title: Loss of function at RAE2, a previously unidentified EPFL, is required for awnlessness in cultivated Asian rice.
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.
authors.affiliation: Bioscience and Biotechnology Center, Nagoya University, Furo-cho, Chikusa, Nagoya, Aichi 464-8601, Japan;
authors.forename: Kanako
authors.initials: K
authors.lastname: Bessho-Uehara
authors.affiliation: Section of Plant Breeding and Genetics, School of Integrated Plant Sciences, Cornell University, Ithaca, NY 14853-1901;
authors.forename: Diane R
authors.initials: DR
authors.lastname: Wang
authors.affiliation: Bioscience and Biotechnology Center, Nagoya University, Furo-cho, Chikusa, Nagoya, Aichi 464-8601, Japan;
authors.forename: Tomoyuki
authors.initials: T
authors.lastname: Furuta
authors.affiliation: Bioscience and Biotechnology Center, Nagoya University, Furo-cho, Chikusa, Nagoya, Aichi 464-8601, Japan;
authors.forename: Anzu
authors.initials: A
authors.lastname: Minami
authors.affiliation: Bioscience and Biotechnology Center, Nagoya University, Furo-cho, Chikusa, Nagoya, Aichi 464-8601, Japan;
authors.forename: Keisuke
authors.initials: K
authors.lastname: Nagai
authors.affiliation: Bioscience and Biotechnology Center, Nagoya University, Furo-cho, Chikusa, Nagoya, Aichi 464-8601, Japan;
authors.forename: Rico
authors.initials: R
authors.lastname: Gamuyao
authors.affiliation: Bioscience and Biotechnology Center, Nagoya University, Furo-cho, Chikusa, Nagoya, Aichi 464-8601, Japan;
authors.forename: Kenji
authors.initials: K
authors.lastname: Asano
authors.affiliation: Bioscience and Biotechnology Center, Nagoya University, Furo-cho, Chikusa, Nagoya, Aichi 464-8601, Japan;
authors.forename: Rosalyn B
authors.initials: RB
authors.lastname: Angeles-Shim
authors.affiliation: Bioscience and Biotechnology Center, Nagoya University, Furo-cho, Chikusa, Nagoya, Aichi 464-8601, Japan;
authors.forename: Yoshihiro
authors.initials: Y
authors.lastname: Shimizu
authors.affiliation: Bioscience and Biotechnology Center, Nagoya University, Furo-cho, Chikusa, Nagoya, Aichi 464-8601, Japan;
authors.forename: Madoka
authors.initials: M
authors.lastname: Ayano
authors.affiliation: Bioscience and Biotechnology Center, Nagoya University, Furo-cho, Chikusa, Nagoya, Aichi 464-8601, Japan;
authors.forename: Norio
authors.initials: N
authors.lastname: Komeda
authors.affiliation: Graduate School of Agriculture, Nagoya University, Furo-cho, Chikusa, Nagoya, Aichi 464-8601, Japan;
authors.forename: Kazuyuki
authors.initials: K
authors.lastname: Doi
authors.affiliation: Faculty of Biotechnology, Fukui Prefectural University, 4-1-1 Eiheiji-Town, Fukui 910-1195, Japan;
authors.forename: Kotaro
authors.initials: K
authors.lastname: Miura
authors.affiliation: Institute of Transformative Bio-Molecules, Nagoya University, Furo-cho, Chikusa, Nagoya, Aichi 464-8602, Japan;
authors.forename: Yosuke
authors.initials: Y
authors.lastname: Toda
authors.affiliation: Institute of Transformative Bio-Molecules, Nagoya University, Furo-cho, Chikusa, Nagoya, Aichi 464-8602, Japan;
authors.forename: Toshinori
authors.initials: T
authors.lastname: Kinoshita
authors.affiliation: Institute of Transformative Bio-Molecules, Nagoya University, Furo-cho, Chikusa, Nagoya, Aichi 464-8602, Japan;
authors.forename: Satohiro
authors.initials: S
authors.lastname: Okuda
authors.affiliation: Institute of Transformative Bio-Molecules, Nagoya University, Furo-cho, Chikusa, Nagoya, Aichi 464-8602, Japan;
authors.forename: Tetsuya
authors.initials: T
authors.lastname: Higashiyama
authors.affiliation: Division of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa, Nagoya, Aichi 464-8602, Japan;
authors.forename: Mika
authors.initials: M
authors.lastname: Nomoto
authors.affiliation: Division of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa, Nagoya, Aichi 464-8602, Japan;
authors.forename: Yasuomi
authors.initials: Y
authors.lastname: Tada
authors.affiliation: Division of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa, Nagoya, Aichi 464-8602, Japan;
authors.forename: Hidefumi
authors.initials: H
authors.lastname: Shinohara
authors.affiliation: Division of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa, Nagoya, Aichi 464-8602, Japan;
authors.forename: Yoshikatsu
authors.initials: Y
authors.lastname: Matsubayashi
authors.affiliation: Section of Plant Breeding and Genetics, School of Integrated Plant Sciences, Cornell University, Ithaca, NY 14853-1901;
authors.forename: Anthony
authors.initials: A
authors.lastname: Greenberg
authors.affiliation: National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8634, Japan;
authors.forename: Jianzhong
authors.initials: J
authors.lastname: Wu
authors.affiliation: Faculty of Agriculture, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fukuoka 812-8581, Japan.
authors.forename: Hideshi
authors.initials: H
authors.lastname: Yasui
authors.affiliation: Faculty of Agriculture, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fukuoka 812-8581, Japan.
authors.forename: Atsushi
authors.initials: A
authors.lastname: Yoshimura
authors.affiliation: Graduate School of Agriculture, Nagoya University, Furo-cho, Chikusa, Nagoya, Aichi 464-8601, Japan; morihito@agr.nagoya-u.ac.jp srm4@cornell.edu ashi@agr.nagoya-u.ac.jp.
authors.forename: Hitoshi
authors.initials: H
authors.lastname: Mori
authors.affiliation: Section of Plant Breeding and Genetics, School of Integrated Plant Sciences, Cornell University, Ithaca, NY 14853-1901; morihito@agr.nagoya-u.ac.jp srm4@cornell.edu ashi@agr.nagoya-u.ac.jp.
authors.forename: Susan R
authors.initials: SR
authors.lastname: McCouch
authors.affiliation: Bioscience and Biotechnology Center, Nagoya University, Furo-cho, Chikusa, Nagoya, Aichi 464-8601, Japan; morihito@agr.nagoya-u.ac.jp srm4@cornell.edu ashi@agr.nagoya-u.ac.jp.
authors.forename: Motoyuki
authors.initials: M
authors.lastname: Ashikari
mesh_terms: D000483:Alleles; D018556:Crops, Agricultural / Q000254:growth & development*; D008958:Models, Molecular; D012275:Oryza / Q000235:genetics / Q000254:growth & development*; D010940:Plant Proteins / Q000235:genetics / Q000502:physiology*
chemical_list: D010940:Plant Proteins
keywords: awn; convergent evolution; parallel domestication; rice; signal peptide