IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-50229-9.html
   My bibliography  Save this article

Stress-induced nuclear translocation of ONAC023 improves drought and heat tolerance through multiple processes in rice

Author

Listed:
  • Yu Chang

    (Huazhong Agricultural University
    Huazhong Agricultural University)

  • Yujie Fang

    (Yangzhou University)

  • Jiahan Liu

    (Huazhong Agricultural University
    Huazhong Agricultural University)

  • Tiantian Ye

    (Huazhong Agricultural University
    Huazhong Agricultural University)

  • Xiaokai Li

    (Huazhong Agricultural University
    Huazhong Agricultural University)

  • Haifu Tu

    (Huazhong Agricultural University
    Huazhong Agricultural University)

  • Ying Ye

    (Huazhong Agricultural University
    Huazhong Agricultural University)

  • Yao Wang

    (Huazhong Agricultural University
    Huazhong Agricultural University)

  • Lizhong Xiong

    (Huazhong Agricultural University
    Huazhong Agricultural University)

Abstract

Drought and heat are major abiotic stresses frequently coinciding to threaten rice production. Despite hundreds of stress-related genes being identified, only a few have been confirmed to confer resistance to multiple stresses in crops. Here we report ONAC023, a hub stress regulator that integrates the regulations of both drought and heat tolerance in rice. ONAC023 positively regulates drought and heat tolerance at both seedling and reproductive stages. Notably, the functioning of ONAC023 is obliterated without stress treatment and can be triggered by drought and heat stresses at two layers. The expression of ONAC023 is induced in response to stress stimuli. We show that overexpressed ONAC23 is translocated to the nucleus under stress and evidence from protoplasts suggests that the dephosphorylation of the remorin protein OSREM1.5 can promote this translocation. Under drought or heat stress, the nuclear ONAC023 can target and promote the expression of diverse genes, such as OsPIP2;7, PGL3, OsFKBP20-1b, and OsSF3B1, which are involved in various processes including water transport, reactive oxygen species homeostasis, and alternative splicing. These results manifest that ONAC023 is fine-tuned to positively regulate drought and heat tolerance through the integration of multiple stress-responsive processes. Our findings provide not only an underlying connection between drought and heat responses, but also a promising candidate for engineering multi-stress-resilient rice.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50229-9
    DOI: 10.1038/s41467-024-50229-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-50229-9
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-50229-9?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. Vân Anh Huynh-Thu & Alexandre Irrthum & Louis Wehenkel & Pierre Geurts, 2010. "Inferring Regulatory Networks from Expression Data Using Tree-Based Methods," PLOS ONE, Public Library of Science, vol. 5(9), pages 1-10, September.
    2. Sangtae Kim & Pavel A. Pevzner, 2014. "MS-GF+ makes progress towards a universal database search tool for proteomics," Nature Communications, Nature, vol. 5(1), pages 1-10, 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. 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.
    5. Lun Zhao & Liang Xie & Qing Zhang & Weizhi Ouyang & Li Deng & Pengpeng Guan & Meng Ma & Yue Li & Ying Zhang & Qin Xiao & Jingwen Zhang & Hongmeijuan Li & Shunyao Wang & Jiangwei Man & Zhilin Cao & Qin, 2020. "Integrative analysis of reference epigenomes in 20 rice varieties," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    6. Moysés Nascimento & Fabyano Fonseca e Silva & Thelma Sáfadi & Ana Carolina Campana Nascimento & Talles Eduardo Maciel Ferreira & Laís Mayara Azevedo Barroso & Camila Ferreira Azevedo & Simone Eliza Fa, 2017. "Independent Component Analysis (ICA) based-clustering of temporal RNA-seq data," PLOS ONE, Public Library of Science, vol. 12(7), pages 1-12, July.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. 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.

    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. Natalie M. Clark & Trevor M. Nolan & Ping Wang & Gaoyuan Song & Christian Montes & Conner T. Valentine & Hongqing Guo & Rosangela Sozzani & Yanhai Yin & Justin W. Walley, 2021. "Integrated omics networks reveal the temporal signaling events of brassinosteroid response in Arabidopsis," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    2. 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.
    3. Xi Wang & Juan Li & Linqian Han & Chengyong Liang & Jiaxin Li & Xiaoyang Shang & Xinxin Miao & Zi Luo & Wanchao Zhu & Zhao Li & Tianhuan Li & Yongwen Qi & Huihui Li & Xiaoduo Lu & Lin Li, 2023. "QTG-Miner aids rapid dissection of the genetic base of tassel branch number in maize," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. 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.
    5. Cecilia Pessoa Rodrigues & Aindrila Chatterjee & Meike Wiese & Thomas Stehle & Witold Szymanski & Maria Shvedunova & Asifa Akhtar, 2021. "Histone H4 lysine 16 acetylation controls central carbon metabolism and diet-induced obesity in mice," Nature Communications, Nature, vol. 12(1), pages 1-21, December.
    6. 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).
    7. 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.
    8. Zheng Fang & Hongqiang Qin & Jiawei Mao & Zhongyu Wang & Na Zhang & Yan Wang & Luyao Liu & Yongzhan Nie & Mingming Dong & Mingliang Ye, 2022. "Glyco-Decipher enables glycan database-independent peptide matching and in-depth characterization of site-specific N-glycosylation," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. Marius Arend & Yizhong Yuan & M. Águila Ruiz-Sola & Nooshin Omranian & Zoran Nikoloski & Dimitris Petroutsos, 2023. "Widening the landscape of transcriptional regulation of green algal photoprotection," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    10. Ruonan Wu & Michelle R. Davison & William C. Nelson & Montana L. Smith & Mary S. Lipton & Janet K. Jansson & Ryan S. McClure & Jason E. McDermott & Kirsten S. Hofmockel, 2023. "Hi-C metagenome sequencing reveals soil phage–host interactions," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    11. 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.
    12. 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.
    13. 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.
    14. 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.
    15. Fei Liu & Shao-Wu Zhang & Wei-Feng Guo & Ze-Gang Wei & Luonan Chen, 2016. "Inference of Gene Regulatory Network Based on Local Bayesian Networks," PLOS Computational Biology, Public Library of Science, vol. 12(8), pages 1-17, August.
    16. 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.
    17. Cheng Ding & Guoting Chen & Shiping Luan & Runxin Gao & Yudong Fan & Ying Zhang & Xiaoting Wang & Guoliang Li & Mohamed F. Foda & Jiapei Yan & Xingwang Li, 2025. "Simultaneous profiling of chromatin-associated RNA at targeted DNA loci and RNA-RNA Interactions through TaDRIM-seq," Nature Communications, Nature, vol. 16(1), pages 1-14, December.
    18. Kaiyuan Liu & Yuzhen Ye & Sujun Li & Haixu Tang, 2023. "Accurate de novo peptide sequencing using fully convolutional neural networks," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    19. Mingyi Wang & Jerome Verdier & Vagner A Benedito & Yuhong Tang & Jeremy D Murray & Yinbing Ge & Jörg D Becker & Helena Carvalho & Christian Rogers & Michael Udvardi & Ji He, 2013. "LegumeGRN: A Gene Regulatory Network Prediction Server for Functional and Comparative Studies," PLOS ONE, Public Library of Science, vol. 8(7), pages 1-7, July.
    20. 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.

    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:15:y:2024:i:1:d:10.1038_s41467-024-50229-9. 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.