Enhancing rice grain production by manipulating the naturally evolved cis-regulatory element-containing inverted repeat sequence of OsREM20.

Xiaowei Wu, Yan Liang, Hengbin Gao, Jiyao Wang, Yan Zhao, Lekai Hua, Yundong Yuan, Ahong Wang, Xiaohui Zhang, Jiafan Liu, Jie Zhou, Xiangbing Meng, Dahan Zhang, Shaoyang Lin, Xuehui Huang, Bin Han, Jiayang Li, Yonghong Wang
Author Information
  1. Xiaowei Wu: State Key Laboratory of Plant Genomics and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, China.
  2. Yan Liang: State Key Laboratory of Plant Genomics and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China; College of Life Sciences, Shandong Agricultural University, Taian, Shandong 271018, China.
  3. Hengbin Gao: College of Life Sciences, Shandong Agricultural University, Taian, Shandong 271018, China.
  4. Jiyao Wang: State Key Laboratory of Plant Genomics and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, China.
  5. Yan Zhao: National Center for Gene Research, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200233, China.
  6. Lekai Hua: College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou 350002, China.
  7. Yundong Yuan: State Key Laboratory of Plant Genomics and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
  8. Ahong Wang: National Center for Gene Research, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200233, China.
  9. Xiaohui Zhang: State Key Laboratory of Plant Genomics and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, China.
  10. Jiafan Liu: State Key Laboratory of Plant Genomics and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
  11. Jie Zhou: State Key Laboratory of Plant Genomics and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
  12. Xiangbing Meng: State Key Laboratory of Plant Genomics and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
  13. Dahan Zhang: State Key Laboratory of Plant Genomics and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, China.
  14. Shaoyang Lin: State Key Laboratory of Plant Genomics and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
  15. Xuehui Huang: Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai 200234, China.
  16. Bin Han: CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai 200032, China; National Center for Gene Research, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200233, China.
  17. Jiayang Li: State Key Laboratory of Plant Genomics and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China; Innovation Academy for Seed Design, Chinese Academy of Sciences, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, China.
  18. Yonghong Wang: State Key Laboratory of Plant Genomics and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China; CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai 200032, China; University of Chinese Academy of Sciences, Beijing 100049, China; College of Life Sciences, Shandong Agricultural University, Taian, Shandong 271018, China. Electronic address: yhwang@genetics.ac.cn.

Abstract

Grain number per panicle (GNP) is an important agronomic trait that contributes to rice grain yield. Despite its importance in rice breeding, the molecular mechanism underlying GNP regulation remains largely unknown. In this study, we identified a previously unrecognized regulatory gene that controls GNP in rice, Oryza sativa REPRODUCTIVE MERISTEM 20 (OsREM20), which encodes a B3 domain transcription factor. Through genetic analysis and transgenic validation we found that genetic variation in the CArG box-containing inverted repeat (IR) sequence of the OsREM20 promoter alters its expression level and contributes to GNP variation among rice varieties. Furthermore, we revealed that the IR sequence regulates OsREM20 expression by affecting the direct binding of OsMADS34 to the CArG box within the IR sequence. Interestingly, the divergent pOsREM20 and pOsREM20 alleles were found to originate from different Oryza rufipogon accessions, and were independently inherited into the japonica and indica subspecies, respectively, during domestication. Importantly, we demonstrated that IR sequence variations in the OsREM20 promoter can be utilized for germplasm improvement through either genome editing or traditional breeding. Taken together, our study characterizes novel genetic variations responsible for GNP diversity in rice, reveals the underlying molecular mechanism in the regulation of agronomically important gene expression, and provides a promising strategy for improving rice production by manipulating the cis-regulatory element-containing IR sequence.

Keywords

MeSH Term

Alleles
Domestication
Edible Grain
Gene Expression Regulation, Plant
Genes, Plant
Inverted Repeat Sequences
Oryza
Plant Breeding
Plant Proteins
Promoter Regions, Genetic
Quantitative Trait Loci

Chemicals

Plant Proteins