MutS HOMOLOG1 Is a Nucleoid Protein That Alters Mitochondrial and Plastid Properties and Plant Response to High Light  

Abstract

Mitochondrial-plastid interdependence within the plant cell is presumed to be essential, but measurable demonstration of this intimate interaction is difficult. At the level of cellular metabolism, several biosynthetic pathways involve both mitochondrial-and plastid-localized steps. However, at an environmental response level, it is not clear how the two organelles intersect in programmed cellular responses. Here, we provide evidence, using genetic perturbation of the MutS Homolog1 (MSH1) nuclear gene in five plant species, that MSH1 functions within the mitochondrion and plastid to influence organellar genome behavior and plant growth patterns. The mitochondrial form of the protein participates in DNA recombination surveillance, with disruption of the gene resulting in enhanced mitochondrial genome recombination at numerous repeated sequences. The plastid-localized form of the protein interacts with the plastid genome and influences genome stability and plastid development, with its disruption leading to variegation of the plant. These developmental changes include altered patterns of nuclear gene expression. Consistency of plastid and mitochondrial response across both monocot and dicot species indicate that the dual-functioning nature of MSH1 is well conserved. Variegated tissues show changes in redox status together with enhanced plant survival and reproduction under photooxidative light conditions, evidence that the plastid changes triggered in this study comprise an adaptive response to naturally occurring light stress.

Multi-step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes

“…New mitochondrial genes may provide unique sources of genetic variation that have phenotypic consequences. These consequences can benefit natural adaptation and prove useful for crop breeding [10,42,[49][50][51]. In addition, the new CMS genes identified in this study could greatly expand the germplasm for hybrid rice breeding.…”

The Chloroplast Triggers Developmental Reprogramming When MUTS HOMOLOG1 Is Suppressed in Plants

“…Epigenomic changes appear to underlie at least some of the environmentally responsive phenotypic plasticity observed in natural systems (Bonduriansky and Day, 2009). In fact, MSH1 transcript levels show environmental responsiveness, with dramatically reduced levels under conditions of stress (Hruz et al, 2008;Shedge et al, 2010;Xu et al, 2011). Moreover, disruption of MSH1 produces an altered redox state of the plastid , implying one means of signaling cellular change.…”

“…The development of RNAi suppression lines of tomato (Solanum lycopersicum) and tobacco (Nicotiana tabacum; Sandhu et al, 2007), millet (Pennisetum americanum) and sorghum (Sorghum bicolor; Xu et al, 2011), and Arabidopsis hemicomplementation lines ) is described elsewhere. Individual RNAi constructs were developed to target the same region of MSH1 domain VI in each species, and analysis of phenotypes is based on five lead events carried forward of tomato and tobacco, three of millet, and one of sorghum.…”

“…Microarray experiments were carried out as described by Xu et al (2011). Total RNA was extracted from 8-week-old Col-0 and msh1 mutant Arabidopsis plants using TRIzol (Invitrogen) extraction procedures followed by purification on RNeasy columns (Qiagen).…”

Widespread dual targeting of proteins in land plants: When, where, how and why

“…19 With the dual-targeted MUTS homolog 1, targeted to mitochondria and plastids, plastid dysfunction was concluded to be the primary lesion in the mutant line. 20 Several proposals have been put forward to explain dual targeting of proteins. One proposal is simply that fewer proteins remains the most cost effective and simple approach to identify dual targeted proteins.…”