ERF Transcription Factor PagERF135A Negatively Regulates Drought Tolerance in Poplar by Modulating Sucrose Metabolism and Brassinosteroid Biosynthesis

ABSTRACT

Drought is one of the primary environmental constraints limiting poplar growth. Identifying key drought‐resistance genes and their regulatory mechanisms is crucial for genetic improvement of drought tolerance in poplar. Time‐course transcriptome analysis of 84K poplar ( Populus alba  ×  P. glandulosa ) under drought stress revealed that the ERF family is among the most responsive transcription factor families, and PagERF135A exhibited the most significant upregulation, suggesting a key regulatory role. Genome‐wide identification of the ERF family in 84K poplar identified 276 members, with expansion primarily through segmental duplication, and purifying selection dominated their evolution. PagERF135A is a nuclear‐localized transcription factor with transcriptional activation activity. Overexpression of PagERF135A reduced drought tolerance in transgenic poplars, manifested by aggravated oxidative damage, diminished osmotic adjustments, and impaired PSII and PSI activities. Integrated transcriptomic and WGCNA analyses showed that PagERF135A overexpression suppressed drought‐induced expression of soluble sugar synthesis genes in starch‐sucrose metabolism, down‐regulated brassinosteroid biosynthesis and signaling genes, and promoted catabolic genes. Thus, PagERF135A negatively regulates drought tolerance by disrupting carbon metabolic flow and brassinosteroid signaling homeostasis. Our findings provide new insights into ERF‐mediated drought response mechanisms in poplar.