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Plastid Genome Instability Leads to Reactive Oxygen Species Production and Plastid-to-Nucleus Retrograde Signaling in Arabidopsis1[C][W][OPEN]

Instability of the plastid genome leads to the production of reactive oxygen species and to nuclear genetic reprogramming. The plastid genome is highly conserved among plant species, suggesting that alterations of its structure would have dramatic impacts on plant fitness. Nevertheless, little is known about the direct consequences of plastid genome instability. Recently, it was reported that the plastid Whirly proteins WHY1 and WHY3 and a specialized type-I polymerase, POLIB, act as safeguards against plastid genome instability in Arabidopsis (Arabidopsis thaliana). In this study, we use ciprofloxacin, an organelle double-strand break-inducing agent, and the why1why3polIb-1 variegated mutant to evaluate the impact of generalized plastid DNA instability. First, we show that in why1why3polIb-1 and ciprofloxacin-treated plants, plastid genome instability is associated with increased reactive oxygen species production. Then, using different light regimens, we show that the elevated reactive oxygen species production correlates with the appearance of a yellow-variegated phenotype in the why1why3polIb-1 population. This redox imbalance also correlates to modifications of nuclear gene expression patterns, which in turn leads to acclimation to high light. Taken together, these results indicate that plastid genome instability induces an oxidative burst that favors, through nuclear genetic reprogramming, adaptation to subsequent oxidative stresses.