IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v16y2025i1d10.1038_s41467-025-56992-7.html
   My bibliography  Save this article

Natural variation of indels in the CTB3 promoter confers cold tolerance in japonica rice

Author

Listed:
  • Jin Li

    (China Agricultural University)

  • Haifeng Guo

    (China Agricultural University)

  • Qijin Lou

    (China Agricultural University)

  • Yawen Zeng

    (Yunnan Academy of Agricultural Sciences)

  • Zhenhua Guo

    (Rice Research Institute of Heilongjiang Academy of Agricultural Sciences)

  • Penghui Xu

    (China Agricultural University)

  • Yunsong Gu

    (China Agricultural University)

  • Shilei Gao

    (China Agricultural University)

  • Bingxia Xu

    (China Agricultural University)

  • Shichen Han

    (China Agricultural University)

  • Runbin Su

    (China Agricultural University)

  • Andong Zou

    (China Agricultural University)

  • Wei Ye

    (China Agricultural University)

  • Meng Zhang

    (China Agricultural University)

  • Yingxiu Li

    (China Agricultural University)

  • Xingming Sun

    (China Agricultural University)

  • Zhanying Zhang

    (China Agricultural University)

  • Hongliang Zhang

    (China Agricultural University)

  • Wendong Ma

    (Rice Research Institute of Heilongjiang Academy of Agricultural Sciences)

  • Chao Chen

    (Ltd)

  • Zichao Li

    (China Agricultural University)

  • Jinjie Li

    (China Agricultural University)

Abstract

Improvement of cold tolerance at the booting stage (CTB) in rice is a key strategy for cultivation in high-altitude and high-latitude regions. Here, we identify CTB3 gene, encoding a calmodulin-binding transcriptional activator that positively regulates cold tolerance at the booting stage in japonica rice. Two indels (57-bp and 284-bp) in the CTB3 promoter confer a differential transcriptional response to cold between the japonica and indica subspecies. OsTCP19 suppresses CTB3 expression by binding to these indels, negatively regulating cold tolerance. CTB3 activates the expression of TREHALOSE-6-PHOSPHATE PHOSPHATASE1 (OsTPP1), reducing trehalose 6-phosphate (Tre6P) levels, which increases sugar accumulation in panicles and improves cold tolerance. Additionally, favorable alleles of OsTCP19 and CTB3 are selected in japonica rice for cold adaptation. These findings highlight the important role of CTB3 in cold adaptation and its potential for improving cold tolerance in rice breeding.

Suggested Citation

  • Jin Li & Haifeng Guo & Qijin Lou & Yawen Zeng & Zhenhua Guo & Penghui Xu & Yunsong Gu & Shilei Gao & Bingxia Xu & Shichen Han & Runbin Su & Andong Zou & Wei Ye & Meng Zhang & Yingxiu Li & Xingming Sun, 2025. "Natural variation of indels in the CTB3 promoter confers cold tolerance in japonica rice," Nature Communications, Nature, vol. 16(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-56992-7
    DOI: 10.1038/s41467-025-56992-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-025-56992-7
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-025-56992-7?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Chuanzhong Zhang & Hongru Wang & Xiaojie Tian & Xinyan Lin & Yunfei Han & Zhongmin Han & Hanjing Sha & Jia Liu & Jianfeng Liu & Jian Zhang & Qingyun Bu & Jun Fang, 2024. "A transposon insertion in the promoter of OsUBC12 enhances cold tolerance during japonica rice germination," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Changxuan Xia & Guohua Liang & Kang Chong & Yunyuan Xu, 2023. "The COG1-OsSERL2 complex senses cold to trigger signaling network for chilling tolerance in japonica rice," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Xuehui Huang & Nori Kurata & Xinghua Wei & Zi-Xuan Wang & Ahong Wang & Qiang Zhao & Yan Zhao & Kunyan Liu & Hengyun Lu & Wenjun Li & Yunli Guo & Yiqi Lu & Congcong Zhou & Danlin Fan & Qijun Weng & Chu, 2012. "A map of rice genome variation reveals the origin of cultivated rice," Nature, Nature, vol. 490(7421), pages 497-501, October.
    4. Yong Zhou & Zhichao Yu & Dmytro Chebotarov & Kapeel Chougule & Zhenyuan Lu & Luis F. Rivera & Nagarajan Kathiresan & Noor Al-Bader & Nahed Mohammed & Aseel Alsantely & Saule Mussurova & João Santos & , 2023. "Pan-genome inversion index reveals evolutionary insights into the subpopulation structure of Asian rice," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    5. Citao Liu & Shujun Ou & Bigang Mao & Jiuyou Tang & Wei Wang & Hongru Wang & Shouyun Cao & Michael R. Schläppi & Bingran Zhao & Guoying Xiao & Xiping Wang & Chengcai Chu, 2018. "Early selection of bZIP73 facilitated adaptation of japonica rice to cold climates," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    6. Zhanying Zhang & Jinjie Li & Yinghua Pan & Jilong Li & Lei zhou & Hongli Shi & Yawen Zeng & Haifeng Guo & Shuming Yang & Weiwei Zheng & Jianping Yu & Xingming Sun & Gangling Li & Yanglin Ding & Liang , 2017. "Natural variation in CTB4a enhances rice adaptation to cold habitats," Nature Communications, Nature, vol. 8(1), pages 1-13, April.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Haifeng Guo & Shilei Gao & Huahui Li & Jiazhen Yang & Jin Li & Yunsong Gu & Qijin Lou & Runbin Su & Wei Ye & Andong Zou & Yulong Wang & Xingming Sun & Zhanying Zhang & Hongliang Zhang & Yawen Zeng & P, 2025. "Natural variation of CTB5 confers cold adaptation in plateau japonica rice," Nature Communications, Nature, vol. 16(1), pages 1-18, December.
    2. Dunpin Xiong & Juan Wang & Ruci Wang & Yueming Wang & Yi Li & Ge Sun & Shanguo Yao, 2024. "A point mutation in VIG1 boosts development and chilling tolerance in rice," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. Chuanzhong Zhang & Hongru Wang & Xiaojie Tian & Xinyan Lin & Yunfei Han & Zhongmin Han & Hanjing Sha & Jia Liu & Jianfeng Liu & Jian Zhang & Qingyun Bu & Jun Fang, 2024. "A transposon insertion in the promoter of OsUBC12 enhances cold tolerance during japonica rice germination," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    4. Changxuan Xia & Guohua Liang & Kang Chong & Yunyuan Xu, 2023. "The COG1-OsSERL2 complex senses cold to trigger signaling network for chilling tolerance in japonica rice," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    5. Seung Young Lee & Hyun-Sook Lee & Chang-Min Lee & Su-Kyung Ha & Hyang-Mi Park & So-Myeong Lee & Youngho Kwon & Ji-Ung Jeung & Youngjun Mo, 2023. "Multi-Environment Trials and Stability Analysis for Yield-Related Traits of Commercial Rice Cultivars," Agriculture, MDPI, vol. 13(2), pages 1-13, January.
    6. Xiaofeng Cai & Xuepeng Sun & Chenxi Xu & Honghe Sun & Xiaoli Wang & Chenhui Ge & Zhonghua Zhang & Quanxi Wang & Zhangjun Fei & Chen Jiao & Quanhua Wang, 2021. "Genomic analyses provide insights into spinach domestication and the genetic basis of agronomic traits," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    7. Chew, Soo Hong & Ebstein, Richard P. & Lu, Yunfeng, 2023. "Rice culture and the cushion hypothesis: Experimental evidence from incentivized risk taking tasks," Economics Letters, Elsevier, vol. 223(C).
    8. Rujia Chen & Ning Xiao & Yue Lu & Tianyun Tao & Qianfeng Huang & Shuting Wang & Zhichao Wang & Mingli Chuan & Qing Bu & Zhou Lu & Hanyao Wang & Yanze Su & Yi Ji & Jianheng Ding & Ahmed Gharib & Huixin, 2023. "A de novo evolved gene contributes to rice grain shape difference between indica and japonica," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    9. Zihao Wang & Wenxi Wang & Xiaoming Xie & Yongfa Wang & Zhengzhao Yang & Huiru Peng & Mingming Xin & Yingyin Yao & Zhaorong Hu & Jie Liu & Zhenqi Su & Chaojie Xie & Baoyun Li & Zhongfu Ni & Qixin Sun &, 2022. "Dispersed emergence and protracted domestication of polyploid wheat uncovered by mosaic ancestral haploblock inference," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    10. Elisa Zampieri & Michele Pesenti & Fabio Francesco Nocito & Gian Attilio Sacchi & Giampiero Valè, 2023. "Rice Responses to Water Limiting Conditions: Improving Stress Management by Exploiting Genetics and Physiological Processes," Agriculture, MDPI, vol. 13(2), pages 1-23, February.
    11. Xin Dong & Tianyi Zhang & Xiaoguang Yang & Tao Li, 2023. "Breeding priorities for rice adaptation to climate change in Northeast China," Climatic Change, Springer, vol. 176(6), pages 1-19, June.
    12. Decha Songtoasesakul & Wanchana Aesomnuk & Sarinthip Pannak & Jonaliza Lanceras Siangliw & Meechai Siangliw & Theerayut Toojinda & Samart Wanchana & Siwaret Arikit, 2023. "QTL-seq Identifies Pokkali-Derived QTLs and Candidate Genes for Salt Tolerance at Seedling Stage in Rice ( Oryza sativa L.)," Agriculture, MDPI, vol. 13(8), pages 1-15, August.
    13. Yu Chang & Yujie Fang & Jiahan Liu & Tiantian Ye & Xiaokai Li & Haifu Tu & Ying Ye & Yao Wang & Lizhong Xiong, 2024. "Stress-induced nuclear translocation of ONAC023 improves drought and heat tolerance through multiple processes in rice," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    14. Weixiong Long & Qiang He & Yitao Wang & Yu Wang & Jie Wang & Zhengqing Yuan & Meijia Wang & Wei Chen & Lihua Luo & Laiyang Luo & Weibiao Xu & Yonghui Li & Wei Li & Longan Yan & Yaohui Cai & Huilong Du, 2024. "Genome evolution and diversity of wild and cultivated rice species," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    15. Jingfen Huang & Yilin Zhang & Yapeng Li & Meng Xing & Cailin Lei & Shizhuang Wang & Yamin Nie & Yanyan Wang & Mingchao Zhao & Zhenyun Han & Xianjun Sun & Han Zhou & Yan Wang & Xiaoming Zheng & Xiaoron, 2024. "Haplotype-resolved gapless genome and chromosome segment substitution lines facilitate gene identification in wild rice," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    16. Xuezhu Liao & Dejin Xie & Tingting Bao & Mengmeng Hou & Cheng Li & Bao Nie & Shichao Sun & Dan Peng & Haixiao Hu & Hongru Wang & Yongfu Tao & Yu Zhang & Wei Li & Li Wang, 2024. "Inversions encounter relaxed genetic constraints and balance birth and death of TPS genes in Curcuma," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    17. Xingming Sun & Haiyan Xiong & Conghui Jiang & Dongmei Zhang & Zengling Yang & Yuanping Huang & Wanbin Zhu & Shuaishuai Ma & Junzhi Duan & Xin Wang & Wei Liu & Haifeng Guo & Gangling Li & Jiawei Qi & C, 2022. "Natural variation of DROT1 confers drought adaptation in upland rice," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    18. Lin-Feng Li & Tonapha Pusadee & Marshall J. Wedger & Ya-Ling Li & Ming-Rui Li & Yee-Ling Lau & Soo-Joo Yap & Sansanee Jamjod & Benjavan Rerkasem & Yan Hao & Beng-Kah Song & Kenneth M. Olsen, 2024. "Porous borders at the wild-crop interface promote weed adaptation in Southeast Asia," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    19. Huaijun Wang & Tiantian Ye & Zilong Guo & Yilong Yao & Haifu Tu & Pengfei Wang & Yu Zhang & Yao Wang & Xiaokai Li & Bingchen Li & Haiyan Xiong & Xuelei Lai & Lizhong Xiong, 2024. "A double-stranded RNA binding protein enhances drought resistance via protein phase separation in rice," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    20. Paris Veltsos & Luis J. Madrigal-Roca & John K. Kelly, 2024. "Testing the evolutionary theory of inversion polymorphisms in the yellow monkeyflower (Mimulus guttatus)," Nature Communications, Nature, vol. 15(1), pages 1-10, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-56992-7. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.