Impaired Chloroplast Biogenesis in Immutans, an Arabidopsis Variegation Mutant, Modifies Developmental Programming, Cell Wall Composition and Resistance to Pseudomonas syringae

Pogorelko, Gennady V.; Kambakam, Sekhar; Nolan, Trevor; Foudree, Andrew; Zabotina, Olga A.; Rodermel, Steven R.

doi:10.1371/journal.pone.0150983

Title: Impaired Chloroplast Biogenesis in Immutans, an Arabidopsis Variegation Mutant, Modifies Developmental Programming, Cell Wall Composition and Resistance to Pseudomonas syringae

Journal Article · Wed Apr 06 00:00:00 EDT 2016 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0150983· OSTI ID:1254840

Pogorelko, Gennady V. ^[1]; Kambakam, Sekhar ^[2]; Nolan, Trevor ^[2]; Foudree, Andrew ^[2]; Zabotina, Olga A. ^[2]; Rodermel, Steven R. ^[2]

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)

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.

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Research Organization:: Iowa State Univ., Ames, IA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: FG02-94ER20147

OSTI ID:: 1254840

Journal Information:: PLoS ONE, Vol. 11, Issue 4; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 16 works

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References (58)

Arabidopsis variegation mutants: new insights into chloroplast biogenesis Aluru, M. R. Journal of Experimental Botany, Vol. 57, Issue 9 https://doi.org/10.1093/jxb/erj008	journal	January 2006
Variegation mutants and mechanisms of chloroplast biogenesis: Variegation mutants Yu, Fei; Fu, Aigen; Aluru, Maneesha Plant, Cell & Environment, Vol. 30, Issue 3 https://doi.org/10.1111/j.1365-3040.2006.01630.x	journal	January 2007
Flexibility in photosynthetic electron transport: The physiological role of plastoquinol terminal oxidase (PTOX) McDonald, Allison E.; Ivanov, Alex G.; Bode, Rainer Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 8 https://doi.org/10.1016/j.bbabio.2010.10.024	journal	August 2011
Understanding chloroplast biogenesis using second-site suppressors of immutans and var2 Putarjunan, Aarthi; Liu, Xiayan; Nolan, Trevor Photosynthesis Research, Vol. 116, Issue 2-3 https://doi.org/10.1007/s11120-013-9855-9	journal	May 2013
The Mechanism of Variegation in immutans Provides Insight into Chloroplast Biogenesis Foudree, Andrew; Putarjunan, Aarthi; Kambakam, Sekhar Frontiers in Plant Science, Vol. 3 https://doi.org/10.3389/fpls.2012.00260	journal	January 2012
The IMMUTANS Variegation Locus of Arabidopsis Defines a Mitochondrial Alternative Oxidase Homolog That Functions during Early Chloroplast Biogenesis Wu, Dongying; Wright, David A.; Wetzel, Carolyn The Plant Cell, Vol. 11, Issue 1 https://doi.org/10.1105/tpc.11.1.43	journal	January 1999
Mutations in the Arabidopsis Gene IMMUTANS Cause a Variegated Phenotype by Inactivating a Chloroplast Terminal Oxidase Associated with Phytoene Desaturation Carol, Pierre; Stevenson, David; Bisanz, Cordelia The Plant Cell, Vol. 11, Issue 1 https://doi.org/10.1105/tpc.11.1.57	journal	January 1999
The Plastid Terminal Oxidase: Its Elusive Function Points to Multiple Contributions to Plastid Physiology Nawrocki, Wojciech J.; Tourasse, Nicolas J.; Taly, Antoine Annual Review of Plant Biology, Vol. 66, Issue 1 https://doi.org/10.1146/annurev-arplant-043014-114744	journal	April 2015
Photosynthetic Redox Imbalance Governs Leaf Sectoring in the Arabidopsis thaliana Variegation Mutants immutans , spotty , var1 , and var2 Rosso, Dominic; Bode, Rainer; Li, Wenze The Plant Cell, Vol. 21, Issue 11 https://doi.org/10.1105/tpc.108.062752	journal	November 2009
IMMUTANS Does Not Act as a Stress-Induced Safety Valve in the Protection of the Photosynthetic Apparatus of Arabidopsis during Steady-State Photosynthesis Rosso, Dominic; Ivanov, Alexander G.; Fu, Aigen Plant Physiology, Vol. 142, Issue 2 https://doi.org/10.1104/pp.106.085886	journal	August 2006
Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response Rumeau, Dominique; Peltier, Gilles; Cournac, Laurent Plant, Cell & Environment, Vol. 30, Issue 9 https://doi.org/10.1111/j.1365-3040.2007.01675.x	journal	September 2007
C HLORORESPIRATION Peltier, Gilles; Cournac, Laurent Annual Review of Plant Biology, Vol. 53, Issue 1 https://doi.org/10.1146/annurev.arplant.53.100301.135242	journal	June 2002
Multistep Assembly of Chloroplast NADH Dehydrogenase-Like Subcomplex A Requires Several Nucleus-Encoded Proteins, Including CRR41 and CRR42, in Arabidopsis Peng, Lianwei; Fukao, Yoichiro; Fujiwara, Masayuki The Plant Cell, Vol. 24, Issue 1 https://doi.org/10.1105/tpc.111.090597	journal	January 2012
Physiological links among alternative electron transport pathways that reduce and oxidize plastoquinone in Arabidopsis: PSI cyclic electron transport and PTOX Okegawa, Yuki; Kobayashi, Yoshichika; Shikanai, Toshiharu The Plant Journal, Vol. 63, Issue 3 https://doi.org/10.1111/j.1365-313X.2010.04252.x	journal	May 2010
Implications of alternative electron sinks in increased resistance of PSII and PSI photochemistry to high light stress in cold-acclimated Arabidopsis thaliana Ivanov, A. G.; Rosso, D.; Savitch, L. V. Photosynthesis Research, Vol. 113, Issue 1-3 https://doi.org/10.1007/s11120-012-9769-y	journal	July 2012
The Initiation and Determination of Leaves. Smith, L. G.; Hake, S. The Plant Cell https://doi.org/10.1105/tpc.4.9.1017	journal	September 1992
Chloroplast Development and Gene Expression Mullet, J. E. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 39, Issue 1 https://doi.org/10.1146/annurev.pp.39.060188.002355	journal	June 1988
Cellular Differentiation and Leaf Morphogenesis in Arabdopsis Pyke, K. Critical Reviews in Plant Sciences, Vol. 18, Issue 4 https://doi.org/10.1016/S0735-2689(99)00390-1	journal	July 1999
The Arabidopsis immutans Mutation Affects Plastid Differentiation and the Morphogenesis of White and Green Sectors in Variegated Plants Aluru, Maneesha R.; Bae, Hanhong; Wu, Dongying Plant Physiology, Vol. 127, Issue 1 https://doi.org/10.1104/pp.127.1.67	journal	September 2001
Alterations in photosynthesis in Arabidopsis lacking IMMUTANS, a chloroplast terminal oxidase Aluru, Maneesha R.; Stessman, Dan J.; Spalding, Martin H. Photosynthesis Research, Vol. 91, Issue 1 https://doi.org/10.1007/s11120-005-9021-0	journal	March 2007
Chloroplast Photooxidation-Induced Transcriptome Reprogramming in Arabidopsis immutans White Leaf Sectors Aluru, Maneesha R.; Zola, Jaroslaw; Foudree, Andrew Plant Physiology, Vol. 150, Issue 2 https://doi.org/10.1104/pp.109.135780	journal	April 2009
DAPI: a DNA-Specific Fluorescent Probe Kapuscinski, Jan Biotechnic & Histochemistry, Vol. 70, Issue 5 https://doi.org/10.3109/10520299509108199	journal	January 1995
A Comprehensive Toolkit of Plant Cell Wall Glycan-Directed Monoclonal Antibodies Pattathil, S.; Avci, U.; Baldwin, D. Plant Physiology, Vol. 153, Issue 2, p. 514-525 https://doi.org/10.1104/pp.109.151985	journal	April 2010
Eine neue Reihe organischer Diamine; Schiff, Hugo Annalen der Chemie und Pharmacie, Vol. 140, Issue 1 https://doi.org/10.1002/jlac.18661400106	journal	January 1866
The Association of Druse Crystals with the Developing Stomium of Capsicum annuum (Solanaceae) Anthers Horner, Harry T.; Wagner, Bruce L. American Journal of Botany, Vol. 67, Issue 9 https://doi.org/10.2307/2442137	journal	October 1980
Arabidopsis XXT5 gene encodes a putative α-1,6-xylosyltransferase that is involved in xyloglucan biosynthesis Zabotina, Olga A.; van de Ven, Wilhelmina T. G.; Freshour, Glenn The Plant Journal, Vol. 56, Issue 1 https://doi.org/10.1111/j.1365-313X.2008.03580.x	journal	October 2008
Post-synthetic modification of plant cell walls by expression of microbial hydrolases in the apoplast Pogorelko, Gennady; Fursova, Oksana; Lin, Ming Plant Molecular Biology, Vol. 77, Issue 4-5 https://doi.org/10.1007/s11103-011-9822-9	journal	September 2011
Lhcb Transcription Is Coordinated with Cell Size and Chlorophyll Accumulation (Studies on Fluorescence-Activated, Cell-Sorter-Purified Single Cells from Wild-Type and immutans Arabidopsis thaliana) Meehan, L.; Harkins, K.; Chory, J. Plant Physiology, Vol. 112, Issue 3 https://doi.org/10.1104/pp.112.3.953	journal	November 1996
gigantea Suppresses immutans Variegation by Interactions with Cytokinin and Gibberellin Signaling Pathways Putarjunan, Aarthi; Rodermel, Steve Plant Physiology, Vol. 166, Issue 4 https://doi.org/10.1104/pp.114.250647	journal	October 2014
White Leaf Sectors in yellow variegated2 Are Formed by Viable Cells with Undifferentiated Plastids Kato, Yusuke; Miura, Eiko; Matsushima, Ryo Plant Physiology, Vol. 144, Issue 2 https://doi.org/10.1104/pp.107.099002	journal	April 2007
Elevated Early Callose Deposition Results in Complete Penetration Resistance to Powdery Mildew in Arabidopsis Ellinger, Dorothea; Naumann, Marcel; Falter, Christian Plant Physiology, Vol. 161, Issue 3 https://doi.org/10.1104/pp.112.211011	journal	January 2013
Proteomic comparison of etioplast and chloroplast protein complexes Plöscher, Matthias; Reisinger, Veronika; Eichacker, Lutz A. Journal of Proteomics, Vol. 74, Issue 8 https://doi.org/10.1016/j.jprot.2011.03.020	journal	August 2011
Somatic Instability Caused by a Cysteine-Sensitive Gene in Arabidopsis Redei, G. P. Science, Vol. 139, Issue 3556 https://doi.org/10.1126/science.139.3556.767	journal	February 1963
Plastid Signals Remodel Light Signaling Networks and Are Essential for Efficient Chloroplast Biogenesis in Arabidopsis Ruckle, Michael E.; DeMarco, Stephanie M.; Larkin, Robert M. The Plant Cell, Vol. 19, Issue 12 https://doi.org/10.1105/tpc.107.054312	journal	December 2007
ABI4 and its role in chloroplast retrograde communication León, Patricia; Gregorio, Josefat; Cordoba, Elizabeth Frontiers in Plant Science, Vol. 3 https://doi.org/10.3389/fpls.2012.00304	journal	January 2013
A model for tetrapyrrole synthesis as the primary mechanism for plastid-to-nucleus signaling during chloroplast biogenesis Terry, Matthew J.; Smith, Alison G. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00014	journal	January 2013
Biogenesis and homeostasis of chloroplasts and other plastids Jarvis, Paul; López-Juez, Enrique Nature Reviews Molecular Cell Biology, Vol. 14, Issue 12 https://doi.org/10.1038/nrm3702	journal	November 2013
Steering the solar panel: plastids influence development: Commentary López-Juez, Enrique New Phytologist, Vol. 182, Issue 2 https://doi.org/10.1111/j.1469-8137.2009.02808.x	journal	March 2009
Chloroplast Redox Control of Nuclear Gene Expression—A New Class of Plastid Signals in Interorganellar Communication Pfannschmidt, Thomas; Schütze, Katia; Fey, Vidal Antioxidants & Redox Signaling, Vol. 5, Issue 1 https://doi.org/10.1089/152308603321223586	journal	February 2003
Proteomic Analysis of the Proplastid Envelope Membrane Provides Novel Insights into Small Molecule and Protein Transport across Proplastid Membranes Bräutigam, Andrea; Weber, Andreas P. M. Molecular Plant, Vol. 2, Issue 6 https://doi.org/10.1093/mp/ssp070	journal	November 2009
Subset of heat-shock transcription factors required for the early response of Arabidopsis to excess light Jung, H. -S.; Crisp, P. A.; Estavillo, G. M. Proceedings of the National Academy of Sciences, Vol. 110, Issue 35 https://doi.org/10.1073/pnas.1311632110	journal	August 2013
Let there be light: Regulation of gene expression in plants Petrillo, Ezequiel; Godoy Herz, Micaela A.; Barta, Andrea RNA Biology, Vol. 11, Issue 10 https://doi.org/10.4161/15476286.2014.972852	journal	October 2014
Identification of Early Nuclear Target Genes of Plastidial Redox Signals that Trigger the Long-Term Response of Arabidopsis to Light Quality Shifts Dietzel, Lars; Gläßer, Christine; Liebers, Monique Molecular Plant, Vol. 8, Issue 8 https://doi.org/10.1016/j.molp.2015.03.004	journal	August 2015
Plastid Alternative Oxidase (PTOX) Promotes Oxidative Stress When Overexpressed in Tobacco Heyno, Eiri; Gross, Christine M.; Laureau, Constance Journal of Biological Chemistry, Vol. 284, Issue 45 https://doi.org/10.1074/jbc.M109.021667	journal	September 2009
Functional and molecular characterization of plastid terminal oxidase from rice (Oryza sativa) Yu, Qiuju; Feilke, Kathleen; Krieger-Liszkay, Anja Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 8 https://doi.org/10.1016/j.bbabio.2014.04.007	journal	August 2014
Singlet oxygen-mediated signaling in plants: moving from flu to wild type reveals an increasing complexity Kim, Chanhong; Apel, Klaus Photosynthesis Research, Vol. 116, Issue 2-3 https://doi.org/10.1007/s11120-013-9876-4	journal	July 2013
1O2-Mediated and EXECUTER-Dependent Retrograde Plastid-to-Nucleus Signaling in Norflurazon-Treated Seedlings of Arabidopsis thaliana Kim, Chanhong; Apel, Klaus Molecular Plant, Vol. 6, Issue 5 https://doi.org/10.1093/mp/sst020	journal	September 2013
Reactive oxygen gene network of plants Mittler, Ron; Vanderauwera, Sandy; Gollery, Martin Trends in Plant Science, Vol. 9, Issue 10 https://doi.org/10.1016/j.tplants.2004.08.009	journal	October 2004
The Roles of Reactive Oxygen Species in Plant Cells: Figure 1. Bailey-Serres, Julia; Mittler, Ron Plant Physiology, Vol. 141, Issue 2 https://doi.org/10.1104/pp.104.900191	journal	June 2006
A Major Role of the MEKK1–MKK1/2–MPK4 Pathway in ROS Signalling Pitzschke, Andrea; Djamei, Armin; Bitton, Frédérique Molecular Plant, Vol. 2, Issue 1 https://doi.org/10.1093/mp/ssn079	journal	January 2009
Methyl esterification of pectin plays a role during plant–pathogen interactions and affects plant resistance to diseases Lionetti, Vincenzo; Cervone, Felice; Bellincampi, Daniela Journal of Plant Physiology, Vol. 169, Issue 16 https://doi.org/10.1016/j.jplph.2012.05.006	journal	November 2012
The role of the secondary cell wall in plant resistance to pathogens Miedes, Eva; Vanholme, Ruben; Boerjan, Wout Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00358	journal	August 2014
Mutations in the cinnamate 4-hydroxylase gene impact metabolism, growth and development in Arabidopsis: Arabidopsis C4H mutants Schilmiller, Anthony L.; Stout, Jake; Weng, Jing-Ke The Plant Journal, Vol. 60, Issue 5 https://doi.org/10.1111/j.1365-313X.2009.03996.x	journal	December 2009
Pathways of plastid-to-nucleus signaling Rodermel, Steve Trends in Plant Science, Vol. 6, Issue 10 https://doi.org/10.1016/s1360-1385(01)02085-4	journal	October 2001
Complexity, Cross Talk and Integration of Plant MAP Kinase Signalling Jonak, C. Current Opinion in Plant Biology, Vol. 5, Issue 5 https://doi.org/10.1016/s1369-5266(02)00285-6	journal	October 2002
Cellular Differentiation and Leaf Morphogenesis in Arabdopsis Pyke, Kevin; López-Juez, Enrique Critical Reviews in Plant Sciences, Vol. 18, Issue 4 https://doi.org/10.1080/07352689991309388	journal	July 1999
The Initiation and Determination of Leaves Smith, Laurie G.; Hake, Sarah The Plant Cell, Vol. 4, Issue 9 https://doi.org/10.2307/3869471	journal	September 1992
Isolation and characterization of CCoAOMT in interspecific hybrid of Acacia auriculiformis x Acacia mangium - a key gene in lignin biosynthesis Pang, S. L.; Ong, S. S.; Lee, H. H. Genetics and Molecular Research, Vol. 13, Issue 3 https://doi.org/10.4238/2014.september.5.7	journal	January 2014

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