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A novel nitrogen-dependent gene associates with the lesion mimic trait in wheat

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Using bulk segregant analysis (BSA) coupling with RNA-seq and DNA markers identified a potentially novel nitrogen-dependent lesion mimic gene Ndhrl1 on 2BS in wheat.

Abstract

Lesion mimic (LM) refers to hypersensitive reaction-like (HRL) traits that appear on leaf tissue in the absence of plant pathogens. In a wheat line P7001, LM showed up on the leaves under the 0 g nitrogen (N) treatment, but disappeared when sufficient N was supplied, suggesting that LM is N-responsive and N dosage dependent. Using BSA strategy together with RNA-seq and DNA markers, we identified an N-dependent LM gene (Ndhrl1) and mapped it to the short arm of chromosome 2B using an F5 recombinant inbred population developed from the cross of P7001 × P216. The putative gene was delimited into an interval of 8.1 cM flanked by the CAPS/dCAPS markers 7hrC9 and 7hr2dc14, and co-segregated with the dCAPS marker 7hrdc2. This gene is most likely a novel gene for LM in wheat based on its chromosomal location. Further analysis of RNA-seq data showed that plant–pathogen interaction, nitrogen metabolism, zeatin biosynthesis and plant hormone signal transduction pathways were significantly differentially expressed between LM and non-LM lines.

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References

  • Anand A, Schmelz EA, Muthukrishnan S (2003) Development of a lesion-mimic phenotype in a transgenic wheat line overexpressing genes for pathogenesis-related (PR) proteins is dependent on salicylic acid concentration. Mol Plant Microbe Interact 16:916–925

    Article  CAS  PubMed  Google Scholar 

  • Anand A, Lei Z, Sumner LW, Mysore KS, Arakane Y, Bockus WW, Muthukrishnan S (2004) Apoplastic extracts from a transgenic wheat line exhibiting lesion-mimic phenotype have multiple pathogenesis-related proteins that are antifungal. Mol Plant Microbe Interact 17:1306–1317

    Article  CAS  PubMed  Google Scholar 

  • Andersson MX, Newman MA, Somerville SC, Thordalchristensen H (2008) A lesion-mimic syntaxin double mutant in Arabidopsis reveals novel complexity of pathogen defense signaling. Mol Plant 1:510–527

    Article  PubMed  Google Scholar 

  • Arase S, Fujita K, Uehara T, Honda Y, Isota J (2000) Light-enhanced resistance to Magnaporthe grisea infection in the rice Sekiguchi lesion mutants. J Phytopathol 148:197–203

    Article  Google Scholar 

  • Balagué C, Lin B, Alcon C, Flottes G, Malmström S, Köhler C, Neuhaus G, Pelletier G, Gaymard F, Roby D (2003) HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family. Plant Cell 15:365–379

    Article  PubMed  PubMed Central  Google Scholar 

  • Borghi M, Rus A, Salt DE (2011) Loss-of-Function of constitutive expresser of pathogenesis related genes5 affects potassium homeostasis in Arabidopsis thaliana. PLoS One 6:4131–4142

    Article  Google Scholar 

  • Boyd LA, Minchin PN (2001) Wheat mutants showing altered adult plant disease resistance. Euphytica 122:361–368

    Article  Google Scholar 

  • Boyd LA, Smith PH, Wilson AH, Minchin PN (2002) Mutations in wheat showing altered field resistance to yellow and brown rust. Genome 45:1035–1040

    Article  CAS  PubMed  Google Scholar 

  • Bremner JM (1965) Inorganic Forms of Nitrogen1. In: Norman AG (ed) Methods of soil analysis. Part 2 chemical and microbiological properties. American Society of Agronomy, Soil Science Society of America, Madison

    Google Scholar 

  • Brosché M, Blomster T, Salojärvi J, Cui F, Sipari N, Leppälä J, Lamminmäki A, Tomai G, Narayanasamy S, Reddy RA, Keinänen M, Overmyer K, Kangasjärvi J (2014) Transcriptomics and functional genomics of ROS-induced cell death regulation by radical-induced cell death1. PLoS Gesnet 10:e1004112

    Article  Google Scholar 

  • Bruggeman Q, Raynaud C, Benhamed M, Delarue M (2015) To die or not to die? Lessons from lesion mimic mutants. Front Plant Sci 6:24

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen J, Vandelle E, Bellin D, Delledonne M (2014) Detection and function of nitric oxide during the hypersensitive response in Arabidopsis thaliana: where there’s a will there’s a way. Nitric Oxide Biol Chem 43:81–88

    Article  CAS  Google Scholar 

  • Fan XR, Gordon-Weeks R, Shen QR, Miller AJ (2006) Glutamine transport and feedback regulation of nitrate reductase activity in barley roots leads to changes in cytosolic nitrate pools. J Exp Bot 57:1333–1340

    Article  CAS  PubMed  Google Scholar 

  • Fekih R, Tamiru M, Kanzaki H, Abe A, Yoshida K, Kanzaki E, Saitoh H, Takagi H, Natsume S, Undan JR, Undan J, Terauchi R (2015) The rice (Oryza sativa L.) lesion mimic resembling, which encodes an AAA-type ATPase, is implicated in defense response. Mol Genet Genom 290:611–622

    Article  CAS  Google Scholar 

  • Fujiwara T, Maisonneuve S, Isshiki M, Mizutani M, Chen LT, Wong HL, Kawasaki T, Shimamoto K (2010) Sekiguchi lesion gene encodes a cytochrome P450 monooxygenase that catalyzes conversion of tryptamine to serotonin in rice. J Biol Chem 285:11308–11313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gray J, Janick-Buckner D, Buckner B, Close PS, Johal GS (2002) Light-dependent death of maize lls1 cells is mediated by mature chloroplasts. Plant Physiol 130:1894–1907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu G, Yalpani N, Briggs SP, Johal GS (1998) A porphyrin pathway impairment is responsible for the phenotype of a dominant disease lesion mimic mutant of maize. Plant Cell 10:1095–1105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishikawa A, Okamoto H, Iwasaki Y, Asahi T (2001) A deficiency of coproporphyrinogen III oxidase causes lesion formation in Arabidopsis. Plant J 27:89–99

    Article  CAS  PubMed  Google Scholar 

  • Johnson R (1981) Durable resistance: definition of, genetic control, and attainment in plant breeding. Phytopathology 71:567–568

    Article  Google Scholar 

  • Kamlofski CA, Antonelli E, Bender C, Jaskelioff M, Danna CH, Ugalde R, Acevedo A (2007) A lesion-mimic mutant of wheat with enhanced resistance to leaf rust. Plant Pathol 56:46–54

    Article  Google Scholar 

  • Li T, Bai G (2009) Lesion mimic associates with adult plant resistance to leaf rust infection in wheat. Theor Appl Genet 119:13–21

    Article  CAS  PubMed  Google Scholar 

  • Li R, Li Y, Fang X, Yang H, Wang J, Kristiansen K, Wang J (2009) SNP detection for massively parallel whole-genome resequencing. Genome Res 19:1124–2132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li T, Bai GH, Gu SL (2012) A combination of leaf rust resistance gene Lr34 and lesion mimic gene lm significantly enhances adult plant resistance to Puccinia triticina in wheat. Chin Sci Bull 57:2113–2119

    Article  CAS  Google Scholar 

  • Li YS, Chen LC, Mu JY, Zuo JR (2013) Lesion simulating disease1 interacts with catalases to regulate hypersensitive cell death in Arabidopsis. Plant Physiol 163:1059–1070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ling T, Vandelle E, Bellin D, Kleinfelder-Fontanesi K, Huang JJ, Chen J, Digby AM, Delledonne M (2012) Nitric oxide produced during the hypersensitive response modulates the plant signaling network and inhibits the pathogen’s virulence machinery. Nitric Oxide Biol Chem 27:S9

    Article  Google Scholar 

  • Lorrain S, Vailleau F, Balagué C, Roby D (2003) Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci 8:263–271

    Article  CAS  PubMed  Google Scholar 

  • Lorrain S, Lin B, Auriac MC, Kroj T, Saindrenan P, Nicole M, Balagué C, Roby D (2004) Vascular associated death1, a novel GRAM domain-containing protein, is a regulator of cell death and defense responses in vascular tissues. Plant Cell 16:2217–2232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mayer KFX, Rogers J, Doležel J, Pozniak C, Eversole K, Feuillet C, Gill B, Friebe B, Lukaszewski AJ, Sourdille P (2014) A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345:1251788

    Article  Google Scholar 

  • McGrann GRD, Steed A, Burt C, Nicholson P, Brown JKM (2015) Differential effects of lesion mimic mutants in barley on disease development by facultative pathogens. J Exp Bot 66:3417–3428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moeder W, Yoshioka K (2008) Lesion mimic mutants: a classical, yet still fundamental approach to study programmed cell death. Plant Signal Behav 3:764–767

    Article  PubMed  PubMed Central  Google Scholar 

  • Mortazavi A, Williams BA, Mccue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628

    Article  CAS  PubMed  Google Scholar 

  • Neff MM, Neff JD, Chory J, Pepper AE (1998) dCAPS, a simple technique for the genetic analysis of single nucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics. Plant J 14:387–392

    Article  CAS  PubMed  Google Scholar 

  • Neff MM, Turk E, Kalishman M (2002) Web-based primer design for single nucleotide polymorphism analysis. Trends Genet 18:613–615

    Article  CAS  PubMed  Google Scholar 

  • Noutoshi Y, Ito T, Hobo T, Shinozaki K (2003) Analysis of Arabidopsis slh1 (sensitive to low humidity 1) mutant. Plant Cell Physiol 44:S81

    Google Scholar 

  • Penning BW, Johal GS, McMullen MD (2004) A major suppressor of cell death, slm1, modifies the expression of the maize (Zea mays L.) lesion mimic mutation les23. Genome 47:961–969

    Article  CAS  PubMed  Google Scholar 

  • Pertea G, Huang X, Liang F, Antonescu V, Sultana R, Karamycheva S, Lee Y, White J, Cheung F, Parvizi B (2003) TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19:651–652

    Article  CAS  PubMed  Google Scholar 

  • Poland JA, Brown PJ, Sorrells ME, Jannink JL (2012) Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS One 7:251–264

    Article  Google Scholar 

  • Porebski S, Bailey LG, Baum BR (1997) Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Mol Biol Rep 15:8–15

    Article  CAS  Google Scholar 

  • Qian L, Wang YJ (2014) Transcriptome sequencing and metabolite analysis reveals the role of delphinidin metabolism in flower colour in grape hyacinth. J Exp Bot 65:3157–3164

    Article  Google Scholar 

  • Shirsekar GS, Vega-Sanchez ME, Bordeos A, Baraoidan M, Swisshelm A, Fan JB, Park CH, Leung H, Wang GL (2014) Identification and characterization of suppressor mutants of spl11-mediated cell death in rice. Mol Plant Microbe Interact 27:528–536

    Article  CAS  PubMed  Google Scholar 

  • Sohn KH, Segonzac C, Rallapalli G, Sarris PF, Woo JY, Williams SJ, Newman TE, Paek KH, Kobe B, Jones JDG (2014) The nuclear immune receptor RPS4 is required for RRS1(SLH1)-dependent constitutive defense activation in Arabidopsis thaliana. PLoS Genet 10:e1004655

    Article  PubMed  PubMed Central  Google Scholar 

  • Soussana JF, Minchin FR, Macduff JH, Raistrick N, Abberton MT, Michaelson-Yeates TPT (2002) A simple model of feedback regulation for nitrate uptake and N-2 fixation in contrasting phenotypes of white clover. Ann Bot 90:139–147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugie A, Murai K, Takumi S (2007) Alteration of respiration capacity and transcript accumulation level of alternative oxidase genes in necrosis lines of common wheat. Genes Genet Syst 82:231–239

    Article  CAS  PubMed  Google Scholar 

  • Tarazona S, García-Alcalde F, Dopazo J, Ferrer A, Conesa A (2011) Differential expression in RNA-seq: a matter of depth. Genome Res 21:2213–2223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ueno M, Kihara J, Arase S (2015) Tryptamine and sakuranetin accumulation in Sekiguchi lesions associated with the light-enhanced resistance of the lesion mimic mutant of rice to Magnaporthe oryzae. J Gen Plant Pathol 81:1–4

    Article  CAS  Google Scholar 

  • Wang J, Bayles KW (2013) Programmed cell death in plants: lessons from bacteria? Trends Plant Sci 18:133–139

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Qu B, Dou S, Li L, Yin DD, Pang ZQ, Zhou ZZ, Tian MM, Liu GZ, Xie Q, Tang DZ, Chen XW, Zhu L (2015) The E3 ligase OsPUB15 interacts with the receptor-like kinase PID2 and regulates plant cell death and innate immunity. BMC Plant Biol 15:1–15

    Article  Google Scholar 

  • Yamaguchi M, Takechi K, Myouga F, Imura S, Sato H, Takio S, Shinozaki K, Takano H (2012) Loss of the plastid envelope protein AtLrgB causes spontaneous chlorotic cell death in Arabidopsis thaliana. Plant Cell Physiol 53:125–134

    Article  CAS  PubMed  Google Scholar 

  • Yamamura C, Mizutani E, Okada K, Nakagawa H, Fukushima S, Tanaka A, Maeda S, Kamakura T, Yamane H, Takatsuji H, Mori M (2015) Diterpenoid phytoalexin factor, a bHLH transcription factor, plays a central role in the biosynthesis of diterpenoid phytoalexins in rice. Plant J 84:1100–1113

    Article  CAS  PubMed  Google Scholar 

  • Yao Q, Zhou RH, Fu TH, Wu WR, Zhu ZD, Li AL, Jia JZ (2009) Characterization and mapping of complementary lesion-mimic genes lm1 and lm2 in common wheat. Theor Appl Genet 119:1005–1012

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank the financial support provided by the National Natural Science Foundation of China (31270704), the Vital Project of Natural Science of Universities in Jiangsu Province (12KJA210002), the China Postdoctoral Science Foundation (2014M560449), and by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD). Our thanks also go to Dr. Mei Han and Dr. Tao Su for improving English language of this manuscript.

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Correspondence to Tao Li.

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Communicated by E. Lagudah.

Xuan Shi and Fei Zheng contributed equally to this work.

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Li, L., Shi, X., Zheng, F. et al. A novel nitrogen-dependent gene associates with the lesion mimic trait in wheat. Theor Appl Genet 129, 2075–2084 (2016). https://doi.org/10.1007/s00122-016-2758-3

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