MutS homolog 1 mutant of arabidopsis integrates organellenuclear signaling to create a complex, stress-primed and epigenetic phenotype

The plant-specific gene MSH1 is a dual-targeted protein localized to both plastids and mitochondria and participates in stability of the organelle genomes. Mutation in MSH1 resulted in the emergence of complex phenotype. To understand the nature of cellular responses to MSH1 depletion, we investigated the msh1 phenotype using hemi-complementation mutants. Depletion of MSH1 from the plastids results in variegation together with highly variable growth rate, enhanced drought and high light tolerance. Depletion of MSH1 from the plastids also associated with heritable, non-genetic changes in plant development (developmental reprogramming) such as delayed transition of maturity, flowering and DNA methylation. Depletion of MSH1 from the mitochondria results in 7-10% of plants displaying altered leaf morphologies, enhanced heat tolerance and mitochondrial genome rearrangements. Crossing msh1-developmentally reprogrammed plants with isogenic wild type produce epi-lines with heritable, enhanced growth vigor. Graft of wild type floral stems to msh1 root stock produce progeny with enhanced growth and altered CG methylation similar to epi-lines, suggesting that the MSH1 effect produces mobile signals. Genetic, biochemical and physiological studies indicate that MSH1 binds DNA and localize to plastid and mitochondrial nucleoids, associates with the thylakoid membrane and alters plastidial redox behavior. Confocal and light microcopy of GUS and GFP fusions to MSH1 show that the protein is expressed in meristems, floral organs, the vasculature and epidermis, and localizes to a subset of plastids that reside in the vascular parenchyma and epidermis. Fluorescence Activated Cell Sorting (FACS) revealed about 12 percent and 3 percent of MSH1 enrichment in stems and leaves, respectively. Ectopic expression of MSH1 produces deleterious growth effects, underlining its strict expression control. The MSH1 effect is a complex, inter-organellar, programmed signal integration conditioned by depletion of this singular plant-specific protein