TY - JOUR
T1 - Regulator of Awn Elongation 3, an E3 ubiquitin ligase, is responsible for loss of awns during African rice domestication
AU - Bessho-Uehara, Kanako
AU - Masuda, Kengo
AU - Wang, Diane R.
AU - Angeles-Shim, Rosalyn B.
AU - Obara, Keisuke
AU - Nagai, Keisuke
AU - Murase, Riri
AU - Aoki, Shin Ichiro
AU - Furuta, Tomoyuki
AU - Miura, Kotaro
AU - Wu, Jianzhong
AU - Yamagata, Yoshiyuki
AU - Yasui, Hideshi
AU - Kantar, Michael B.
AU - Yoshimura, Atsushi
AU - Kamura, Takumi
AU - McCouch, Susan R.
AU - Ashikari, Motoyuki
N1 - Funding Information:
This work was funded by JSPS KAKENHI (grant no. JP 20H05912 to M.A., 15J03740 and 20K22644 to K.B.-U.), the SATREPS program (no. JPMJSA1706 to M.A.) of the JST and JICA, JST-Mirai Program Grant Number JPMJMI20C8, and the US NSF (grant no. 1444511 to S.R.M.). We thank the National Bio-Resource Project (NBRP), Honda Research Institute Japan Co., Ltd., Mr. Tomonori Takashi and Dr. Kazuyuki Doi for providing the inbred lines. We gratefully acknowledge Yuxin Shi and Francisco Agosto Perez for technical assistance in integrating the resequencing datasets.
Funding Information:
ACKNOWLEDGMENTS. This work was funded by JSPS KAKENHI (grant no. JP 20H05912 to M.A., 15J03740 and 20K22644 to K.B.-U.), the SATREPS program (no. JPMJSA1706 to M.A.) of the JST and JICA, JST-Mirai Program Grant Number JPMJMI20C8, and the US NSF (grant no. 1444511 to S.R.M.). We thank the National Bio-Resource Project (NBRP), Honda Research Institute Japan Co., Ltd., Mr. Tomonori Takashi and Dr. Kazuyuki Doi for providing the inbred lines. We gratefully acknowledge Yuxin Shi and Francisco Agosto Perez for technical assistance in integrating the resequencing datasets.
Publisher Copyright:
Copyright © 2023 the Author(s).
PY - 2023/1/24
Y1 - 2023/1/24
N2 - Two species of rice have been independently domesticated from different ancestral wild species in Asia and Africa. Comparison of mutations that underlie phenotypic and physiological alterations associated with domestication traits in these species gives insights into the domestication history of rice in both regions. Asian cultivated rice, Oryza sativa, and African cultivated rice, Oryza glaberrima, have been modified and improved for common traits beneficial for humans, including erect plant architecture, nonshattering seeds, nonpigmented pericarp, and lack of awns. Independent mutations in orthologous genes associated with these traits have been documented in the two cultivated species. Contrary to this prevailing model, selection for awnlessness targeted different genes in O. sativa and O. glaberrima. We identify Regulator of Awn Elongation 3 (RAE3) a gene that encodes an E3 ubiquitin ligase and is responsible for the awnless phenotype only in O. glaberrima. A 48-bp deletion may disrupt the substrate recognition domain in RAE3 and diminish awn elongation. Sequencing analysis demonstrated low nucleotide diversity in a ~600-kb region around the derived rae3 allele on chromosome 6 in O. glaberrima compared with its wild progenitor. Identification of RAE3 sheds light on the molecular mechanism underlying awn development and provides an example of how selection on different genes can confer the same domestication phenotype in Asian and African rice.
AB - Two species of rice have been independently domesticated from different ancestral wild species in Asia and Africa. Comparison of mutations that underlie phenotypic and physiological alterations associated with domestication traits in these species gives insights into the domestication history of rice in both regions. Asian cultivated rice, Oryza sativa, and African cultivated rice, Oryza glaberrima, have been modified and improved for common traits beneficial for humans, including erect plant architecture, nonshattering seeds, nonpigmented pericarp, and lack of awns. Independent mutations in orthologous genes associated with these traits have been documented in the two cultivated species. Contrary to this prevailing model, selection for awnlessness targeted different genes in O. sativa and O. glaberrima. We identify Regulator of Awn Elongation 3 (RAE3) a gene that encodes an E3 ubiquitin ligase and is responsible for the awnless phenotype only in O. glaberrima. A 48-bp deletion may disrupt the substrate recognition domain in RAE3 and diminish awn elongation. Sequencing analysis demonstrated low nucleotide diversity in a ~600-kb region around the derived rae3 allele on chromosome 6 in O. glaberrima compared with its wild progenitor. Identification of RAE3 sheds light on the molecular mechanism underlying awn development and provides an example of how selection on different genes can confer the same domestication phenotype in Asian and African rice.
KW - African rice
KW - awn
KW - convergent evolution
KW - domestication
KW - E3 ubiquitin ligase
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U2 - 10.1073/pnas.2207105120
DO - 10.1073/pnas.2207105120
M3 - Article
C2 - 36649409
AN - SCOPUS:85146412078
SN - 0027-8424
VL - 120
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 4
M1 - e2207105120
ER -