Cold‐adaptive evolution at the reproductive stage in Geng/japonica subspecies reveals the role of OsMAPK3 and OsLEA9

SUMMARY Cold stress at the reproductive stage severely affects the production and geographic distribution of rice. The Geng/japonica subpopulation gradually developed stronger cold adaptation than the Xian/indica subpopulation during the long‐term domestication of cultivated rice. However, the evolu...

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Published in:The Plant journal : for cell and molecular biology 2022-08, Vol.111 (4), p.1032-1051
Main Authors: Lou, Qijin, Guo, Haifeng, Li, Jin, Han, Shichen, Khan, Najeeb Ullah, Gu, Yunsong, Zhao, Weitong, Zhang, Zhanying, Zhang, Hongliang, Li, Zichao, Li, Jinjie
Format: Article
Language:English
Subjects:
Adaptability
Adaptation
Climatic conditions
Cold
cold adaptation
Cold tolerance
Cultivation
Domestication
Embryogenesis
Embryonic growth stage
Evolution
Evolution & development
Genetic resources
Geng subspecies
Genomes
Geographical distribution
Grain cultivation
Kinases
Latitude
Low temperature
natural variation
Nucleotides
Oryza sativa indica
Oryza sativa japonica
OsLEA9
OsMAPK3
Plant breeding
Polymorphism
Protein kinase
Proteins
reproductive stage
Rice
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Summary:SUMMARY Cold stress at the reproductive stage severely affects the production and geographic distribution of rice. The Geng/japonica subpopulation gradually developed stronger cold adaptation than the Xian/indica subpopulation during the long‐term domestication of cultivated rice. However, the evolutionary path and natural alleles underlying the cold adaptability of intra‐Geng subspecies remain largely unknown. Here, we identified MITOGEN‐ACTIVATED PROTEIN KINASE 3 (OsMAPK3) and LATE EMBRYOGENESIS ABUNDANT PROTEIN 9 (OsLEA9) as two important regulators for the cold adaptation of Geng subspecies from a combination of transcriptome analysis and genome‐wide association study. Transgenic validation showed that OsMAPK3 and OsLEA9 confer cold tolerance at the reproductive stage. Selection and evolution analysis suggested that the Geng version of OsMAPK3 (OsMAPK3Geng) directly evolved from Chinese Oryza rufipogon III and was largely retained in high‐latitude and high‐altitude regions with low temperatures during domestication. Later, the functional nucleotide polymorphism (FNP‐776) in the Kunmingxiaobaigu and Lijiangxiaoheigu version of the OsLEA9 (OsLEA9KL) promoter originated from novel variation of intra‐Geng was selected and predominantly retained in temperate Geng to improve the adaptation of Geng together with OsMAPK3Geng to colder climatic conditions in high‐latitude areas. Breeding potential analysis suggested that pyramiding of OsMAPK3Geng and OsLEA9KL enhanced the cold tolerance of Geng and promotes the expansion of cultivated rice to colder regions. This study not only highlights the evolutionary path taken by the cold‐adaptive differentiation of intra‐Geng, but also provides new genetic resources for rice molecular breeding in low‐temperature areas. Significance Statement In this study, we identified variants in the two genes, OsMAPK3 and OsLEA9, as conferring cold tolerance of the Geng subspecies at the reproductive stage. OsMAPK3Geng originated from Chinese Oryza rufipogon III before following two evolutionary routes during domestication. It first genetically interacts with an allele of OsLEA9KL, which harbors a novel polymorphism in its promoter in Geng, to improve jointly the cold adaptability of Geng and promote its expansion to high‐altitude regions with a colder climate. In parallel, variation in OsMAPK3Geng sequentially move northward and enhance the tolerance of Geng to lower temperatures, eventually promoting the planting of Geng in higher‐l
ISSN:0960-7412
1365-313X
DOI:10.1111/tpj.15870