Loss of function at RAE2, a previously unidentified EPFL, is required for awnlessness in cultivated Asian rice

Kanako Bessho-Uehara, Diane R. Wang, Tomoyuki Furuta, Anzu Minami, Keisuke Nagai, Rico Gamuyao, Kenji Asano, Rosalyn B. Angeles-Shim, Yoshihiro Shimizu, Madoka Ayano, Norio Komeda, Kazuyuki Doi, Kotaro Miura, Yosuke Toda, Toshinori Kinoshita, Satohiro Okuda, Tetsuya Higashiyama, Mika Nomoto, Yasuomi Tada, Hidefumi ShinoharaYoshikatsu Matsubayashi, Anthony Greenberg, Jianzhong Wu, Hideshi Yasui, Atsushi Yoshimurah, Hitoshi Mori, Susan R. McCouch, Motoyuki Ashikari

Research output: Contribution to journalArticle

29 Citations (Scopus)

Abstract

Domestication of crops based on artificial selection has contributed numerous beneficial traits for agriculture. Wild characteristics such as red pericarp and seed shattering were lost in both Asian (Oryza sativa) and African (Oryza glaberrima) cultivated rice species as a result of human selection on common genes. Awnedness, in contrast, is a trait that has been lost in both cultivated species due to selection on different sets of genes. In a previous report, we revealed that at least three loci regulate awn development in rice; however, the molecular mechanism underlying awnlessness remains unknown. Here we isolate and characterize a previously unidentified EPIDERMAL PATTERNING FACTOR-LIKE (EPFL) family member named REGULATOR OF AWN ELONGATION 2 (RAE2) and identify one of its requisite processing enzymes, SUBTILISIN-LIKE PROTEASE 1 (SLP1). The RAE2 precursor is specifically cleaved by SLP1 in the rice spikelet, where the mature RAE2 peptide subsequently induces awn elongation. Analysis of RAE2 sequence diversity identified a highly variable GC-rich region harboring multiple independent mutations underlying protein-length variation that disrupt the function of the RAE2 protein and condition the awnless phenotype in Asian rice. Cultivated African rice, on the other hand, retained the functional RAE2 allele despite its awnless phenotype. Our findings illuminate the molecular function of RAE2 in awn development and shed light on the independent domestication histories of Asian and African cultivated rice.

Original languageEnglish
Pages (from-to)8969-8974
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume113
Issue number32
DOIs
Publication statusPublished - Aug 9 2016
Externally publishedYes

Fingerprint

Subtilisin
Peptide Hydrolases
GC Rich Sequence
Phenotype
Oryza
Agriculture
Genes
Seeds
Proteins
Alleles
Peptides
Mutation
Enzymes
Domestication

Keywords

  • Awn|
  • Convergent evolution
  • Parallel domestication
  • Rice
  • Signal peptide

ASJC Scopus subject areas

  • General

Cite this

Loss of function at RAE2, a previously unidentified EPFL, is required for awnlessness in cultivated Asian rice. / Bessho-Uehara, Kanako; Wang, Diane R.; Furuta, Tomoyuki; Minami, Anzu; Nagai, Keisuke; Gamuyao, Rico; Asano, Kenji; Angeles-Shim, Rosalyn B.; Shimizu, Yoshihiro; Ayano, Madoka; Komeda, Norio; Doi, Kazuyuki; Miura, Kotaro; Toda, Yosuke; Kinoshita, Toshinori; Okuda, Satohiro; Higashiyama, Tetsuya; Nomoto, Mika; Tada, Yasuomi; Shinohara, Hidefumi; Matsubayashi, Yoshikatsu; Greenberg, Anthony; Wu, Jianzhong; Yasui, Hideshi; Yoshimurah, Atsushi; Mori, Hitoshi; McCouch, Susan R.; Ashikari, Motoyuki.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 113, No. 32, 09.08.2016, p. 8969-8974.

Research output: Contribution to journalArticle

Bessho-Uehara, K, Wang, DR, Furuta, T, Minami, A, Nagai, K, Gamuyao, R, Asano, K, Angeles-Shim, RB, Shimizu, Y, Ayano, M, Komeda, N, Doi, K, Miura, K, Toda, Y, Kinoshita, T, Okuda, S, Higashiyama, T, Nomoto, M, Tada, Y, Shinohara, H, Matsubayashi, Y, Greenberg, A, Wu, J, Yasui, H, Yoshimurah, A, Mori, H, McCouch, SR & Ashikari, M 2016, 'Loss of function at RAE2, a previously unidentified EPFL, is required for awnlessness in cultivated Asian rice', Proceedings of the National Academy of Sciences of the United States of America, vol. 113, no. 32, pp. 8969-8974. https://doi.org/10.1073/pnas.1604849113
Bessho-Uehara, Kanako ; Wang, Diane R. ; Furuta, Tomoyuki ; Minami, Anzu ; Nagai, Keisuke ; Gamuyao, Rico ; Asano, Kenji ; Angeles-Shim, Rosalyn B. ; Shimizu, Yoshihiro ; Ayano, Madoka ; Komeda, Norio ; Doi, Kazuyuki ; Miura, Kotaro ; Toda, Yosuke ; Kinoshita, Toshinori ; Okuda, Satohiro ; Higashiyama, Tetsuya ; Nomoto, Mika ; Tada, Yasuomi ; Shinohara, Hidefumi ; Matsubayashi, Yoshikatsu ; Greenberg, Anthony ; Wu, Jianzhong ; Yasui, Hideshi ; Yoshimurah, Atsushi ; Mori, Hitoshi ; McCouch, Susan R. ; Ashikari, Motoyuki. / Loss of function at RAE2, a previously unidentified EPFL, is required for awnlessness in cultivated Asian rice. In: Proceedings of the National Academy of Sciences of the United States of America. 2016 ; Vol. 113, No. 32. pp. 8969-8974.
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AU - Nagai, Keisuke

AU - Gamuyao, Rico

AU - Asano, Kenji

AU - Angeles-Shim, Rosalyn B.

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AU - Greenberg, Anthony

AU - Wu, Jianzhong

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