Abstract
Key message
Loci associated with variation in maize responses to two microbe-associated molecular patterns (MAMPs) were identified. MAMP responses were correlated. No relationship between MAMP responses and quantitative disease resistance was identified.
Abstract
Microbe-associated molecular patterns (MAMPs) are highly conserved molecules commonly found in microbes which can be recognized by plant pattern recognition receptors. Recognition triggers a suite of responses including production of reactive oxygen species (ROS) and nitric oxide (NO) and expression changes of defense-related genes. In this study, we used two well-studied MAMPs (flg22 and chitooctaose) to challenge different maize lines to determine whether there was variation in the level of responses to these MAMPs, to dissect the genetic basis underlying that variation and to understand the relationship between MAMP response and quantitative disease resistance (QDR). Naturally occurring quantitative variation in ROS, NO production, and defense genes expression levels triggered by MAMPs was observed. A major quantitative traits locus (QTL) associated with variation in the ROS production response to both flg22 and chitooctaose was identified on chromosome 2 in a recombinant inbred line (RIL) population derived from the maize inbred lines B73 and CML228. Minor QTL associated with variation in the flg22 ROS response was identified on chromosomes 1 and 4. Comparison of these results with data previously obtained for variation in QDR and the defense response in the same RIL population did not provide any evidence for a common genetic basis controlling variation in these traits.
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References
Ahlfors R, Brosché M, Kangasjärvi J (2009) Ozone and nitric oxide interaction in Arabidopsis thaliana: a role for ethylene? Plant Signal Behav 4:878–879
Ahmad S, Van Hulten M, Martin J, Pieterse CMJ, Van Wees SCM, Ton J (2011) Genetic dissection of basal defence responsiveness in accessions of Arabidopsis thaliana. Plant Cell Environ 34:1191–1206
Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signaling. J Exp Bot 65:1229–1240
Benson JM, Poland JA, Benson BM, Stromberg EL, Nelson RJ (2015) Resistance to gray leaf spot of maize: genetic architecture and mechanisms elucidated through nested association mapping and near-isogenic line analysis. PLoS Genet 11:e1005045
Bigeard J, Colcombet J, Hirt H (2015) Signaling mechanisms in pattern-triggered immunity (PTI). Mol Plant 8:521–539
Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406
Brown JKM (2015) Durable resistance of crops to disease: a Darwinian perspective. Annu Rev Phytopathol 53:513–539
Brown I, Trethowan J, Kerry M, Mansfield J, Bolwell GP (1998) Localization of components of the oxidative cross-linking of glycoproteins and of callose synthesis in papillae formed during the interaction between non-pathogenic strains of Xanthomonas campestris and French bean mesophyll cells. Plant J 15:333–343
Cai R, Lewis J, Yan S, Liu H, Clarke CR, Campanile F, Almeida NF, Studholme DJ, Lindeberg M, Schneider D, Zaccardelli M, Setubal JC, Morales-Lizcano NP, Bernal A, Coaker G, Baker C, Bender CL, Leman S, Vinatzer BA (2011) The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity. PLoS Pathog 7:e1002130
Cao Y, Liang Y, Tanaka K, Nguyen CT, Jedrzejczak RP, Joachimiak A, Stacey G (2014) The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. eLife 3:e03766
Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G (2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18:465–476
Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JDG, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500
Choi HW, Klessig DF (2016) DAMPs, MAMPs, and NAMPs in plant innate immunity. BMC Plant Biol 16:232
Clarke CR, Chinchilla D, Hind SR, Taguchi F, Miki R, Ichinose Y, Martin GB, Leman S, Felix G, Vinatzer BA (2013) Allelic variation in two distinct Pseudomonas syringae flagellin epitopes modulates the strength of plant immune responses but not bacterial motility. New Phytol 200:847–860
Cole SJ, Diener AC (2013) Diversity in receptor-like kinase genes is a major determinant of quantitative resistance to Fusarium oxysporum f.sp. matthioli. New Phytol 200:172–184
Couto D, Zipfel C (2016) Regulation of pattern recognition receptor signalling in plants. Nat Rev Immunol 16:537–552
Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11:539–548
Dow M, Newman MA, von Roepenack E (2000) The induction and modulation of plant defense responses by bacterial lipopolysaccharides. Annu Rev Phytopathol 38:241–261
Felix G, Duran JD, Volko S, Boller T (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flT (1999. Plant J 18:265–276
Felix G, Regenass M, Boller T (1993) Specific perception of subnanomolar concentrations of chitin fragments by tomato cells: induction of extracellular alkalinization, changes in protein phosphorylation, and establishment of a refractory state. Plant J 4:307–316
Foissner I, Wendehenne D, Langebartels C, Durner J (2000) In vivo imaging of an elicitor-induced nitric oxide burst in tobacco. Plant J 23:817–824
Forsyth A, Mansfield JW, Grabov N, de Torres M, Sinapidou E, Grant MR (2010) Genetic dissection of basal resistance to Pseudomonas syringae pv. phaseolicola in accessions of Arabidopsis. Mol Plant Microbe Interact 23:1545–1552
Furch ACU, Zimmermann MR, Kogel KH, Reichelt M, Mithöfer A (2014) Direct and individual analysis of stress-related phytohormone dispersion in the vascular system of Cucurbita maxima after flagellin22 treatment. New Phytol 201:1176–1182
Gust AA, Biswas R, Lenz HD, Rauhut T, Ranf S, Kemmerling B, Götz F, Glawischnig E, Lee J, Felix G, Nürnberger T (2007) Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in Arabidopsis. J Biol Chem 282:32338–32348
Gómez-Gómez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011
Gómez-Gómez L, Felix G, Boller T (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J 18:277–284
Habib H, Fazili KM (2007) Plant protease inhibitors: a defense strategy in plants. Biotechnol Mol Biol Rev 2:068–085
Halim VA, Altmann S, Ellinger D, Eschen-Lippold L, Miersch O, Scheel D, Rosahl S (2009) PAMP-induced defense responses in potato require both salicylic acid and jasmonic acid. Plant J 57:230–242
Heese A, Hann DR, Gimenez-Ibanez S, Jones AME, He K, Li J, Schroeder JI, Peck SC, Rathjen JP (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci USA 104:12217–12222
Huffaker A, Dafoe NJ, Schmelz EA (2011) ZmPep1, an ortholog of Arabidopsis elicitor peptide 1, regulates maize innate immunity and enhances disease resistance. Plant Physiol 155:1325–1338
Huffaker A, Ryan CA (2007) Endogenous peptide defense signals in Arabidopsis differentially amplify signaling for the innate immune response. Proc Natl Acad Sci USA 104:10732–10736
Jabs T, Tschöpe M, Colling C, Hahlbrock K, Scheel D (1997) Elicitor-stimulated ion fluxes and O2 – from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proc Natl Acad Sci USA 94:4800–4805
Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329
Kump KL, Bradbury PJ, Wisser RJ, Buckler ES, Belcher AR, Oropeza-Rosas MA, Zwonitzer JC, Kresovich S, McMullen MD, Ware D, Balint-Kurti PJ, Holland JB (2011) Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population. Nat Genet 43:163–168
Kump KL, Holland JB, Jung MT, Wolters P, Balint-Kurti PJ (2010) Joint analysis of near-isogenic and recombinant inbred line populations yields precise positional estimates for quantitative trait loci. Plant Gen 3:142–153
Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G (2004) The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16:3496–3507
Lamotte O, Gould K, Lecourieux D, Sequeira-Legrand A, Lebrun-Garcia A, Durner J, Pugin A, Wendehenne D (2004) Analysis of nitric oxide signaling functions in tobacco cells challenged by the elicitor cryptogein. Plant Physiol 135:516–529
Laxalt AM, Raho N, Have AT, Lamattina L (2007) Nitric oxide is critical for inducing phosphatidic acid accumulation in Xylanase-elicited tomato cells. J Biol Chem 282:21160–21168
Lee H-A, Lee H-Y, Seo E, Lee J, Kim S-B, Oh S, Choi E, Choi E, Lee SE, Choi D (2016) Current understandings on plant nonhost resistance. Mol Plant Microbe Interact. doi:10.1094/MPMI-10-16-0213-CR
Libault M, Farmer A, Brechenmacher L, Drnevich J, Langley RJ, Bilgin DD, Radwan O, Neece DJ, Clough SJ, May GD, Stacey G (2010) Complete transcriptome of the soybean root hair cell, a single-cell model, and its alteration in response to Bradyrhizobium japonicum infection. Plant Physiol 152:541–552
Libault M, Thibivilliers S, Bilgin DD, Radwan O, Benitez M, Clough SJ, Stacey G (2008) Identification of four soybean reference genes for gene expression normalization. Plant Genome 1:44–54
Lloyd SR, Schoonbeek H, Trick M, Zipfel C, Ridout CJ (2014) Methods to study PAMP-triggered immunity in Brassica species. Mol Plant Microbe Interact 27:286–295
Lori M, van Verk MC, Hander T, Schatowitz H, Klauser D, Flury P, Gehring CA, Boller T, Bartels S (2015) Evolutionary divergence of the plant elicitor peptides (Peps) and their receptors: interfamily incompatibility of perception but compatibility of downstream signalling. J Exp Bot 66:5315–5325
Lotze MT, Zeh HJ, Rubartelli A, Sparvero LJ, Amoscato AA, Washburn NR, DeVera ME, Liang X, Tör M, Billiar T (2007) The grateful dead: damage-associated molecular pattern molecules and reduction/oxidation regulate immunity. Immunol Rev 220:60–81
Luna E, Pastor V, Robert J, Flors V, Mauch-Mani B, Ton J (2011) Callose deposition: a multifaceted plant defense response. Mol Plant Microbe Interact 24:183–193
McMullen MD, Kresovich S, Villeda HS, Bradbury P, Li H, Sun Q, Flint-Garcia S, Thornsberry J, Acharya C, Bottoms C, Brown P, Browne C, Eller M, Guill K, Harjes C, Kroon D, Lepak N, Mitchell SE, Peterson B, Pressoir G, Romero S, Oropeza Rosas M, Salvo S, Yates H, Hanson M, Jones E, Smith S, Glaubitz JC, Goodman M, Ware D, Holland JB, Buckler ES (2009) Genetic properties of the maize nested association mapping population. Science 325:737–740
Millet YA, Danna CH, Clay NK, Songnuan W, Simon MD, Werck-Reichhart D, Ausubel FM (2010) Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell 22:973–990
Mithöfer A, Ebel J, Felle HH (2005) Cation fluxes cause plasma membrane depolarization involved in β-glucan elicitor-signaling in soybean roots. Mol Plant Microbe Interact 18:983–990
Monaghan J, Zipfel C (2012) Plant pattern recognition receptor complexes at the plasma membrane. Curr Opin Plant Biol 15:349–357
Nandety RS, Caplan JL, Cavanaugh K, Perroud B, Wroblewski T, Michelmore RW, Meyers BC (2013) The role of TIR-NBS and TIR-X proteins in plant basal defense responses. Plant Physiol 162:1459–1472
Navarro L, Zipfel C, Rowland O, Keller I, Robatzek S, Boller T, Jones JDG (2004) The transcriptional innate immune response to flg22. interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol 135:1113–1128
Nishizawa Y, Kawakami A, Hibi T, He DY, Shibuya N, Minami E (1999) Regulation of the chitinase gene expression in suspension-cultured rice cells by N-acetylchitooligosaccharides: differences in the signal transduction pathways leading to the activation of elicitor-responsive genes. Plant Mol Biol 39:907–914
Oliveira-Garcia E, Deising HB (2016) Attenuation of PAMP-triggered immunity in maize requires down-regulation of the key β-1,6-glucan synthesis genes KRE5 and KRE6 in biotrophic hyphae of Colletotrichum graminicola. Plant J 87:355–375
Olukolu BA, Bian Y, De Vries B, Tracy WF, Wisser RJ, Holland JB, Balint-Kurti PJ (2016) The genetics of leaf flecking in maize and its relationship to plant defense and disease resistance. Plant Physiol 172:1787–1803
Olukolu BA, Wang GF, Vontimitta V, Venkata BP, Marla S, Ji J, Gachomo E, Chu K, Negeri A, Benson J, Nelson R, Bradbury P, Nielsen D, Holland JB, Balint-Kurti PJ, Johal G (2014) A genome-wide association study of the maize hypersensitive defense response identifies genes that cluster in related pathways. PLoS Genet 10:e1004562
Pearce G, Yamaguchi Y, Barona G, Ryan CA (2010) A subtilisin-like protein from soybean contains an embedded, cryptic signal that activates defense-related genes. Proc Natl Acad Sci USA 107:14921–14925
Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ (2009) Shades of gray: the world of quantitative disease resistance. Trends Plant Sci 14:21–29
Poland JA, Bradbury PJ, Buckler ES, Nelson RJ (2011) Genome-wide nested association mapping of quantitative resistance to northern leaf blight in maize. Proc Natl Acad Sci USA 108:6893–6898
Pugin A, Frachisse JM, Tavernier E, Bligny R, Gout E, Douce R, Guernb J (1997) Early events induced by the elicitor cryptogein in tobacco cells: involvement of a plasma membrane NADPH oxidase and activation of glycolysis and the pentose phosphate pathway. Plant Cell 9:2077–2091
Ramakers C, Ruijter JM, Lekanne Deprez RH, Moorman AFM (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66
Rasul S, Dubreuil-Maurizi C, Lamotte O, Koen E, Poinssot B, Alcaraz G, Wendehenne D, Jeandroz S (2012) Nitric oxide production mediates oligogalacturonide-triggered immunity and resistance to Botrytis cinerea in Arabidopsis thaliana. Plant Cell Environ 35:1483–1499
Rosli HG, Zheng Y, Pombo MA, Zhong S, Bombarely A, Fei Z, Collmer A, Martin GB (2013) Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity. Genome Biol 14:R139
Schieber M, Chandel NS (2014) ROS function in redox signaling and oxidative stress. Curr Biol 24:453–462
Segonzac C, Feike D, Gimenez-Ibanez S, Hann DR, Zipfel C, Rathjen JP (2011) Hierarchy and roles of pathogen-associated molecular pattern-induced responses in Nicotiana benthamiana. Plant Physiol 156:687–699
Segonzac C, Zipfel C (2011) Activation of plant pattern-recognition receptors by bacteria. Curr Opin Microbiol 14:54–61
Shi Q, Febres VJ, Jones JB, Moore GA (2015) Responsiveness of different citrus genotypes to the Xanthomonas citri ssp. citri-derived pathogen-associated molecular pattern (PAMP) flg22 correlates with resistance to citrus canker. Mol Plant Pathol 16:507–520
Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, Minami E, Okada K, Yamane H, Kaku H, Shibuya N (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 64:204–214
Silva LDCE, Wang S, Zeng ZB (2012) Composite interval mapping and multiple interval mapping: procedures and guidelines for using Windows QTL Cartographer. Methods Mol Biol 871:75–119
Sun Y, Li L, Macho AP, Han Z, Hu Z, Zipfel C, Zhou JM, Chai J (2013) Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 342:624–628
Szatmári Á, Zvara Á, Móricz ÁM, Besenyei E, Szabó E, Ott PG, Puskás LG, Bozsó Z (2014) Pattern triggered immunity (PTI) in tobacco: isolation of activated genes suggests role of the phenylpropanoid pathway in inhibition of bacterial pathogens. PLoS One 9:e102869
Tanaka K, Choi J, Cao Y, Stacey G (2014) Extracellular ATP acts as a damage-associated molecular pattern (DAMP) signal in plants. Front Plant Sci 5:446
Thomma BPHJ, Nürnberger T, Joosten MHAJ (2011) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4–15
Tsuda K, Sato M, Glazebrook J, Cohen JD, Katagiri F (2008) Interplay between MAMP-triggered and SA-mediated defense responses. Plant J 53:763–775
Valdés-López O, Thibivilliers S, Qiu J, Xu WW, Nguyen THN, Libault M, Le BH, Goldberg RB, Hill CB, Hartman GL, Diers B, Stacey G (2011) Identification of quantitative trait loci controlling gene expression during the innate immunity response of soybean. Plant Physiol 157:1975–1986
Veluchamy S, Hind SR, Dunham DM, Martin GB, Panthee DR (2014) Natural variation for responsiveness to flg22, flgII-28, and csp22 and Pseudomonas syringae pv. tomato in heirloom tomatoes. PLoS One 9:e106119
Vetter M, Karasov TL, Bergelson J (2016) Differentiation between MAMP triggered defenses in Arabidopsis thaliana. PLoS Genet 12:e1006068
Vetter MM, Kronholm I, He F, Häweker H, Reymond M, Bergelson J, Robatzek S, de Meaux J (2012) Flagellin perception varies quantitatively in Arabidopsis thaliana and its relatives. Mol Biol Evol 29:1655–1667
Vidhyasekaran P (2014) PAMP signals in plant innate immunity: signal perception and transduction. Springer, Dordrecht, pp 85–87
Vidhyasekaran P (2016) Switching on plant innate immunity signaling systems: bioengineering and molecular manipulation of PAMP-PIMP-PRR signaling complex. Springer, Switzerland, pp 33–34
Wan J, Zhang XC, Neece D, Ramonell KM, Clough S, Kim SY, Stacey MG, Stacey G (2008) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20:471–481
Wendehenne D, Lamotte O, Frachisse JM, Barbier-Brygoo H, Pugina A (2002) Nitrate efflux is an essential component of the cryptogein signaling pathway leading to defense responses and hypersensitive cell death in tobacco. Plant Cell 14:1937–1951
Wojtaszek P (1997) Oxidative burst: an early plant response to pathogen infection. Biochem J 322:681–692
Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JDG, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–767
Acknowledgements
This work was funded in part by DOE grant #DE-SC0014116, “Physiological and Molecular-Genetic Characterization of Basal Resistance in Sorghum”; XZ’s fellowship was funded by the China Scholarship Council Fellowship; we would like to thank Carole Saravitz, Joe Chiera, and the staff in NCSU Phytotron for their management of our plant materials, Jim Holland (USDA-ARS) and Sherry Flint-Garcia (USDA-ARS) for seed of the CML228 × B73 mapping population; we also would like to thank Jonathan Kressin (NCSU Department of Horticultural Science), Wall Crumpler, and John Godwin for access to and help with using the plate-reader, and Jenny Kimball, Yangrong Cao, Qin Yang, Yijian He, Guanfeng Wang, and Shannon Sermons for help, advice, and access to various materials.
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PBK, GS, XZ and OVL planned the research, XZ and OVL performed the research and analyzed the data, CA performed statistical analyses, XZ and PBK wrote the manuscript, and GA, OVL, and CA edited the manuscript.
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This work was funded in part by DOE Grant #DE-SC0014116, “Physiological and Molecular-Genetic Characterization of Basal Resistance in Sorghum”; XZ’s fellowship was funded by the China Scholarship Council Fellowship.
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This article does not contain any studies with human participants or animals performed by any of the authors.
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Communicated by Jianbing Yan.
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Zhang, X., Valdés-López, O., Arellano, C. et al. Genetic dissection of the maize (Zea mays L.) MAMP response. Theor Appl Genet 130, 1155–1168 (2017). https://doi.org/10.1007/s00122-017-2876-6
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DOI: https://doi.org/10.1007/s00122-017-2876-6