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Title: MSH1 is a plant organellar DNA binding and thylakoid protein under precise spatial regulation to alter development

item VIRDI, KAMALDEEP - University Of Nebraska
item WAMBOLDT, YASHITOLA - University Of Nebraska
item KUNDARIYA, HARDIK - University Of Nebraska
item LAURIE, JOHN - University Of Nebraska
item KEREN, IDO - University Of Nebraska
item KUMAR, SUNIL - University Of Nebraska
item Block, Anna
item BASSET, GILLES - University Of Nebraska
item LUEBKER, STEVE - University Of Nebraska
item ELOWSKY, CHRISTIAN - University Of Nebraska
item DAY, PHILIP - University Of Nebraska
item ROOSE, JOHNNA - Louisiana State University
item BRICKER, TERRY - Louisiana State University
item ELTHON, THOMAS - University Of Nebraska
item MACKENZIE, SALLY - University Of Nebraska

Submitted to: Molecular Plant
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/30/2015
Publication Date: 2/1/2016
Citation: Virdi, K.S., Wamboldt, Y., Kundariya, H., Laurie, J.D., Keren, I., Kumar, S., Block, A.K., Basset, G., Luebker, S., Elowsky, C., Day, P.M., Roose, J.L., Bricker, T.M., Elthon, T., Mackenzie, S.A. 2016. MSH1 is a plant organellar DNA binding and thylakoid protein under precise spatial regulation to alter development. Molecular Plant. 9(2):245-260.

Interpretive Summary: In order to survive in changing environmental conditions plants must be able to adapt to new conditions and transmit these adaptations to their progeny. Little is currently known about how plants perform these adaptations. Here we show that a plant protein called MSH1 plays a role in such adaptations by targeting plant organelles in specific cell types leading to heritable, non-genetic changes in development. Loss of this protein leads to variegation, heat tolerance, variable growth rate, and delayed maturity and flowering times. Interestingly we showed that even when MSH1 is restored to the plant, the phenotypic changes caused by its loss remain through subsequent generations. Unraveling the complex response to MSH1 offers insight into plants adaptive responses beyond the level of classical genetics and in the long term could aid in the development of stress resistant crops.

Technical 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, yet 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 nongenetic 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 subset 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, trans-generational adaptation behaviors.