A newly evolved rice-specific gene JAUP1 regulates jasmonate biosynthesis and signalling to promote root development and multi-stress tolerance

Adnan Muzaffar, Yi Shih Chen, Hsiang Ting Lee, Cheng Chieh Wu, Trang Thi Le, Jin Zhang Liang, Chun Hsien Lu, Hariharan Balasubramaniam, Shuen Fang Lo, Lin Chih Yu, Chien Hao Chan, Ku Ting Chen, Miin Huey Lee, Yue Ie Hsing, Tuan Hua David Ho, Su May Yu

Research output: Contribution to journalArticlepeer-review

5 Scopus citations

Abstract

Root architecture and function are critical for plants to secure water and nutrient supply from the soil, but environmental stresses alter root development. The phytohormone jasmonic acid (JA) regulates plant growth and responses to wounding and other stresses, but its role in root development for adaptation to environmental challenges had not been well investigated. We discovered a novel JA Upregulated Protein 1 gene (JAUP1) that has recently evolved in rice and is specific to modern rice accessions. JAUP1 regulates a self-perpetuating feed-forward loop to activate the expression of genes involved in JA biosynthesis and signalling that confers tolerance to abiotic stresses and regulates auxin-dependent root development. Ectopic expression of JAUP1 alleviates abscisic acid- and salt-mediated suppression of lateral root (LR) growth. JAUP1 is primarily expressed in the root cap and epidermal cells (EPCs) that protect the meristematic stem cells and emerging LRs. Wound-activated JA/JAUP1 signalling promotes crosstalk between the root cap of LR and parental root EPCs, as well as induces cell wall remodelling in EPCs overlaying the emerging LR, thereby facilitating LR emergence even under ABA-suppressive conditions. Elevated expression of JAUP1 in transgenic rice or natural rice accessions enhances abiotic stress tolerance and reduces grain yield loss under a limited water supply. We reveal a hitherto unappreciated role for wound-induced JA in LR development under abiotic stress and suggest that JAUP1 can be used in biotechnology and as a molecular marker for breeding rice adapted to extreme environmental challenges and for the conservation of water resources.

Original languageEnglish
Pages (from-to)1417-1432
Number of pages16
JournalPlant Biotechnology Journal
Volume22
Issue number5
DOIs
StatePublished - May 2024
Externally publishedYes

Funding

We thank Dr John O'Brien for critical review of this manuscript, Ms Min\u2010Wei Tsai for rice transformation and Ms Ting\u2010Hsiang Chang at the Metabolomics Core Facility of the Agricultural Biotechnology Research Center at Academia Sinica for the UPLC\u2010MS/MS analysis. We also thank the Genomics Core, Bioinformatics\u2010Biology Service Core and Imaging Core at the Institute of Molecular Biology, Academia Sinica, for bioinformatics and imaging analyses. This work was supported by grants from the Innovative Translational Agricultural Research (ITAR) Program of Academia Sinica (AS\u2010108\u2010ITAR\u2010TD08, AS\u2010109\u2010ITAR\u2010TD08, AS\u2010110\u2010ITAR\u2010TD06 and AS\u2010KPQ\u2010111\u2010ITAR\u201011108), Ministry of Science and Technology (MOST 109\u20102326\u2010B\u2010001\u2010004 and MOST 110\u20102326\u2010B\u2010001\u2010011) and in part by the Advanced Plant Biotechnology Center from the Featured Areas Research Center Program within the framework of the Higher Education Sprout Project by the Ministry of Education (MOE) in Taiwan. We thank Dr John O'Brien for critical review of this manuscript, Ms Min-Wei Tsai for rice transformation and Ms Ting-Hsiang Chang at the Metabolomics Core Facility of the Agricultural\u00A0Biotechnology Research Center at Academia Sinica for the UPLC-MS/MS analysis. We also thank the Genomics Core, Bioinformatics-Biology Service Core and Imaging Core at the Institute of Molecular Biology, Academia Sinica, for bioinformatics and imaging analyses. This work was supported by grants from the Innovative Translational Agricultural Research (ITAR) Program of Academia Sinica (AS-108-ITAR-TD08, AS-109-ITAR-TD08, AS-110-ITAR-TD06 and AS-KPQ-111-ITAR-11108), Ministry of Science and Technology (MOST 109-2326-B-001-004 and MOST 110-2326-B-001-011) and in part by the Advanced Plant Biotechnology Center from the Featured Areas Research\u00A0Center Program within the framework of the Higher Education Sprout Project by the Ministry of Education (MOE) in Taiwan.

FundersFunder number
Ministry of Education
Academia SinicaAS‐109‐ITAR‐TD08, AS‐KPQ‐111‐ITAR‐11108, AS‐110‐ITAR‐TD06, AS-108-ITAR-TD08
Ministry of Science and Technology, Taiwan109‐2326‐B‐001‐004, MOST 110‐2326‐B‐001‐011

    Keywords

    • ABA
    • abiotic stress
    • grain yield
    • jasmonate
    • rice
    • root development

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