the evolution of two sex determination genes on a Y chromosome can determine plant sex, supporting the long-standing hypothesis posited by Mogens Westergaard (Westergaard, 1958) and Brian and Deborah Charlesworth (Charlesworth and Charlesworth, 1978). Earlier work (Harkess et al 2017;Murase et al, 2017;Tsugama et al, 2017) indicated that aspTDF1 was not Y-specific in the last common ancestor of all dioecious Asparagus species. Together these findings suggest that whereas aspTDF1 in necessary for male function, either there was another ancestral male promoter gene responsible for the origin of dioecy in the genus, or there were multiple origins of dioecy through linkage of alternative male promoting genes to SOFF in dioecious lineages with autosomal aspTDF1 genes.…”

Sex is determined by XY chromosomes across the radiation of dioeciousNepenthespitcher plants

“…Such a deletion of DYT1 from the X chromosome would constitute a recessive male‐sterility mutation, as required early in the evolution of dioecy for the transition from a hermaphroditic to a gynodioecious mating system (Charlesworth and Charlesworth ). It is notable that in Arabidopsis , DYT1 directly regulates the expression of TDF1 (Gu et al ), a gene that in dioecious asparagus is essential for male fertility and, like DYT1 in Nepenthes , is located in the MSY (Harkess et al ; Murase et al ). Apparently, this pollen development pathway was involved twice independently in the evolution of angiosperm XY chromosomes, and possibly in the transition to dioecy.…”

“…Only 5–6% of species have female and male flowers on separate individuals (dioecy), but the evolutionary transition to dioecy may have occurred as many as 800 times independently in angiosperms (Renner ). In contrast to outcrossing–selfing transitions due to loss of self‐incompatbility, for some of which the underlying genetic changes have recently been uncovered (e.g., Shimizu and Tsuchimatsu ), relatively little is known about the genes involved in transitions from hermaphroditism to dioecy and in sex determination in plants (Charlesworth ), although sex‐determining genes have been identified in three dioecious plant species: persimmon (Diospyros lotus , Akagi et al ), Asparagus officinalis (Harkess et al ; Murase et al ), and kiwifruit ( Actinidia , Akagi et al ). The main hypotheses for the evolution of separate sexes in plants involve a combination of trade‐offs between the sex functions, plus disadvantage of inbreeding (Charlesworth and Charlesworth ).…”