Impaired Chloroplast Biogenesis in Immutans, an Arabidopsis Variegation Mutant, Modifies Developmental Programming, Cell Wall Composition and Resistance to Pseudomonas syringae
Abstract
The immutans (im) variegation mutation of Arabidopsis has green- and white- sectored leaves due to action of a nuclear recessive gene. IM codes for PTOX, a plastoquinol oxidase in plastid membranes. Previous studies have revealed that the green and white sectors develop into sources (green tissues) and sinks (white tissues) early in leaf development. In this report we focus on white sectors, and show that their transformation into effective sinks involves a sharp reduction in plastid number and size. Despite these reductions, cells in the white sectors have near-normal amounts of plastid RNA and protein, and surprisingly, a marked amplification of chloroplast DNA. The maintenance of protein synthesis capacity in the white sectors might poise plastids for their development into other plastid types. The green and white im sectors have different cell wall compositions: whereas cell walls in the green sectors resemble those in wild type, cell walls in the white sectors have reduced lignin and cellulose microfibrils, as well as alterations in galactomannans and the decoration of xyloglucan. These changes promote susceptibility to the pathogen Pseudomonas syringae. Enhanced susceptibility can also be explained by repressed expression of some, but not all, defense genes. We suggest that differences in morphology,more »
- Authors:
-
- Iowa State Univ., Ames, IA (United States); Russian Academy of Sciences (RAS), Moscow (Russian Federation). N.I. Vavilov Institute of General Genetics
- Iowa State Univ., Ames, IA (United States)
- Publication Date:
- Research Org.:
- Iowa State Univ., Ames, IA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1254840
- Grant/Contract Number:
- FG02-94ER20147
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Volume: 11; Journal Issue: 4; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Pogorelko, Gennady V., Kambakam, Sekhar, Nolan, Trevor, Foudree, Andrew, Zabotina, Olga A., and Rodermel, Steven R. Impaired Chloroplast Biogenesis in Immutans, an Arabidopsis Variegation Mutant, Modifies Developmental Programming, Cell Wall Composition and Resistance to Pseudomonas syringae. United States: N. p., 2016.
Web. doi:10.1371/journal.pone.0150983.
Pogorelko, Gennady V., Kambakam, Sekhar, Nolan, Trevor, Foudree, Andrew, Zabotina, Olga A., & Rodermel, Steven R. Impaired Chloroplast Biogenesis in Immutans, an Arabidopsis Variegation Mutant, Modifies Developmental Programming, Cell Wall Composition and Resistance to Pseudomonas syringae. United States. https://doi.org/10.1371/journal.pone.0150983
Pogorelko, Gennady V., Kambakam, Sekhar, Nolan, Trevor, Foudree, Andrew, Zabotina, Olga A., and Rodermel, Steven R. Wed .
"Impaired Chloroplast Biogenesis in Immutans, an Arabidopsis Variegation Mutant, Modifies Developmental Programming, Cell Wall Composition and Resistance to Pseudomonas syringae". United States. https://doi.org/10.1371/journal.pone.0150983. https://www.osti.gov/servlets/purl/1254840.
@article{osti_1254840,
title = {Impaired Chloroplast Biogenesis in Immutans, an Arabidopsis Variegation Mutant, Modifies Developmental Programming, Cell Wall Composition and Resistance to Pseudomonas syringae},
author = {Pogorelko, Gennady V. and Kambakam, Sekhar and Nolan, Trevor and Foudree, Andrew and Zabotina, Olga A. and Rodermel, Steven R.},
abstractNote = {The immutans (im) variegation mutation of Arabidopsis has green- and white- sectored leaves due to action of a nuclear recessive gene. IM codes for PTOX, a plastoquinol oxidase in plastid membranes. Previous studies have revealed that the green and white sectors develop into sources (green tissues) and sinks (white tissues) early in leaf development. In this report we focus on white sectors, and show that their transformation into effective sinks involves a sharp reduction in plastid number and size. Despite these reductions, cells in the white sectors have near-normal amounts of plastid RNA and protein, and surprisingly, a marked amplification of chloroplast DNA. The maintenance of protein synthesis capacity in the white sectors might poise plastids for their development into other plastid types. The green and white im sectors have different cell wall compositions: whereas cell walls in the green sectors resemble those in wild type, cell walls in the white sectors have reduced lignin and cellulose microfibrils, as well as alterations in galactomannans and the decoration of xyloglucan. These changes promote susceptibility to the pathogen Pseudomonas syringae. Enhanced susceptibility can also be explained by repressed expression of some, but not all, defense genes. We suggest that differences in morphology, physiology and biochemistry between the green and white sectors is caused by a reprogramming of leaf development that is coordinated, in part, by mechanisms of retrograde (plastid-tonucleus) signaling, perhaps mediated by ROS. Lastly, we conclude that variegation mutants offer a novel system to study leaf developmental programming, cell wall metabolism and hostpathogen interactions.},
doi = {10.1371/journal.pone.0150983},
journal = {PLoS ONE},
number = 4,
volume = 11,
place = {United States},
year = {Wed Apr 06 00:00:00 EDT 2016},
month = {Wed Apr 06 00:00:00 EDT 2016}
}
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The Roles of Reactive Oxygen Species in Plant Cells: Figure 1.
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IMMUTANS Does Not Act as a Stress-Induced Safety Valve in the Protection of the Photosynthetic Apparatus of Arabidopsis during Steady-State Photosynthesis
journal, August 2006
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Chloroplast Photooxidation-Induced Transcriptome Reprogramming in Arabidopsis immutans White Leaf Sectors
journal, April 2009
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A Comprehensive Toolkit of Plant Cell Wall Glycan-Directed Monoclonal Antibodies
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- Pattathil, S.; Avci, U.; Baldwin, D.
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Elevated Early Callose Deposition Results in Complete Penetration Resistance to Powdery Mildew in Arabidopsis
journal, January 2013
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gigantea Suppresses immutans Variegation by Interactions with Cytokinin and Gibberellin Signaling Pathways
journal, October 2014
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Plastid Signals Remodel Light Signaling Networks and Are Essential for Efficient Chloroplast Biogenesis in Arabidopsis
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The IMMUTANS Variegation Locus of Arabidopsis Defines a Mitochondrial Alternative Oxidase Homolog That Functions during Early Chloroplast Biogenesis
journal, January 1999
- Wu, Dongying; Wright, David A.; Wetzel, Carolyn
- The Plant Cell, Vol. 11, Issue 1
Mutations in the Arabidopsis Gene IMMUTANS Cause a Variegated Phenotype by Inactivating a Chloroplast Terminal Oxidase Associated with Phytoene Desaturation
journal, January 1999
- Carol, Pierre; Stevenson, David; Bisanz, Cordelia
- The Plant Cell, Vol. 11, Issue 1
Multistep Assembly of Chloroplast NADH Dehydrogenase-Like Subcomplex A Requires Several Nucleus-Encoded Proteins, Including CRR41 and CRR42, in Arabidopsis
journal, January 2012
- Peng, Lianwei; Fukao, Yoichiro; Fujiwara, Masayuki
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journal, September 2007
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Somatic Instability Caused by a Cysteine-Sensitive Gene in Arabidopsis
journal, February 1963
- Redei, G. P.
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The Plastid Terminal Oxidase: Its Elusive Function Points to Multiple Contributions to Plastid Physiology
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C HLORORESPIRATION
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The Initiation and Determination of Leaves
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The Mechanism of Variegation in immutans Provides Insight into Chloroplast Biogenesis
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ABI4 and its role in chloroplast retrograde communication
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The role of the secondary cell wall in plant resistance to pathogens
journal, August 2014
- Miedes, Eva; Vanholme, Ruben; Boerjan, Wout
- Frontiers in Plant Science, Vol. 5
Let there be light: Regulation of gene expression in plants
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