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 language | English |
|---|---|
| Pages (from-to) | 801-809 |
| Number of pages | 9 |
| Journal | Nature Plants |
| Volume | 5 |
| Issue number | 8 |
| DOIs | |
| Publication status | Published - Aug 1 2019 |
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ASJC Scopus subject areas
- Plant Science
Cite this
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 journal › Letter
}
TY - JOUR
T1 - Two Y-chromosome-encoded genes determine sex in kiwifruit
AU - Akagi, Takashi
AU - Pilkington, Sarah M.
AU - Varkonyi-Gasic, Erika
AU - Henry, Isabelle M.
AU - Sugano, Shigeo S.
AU - Sonoda, Minori
AU - Firl, Alana
AU - McNeilage, Mark A.
AU - Douglas, Mikaela J.
AU - Wang, Tianchi
AU - Rebstock, Ria
AU - Voogd, Charlotte
AU - Datson, Paul
AU - Allan, Andrew C.
AU - Beppu, Kenji
AU - Kataoka, Ikuo
AU - Tao, Ryutaro
PY - 2019/8/1
Y1 - 2019/8/1
N2 - 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.
AB - 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.
UR - http://www.scopus.com/inward/record.url?scp=85070235757&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85070235757&partnerID=8YFLogxK
U2 - 10.1038/s41477-019-0489-6
DO - 10.1038/s41477-019-0489-6
M3 - Letter
C2 - 31383971
AN - SCOPUS:85070235757
VL - 5
SP - 801
EP - 809
JO - Nature Plants
JF - Nature Plants
SN - 2055-026X
IS - 8
ER -