J Integr Plant Biol. ›› 2025, Vol. 67 ›› Issue (2): 345-354.DOI: 10.1111/jipb.13814

• Molecular Physiology • Previous Articles     Next Articles

Identification of new salicylic acid signaling regulators for root development and microbiota composition in plants

Xianqing Jia1†*, Zhuang Xu2†, Lei Xu2†, Juan P. Frene3†, Mathieu Gonin3, Long Wang2, Jiahong Yu2, Gabriel Castrillo3* and Keke Yi2*   

  1. 1. Key Laboratory of Resource Biology and Biotechnology Western China, Ministry of Education, Provincial Key Laboratory of Biotechnology of Shaanxi Province, College of Life Sciences, Northwest University, Xi'an 710069, China
    2. State Key Laboratory of Efficient Utilization of Arid and Semi‐arid Arable Land in Northern China, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, China
    3. School of Biosciences, University of Nottingham, Sutton Bonington LE12 5RD, UK
    These authors contributed equally to this work.
    *Correspondences: Xianqing Jia (jiaxianqing@nwu.edu.cn); Gabriel Castrillo (gabriel.castrillo@nottingham.ac.uk); Keke Yi (yikeke@gmail.com, Dr. Yi is responsible for the distribution of all materials associated with this article)
  • Received:2024-05-13 Accepted:2024-11-15 Online:2024-12-04 Published:2025-02-01
  • Supported by:
    This work was supported by the National Key Research and Development Program of China (2021YFF1000404), the National Natural Science Foundation of China (Grant Nos. U23A20178 and 32202593), and the Central Public‐interest Scientific Institution Basal Research Fund (Y2022QC14). K.Y. and L.X. were supported by the Innovation Program of Chinese Academy of Agricultural Sciences (CAAS‐CSAL‐202301). L.X. was supported by the Central Public‐interest Scientific Institution Basal Research Fund (Y2023XK06). 6). M.G. and G.C were supported by The Leverhulme Trust Grant No. RPG‐2019‐337 and J.P.F. and G.C. by the Biotechnology and Biological Sciences Research Council Grant BB/W018756/1.

Abstract: Besides playing a crucial role in plant immunity via the nonexpressor of pathogenesis-related (NPR) proteins, increasing evidence shows that salicylic acid (SA) can also regulate plant root growth. However, the transcriptional regulatory network controlling this SA response in plant roots is still unclear. Here, we found that NPR1 and WRKY45, the central regulators of SA response in rice leaves, control only a reduced sector of the root SA signaling network. We demonstrated that SA attenuates root growth via a novel NPR1/WRKY45-independent pathway. Furthermore, using regulatory network analysis and mutant characterization, we identified a set of new NPR1/WRKY45-independent regulators that conservedly modulate the root development and root-associated microbiota composition in both Oryza sativa (monocot) and Arabidopsis thaliana (dicot) in response to SA. Our results established the SA signaling as a central element regulating plant root functions under ecologically relevant conditions. These results provide new insights to understand how regulatory networks control plant responses to abiotic and biotic stresses.

Key words: gene regulatory network, microbiota colonization, root growth, ROS, salicylic acid

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