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A stepwise route to domesticate rice by controlling seed shattering and panicle shape

Asian rice (Oryza sativa L.) is consumed by more than half of the world's population. Despite its global importance, the process of early rice domestication remains unclear. During domestication, wild rice (Oryza rufipogon Griff.) acquired non-seed-shattering behavior, allowing humans to increa...

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Autores principales: Ishikawa, Ryo, Castillo, Cristina Cobo, Htun, Than Myint, Numaguchi, Koji, Inoue, Kazuya, Oka, Yumi, Ogasawara, Miki, Sugiyama, Shohei, Takama, Natsumi, Orn, Chhourn, Inoue, Chizuru, Nonomura, Ken-Ichi, Allaby, Robin, Fuller, Dorian Q., Ishii, Takashige
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9245615/
https://www.ncbi.nlm.nih.gov/pubmed/35733263
http://dx.doi.org/10.1073/pnas.2121692119
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author Ishikawa, Ryo
Castillo, Cristina Cobo
Htun, Than Myint
Numaguchi, Koji
Inoue, Kazuya
Oka, Yumi
Ogasawara, Miki
Sugiyama, Shohei
Takama, Natsumi
Orn, Chhourn
Inoue, Chizuru
Nonomura, Ken-Ichi
Allaby, Robin
Fuller, Dorian Q.
Ishii, Takashige
author_facet Ishikawa, Ryo
Castillo, Cristina Cobo
Htun, Than Myint
Numaguchi, Koji
Inoue, Kazuya
Oka, Yumi
Ogasawara, Miki
Sugiyama, Shohei
Takama, Natsumi
Orn, Chhourn
Inoue, Chizuru
Nonomura, Ken-Ichi
Allaby, Robin
Fuller, Dorian Q.
Ishii, Takashige
author_sort Ishikawa, Ryo
collection PubMed
description Asian rice (Oryza sativa L.) is consumed by more than half of the world's population. Despite its global importance, the process of early rice domestication remains unclear. During domestication, wild rice (Oryza rufipogon Griff.) acquired non-seed-shattering behavior, allowing humans to increase grain yield. Previous studies argued that a reduction in seed shattering triggered by the sh4 mutation led to increased yield during rice domestication, but our experiments using wild introgression lines show that the domesticated sh4 allele alone is insufficient for shattering loss in O. rufipogon. The interruption of abscission layer formation requires both sh4 and qSH3 mutations, demonstrating that the selection of shattering loss in wild rice was not as simple as previously suggested. Here we identified a causal single-nucleotide polymorphism at qSH3 within the seed-shattering gene OsSh1, which is conserved in indica and japonica subspecies but absent in the circum-aus group of rice. Through harvest experiments, we further demonstrated that seed shattering alone did not significantly impact yield; rather, yield increases were observed with closed panicle formation controlled by SPR3 and further augmented by nonshattering, conferred by integration of sh4 and qSH3 alleles. Complementary manipulation of panicle shape and seed shattering results in a mechanically stable panicle structure. We propose a stepwise route for the earliest phase of rice domestication, wherein selection of visible SPR3-controlled closed panicle morphology was instrumental in the sequential recruitment of sh4 and qSH3, which together led to the loss of shattering.
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spelling pubmed-92456152022-12-22 A stepwise route to domesticate rice by controlling seed shattering and panicle shape Ishikawa, Ryo Castillo, Cristina Cobo Htun, Than Myint Numaguchi, Koji Inoue, Kazuya Oka, Yumi Ogasawara, Miki Sugiyama, Shohei Takama, Natsumi Orn, Chhourn Inoue, Chizuru Nonomura, Ken-Ichi Allaby, Robin Fuller, Dorian Q. Ishii, Takashige Proc Natl Acad Sci U S A Biological Sciences Asian rice (Oryza sativa L.) is consumed by more than half of the world's population. Despite its global importance, the process of early rice domestication remains unclear. During domestication, wild rice (Oryza rufipogon Griff.) acquired non-seed-shattering behavior, allowing humans to increase grain yield. Previous studies argued that a reduction in seed shattering triggered by the sh4 mutation led to increased yield during rice domestication, but our experiments using wild introgression lines show that the domesticated sh4 allele alone is insufficient for shattering loss in O. rufipogon. The interruption of abscission layer formation requires both sh4 and qSH3 mutations, demonstrating that the selection of shattering loss in wild rice was not as simple as previously suggested. Here we identified a causal single-nucleotide polymorphism at qSH3 within the seed-shattering gene OsSh1, which is conserved in indica and japonica subspecies but absent in the circum-aus group of rice. Through harvest experiments, we further demonstrated that seed shattering alone did not significantly impact yield; rather, yield increases were observed with closed panicle formation controlled by SPR3 and further augmented by nonshattering, conferred by integration of sh4 and qSH3 alleles. Complementary manipulation of panicle shape and seed shattering results in a mechanically stable panicle structure. We propose a stepwise route for the earliest phase of rice domestication, wherein selection of visible SPR3-controlled closed panicle morphology was instrumental in the sequential recruitment of sh4 and qSH3, which together led to the loss of shattering. National Academy of Sciences 2022-06-22 2022-06-28 /pmc/articles/PMC9245615/ /pubmed/35733263 http://dx.doi.org/10.1073/pnas.2121692119 Text en Copyright © 2022 the Author(s). Published by PNAS https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Ishikawa, Ryo
Castillo, Cristina Cobo
Htun, Than Myint
Numaguchi, Koji
Inoue, Kazuya
Oka, Yumi
Ogasawara, Miki
Sugiyama, Shohei
Takama, Natsumi
Orn, Chhourn
Inoue, Chizuru
Nonomura, Ken-Ichi
Allaby, Robin
Fuller, Dorian Q.
Ishii, Takashige
A stepwise route to domesticate rice by controlling seed shattering and panicle shape
title A stepwise route to domesticate rice by controlling seed shattering and panicle shape
title_full A stepwise route to domesticate rice by controlling seed shattering and panicle shape
title_fullStr A stepwise route to domesticate rice by controlling seed shattering and panicle shape
title_full_unstemmed A stepwise route to domesticate rice by controlling seed shattering and panicle shape
title_short A stepwise route to domesticate rice by controlling seed shattering and panicle shape
title_sort stepwise route to domesticate rice by controlling seed shattering and panicle shape
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9245615/
https://www.ncbi.nlm.nih.gov/pubmed/35733263
http://dx.doi.org/10.1073/pnas.2121692119
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