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Wheat hypersensitive-induced reaction genes TaHIR1 and TaHIR3 are involved in response to stripe rust fungus infection and abiotic stresses

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TaHIR1 and TaHIR3 play positive roles in resistance to the stripe rust fungus via inducing HR and regulating defense-related genes, but are negatively regulated by various abiotic stimuli.

Abstract

Plant hypersensitive-induced reaction (HIR) genes are known to be associated with the hypersensitive response and disease defense. In wheat, two HIR genes, TaHIR1 and TaHIR3, have been identified and found to be up-regulated after infection with the stripe rust fungus. Here, we further determined their roles in defense against abiotic stresses and the stripe rust pathogen, Puccinia striiformis f. sp. tritici. TaHIR1 and TaHIR3 proteins were localized in the plasma membrane of tobacco cells. The expression of TaHIR1 and TaHIR3 was reduced by the environmental stimuli, including low temperature, drought, and high salinity stresses. In addition, the expression of TaHIR1 and TaHIR3 was down-regulated by exogenously applied ethrel and abscisic acid, whereas expression was not affected by treatments with salicylic acid and methyl jasmonate. Furthermore, barley stripe mosaic virus-induced gene silencing of TaHIR1 and TaHIR3 reduced resistance in wheat cultivar Suwon11 against an avirulent stripe rust pathotype CYR23 and area of necrotic cells neighboring the infection sites, and altered the expression levels of defense-related genes. These results suggest that TaHIR1 and TaHIR3 function positively in the incompatible interaction of wheat-stripe rust fungus, but exhibit negative transcriptional response to abiotic stresses.

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References

  • Asthir B, Koundal A, Bains NS, Mann SK (2010) Stimulation of antioxidative enzymes and polyamines during stripe rust disease of wheat. Biol Plant 54:329–333

    Article  CAS  Google Scholar 

  • Atkinson MM, Mildland SL, Sims JJ, Keen NT (1996) Syringolide triggers Ca2+ influx, K+ efflux, and extracellular alkalization in soybean cells carrying the disease resistance gene rpG4. Plant Physiol 112:297–302

    PubMed  CAS  Google Scholar 

  • Browman DT, Hoegg MB, Robbins SM (2007) The SPFH domain-containing proteins: more than lipid raft markers. Trends Cell Biol 17:394–402

    Article  PubMed  CAS  Google Scholar 

  • Choi HW, Kim YJ, Hwang BK (2011) The hypersensitive induced reaction and leucine-rich repeat proteins regulate plant cell death associated with disease and plant immunity. Mol Plant Microbe Interact 24:68–78

    Article  PubMed  CAS  Google Scholar 

  • Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833

    Article  PubMed  CAS  Google Scholar 

  • Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci USA 98:13454–13459

    Article  PubMed  CAS  Google Scholar 

  • Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442

    Article  PubMed  Google Scholar 

  • Greenberg JT, Yao N (2004) The role and regulation of programmed cell death in plant-pathogen interactions. Cell Microbiol 6:201–211

    Article  PubMed  CAS  Google Scholar 

  • Heath MC (1998) Apoptosis, programmed cell death and the hypersensitive response. Eur J Plant Path 104:117–124

    Article  CAS  Google Scholar 

  • Heath MC (2000) Hypersensitive response-related death. Plant Mol Biol 44:321–334

    Article  PubMed  CAS  Google Scholar 

  • Hofius D, Tsitsigiannis DI, Jones JD, Mundy J (2007) Inducible cell death in plant immunity. Semin Cancer Biol 17:166–187

    Article  PubMed  CAS  Google Scholar 

  • Holzberg S, Brosio P, Gross C, Pogue GP (2002) Barley stripe mosaic virus-induced gene silencing in a monocot plant. Plant J 30:315–327

    Article  PubMed  CAS  Google Scholar 

  • Huber TB, Benzing T (2005) The slit diaphragm: a signaling platform to regulate podocyte function. Curr Opin Nephrol Hypertens 14:211–216

    Article  PubMed  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  PubMed  CAS  Google Scholar 

  • Jones JD, Robert-Seilaniantz A, Navarro L, Bari R (2007) Pathological hormone imbalances. Curr Opin Plant Biol 10:372–379

    Article  PubMed  Google Scholar 

  • Jung HW, Hwang BK (2007) The leucine-rich repeat (LRR) protein, CaLRR1, interacts with the hypersensitive induced reaction (HIR) protein, CaHIR1, and suppresses cell death induced by the CaHIR1 protein. Mol Plant Pathol 8:503–514

    Article  PubMed  CAS  Google Scholar 

  • Jung HW, Lim CW, Lee SC, Choi HW, Hwang CH, Hwang BK (2008) Distinct roles of the pepper hypersensitive induced reaction protein gene CaHIR1 in disease and osmotic stress, as determined by comparative transcriptome and proteome analyses. Planta 227:409–425

    Article  PubMed  CAS  Google Scholar 

  • Kale SD, Gu B, Capelluto DG, Dou D, Feldman E, Rumore A, Arredondo FD, Hanlon R, Fudal I, Rouxel T, Lawrence CB, Shan W, Tyler BM (2010) External lipid pi-3-p mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142:284–295

    Article  PubMed  CAS  Google Scholar 

  • Kang ZS, Li Z (1984) Discovery of a normal T. type new pathogenic strain to Lovrin10. Acta Cllegii Septentrionali Occidentali Agriculturae 4:18–28

    Google Scholar 

  • Karrer EE, Beachy RN, Holt CA (1998) Cloning of tobacco genes that elicit the hypersensitive response. Plant Mol Biol 36:681–690

    Article  PubMed  CAS  Google Scholar 

  • Lu ZX, Gaudet D, Puchalski B, Despins T, Frick M, Laroche A (2006) Inducers of resistance reduce common bunt infection in wheat seedlings while differentially regulating defence-gene expression. Physiol Mol Plant Pathol 67:138–148

    Article  Google Scholar 

  • Mishra S, Murphy LC, Nyomba BL, Murphy LJ (2005) Prohibitin: a potential target for new therapeutics. Trends Mol Med 11:192–197

    Article  PubMed  CAS  Google Scholar 

  • Molina A, Gorlach J, Volrath S, Ryals J (1999) Wheat genes encoding two types of PR-1 proteins are pathogen inducible, but do not respond to activators of systemic acquired resistance. Mol Plant Microbe Interact 12:53–58

    Article  PubMed  CAS  Google Scholar 

  • Morel JB, Dangl JL (1997) The hypersensitive response and the induction of cell death in plants. Cell Death Differ 4:671–683

    Article  PubMed  CAS  Google Scholar 

  • Morrow IC, Parton RG (2005) Flotillins and the PHB domain protein family: rafts, worms and anaesthetics. Traffic 6:725–740

    Article  PubMed  CAS  Google Scholar 

  • Nadimpalli R, Yalpani N, Johal GS, Simmons CR (2000) Prohibitins, stomatins, and plant-disease response genes compose a protein superfamily that controls cell proliferation, ion channel regulation, and death. J Biol Chem 275:29579–29586

    Article  PubMed  CAS  Google Scholar 

  • Niu J, Liu R, Zheng L (2007) Expression analysis of wheat PR-1, PR-2, PR-5 activated by Bgt and SA, and powdery mildew resistance. J Triticeae Crops 27:1132–1137

    CAS  Google Scholar 

  • Norman-Setterblad C, Vital S, Palva ET (2000) Interacting signal pathways control defense gene expression in Arabidopsis in response to cell wall-degrading enzymes from Erwinia carotovera. Mol Plant Microbe Interact 4:430–438

    Article  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45

    Article  PubMed  CAS  Google Scholar 

  • Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316

    Article  PubMed  CAS  Google Scholar 

  • Qi Y, Tsuda K, Nguyen LV, Wang X, Lin J, Murphy AS, Glazebrook J, Thordal-Christensen H, Katagiri F (2011) Physical association of Arabidopsis hypersensitive induced reaction proteins (HIRs) with the immune receptor RPS2. J Biol Chem 286:31297–31307

    Article  PubMed  CAS  Google Scholar 

  • Rostoks N, Schmierer D, Kudrna D, Kleinhofs A (2003) Barley putative hypersensitive induced reaction genes: genetic mapping, sequence analyses and differential expression in disease lesion mimic mutants. Theor Appl Genet 107:1094–1101

    Article  PubMed  CAS  Google Scholar 

  • Scofield SR, Huang L, Brandt AS, Gill BS (2005) Development of a virus-induced gene-silencing system for hexaploid wheat and its use in functional analysis of the Lr21-mediated leaf rust resistance pathway. Plant Physiol 138:2165–2173

    Article  PubMed  CAS  Google Scholar 

  • Tavernarakis N, Driscoll M, Kyrpides NC (1999) The SPFH domain: implicated in regulating targeted protein turnover in stomatins and other membrane-associated proteins. Trends Biochem Sci 24:425–427

    Article  PubMed  CAS  Google Scholar 

  • Teardo E, Formentin E, Segalla A, Giacometti GM, Marin O, Zanetti M, Schiavo FL, Zoratti M, Szabò I (2011) Dual localization of plant glutamate receptor AtGLR3.4 to plastids and plasmamembrane. Biochim Biophys Acta 1807:359–367

    Article  PubMed  CAS  Google Scholar 

  • Torres MA, Jones JD, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141:373–378

    Article  PubMed  CAS  Google Scholar 

  • Wang CF, Huang LL, Buchenauer H, Han QM, Zhang HC, Kang ZS (2007) Histochemical studies on the accumulation of reactive oxygen species (O2− and H2O2) in the incompatible and compatible interaction of wheat-Puccinia striiformis f. sp. tritici. Physiol Mol Plant Pathol 71:230–239

    Article  CAS  Google Scholar 

  • Wang XJ, Tang CL, Zhang HC, Xu JR, Liu B, Jie LV, Han DJ, Huang LL, Kang ZS (2011) TaDAD2, a negative regulator of programmed cell death, is important for the interaction between wheat and the stripe rust fungus. Mol Plant Microbe Interact 24:79–90

    Article  PubMed  CAS  Google Scholar 

  • Yu XM, Yu XD, Qu ZP, Huang XJ, Guo J, Han QM, Zhao J, Huang LL, Kang ZS (2008) Cloning of a putative hypersensitive induced reaction gene from wheat infected by stripe rust fungus. Gene 407:193–198

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Zhou JM (2010) Plant immunity triggered by microbial molecular signatures. Mol Plant 3:783–793

    Article  PubMed  CAS  Google Scholar 

  • Zhang G, Dong YL, Zhang Y, Li YM, Wang XJ, Han QM, Guo J, Huang LL, Kang ZS (2009) Cloning and characterization of a novel hypersensitive induced-reaction gene from wheat infected by stripe rust pathogen. J Phytopathol 157:722–728

    Article  CAS  Google Scholar 

  • Zhang H, Wang C, Cheng Y, Wang X, Li F, Han Q, Xu J, Chen X, Huang L, Wei G, Kang Z (2011) Histological and molecular studies of the non-host interaction between wheat and Uromyces fabae. Planta 234:979–991

    Article  PubMed  CAS  Google Scholar 

  • Zhou L, Cheung MY, Zhang Q, Lei CL, Zhang SH, Sun SSM, Lam HM (2009) A novel simple extracellular leucine-rich repeat (eLRR) domain protein from rice (OsLRR1) enters the endosomal pathway and interacts with the hypersensitive-induced reaction protein 1 (OsHIR1). Plant Cell Environ 32:1804–1820

    Article  PubMed  CAS  Google Scholar 

  • Zhou L, Cheung MY, Li MW, Fu Y, Sun Z, Sun SSM, Lam HM (2010) Rice Hypersensitive Induced Reaction Protein 1 (OsHIR1) associates with plasma membrane and triggers hypersensitive cell death. BMC Plant Biol 10:290

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the National Major Project of Breeding for New Transgenic Organisms in China (2011ZX08002-001), the National Basic Research Program of China (No.2013CB127700), the National Natural Science Foundation of China (No. 30930064, 31171795 and 30800712), the 111 Project from the Ministry of Education of China (No.B07049) and the Fundamental Research Funds for the Central Universities of China (QN2009035). We specially thank Dr. Larry Dunkle, U. S. Department of Agriculture-Agricultural Research Service at Purdue University, for improvement of this manuscript.

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Authors and Affiliations

  1. State Key Laboratory of Crop Stress Biology for Arid Areas and College of Life Science, Northwest A&F University, Yangling, Shaanxi, 712100, People’s Republic of China

    Yinghui Duan

  2. State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, Shaanxi, 712100, People’s Republic of China

    Jun Guo, Xuexia Shi, Xiangnan Guan, Furong Liu, Pengfei Bai, Lili Huang & Zhensheng Kang

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  1. Yinghui Duan
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Correspondence to Jun Guo or Zhensheng Kang.

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Communicated by M. Jordan.

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Duan, Y., Guo, J., Shi, X. et al. Wheat hypersensitive-induced reaction genes TaHIR1 and TaHIR3 are involved in response to stripe rust fungus infection and abiotic stresses. Plant Cell Rep 32, 273–283 (2013). https://doi.org/10.1007/s00299-012-1361-6

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  • DOI: https://doi.org/10.1007/s00299-012-1361-6

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