EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus ofArabidopsis thaliana

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Abstract
Shortly after the release of singlet oxygen (1O2), drastic changes in nuclear gene expression occur in the conditionalflumutant ofArabidopsisthat reveal a rapid transfer of signals from the plastid to the nucleus. In contrast to retrograde control of nuclear gene expression by plastid signals described earlier, the primary effect of1O2generation in theflumutant is not the control of chloroplast biogenesis but the activation of a broad range of signaling pathways known to be involved in biotic and abiotic stress responses. This activity of a plastid-derived signal suggests a new function of the chloroplast, namely that of a sensor of environmental changes that activates a broad range of stress responses. Inactivation of the plastid protein EXECUTER1 attenuates the extent of1O2-induced up-regulation of nuclear gene expression, but it does not fully eliminate these changes. A second related nuclear-encoded protein, dubbed EXECUTER2, has been identified that is also implicated with the signaling of1O2-dependent nuclear gene expression changes. Like EXECUTER1, EXECUTER2 is confined to the plastid. Inactivation of both EXECUTER proteins in theex1/ex2/flutriple mutant is sufficient to suppress the up-regulation of almost all1O2-responsive genes. Retrograde control of1O2-responsive genes requires the concerted action of both EXECUTER proteins within the plastid compartment.