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

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, transgenerationalmore » adaptation behaviors.« less
Authors:
 [1] ;  [2] ;  [2] ;  [2] ;  [2] ;  [2] ;  [2] ;  [2] ;  [2] ;  [3] ;  [2] ;  [4] ;  [4] ;  [2] ;  [2]
  1. Univ. of Nebraska, Lincoln, NE (United States). School of Biological Sciences
  2. Univ. of Nebraska, Lincoln, NE (United States). Dept. of Agronomy and Horticulture
  3. Univ. of Nebraska, Lincoln, NE (United States). Center for Biotechnology
  4. Louisiana State Univ., Baton Rouge, LA (United States). Dept. of Biological Sciences
Publication Date:
Grant/Contract Number:
FG02-98ER20310; OPP1088661
Type:
Accepted Manuscript
Journal Name:
Molecular Plant
Additional Journal Information:
Journal Volume: 9; Journal Issue: 2; Journal ID: ISSN 1674-2052
Publisher:
Elsevier
Research Org:
Louisiana State Univ., Baton Rouge, LA (United States); Univ. of Nebraska, Lincoln, NE (United States)
Sponsoring Org:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); Bill and Melinda Gates Foundation (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; thylakoid protein; organellar DNA binding; MSH1; epigenetic variation
OSTI Identifier:
1437105

Virdi, Kamaldeep S., Wamboldt, Yashitola, Kundariya, Hardik, Laurie, John D., Keren, Ido, Kumar, K. R.  Sunil, Block, Anna, Basset, Gilles, Luebker, Steve, Elowsky, Christian, Day, Philip M., Roose, Johnna L., Bricker, Terry M., Elthon, Thomas, and Mackenzie, Sally A.. MSH1 Is a Plant Organellar DNA Binding and Thylakoid Protein under Precise Spatial Regulation to Alter Development. United States: N. p., Web. doi:10.1016/j.molp.2015.10.011.
Virdi, Kamaldeep S., Wamboldt, Yashitola, Kundariya, Hardik, Laurie, John D., Keren, Ido, Kumar, K. R.  Sunil, Block, Anna, Basset, Gilles, Luebker, Steve, Elowsky, Christian, Day, Philip M., Roose, Johnna L., Bricker, Terry M., Elthon, Thomas, & Mackenzie, Sally A.. MSH1 Is a Plant Organellar DNA Binding and Thylakoid Protein under Precise Spatial Regulation to Alter Development. United States. doi:10.1016/j.molp.2015.10.011.
Virdi, Kamaldeep S., Wamboldt, Yashitola, Kundariya, Hardik, Laurie, John D., Keren, Ido, Kumar, K. R.  Sunil, Block, Anna, Basset, Gilles, Luebker, Steve, Elowsky, Christian, Day, Philip M., Roose, Johnna L., Bricker, Terry M., Elthon, Thomas, and Mackenzie, Sally A.. 2015. "MSH1 Is a Plant Organellar DNA Binding and Thylakoid Protein under Precise Spatial Regulation to Alter Development". United States. doi:10.1016/j.molp.2015.10.011. https://www.osti.gov/servlets/purl/1437105.
@article{osti_1437105,
title = {MSH1 Is a Plant Organellar DNA Binding and Thylakoid Protein under Precise Spatial Regulation to Alter Development},
author = {Virdi, Kamaldeep S. and Wamboldt, Yashitola and Kundariya, Hardik and Laurie, John D. and Keren, Ido and Kumar, K. R.  Sunil and Block, Anna and Basset, Gilles and Luebker, Steve and Elowsky, Christian and Day, Philip M. and Roose, Johnna L. and Bricker, Terry M. and Elthon, Thomas and Mackenzie, Sally A.},
abstractNote = {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.},
doi = {10.1016/j.molp.2015.10.011},
journal = {Molecular Plant},
number = 2,
volume = 9,
place = {United States},
year = {2015},
month = {11}
}