The WRKY76-miR528-SOD2 module: regulating submergence tolerance through ROS scavenging in sorghum

New Phytol. 2025 Nov;248(4):1841-1856. doi: 10.1111/nph.70542. Epub 2025 Sep 4.

Abstract

Flooding significantly threatens global agricultural productivity, especially under the pressures of climate change. To address this urgent environmental challenge, the development of flooding-tolerant crops is imperative. However, our understanding of the molecular mechanisms underlying flooding tolerance in plants, particularly in crops, remains limited. Our findings demonstrate natural variation in submergence tolerance among diverse sorghum populations. Comparative transcriptomic analyses reveal that the submergence-tolerant accession SC473 exhibits a lower abundance of SbmiR528, a monocot-specific microRNA, compared with its sensitive counterpart SC449. This reduction correlates with an increased accumulation of Superoxide dismutase 2 (SOD2) transcript, which encodes one of the reactive oxygen species (ROS)-scavenging enzymes. We further reveal that the transcription factor SbWRKY76 directly binds the SbMIR528 promoter to activate its transcription. Notably, SbWRKY76 expression is significantly elevated in the submergence-sensitive variety SC449. Overexpression of either SbWRKY76 or SbMIR528 in sorghum results in reduced submergence tolerance. This study represents the first identification of the SbWRKY76-SbmiR528-SbSOD2 module as a novel regulatory axis governing sorghum submergence response by fine-tuning ROS scavenging. These findings offer pivotal targets for breeding or engineering climate-resilient crops to mitigate flooding impacts.

Keywords: ROS scavenging; SOD2; Sorghum; WRKY76; miR528; oxidative stress; submergence tolerance.

MeSH terms

  • Adaptation, Physiological* / genetics
  • Floods
  • Free Radical Scavengers* / metabolism
  • Gene Expression Regulation, Plant
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism
  • Plant Proteins* / genetics
  • Plant Proteins* / metabolism
  • Promoter Regions, Genetic / genetics
  • Reactive Oxygen Species* / metabolism
  • Sorghum* / genetics
  • Sorghum* / physiology
  • Superoxide Dismutase 2
  • Superoxide Dismutase* / genetics
  • Superoxide Dismutase* / metabolism
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism

Substances

  • Reactive Oxygen Species
  • MicroRNAs
  • Plant Proteins
  • Superoxide Dismutase
  • Transcription Factors
  • Free Radical Scavengers
  • Superoxide Dismutase 2