Brassinosteroids mediate arbuscular mycorrhizal symbiosis through multiple potential pathways and partial identification in tomato

Ying Ren; Brian Tobin; Shuyi Yang; Tingying Xu; Hui Chen; Ming Tang

doi:10.1016/j.micres.2024.127924

Brassinosteroids mediate arbuscular mycorrhizal symbiosis through multiple potential pathways and partial identification in tomato

Microbiol Res. 2024 Oct 5:289:127924. doi: 10.1016/j.micres.2024.127924. Online ahead of print.

Authors

Ying Ren¹, Brian Tobin², Shuyi Yang³, Tingying Xu⁴, Hui Chen⁵, Ming Tang⁶

Affiliations

¹ State Key Laboratory of Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Guangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou 510642, China. Electronic address: yingren@stu.scau.edu.cn.
² School of Agriculture & Food Science and UCD Earth Institute, University College Dublin, Ireland. Electronic address: brian.tobin@ucd.ie.
³ School of Agriculture & Food Science and UCD Earth Institute, University College Dublin, Ireland. Electronic address: shuyi.yang@ucdconnect.ie.
⁴ Boone Pickens School of Geology, Oklahoma State University, Stillwater, OK 74074, United States. Electronic address: tingying.xu@okstate.edu.
⁵ State Key Laboratory of Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Guangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou 510642, China. Electronic address: chenhui@scau.edu.cn.
⁶ State Key Laboratory of Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Guangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou 510642, China. Electronic address: tangm@nwafu.edu.cn.

PMID: 39395377
DOI: 10.1016/j.micres.2024.127924

Abstract

Currently, little is known regarding the specific processes through which brassinosteroids (BR) affect arbuscular mycorrhizal (AM) symbiosis. Understanding this relationship is vital for advancing plant physiology and agricultural applications. In this study, we aimed to elucidate the regulatory mechanisms of BR in AM symbiosis. According to the log2 fold change-value and adjP-value, we integrated the common differentially expressed genes (DEGs) in maize (Zea mays L.) treated with BR and AM, Arabidopsis (Arabidopsis thaliana) mutants deficient in BR receptors, and tomato (Solanum lycopersicum) plants inoculated with AM fungi. In addition, we characterized the symbiotic performance of tomato plants with BR receptor defects and overexpression. The results indicated that the common differential genes induced by BR and AM were involved in metabolic processes, such as cell wall modification, cytoskeleton remodeling, auxin and ethylene signaling, photosynthesis, mineral nutrient transport, and stress defense. Specifically, these include the BR1 gene, which modifies the cell wall. However, the fungal colonization rate of BR receptor-deficient tomato plants was significantly reduced, and the total phosphorus concentration was increased. Conversely, the performance of the overexpressing tomato transformation plants demonstrated a significant contrast. Additionally, the mild rescue of mycorrhizal attenuation in mutants treated with exogenous BR suggests the possibility of direct feedback from BR synthesis to AM. Notably, the cell wall modification gene (SlBR1) and calcium spike gene (SlIPD3) were induced by both BR and AM, suggesting that BR may influence cell penetration during the early stages of AM colonization. Synthesis: Our results demonstrated that BR positively regulates AM symbiosis through multiple pathways. These findings pave the way for future research, including isolation of the individual contributions of each pathway to this complex process and exploration of possible agricultural applications.

Keywords: Arbuscular mycorrhiza; Brassinosteroid; Differential gene; Symbiotic regulation.