title: 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.
authors.affiliation: School of Biological Sciences, University of Nebraska, Lincoln, NE 68588, USA.
authors.forename: Kamaldeep S
authors.initials: KS
authors.lastname: Virdi
authors.affiliation: Department of Agronomy and Horticulture, University of Nebraska, Lincoln, NE 68588, USA.
authors.forename: Yashitola
authors.initials: Y
authors.lastname: Wamboldt
authors.affiliation: Department of Agronomy and Horticulture, University of Nebraska, Lincoln, NE 68588, USA.
authors.forename: Hardik
authors.initials: H
authors.lastname: Kundariya
authors.affiliation: Department of Agronomy and Horticulture, University of Nebraska, Lincoln, NE 68588, USA.
authors.forename: John D
authors.initials: JD
authors.lastname: Laurie
authors.affiliation: Department of Agronomy and Horticulture, University of Nebraska, Lincoln, NE 68588, USA.
authors.forename: Ido
authors.initials: I
authors.lastname: Keren
authors.affiliation: Department of Agronomy and Horticulture, University of Nebraska, Lincoln, NE 68588, USA.
authors.forename: K R Sunil
authors.initials: KRS
authors.lastname: Kumar
authors.affiliation: Department of Agronomy and Horticulture, University of Nebraska, Lincoln, NE 68588, USA.
authors.forename: Anna
authors.initials: A
authors.lastname: Block
authors.affiliation: Department of Agronomy and Horticulture, University of Nebraska, Lincoln, NE 68588, USA.
authors.forename: Gilles
authors.initials: G
authors.lastname: Basset
authors.affiliation: Department of Agronomy and Horticulture, University of Nebraska, Lincoln, NE 68588, USA.
authors.forename: Steve
authors.initials: S
authors.lastname: Luebker
authors.affiliation: Center for Biotechnology, University of Nebraska, Lincoln, NE 68588, USA.
authors.forename: Christian
authors.initials: C
authors.lastname: Elowsky
authors.affiliation: Department of Agronomy and Horticulture, University of Nebraska, Lincoln, NE 68588, USA.
authors.forename: Philip M
authors.initials: PM
authors.lastname: Day
authors.affiliation: Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA.
authors.forename: Johnna L
authors.initials: JL
authors.lastname: Roose
authors.affiliation: Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA.
authors.forename: Terry M
authors.initials: TM
authors.lastname: Bricker
authors.affiliation: Department of Agronomy and Horticulture, University of Nebraska, Lincoln, NE 68588, USA.
authors.forename: Thomas
authors.initials: T
authors.lastname: Elthon
authors.affiliation: Department of Agronomy and Horticulture, University of Nebraska, Lincoln, NE 68588, USA. Electronic address: smackenzie2@unl.edu.
authors.forename: Sally A
authors.initials: SA
authors.lastname: Mackenzie
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D018744:DNA, Plant / Q000235:genetics / Q000378:metabolism; D004268:DNA-Binding Proteins / Q000235:genetics / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant; D008928:Mitochondria / Q000235:genetics / Q000378:metabolism; D051719:MutS DNA Mismatch-Binding Protein / Q000235:genetics / Q000378:metabolism*; D018087:Plastids / Q000235:genetics / Q000378:metabolism; D020524:Thylakoids / Q000235:genetics / Q000378:metabolism*
chemical_list: D029681:Arabidopsis Proteins; D018744:DNA, Plant; D004268:DNA-Binding Proteins; C523213:MSH1 protein, Arabidopsis; D051719:MutS DNA Mismatch-Binding Protein
keywords: Epigenetic variation; MSH1; Organellar DNA binding; Thylakoid protein