Singlet oxygen induces cell wall thickening and stomatal density reducing by transcriptome reprogramming

Abstract

Singlet oxygen (¹O₂) has a very short half-life of 10⁻⁵ s; however, it is a strong oxidant that causes growth arrest and necrotic lesions on plants. Its signaling pathway remains largely unknown. The Arabidopsis flu (FLUORESCENT) mutant accumulates a high level of ¹O₂ and shows drastic changes in nuclear gene expression. Only two plastid proteins, EX1 (EXECUTER 1) and EX2 (EXECUTER 2), have been identified in the singlet oxygen signaling. Here we found that the transcription factor ABI4 (ABSCISIC ACID INSENSITIVE 4) binds the promoters of genes responsive to ¹O₂-signals. Inactivation of the ABI4 protein in the flu/abi4 double mutant was sufficient to compromise the changes of almost all ¹O₂-responsive-genes and rescued the lethal phenotype of flu grown under light / dark cycles, similar to the flu/ex1/ex2 triple mutant. In addition to cell death, we reported for the first time that ¹O₂ also induces cell wall thickening and stomatal development defect. Contrastingly, no apparent growth arrest was observed for the flu mutant under normal light / dim light cycles, but the cell wall thickening (doubled) and stomatal density reduction (by two-thirds) still occurred. These results offer a new idea for breeding stress tolerant plants.