Two Y-chromosome-encoded genes determine sex in kiwifruit

Akagi, Takashi; Pilkington, Sarah M.; Varkonyi‐Gasic, Erika; Henry, Isabelle; Sugano, Shigeo S.; Sonoda, Minori; Firl, Alana; McNeilage, M.A.; Douglas, Mikaela J.; Wang, Tianchi; Rebstock, Ria; Voogd, Charlotte; Datson, P. M.; Allan, Andrew C.; Beppu, Kenji; Kataoka, Isao; Tao, Ryutaro

doi:10.1038/s41477-019-0489-6

Cited by 174 publications

(153 citation statements)

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“…ARR proteins are one of the final targets of the cytokinin signaling system, which is known to play important roles in flower development and floral sex differentiation in several plant species [92]. In particular, a C-type cytokinin response regulator that acts as a dominant suppressor of carpel development, resulting in female lethality, was specifically identified as the possible male sex-determining gene in kiwifruit [93,94], and a regulator of the cytokinin metabolism is also a major potential candidate for sex determination in grapevine [89,95]. Interestingly, within the Salicaceae family, sex-linked polymorphisms in the poplar genome map to a small region on chromosome 19 that includes ARR17 [43,96].…”

Section: Candidate Sex Determination Genes In S Viminalismentioning

confidence: 99%

Genome assembly of the basket willow, Salix viminalis, reveals earliest stages of sex chromosome expansion

et al. 2020

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Background: Sex chromosomes have evolved independently multiple times in eukaryotes and are therefore considered a prime example of convergent genome evolution. Sex chromosomes are known to emerge after recombination is halted between a homologous pair of chromosomes, and this leads to a range of non-adaptive modifications causing gradual degeneration and gene loss on the sex-limited chromosome. However, the proximal causes of recombination suppression and the pace at which degeneration subsequently occurs remain unclear. Results: Here, we use long-and short-read single-molecule sequencing approaches to assemble and annotate a draft genome of the basket willow, Salix viminalis, a species with a female heterogametic system at the earliest stages of sex chromosome emergence. Our single-molecule approach allowed us to phase the emerging Z and W haplotypes in a female, and we detected very low levels of Z/W single-nucleotide divergence in the non-recombining region. Linked-read sequencing of the same female and an additional male (ZZ) revealed the presence of two evolutionary strata supported by both divergence between the Z and W haplotypes and by haplotype phylogenetic trees. Gene order is still largely conserved between the Z and W homologs, although the W-linked region contains genes involved in cytokinin signaling regulation that are not syntenic with the Z homolog. Furthermore, we find no support across multiple lines of evidence for inversions, which have long been assumed to halt recombination between the sex chromosomes. Conclusions: Our data suggest that selection against recombination is a more gradual process at the earliest stages of sex chromosome formation than would be expected from an inversion and may result instead from the accumulation of transposable elements. Our results present a cohesive understanding of the earliest genomic consequences of recombination suppression as well as valuable insights into the initial stages of sex chromosome formation and regulation of sex differentiation.

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Section: Candidate Sex Determination Genes In S Viminalismentioning

confidence: 99%

Genome assembly of the basket willow, Salix viminalis, reveals earliest stages of sex chromosome expansion

et al. 2020

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“…Over the past decade, impressive progress has been made in unraveling the genetic basis of sex determination in several dioecious plants and the evolutionary history of their sex chromosomes, including papaya (Wang et al , 2012), persimmon (Akagi et al , 2014), asparagus (Harkess et al , 2017), strawberry (Tennessen et al , 2018), date palm (Torres et al , 2018) and kiwifruit (Akagi et al , 2018, 2019). Consistent with the independent origins of sex chromosomes, the sex determination genes identified in these species differ from each another, although most of them function in similar hormone response pathways (Feng et al , 2020).…”

Section: Introductionmentioning

confidence: 99%

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

Yang

Zhang

Wang

et al. 2020

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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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“…This gene is homologous to the DEFECTIVE IN TAPETAL DEVELOPMENT AND FUNCTION 1 (TDF1) or MYB35 gene in Arabidopsis, and it is located in the asparagus Y chromosome [38, 41]. In kiwifruit, a fasciclin-like gene, called Friendly Boy ( FrBy ) has been identified as a sex- determination gene [39]. This gene is strongly expressed in tapetal cells at early anther developmental stages, which is believed to contribute to tapetum degradation after programmed cell death (PCD) and it is also located on the kiwifruit Y chromosome [39].…”

Section: Discussionmentioning

confidence: 99%

“…In kiwifruit, a fasciclin-like gene, called Friendly Boy ( FrBy ) has been identified as a sex- determination gene [39]. This gene is strongly expressed in tapetal cells at early anther developmental stages, which is believed to contribute to tapetum degradation after programmed cell death (PCD) and it is also located on the kiwifruit Y chromosome [39]. Despite the male and hermaphrodite biased expression pattern observed for the CpMS1 gene, this gene was found to be autosomal, not Y specific (present in male or hermaphrodite Y chromosomes), and therefore it cannot be considered as the candidate Y specific gene for male sex determination in papaya.…”

Section: Discussionmentioning

confidence: 99%

Differential gene expression among three sex types reveals a MALE STERILITY 1 (CpMS1) for sex differentiation in papaya

et al. 2019

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BackgroundCarica papaya is a trioecious plant species with a genetic sex-determination system defined by sex chromosomes. Under unfavorable environmental conditions male and hermaphrodite exhibit sex-reversal. Previous genomic research revealed few candidate genes for sex differentiation in this species. Nevertheless, more analysis is still needed to identify the mechanism responsible for sex flower organ development in papaya.ResultsThe aim of this study was to identify differentially expressed genes among male, female and hermaphrodite flowers in papaya during early (pre-meiosis) and later (post-meiosis) stages of flower development. RNA-seq was used to evaluate the expression of differentially expressed genes and RT-qPCR was used to verify the results. Putative functions of these genes were analyzed based on their homology with orthologs in other plant species and their expression patterns. We identified a Male Sterility 1 gene (CpMS1) highly up-regulated in male and hermaphrodite flower buds compared to female flower buds, which expresses in small male flower buds (3–8 mm), and that might be playing an important role in male flower organ development due to its homology to MS1 genes previously identified in other plants. This is the first study in which the sex-biased expression of genes related to tapetum development in the anther developmental pathway is being reported in papaya. Besides important transcription factors related to flower organ development and flowering time regulation, we identified differential expression of genes that are known to participate in ABA, ROS and auxin signaling pathways (ABA-8-hydroxylases, AIL5, UPBEAT 1, VAN3-binding protein).ConclusionsCpMS1 was expressed in papaya male and hermaphrodite flowers at early stages, suggesting that this gene might participate in male flower organ development processes, nevertheless, this gene cannot be considered a sex-determination gene. Due to its homology with other plant MS1 proteins and its expression pattern, we hypothesize that this gene participates in anther development processes, like tapetum and pollen development, downstream gender specification. Further gene functional characterization studies in papaya are required to confirm this hypothesis. The role of ABA and ROS signaling pathways in papaya flower development needs to be further explored as well.

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Two Y-chromosome-encoded genes determine sex in kiwifruit

Cited by 174 publications

References 48 publications

Genome assembly of the basket willow, Salix viminalis, reveals earliest stages of sex chromosome expansion

Genome assembly of the basket willow, Salix viminalis, reveals earliest stages of sex chromosome expansion

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

Differential gene expression among three sex types reveals a MALE STERILITY 1 (CpMS1) for sex differentiation in papaya

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