OXI1 and DAD Regulate Light-Induced Cell Death Antagonistically through Jasmonate and Salicylate Levels

Abstract

Singlet oxygen produced from triplet excited chlorophylls in photosynthesis is a signal molecule that can induce programmed cell death (PCD) through the action of the OXIDATIVE STRESS INDUCIBLE 1 (OXI1) kinase. Here, we identify two negative regulators of light-induced PCD that modulate <i>OXI1</i> expression: DAD1 and DAD2, homologs of the human antiapoptotic protein DEFENDER AGAINST CELL DEATH. Overexpressing <i>OXI1</i> in Arabidopsis (<i>Arabidopsis thaliana</i>) increased plant sensitivity to high light and induced early senescence of mature leaves. Both phenomena rely on a marked accumulation of jasmonate and salicylate. <i>DAD1</i> or <i>DAD2</i> overexpression decreased <i>OXI1</i> expression, jasmonate levels, and sensitivity to photooxidative stress. Knock-out mutants of <i>DAD1</i> or <i>DAD2</i> exhibited the opposite responses. Exogenous applications of jasmonate upregulated salicylate biosynthesis genes and caused leaf damage in wild-type plants but not in the salicylate biosynthesis mutant <i>Salicylic acid induction-deficient2</i>, indicating that salicylate plays a crucial role in PCD downstream of jasmonate. Treating plants with salicylate upregulated the <i>DAD</i> genes and downregulated <i>OXI1</i> We conclude that OXI1 and DAD are antagonistic regulators of cell death through modulating jasmonate and salicylate levels. High light-induced PCD thus results from a tight control of the relative activities of these regulating proteins, with DAD exerting a negative feedback control on <i>OXI1</i> expression.