Muts homolog1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light

Ying Zhi Xu, Maria P. Arrieta-Montiel, Kamaldeep S. Virdi, Wilson B.M. de Paula, Joshua R. Widhalm, Gilles J. Basset, Jaime I. Davila, Thomas E. Elthon, Christian G. Elowsky, Shirley J. Sato, Thomas E. Clemente, Sally A. Mackenzie

Research output: Contribution to journalArticle

66 Citations (Scopus)

Abstract

Mitochondrial-plastid interdependence within the plant cell is presumed to be essential, but measurable demonstration of this intimate interaction is difficult. At the level of cellular metabolism, several biosynthetic pathways involve both mitochondrial- and plastid-localized steps. However, at an environmental response level, it is not clear how the two organelles intersect in programmed cellular responses. Here, we provide evidence, using genetic perturbation of the MutS Homolog1 (MSH1) nuclear gene in five plant species, that MSH1 functions within the mitochondrion and plastid to influence organellar genome behavior and plant growth patterns. The mitochondrial form of the protein participates in DNA recombination surveillance, with disruption of the gene resulting in enhanced mitochondrial genome recombination at numerous repeated sequences. The plastid-localized form of the protein interacts with the plastid genome and influences genome stability and plastid development, with its disruption leading to variegation of the plant. These developmental changes include altered patterns of nuclear gene expression. Consistency of plastid and mitochondrial response across both monocot and dicot species indicate that the dual-functioning nature of MSH1 is well conserved. Variegated tissues show changes in redox status together with enhanced plant survival and reproduction under photooxidative light conditions, evidence that the plastid changes triggered in this study comprise an adaptive response to naturally occurring light stress.

Original languageEnglish (US)
Pages (from-to)3428-3441
Number of pages14
JournalPlant Cell
Volume23
Issue number9
DOIs
StatePublished - Sep 1 2011

Fingerprint

Chloroplast Proteins
Plastids
Mitochondrial Proteins
plastids
plant response
Light
proteins
Genetic Recombination
Plastid Genomes
Plant Genome
Mitochondrial Genome
genome
Genomic Instability
Biosynthetic Pathways
Plant Cells
gene targeting
Magnoliopsida
Liliopsida
Organelles
Genes

ASJC Scopus subject areas

  • Plant Science
  • Cell Biology

Cite this

Xu, Y. Z., Arrieta-Montiel, M. P., Virdi, K. S., de Paula, W. B. M., Widhalm, J. R., Basset, G. J., ... Mackenzie, S. A. (2011). Muts homolog1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light. Plant Cell, 23(9), 3428-3441. https://doi.org/10.1105/tpc.111.089136

Muts homolog1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light. / Xu, Ying Zhi; Arrieta-Montiel, Maria P.; Virdi, Kamaldeep S.; de Paula, Wilson B.M.; Widhalm, Joshua R.; Basset, Gilles J.; Davila, Jaime I.; Elthon, Thomas E.; Elowsky, Christian G.; Sato, Shirley J.; Clemente, Thomas E.; Mackenzie, Sally A.

In: Plant Cell, Vol. 23, No. 9, 01.09.2011, p. 3428-3441.

Research output: Contribution to journalArticle

Xu, YZ, Arrieta-Montiel, MP, Virdi, KS, de Paula, WBM, Widhalm, JR, Basset, GJ, Davila, JI, Elthon, TE, Elowsky, CG, Sato, SJ, Clemente, TE & Mackenzie, SA 2011, 'Muts homolog1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light', Plant Cell, vol. 23, no. 9, pp. 3428-3441. https://doi.org/10.1105/tpc.111.089136
Xu YZ, Arrieta-Montiel MP, Virdi KS, de Paula WBM, Widhalm JR, Basset GJ et al. Muts homolog1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light. Plant Cell. 2011 Sep 1;23(9):3428-3441. https://doi.org/10.1105/tpc.111.089136
Xu, Ying Zhi ; Arrieta-Montiel, Maria P. ; Virdi, Kamaldeep S. ; de Paula, Wilson B.M. ; Widhalm, Joshua R. ; Basset, Gilles J. ; Davila, Jaime I. ; Elthon, Thomas E. ; Elowsky, Christian G. ; Sato, Shirley J. ; Clemente, Thomas E. ; Mackenzie, Sally A. / Muts homolog1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light. In: Plant Cell. 2011 ; Vol. 23, No. 9. pp. 3428-3441.
@article{510b0f2c61fc420b97861852bdc6ad71,
title = "Muts homolog1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light",
abstract = "Mitochondrial-plastid interdependence within the plant cell is presumed to be essential, but measurable demonstration of this intimate interaction is difficult. At the level of cellular metabolism, several biosynthetic pathways involve both mitochondrial- and plastid-localized steps. However, at an environmental response level, it is not clear how the two organelles intersect in programmed cellular responses. Here, we provide evidence, using genetic perturbation of the MutS Homolog1 (MSH1) nuclear gene in five plant species, that MSH1 functions within the mitochondrion and plastid to influence organellar genome behavior and plant growth patterns. The mitochondrial form of the protein participates in DNA recombination surveillance, with disruption of the gene resulting in enhanced mitochondrial genome recombination at numerous repeated sequences. The plastid-localized form of the protein interacts with the plastid genome and influences genome stability and plastid development, with its disruption leading to variegation of the plant. These developmental changes include altered patterns of nuclear gene expression. Consistency of plastid and mitochondrial response across both monocot and dicot species indicate that the dual-functioning nature of MSH1 is well conserved. Variegated tissues show changes in redox status together with enhanced plant survival and reproduction under photooxidative light conditions, evidence that the plastid changes triggered in this study comprise an adaptive response to naturally occurring light stress.",
author = "Xu, {Ying Zhi} and Arrieta-Montiel, {Maria P.} and Virdi, {Kamaldeep S.} and {de Paula}, {Wilson B.M.} and Widhalm, {Joshua R.} and Basset, {Gilles J.} and Davila, {Jaime I.} and Elthon, {Thomas E.} and Elowsky, {Christian G.} and Sato, {Shirley J.} and Clemente, {Thomas E.} and Mackenzie, {Sally A.}",
year = "2011",
month = "9",
day = "1",
doi = "10.1105/tpc.111.089136",
language = "English (US)",
volume = "23",
pages = "3428--3441",
journal = "Plant Cell",
issn = "1040-4651",
publisher = "American Society of Plant Biologists",
number = "9",

}

TY - JOUR

T1 - Muts homolog1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light

AU - Xu, Ying Zhi

AU - Arrieta-Montiel, Maria P.

AU - Virdi, Kamaldeep S.

AU - de Paula, Wilson B.M.

AU - Widhalm, Joshua R.

AU - Basset, Gilles J.

AU - Davila, Jaime I.

AU - Elthon, Thomas E.

AU - Elowsky, Christian G.

AU - Sato, Shirley J.

AU - Clemente, Thomas E.

AU - Mackenzie, Sally A.

PY - 2011/9/1

Y1 - 2011/9/1

N2 - Mitochondrial-plastid interdependence within the plant cell is presumed to be essential, but measurable demonstration of this intimate interaction is difficult. At the level of cellular metabolism, several biosynthetic pathways involve both mitochondrial- and plastid-localized steps. However, at an environmental response level, it is not clear how the two organelles intersect in programmed cellular responses. Here, we provide evidence, using genetic perturbation of the MutS Homolog1 (MSH1) nuclear gene in five plant species, that MSH1 functions within the mitochondrion and plastid to influence organellar genome behavior and plant growth patterns. The mitochondrial form of the protein participates in DNA recombination surveillance, with disruption of the gene resulting in enhanced mitochondrial genome recombination at numerous repeated sequences. The plastid-localized form of the protein interacts with the plastid genome and influences genome stability and plastid development, with its disruption leading to variegation of the plant. These developmental changes include altered patterns of nuclear gene expression. Consistency of plastid and mitochondrial response across both monocot and dicot species indicate that the dual-functioning nature of MSH1 is well conserved. Variegated tissues show changes in redox status together with enhanced plant survival and reproduction under photooxidative light conditions, evidence that the plastid changes triggered in this study comprise an adaptive response to naturally occurring light stress.

AB - Mitochondrial-plastid interdependence within the plant cell is presumed to be essential, but measurable demonstration of this intimate interaction is difficult. At the level of cellular metabolism, several biosynthetic pathways involve both mitochondrial- and plastid-localized steps. However, at an environmental response level, it is not clear how the two organelles intersect in programmed cellular responses. Here, we provide evidence, using genetic perturbation of the MutS Homolog1 (MSH1) nuclear gene in five plant species, that MSH1 functions within the mitochondrion and plastid to influence organellar genome behavior and plant growth patterns. The mitochondrial form of the protein participates in DNA recombination surveillance, with disruption of the gene resulting in enhanced mitochondrial genome recombination at numerous repeated sequences. The plastid-localized form of the protein interacts with the plastid genome and influences genome stability and plastid development, with its disruption leading to variegation of the plant. These developmental changes include altered patterns of nuclear gene expression. Consistency of plastid and mitochondrial response across both monocot and dicot species indicate that the dual-functioning nature of MSH1 is well conserved. Variegated tissues show changes in redox status together with enhanced plant survival and reproduction under photooxidative light conditions, evidence that the plastid changes triggered in this study comprise an adaptive response to naturally occurring light stress.

UR - http://www.scopus.com/inward/record.url?scp=80054969644&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=80054969644&partnerID=8YFLogxK

U2 - 10.1105/tpc.111.089136

DO - 10.1105/tpc.111.089136

M3 - Article

C2 - 21934144

AN - SCOPUS:80054969644

VL - 23

SP - 3428

EP - 3441

JO - Plant Cell

JF - Plant Cell

SN - 1040-4651

IS - 9

ER -