Alteration of cell wall xylan acetylation triggers defense responses that counterbalance the immune deficiencies of plants impaired in the &bgr;‐subunit of the heterotrimeric G‐protein

Arabidopsis heterotrimeric G-protein complex modulates pathogen-associated molecular pattern-triggered immunity (PTI) and disease resistance responses to different types of pathogens. It also plays a role in plant cell wall integrity as mutants impaired in the Gβ- (agb1-2) or Gγ-subunits have an altered wall composition compared with wild-type plants. Here we performed a mutant screen to identify suppressors of agb1-2 (sgb) that restore susceptibility to pathogens to wild-type levels. Out of the four sgb mutants (sgb10-sgb13) identified, sgb11 is a new mutant allele of ESKIMO1 (ESK1), which encodes a plant-specific polysaccharide O-acetyltransferase involved in xylan acetylation. Null alleles (sgb11/esk1-7) of ESK1 restore to wild-type levels the enhanced susceptibility of agb1-2 to the necrotrophic fungus Plectosphaerella cucumerina BMM (PcBMM), but not to the bacterium Pseudomonas syringae pv. tomato DC3000 or to the oomycete Hyaloperonospora arabidopsidis. The enhanced resistance to PcBMM of the agb1-2 esk1-7 double mutant was not the result of the re-activation of deficient PTI responses in agb1-2. Alteration of cell wall xylan acetylation caused by ESK1 impairment was accompanied by an enhanced accumulation of abscisic acid, the constitutive expression of genes encoding antibiotic peptides and enzymes involved in the biosynthesis of tryptophan-derived metabolites, and the accumulation of disease resistance-related secondary metabolites and different osmolites. These esk1-mediated responses counterbalance the defective PTI and PcBMM susceptibility of agb1-2 plants, and explain the enhanced drought resistance of esk1 plants. These results suggest that a deficient PTI-mediated resistance is partially compensated by the activation of specific cell-wall-triggered immune responses.

[1]  M. Durand-Tardif,et al.  ESKIMO1 Disruption in Arabidopsis Alters Vascular Tissue and Impairs Water Transport , 2011, PloS one.

[2]  E. A. van der Biezen,et al.  The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6. , 1997, The Plant cell.

[3]  Stephanie N. Hicks,et al.  Acireductone Dioxygenase 1 (ARD1) Is an Effector of the Heterotrimeric G Protein β Subunit in Arabidopsis* , 2011, The Journal of Biological Chemistry.

[4]  B. Thorell,et al.  Dimethylsulphoxide, a Solvent for Hemicelluloses. , 1956 .

[5]  Riyaz Bhat,et al.  Pre- and Postinvasion Defenses Both Contribute to Nonhost Resistance in Arabidopsis , 2005, Science.

[6]  M. Pauly,et al.  The Role of the Plant-Specific ALTERED XYLOGLUCAN9 Protein in Arabidopsis Cell Wall Polysaccharide O-Acetylation1[OPEN] , 2015, Plant Physiology.

[7]  Alan M. Jones,et al.  d‐Glucose sensing by a plasma membrane regulator of G signaling protein, AtRGS1 , 2008, FEBS letters.

[8]  K. Shinozaki,et al.  Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. , 2002, The Plant journal : for cell and molecular biology.

[9]  Alan M. Jones,et al.  A shadow detector for photosynthesis efficiency. , 2017, Journal of theoretical biology.

[10]  E. Ward,et al.  A Central Role of Salicylic Acid in Plant Disease Resistance , 1994, Science.

[11]  D. Jaiswal,et al.  Direct Modulation of Heterotrimeric G Protein-coupled Signaling by a Receptor Kinase Complex* , 2016, The Journal of Biological Chemistry.

[12]  W. Boerjan,et al.  The role of the secondary cell wall in plant resistance to pathogens , 2014, Front. Plant Sci..

[13]  K. Torii,et al.  ERECTA and BAK1 Receptor Like Kinases Interact to Regulate Immune Responses in Arabidopsis , 2016, Front. Plant Sci..

[14]  F. Mauch,et al.  Indolic secondary metabolites protect Arabidopsis from the oomycete pathogen Phytophthora brassicae , 2010, Plant signaling & behavior.

[15]  Alan M. Jones,et al.  Plant Morphology of Heterotrimeric G Protein Mutants. , 2016, Plant & cell physiology.

[16]  K. Niyogi,et al.  Arabidopsis Mutants Define a Central Role for the Xanthophyll Cycle in the Regulation of Photosynthetic Energy Conversion , 1998, Plant Cell.

[17]  Jin-Gui Chen,et al.  Arabidopsis Receptor of Activated C Kinase1 Phosphorylation by WITH NO LYSINE8 KINASE1[OPEN] , 2014, Plant Physiology.

[18]  V. Bulone,et al.  Analyses of Extracellular Carbohydrates in Oomycetes Unveil the Existence of Three Different Cell Wall Types , 2012, Eukaryotic Cell.

[19]  Jian-Kang Zhu,et al.  Disruption of the cellulose synthase gene, AtCesA8/IRX1, enhances drought and osmotic stress tolerance in Arabidopsis. , 2005, The Plant journal : for cell and molecular biology.

[20]  Alan M. Jones,et al.  Heterotrimeric G protein signalling in the plant kingdom , 2013, Open Biology.

[21]  Heather A. Moniz,et al.  Two Arabidopsis proteins synthesize acetylated xylan in vitro. , 2014, The Plant journal : for cell and molecular biology.

[22]  K. Waldron,et al.  Formation of glucuronoxylan linked to protein in plant Golgi and plasma membranes. , 1991, Biochemical Society transactions.

[23]  Alan M. Jones,et al.  The role of Arabidopsis heterotrimeric G-protein subunits in MLO2 function and MAMP-triggered immunity. , 2013, Molecular plant-microbe interactions : MPMI.

[24]  J. Estevez,et al.  Disruption of Abscisic Acid Signaling Constitutively Activates Arabidopsis Resistance to the Necrotrophic Fungus Plectosphaerella cucumerina1[W] , 2012, Plant Physiology.

[25]  J. Kopka,et al.  Metabolome and water status phenotyping of Arabidopsis under abiotic stress cues reveals new insight into ESK1 function. , 2009, Plant, cell & environment.

[26]  Alan M. Jones,et al.  Ligand-induced dynamics of heterotrimeric G protein-coupled receptor-like kinase complexes , 2017, PloS one.

[27]  R. Last,et al.  Arabidopsis ESK1 encodes a novel regulator of freezing tolerance. , 2007, The Plant journal : for cell and molecular biology.

[28]  J. Browse,et al.  Eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[29]  M. Torres.  ROS in biotic interactions. , 2010, Physiologia plantarum.

[30]  J. Selbig,et al.  Involvement of TBL/DUF231 proteins into cell wall biology , 2010, Plant signaling & behavior.

[31]  A. Bogdanove,et al.  Arabidopsis and Brachypodium distachyon Transgenic Plants Expressing Aspergillus nidulans Acetylesterases Have Decreased Degree of Polysaccharide Acetylation and Increased Resistance to Pathogens1[C][W][OA] , 2013, Plant Physiology.

[32]  L. Jordá,et al.  ERECTA receptor-like kinase and heterotrimeric G protein from Arabidopsis are required for resistance to the necrotrophic fungus Plectosphaerella cucumerina. , 2005, The Plant journal : for cell and molecular biology.

[33]  J. Estevez,et al.  The ERECTA Receptor-Like Kinase Regulates Cell Wall-Mediated Resistance to Pathogens in Arabidopsis thaliana. , 2009, Molecular plant-microbe interactions : MPMI.

[34]  D F Klessig,et al.  The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. , 1997, The Plant cell.

[35]  Alan M. Jones,et al.  A Seven-Transmembrane RGS Protein That Modulates Plant Cell Proliferation , 2003, Science.

[36]  R. Zhong,et al.  Roles of Arabidopsis TBL34 and TBL35 in xylan acetylation and plant growth. , 2016, Plant science : an international journal of experimental plant biology.

[37]  O. Dong,et al.  Heterotrimeric G Proteins Serve as a Converging Point in Plant Defense Signaling Activated by Multiple Receptor-Like Kinases1[C][W][OA] , 2013, Plant Physiology.

[38]  Alan M. Jones,et al.  The plant heterotrimeric G-protein complex. , 2007, Annual review of plant biology.

[39]  Sascha Gille,et al.  O-Acetylation of Plant Cell Wall Polysaccharides , 2011, Front. Plant Sci..

[40]  H. Hamm,et al.  Heterotrimeric G protein activation by G-protein-coupled receptors , 2008, Nature Reviews Molecular Cell Biology.

[41]  Henrik Vibe Scheller,et al.  Loss-of-Function Mutation of REDUCED WALL ACETYLATION2 in Arabidopsis Leads to Reduced Cell Wall Acetylation and Increased Resistance to Botrytis cinerea1[W][OA] , 2011, Plant Physiology.

[42]  C. Zipfel,et al.  The Arabidopsis NADPH oxidases RbohD and RbohF display differential expression patterns and contributions during plant immunity. , 2016, Journal of experimental botany.

[43]  C. Lamb,et al.  Pseudomonas sax Genes Overcome Aliphatic Isothiocyanate–Mediated Non-Host Resistance in Arabidopsis , 2011, Science.

[44]  Y. Narusaka,et al.  CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis , 2007, Proceedings of the National Academy of Sciences.

[45]  A. Molina,et al.  Functional genomics tools to decipher the pathogenicity mechanisms of the necrotrophic fungus Plectosphaerella cucumerina in Arabidopsis thaliana. , 2013, Molecular plant pathology.

[46]  M. Durand-Tardif,et al.  ESKIMO1 is a key gene involved in water economy as well as cold acclimation and salt tolerance , 2008, BMC Plant Biology.

[47]  A. Savouré,et al.  Proline: a multifunctional amino acid. , 2010, Trends in plant science.

[48]  Alan M. Jones,et al.  A Golgi-localized hexose transporter is involved in heterotrimeric G protein-mediated early development in Arabidopsis. , 2006, Molecular biology of the cell.

[49]  Alan M. Jones,et al.  Modulation of Cell Proliferation by Heterotrimeric G Protein in Arabidopsis , 2001, Science.

[50]  Jonathan D. G. Jones,et al.  Bacterial disease resistance in Arabidopsis through flagellin perception , 2004, Nature.

[51]  K. Torii,et al.  Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation , 2004, Development.

[52]  M. Pauly,et al.  O-Acetylation of plant cell wall polysaccharides: identification and partial characterization of a rhamnogalacturonan O-acetyl-transferase from potato suspension-cultured cells , 2000, Planta.

[53]  Prakash Venglat,et al.  Target of Rapamycin Signaling Regulates Metabolism, Growth, and Life Span in Arabidopsis[W][OA] , 2012, Plant Cell.

[54]  S. Koutaniemi,et al.  Acetylation of woody lignocellulose: significance and regulation , 2013, Front. Plant Sci..

[55]  J. Botella,et al.  Heterotrimeric G-proteins facilitate resistance to plant pathogenic viruses in Arabidopsis thaliana (L.) Heynh , 2016, Plant signaling & behavior.

[56]  Yuelin Zhang,et al.  Heterotrimeric G proteins interact with defense-related receptor-like kinases in Arabidopsis. , 2015, Journal of plant physiology.

[57]  M. S. Mukhtar,et al.  Arabidopsis G-protein interactome reveals connections to cell wall carbohydrates and morphogenesis , 2011, Molecular systems biology.

[58]  P. Schulze-Lefert,et al.  Tryptophan-derived secondary metabolites in Arabidopsis thaliana confer non-host resistance to necrotrophic Plectosphaerella cucumerina fungi. , 2010, The Plant journal : for cell and molecular biology.

[59]  J. Estevez,et al.  Arabidopsis heterotrimeric G-protein regulates cell wall defense and resistance to necrotrophic fungi. , 2012, Molecular plant.

[60]  R. Zhong,et al.  The Arabidopsis DUF231 domain-containing protein ESK1 mediates 2-O- and 3-O-acetylation of xylosyl residues in xylan. , 2013, Plant & cell physiology.

[61]  S. Assmann,et al.  Arabidopsis extra large G-protein 2 (XLG2) interacts with the Gbeta subunit of heterotrimeric G protein and functions in disease resistance. , 2009, Molecular plant.

[62]  M. Nei,et al.  MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. , 2011, Molecular biology and evolution.

[63]  E. Mellerowicz,et al.  Expression of fungal acetyl xylan esterase in Arabidopsis thaliana improves saccharification of stem lignocellulose. , 2016, Plant biotechnology journal.

[64]  Johannes E. Schindelin,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[65]  S. Somerville,et al.  Mutations in PMR5 result in powdery mildew resistance and altered cell wall composition. , 2004, The Plant journal : for cell and molecular biology.

[66]  Alan M. Jones,et al.  The beta-subunit of the Arabidopsis G protein negatively regulates auxin-induced cell division and affects multiple developmental processes. , 2003, The Plant cell.

[67]  A. Ishikawa.  The Arabidopsis G-Protein β-Subunit Is Required for Defense Response against Agrobacterium tumefaciens , 2009, Bioscience, biotechnology, and biochemistry.

[68]  M. Pauly,et al.  Two Trichome Birefringence-Like Proteins Mediate Xylan Acetylation, Which Is Essential for Leaf Blight Resistance in Rice1[OPEN] , 2016, Plant Physiology.

[69]  P. Schenk,et al.  Heterotrimeric G Proteins Facilitate Arabidopsis Resistance to Necrotrophic Pathogens and Are Involved in Jasmonate Signaling1 , 2005, Plant Physiology.

[70]  M. Pauly,et al.  Xylan O-acetylation impacts xylem development and enzymatic recalcitrance as indicated by the Arabidopsis mutant tbl29. , 2013, Molecular plant.

[71]  J. Botella,et al.  Membrane-Localized Extra-Large G Proteins and Gβγ of the Heterotrimeric G Proteins Form Functional Complexes Engaged in Plant Immunity in Arabidopsis1[OPEN] , 2015, Plant Physiology.

[72]  S. Assmann,et al.  Extra-Large G Proteins Expand the Repertoire of Subunits in Arabidopsis Heterotrimeric G Protein Signaling1[OPEN] , 2015, Plant Physiology.

[73]  She Chen,et al.  Arabidopsis heterotrimeric G proteins regulate immunity by directly coupling to the FLS2 receptor , 2016, eLife.

[74]  J. Dangl,et al.  Functional interplay between Arabidopsis NADPH oxidases and heterotrimeric G protein. , 2013, Molecular plant-microbe interactions : MPMI.

[75]  M. Hahn,et al.  Characterization of Plant Cell Wall Damage-Associated Molecular Patterns Regulating Immune Responses. , 2017, Methods in molecular biology.

[76]  P. Gatenholm,et al.  A GH115 α-glucuronidase from Schizophyllum commune contributes to the synergistic enzymatic deconstruction of softwood glucuronoarabinoxylan , 2016, Biotechnology for Biofuels.

[77]  A. Encina,et al.  Novel type II cell wall architecture in dichlobenil-habituated maize calluses , 2009, Planta.

[78]  Owen Z. Woody,et al.  Pathogen-Secreted Proteases Activate a Novel Plant Immune Pathway , 2015, Nature.

[79]  Paul Dupree,et al.  The pattern of xylan acetylation suggests xylan may interact with cellulose microfibrils as a twofold helical screw in the secondary plant cell wall of Arabidopsis thaliana , 2014, The Plant journal : for cell and molecular biology.

[80]  F. Cervone,et al.  Oligogalacturonides: plant damage-associated molecular patterns and regulators of growth and development , 2013, Front. Plant Sci..

[81]  A. Macone,et al.  A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides , 2010, Proceedings of the National Academy of Sciences.

[82]  Peter Biely,et al.  Microbial carbohydrate esterases deacetylating plant polysaccharides. , 2012, Biotechnology advances.

[83]  Nicholas J. Provart,et al.  An “Electronic Fluorescent Pictograph” Browser for Exploring and Analyzing Large-Scale Biological Data Sets , 2007, PloS one.

[84]  V. Lionetti,et al.  Methyl esterification of pectin plays a role during plant-pathogen interactions and affects plant resistance to diseases. , 2012, Journal of plant physiology.

[85]  Marta Berrocal-Lobo,et al.  Impairment of Cellulose Synthases Required for Arabidopsis Secondary Cell Wall Formation Enhances Disease Resistance[W] , 2007, The Plant Cell Online.