Two Y-chromosome-encoded genes determine sex in kiwifruit

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

Research output: Contribution to journalLetter

5 Citations (Scopus)

Abstract

Dioecy, the presence of male and female individuals, has evolved independently in multiple flowering plant lineages1–3. Although theoretical models for the evolution of dioecy, such as the ‘two-mutations’ model, are well established4,5, little is known about the specific genes determining sex and their evolutionary history3. Kiwifruit, a major tree crop consumed worldwide, is a dioecious species. In kiwifruit we previously identified a Y-encoded sex-determinant candidate gene acting as the suppressor of feminization (SuF), named Shy Girl (SyGI)6. Here, we identify a second Y-encoded sex-determinant that we named Friendly Boy (FrBy), which exhibits strong expression in tapetal cells. Gene-editing and complementation analyses in Arabidopsis thaliana and Nicotiana tabacum indicated that FrBy acts for the maintenance of male (M) functions, independently of SyGI, and that these functions are conserved across angiosperm species. We further characterized the genomic architecture of the small (<1 megabase pairs (Mb)) male-specific region of the Y chromosome (MSY), which harbours only two genes expressed extensively in developing gynoecia and androecia, respectively: SyGI and FrBy. Re-sequencing of the genome of a natural hermaphrodite kiwifruit revealed that this individual is genetically male but carries deletion(s) of parts of the Y chromosome, including SyGI. Additionally, expression of FrBy in female kiwifruit resulted in hermaphrodite plants. These results clearly indicate that Y-encoded SyGI and FrBy act independently as the SuF and M factors in kiwifruit, respectively, and provide insight into not only the evolutionary path leading to a two-factor sex-determination system, but also a new breeding approach for dioecious species.

Original languageEnglish
Pages (from-to)801-809
Number of pages9
JournalNature Plants
Volume5
Issue number8
DOIs
Publication statusPublished - Aug 1 2019

Fingerprint

kiwifruit
Y chromosome
gender
feminization
dioecy
genes
Angiospermae
androecium
gynoecium
Nicotiana tabacum
Arabidopsis thaliana
mutation
genomics
genome
breeding
crops
cells

ASJC Scopus subject areas

  • Plant Science

Cite this

Akagi, T., Pilkington, S. M., Varkonyi-Gasic, E., Henry, I. M., Sugano, S. S., Sonoda, M., ... Tao, R. (2019). Two Y-chromosome-encoded genes determine sex in kiwifruit. Nature Plants, 5(8), 801-809. https://doi.org/10.1038/s41477-019-0489-6

Two Y-chromosome-encoded genes determine sex in kiwifruit. / Akagi, Takashi; Pilkington, Sarah M.; Varkonyi-Gasic, Erika; Henry, Isabelle M.; Sugano, Shigeo S.; Sonoda, Minori; Firl, Alana; McNeilage, Mark A.; Douglas, Mikaela J.; Wang, Tianchi; Rebstock, Ria; Voogd, Charlotte; Datson, Paul; Allan, Andrew C.; Beppu, Kenji; Kataoka, Ikuo; Tao, Ryutaro.

In: Nature Plants, Vol. 5, No. 8, 01.08.2019, p. 801-809.

Research output: Contribution to journalLetter

Akagi, T, Pilkington, SM, Varkonyi-Gasic, E, Henry, IM, Sugano, SS, Sonoda, M, Firl, A, McNeilage, MA, Douglas, MJ, Wang, T, Rebstock, R, Voogd, C, Datson, P, Allan, AC, Beppu, K, Kataoka, I & Tao, R 2019, 'Two Y-chromosome-encoded genes determine sex in kiwifruit', Nature Plants, vol. 5, no. 8, pp. 801-809. https://doi.org/10.1038/s41477-019-0489-6
Akagi T, Pilkington SM, Varkonyi-Gasic E, Henry IM, Sugano SS, Sonoda M et al. Two Y-chromosome-encoded genes determine sex in kiwifruit. Nature Plants. 2019 Aug 1;5(8):801-809. https://doi.org/10.1038/s41477-019-0489-6
Akagi, Takashi ; Pilkington, Sarah M. ; Varkonyi-Gasic, Erika ; Henry, Isabelle M. ; Sugano, Shigeo S. ; Sonoda, Minori ; Firl, Alana ; McNeilage, Mark A. ; Douglas, Mikaela J. ; Wang, Tianchi ; Rebstock, Ria ; Voogd, Charlotte ; Datson, Paul ; Allan, Andrew C. ; Beppu, Kenji ; Kataoka, Ikuo ; Tao, Ryutaro. / Two Y-chromosome-encoded genes determine sex in kiwifruit. In: Nature Plants. 2019 ; Vol. 5, No. 8. pp. 801-809.
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abstract = "Dioecy, the presence of male and female individuals, has evolved independently in multiple flowering plant lineages1–3. Although theoretical models for the evolution of dioecy, such as the ‘two-mutations’ model, are well established4,5, little is known about the specific genes determining sex and their evolutionary history3. Kiwifruit, a major tree crop consumed worldwide, is a dioecious species. In kiwifruit we previously identified a Y-encoded sex-determinant candidate gene acting as the suppressor of feminization (SuF), named Shy Girl (SyGI)6. Here, we identify a second Y-encoded sex-determinant that we named Friendly Boy (FrBy), which exhibits strong expression in tapetal cells. Gene-editing and complementation analyses in Arabidopsis thaliana and Nicotiana tabacum indicated that FrBy acts for the maintenance of male (M) functions, independently of SyGI, and that these functions are conserved across angiosperm species. We further characterized the genomic architecture of the small (<1 megabase pairs (Mb)) male-specific region of the Y chromosome (MSY), which harbours only two genes expressed extensively in developing gynoecia and androecia, respectively: SyGI and FrBy. Re-sequencing of the genome of a natural hermaphrodite kiwifruit revealed that this individual is genetically male but carries deletion(s) of parts of the Y chromosome, including SyGI. Additionally, expression of FrBy in female kiwifruit resulted in hermaphrodite plants. These results clearly indicate that Y-encoded SyGI and FrBy act independently as the SuF and M factors in kiwifruit, respectively, and provide insight into not only the evolutionary path leading to a two-factor sex-determination system, but also a new breeding approach for dioecious species.",
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