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

Authors

Kamaldeep S. Virdi, University of Nebraska - Lincoln
Yashitola Wamboldt, University of Nebraska-LincolnFollow
Hardik Kundariya, University of Nebraska-LincolnFollow
John D. Laurie, University of Nebraska-Lincoln
Ido Keren, University of Nebraska-Lincoln
K.R. Sunil Kumar, University of Nebraska-LincolnFollow
Anna Block, University of Nebraska-Lincoln
Gilles J. Basset, University of Nebraska-LincolnFollow
Steve Luebker, University of Nebraska-Lincoln
Christian Elowsky, University of Nebraska-LincolnFollow
Philip M. Day, University of Nebraska-Lincoln
Johnna L. Roose, Louisiana State University
Terry M. Bricker, Louisiana State University
Thomas Elthon, University of Nebraska - LincolnFollow
Sally A. Mackenzie, Pennsylvania State UniversityFollow

Document Type

Article

Date of this Version

2-2016

Citation

Virdi K.S., Wamboldt Y., Kundariya H., Laurie J.D., Keren I., Kumar K.R.S., Block A., Basset G., Luebker S., Elowsky C., Day P.M., Roose J.L., Bricker T.M., Elthon T., and Mackenzie S.A. (2016). MSH1 Is a Plant Organellar DNA Binding and Thylakoid Protein under Precise Spatial Regulation to Alter Development. Mol. Plant. 9, 245–260.

Comments

(c) The Author 2016. Open access.

Abstract

As metabolic centers, plant organelles participate in maintenance, defense, and signaling. MSH1 is a plantspecific 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.MSH1depletion 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.