MSH1 Is a Plant Organellar DNA Binding and Thylakoid Protein under Precise Spatial Regulation to Alter Development

Abstract

As metabolic centers, plant organelles participate in maintenance, defense, and signaling. MSH1 is a plant-specific protein involved in organellar genome stability in mitochondria and plastids. Plastid depletion of MSH1 causes heritable, non-genetic changes in development and DNA methylation. We investigated the msh1 phenotype using hemi-complementation mutants and transgene-null segregants from RNAi suppression lines to sub-compartmentalize MSH1 effects. We show that MSH1 expression is spatially regulated, specifically localizing to plastids within the epidermis and vascular parenchyma. The protein binds DNA and localizes to plastid and mitochondrial nucleoids, but fractionation and protein-protein interactions data indicate that MSH1 also associates with the thylakoid membrane. Plastid MSH1 depletion results in variegation, abiotic stress tolerance, variable growth rate, and delayed maturity. Depletion from mitochondria results in 7%-10% of plants altered in leaf morphology, heat tolerance, and mitochondrial genome stability. MSH1 does not localize within the nucleus directly, but plastid depletion produces non-genetic changes in flowering time, maturation, and growth rate that are heritable independent of MSH1. MSH1 depletion alters non-photoactive redox behavior in plastids and a sub-set of mitochondrially altered lines. Ectopic expression produces deleterious effects, underlining its strict expression control. Unraveling the complexity of the MSH1 effect offers insight into triggers of plant-specific, transgenerational adaptation behaviors.

An epigenetic breeding system in soybean for increased yield and stability

“…In Arabidopsis msh1 T-DNA insertion lines, phenotypes include leaf variegation, reduced growth rate, delayed flowering, extended juvenility, altered floral morphology, aerial rosettes and enhanced secondary growth (Xu et al, 2012). These mutants also show tolerance to heat, high light and drought stress (Shedge et al, 2010;Virdi et al, 2016;Xu et al, 2011). These pleiotropic phenotypes are largely attributed to depletion of MSH1 from plastids, evidenced by hemi-complementation analysis (Xu et al, 2012), and the msh1-triggered plastid changes condition genomewide methylome repatterning (Virdi et al, 2015).…”

Regulatory Shifts in Plastid Transcription Play a Key Role in Morphological Conversions of Plastids during Plant Development

“…It should be noted that tissue-specific gene expression analyses distinguishing epidermal and mesophyll tissues were never reported and that the results in all studies to date, thus, represent a mixture of both cell types. This is critical with respect to the notion that recent studies suggest a specific sensor function for epidermal chloroplasts (Virdi et al, 2015, 2016). Targeted research on this special type of chloroplasts will be required in order to understand their detailed physiological function.…”

Epigenomic plasticity of Arabidopsismsh1mutants under prolonged cold stress

“…Previous studies have shown that msh1 mutants are more tolerant to drought, high light, and heat stress (Shedge et al, 2010; Virdi et al, 2016; Xu et al, 2011). We tested for other abiotic stress effects, focusing first on salt and freezing temperature.…”

“…Arabidopsis msh1 mutants display a range of altered phenotypes that include variegation, dwarfing, delayed maturity transition, delayed flowering, and partial male sterility (Xu et al, 2011). The msh1 mutants display higher tolerance to heat, high light, and drought stress (Shedge et al, 2010; Virdi et al, 2016; Xu et al, 2011), particularly in individuals showing stronger developmental phenotypes. MSH1 phenotypes are conserved between monocots and eudicots.…”