植物抗病遗传合辑Plant Disease-resistance Genetics
|Pathogenesis-related protein genes involved in race-specific allstage resistance and non-race specific high-temperature adult-plant resistance to Puccinia striiformis f. sp. tritici in wheat
Sumaira Farrakh1, 2, Meinan Wang1, Xianming Chen1, 3
1 Department of Plant Pathology, Washington State University, Pullman, WA 99164-6430, USA
2 Department of Biosciences, COMSATS Institute of Information Technology, Park Road, Islamabad, Pakistan
3 USDA-ARS, Wheat Health, Genetics, and Quality Research Unit, Pullman, WA 99164-6430, USA
Interactions of the stripe rust pathogen (Puccinia striiformis f. sp. tritici) with wheat plants activate a wide range of host responses. Among various genes involved in the plant-pathogen interactions, the expressions of particular pathogenesis-related (PR) protein genes determine different defense responses. Different types of resistance have been recognized and utilized for developing wheat cultivars for resistance to stripe rust. All-stage resistance can be detected in seedling stage and remains at high levels throughout the plant growth stages. This type of resistance is race-specific and not durable. In contrast, plants with only high-temperature adult-plant (HTAP) resistance are susceptible in seedling stage, but become resistant when plants grow older and the weather becomes warmer. HTAP resistance controlled by a single gene is partial, but usually non-race specific and durable. The objective of this study was to analyze the expression of PR protein genes involved in different types of wheat resistance to stripe rust. The expression levels of 8 PR protein genes (PR1, PR1.2, PR2, PR3, PR4, PR5, PR9 and PR10) were quantitatively evaluated at 0, 1, 2, 7 and 14 days after inoculation in single resistance gene lines of wheat with all-stage resistance genes YrTr1, Yr76, YrSP and YrExp2 and lines carrying HTAP resistance genes Yr52, Yr59, Yr62 and Yr7B. Races PSTv-4 and PSTv-37 for compatible and incompatible interactions were used in evaluation of PR protein gene expression in wheat lines carrying all-stage resistance genes in the seedling-stage experiment while PSTv-37 was used in the HTAP experiment. Analysis of quantitative real-time polymerase chain reaction (qRT-PCR) revealed that all of the PR protein genes were involved in the different types of resistance controlled by different Yr genes. However, these genes were upregulated at different time points and at different levels during the infection process among the wheat lines with different Yr genes for either all-stage resistance or HTAP resistance. Some of the genes were also induced in compatible interactions, but the levels were almost always higher in the incompatible interaction than in the compatible interaction at the same time point for each Yr gene. These results indicate that both salicylic acid and jasmonate signaling pathways are involved in both race-specific all-stage resistance and non-race specific HTAP resistance. Although expressing at different stages of infection and at different levels, these PR protein genes work in concert for contribution to different types of resistance controlled by different Yr genes.
Received: 12 September 2017
|Fund: This study was supported by the U.S. Department of Agriculture, Agricultural Research Service (2090-22000-018-00D), the Washington Grain Commission, USA (13C-3061-5665) and the Idaho Wheat Commission, USA (13C-3061-5665; 13C-3061-4232).
Correspondence Xianming Chen, Tel: +1-509-3358086, E-mail: firstname.lastname@example.org
|About author: Sumaira Farrakh, E-mail: email@example.com; Meinan Wang, E-mail: firstname.lastname@example.org;
Cite this article:
Sumaira Farrakh, Meinan Wang, Xianming Chen.
Pathogenesis-related protein genes involved in race-specific allstage resistance and non-race specific high-temperature adult-plant resistance to Puccinia striiformis f. sp. tritici in wheat. Journal of Integrative Agriculture, 17(11): 2478-2491.
| Alonso E, De Carvalho Niebel F, Obregon P, Gheysen G, Inze D, Van Montagu M, Castresana C. 1995. Differential
in vitro DNA-binding activity to a promoter element of the gn1 β-1,3-glucanase gene in hyper sensitively reacting tobacco plants. The Plant Journal, 7, 309–320.
Apel K, Hirt H. 2004. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology, 55, 373–399.
Baker C J, Orlandi E W. 1995. Active oxygen in plant pathogenesis. Annual Review of Phytopathology, 33, 299–321.
Caruso C, Nobile M, Leonardi L, Bertini L, Buonocore V, Caporale C. 2001. Isolation and amino acid sequence of two new PR-4 proteins from wheat. Journal of Protein Chemistry, 20, 327–335.
Casassola A, Brammer S P, Chaves M S, Martinelli J A, Stefanato F, Boyd L A. 2015. Changes in gene expression profiles as they relate to the adult plant leaf rust resistance in the wheat cv. Toropi. Physiological and Molecular Plant Pathology, 89, 49–54.
Chen X M. 2005. Epidemiology and control of stripe rust (Puccinia striiformis f. sp. tritici) on wheat. Canadian Journal of Plant Pathology, 27, 314–337.
Chen X M. 2013. High-temperature adult-plant resistance, key for sustainable control of stripe rust. American Journal of Plant Sciences, 4, 608–627.
Chen X M. 2014. Integration of cultivar resistance and fungicide application for control of wheat stripe rust. Canadian Journal of Plant Pathology, 36, 311–326.
Chen X M, Coram T E, Huang X L, Wang M N, Dolezal A. 2013. Understanding molecular mechanisms of durable and non-durable resistance to stripe rust in wheat using a transcriptomics approach. Current Genomics, 14, 111–126.
Collinge D B, Kragh K M, Mikkelsen J D, Nielsen K K, Rasmussen U, Vad K. 1993. Plant chitinases. The Plant Journal, 3, 31–40.
Coram T E, Huang X L, Zhan G, Settles M L, Chen X. 2010. Meta-analysis of transcripts associated with race-specific resistance to stripe rust in wheat demonstrates common induction of blue copper-binding protein, heat-stress transcription factor, pathogen-induced WIR1A protein, and ent-kaurene synthase transcripts. Functional & Integrative Genomics, 10, 383–392.
Coram T E, Settles M L, Chen X M. 2008a. Transcriptome analysis of high-temperature adult-plant resistance conditioned by Yr39 during the wheat-Puccinia striiformis f. sp. tritici interaction. Molecular Plant Pathology, 9, 479–493.
Coram T E, Wang M N, Chen X M. 2008b. Transcriptome analysis of the wheat-Puccinia striiformis f. sp. tritici interaction. Molecular Plant Pathology, 9, 157–169.
Datta K, Velazhahan R, Oliva N, Ona I, Mew T, Khush G S, Muthukrishnan S, Datta S K. 1999. Over-expression of the cloned rice thaumatin-like protein (PR-5) gene in transgenic rice plants enhances environmental friendly resistance to Rhizoctonia solani causing sheath blight disease. Theoretical and Applied Genetics, 98, 1138–1145.
Desmond O J, Edgar C I, Manners, J M, Maclean D J, Schenk P M, Kazan K. 2006. Methyl jasmonate induced gene expression in wheat delays symptom development by the crown rot pathogen Fusarium pseudograminearum. Physiological and Molecular Plant Pathology, 67, 171–179.
Dmochowska-Boguta M, Alaba S, Yanushevska Y, Piechota U, Lasota E, Nadolska-Orczyk A, Karlowski W M, Orczyk W. 2015. Pathogen-regulated genes in wheat isogenic lines differing in resistance to brown rust Puccinia triticina. BMC Genomics, 16, 742.
Dodds P N, Rathjen J P. 2010. Plant immunity: Towards an integrated view of plant-pathogen interactions. Nature Reviews Genetics, 11, 539–548.
Duan Z, Guizhen LV, Shen C, Li Q, Qin Z, Niu J. 2014. The role of jasmonic acid signaling in wheat (Triticum aestivum L.) powdery mildew resistance reaction. European Journal of Plant Pathology, 140, 169 –183.
Edreva A. 2005. Pathogenesis-related proteins: Research progress in the last 15 years. General and Applied Plant Physiology, 31, 105–124.
Feng J Y, Wang M N, Hou L, Chen X M. 2013. QTL mapping of resistance to stripe rust in spring wheat PI 182103. Phytopathology, 103(Suppl. 2), 42.
Fernandes H, Michalska K, Sikorski M, Jaskolski M. 2013. Structural and functional aspects of PR-10 proteins. FEBS Journal, 280, 1169–1199.
Geddes J, Eudes F, Laroche A, Selinger L B. 2008. Differential expression of proteins in response to the interaction between the pathogen Fusarium graminearum and its host, Hordeum vulgare. Proteomics, 8, 545–554.
Gkizi D, Lehmann S, L’Haridon F, Serrano M, Paplomatas E J, Métraux J P, Tjamos S E. 2016. The innate immune signaling system as a regulator of disease resistance and induced systemic resistance activity against Verticillium dahliae. Molecular Plant-Microbe Interactions, 29, 313–323.
Hao Y B, Wang T, Wang K, Wang X J, Fu Y P, Huang L L, Kang Z S. 2016. Transcriptome analysis provides insights into the mechanisms underlying wheat plant resistance to stripe rust at the adult plant stage. PLoS ONE, 11, e0150717.
Hou M M, Li W J, Bai H, Liu Y M, Li L Y, Liu L J, Liu B, Liu G Z. 2012. Characteristic expression of rice pathogenesis-related proteins in rice leaves during interactions with Xanthomonas oryzae pv. oryzae. Plant Cell Reporter, 31, 895–904.
Huang X L, Ma J B, Chen X M, Wang X J, Ding K, Han D J, Qua Z P, Huang L L, Kang Z S. 2013. Genes involved in adult plant resistance to stripe rust in wheat cultivar Xingzi 9104. Physiological and Molecular Plant Pathology, 81, 26–32.
Lamb C, Dixon R A. 1997. The oxidative burst in plant disease resistance. Plant Molecular Biology, 48, 251–275.
Levy A, Guenoune-Gelbart D, Epel B L. 2007. β-1,3-Glucanases: Plasmodesmal gate keepers for intercellular communication. Plant Signaling & Behavior, 2, 404–407.
Li W L, Faris J D, Muthukrishnan S, Liu D J, Chen P D, Gill B S. 2001. Isolation and characterization of novel cDNA clones of acidic chitinases and β-1,3-glucanases from wheat spikes infected by Fusarium graminearum. Theoretical and Applied Genetics, 102, 353–362.
Li X, Zhang Y, Zhang W, Zhang J, Wang H, Liu D. 2016. Expression profiles of pathogenesis-related gene, TaLr35PR1 as it relate to Lr35-mediated adult plant leaf rust resistance. Plant Molecular Biology Reporter, 34, 1127–1135.
Lin F, Chen X M. 2008. Molecular mapping of genes for race-specific overall resistance to stripe rust in wheat cultivar Express. Theoretical and Applied Genetics, 116, 797–806.
Line R F. 2002. Stripe rust of wheat and barley in North America: A retrospective historical review. Annual Review of Phytopathology, 40, 75–118.
Line R F, Qayoum A. 1992. Virulence, Aggressiveness, Evolution and Distribution of Races of Puccinia Striiformis (The Cause of Stripe Rust of Wheat) in North America, 1968–87. United States Department of Agriculture, Agricultural Research Service. Technical Bulletin No. 1788.
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods, 25, 402–408.
Van Loon L C, Geraats B P J, Linthorst H J M. 2006a. Ethylene as a modulator of disease resistance in plants. Trends in Plant Sciences, 11, 184–191.
Van Loon L C, Rep M, Pieterse C M J. 2006b. Significance of inducible defense-related proteins in infected plants. Annual Review of Phytopathology, 44, 135–162.
Van Loon L C, Van Strien E A. 1999. The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 proteins. Physiological and Molecular Plant Pathology, 55, 85–97.
Lu Y, Wang M N, Chen X M, See D, Chao S M, Jing J X. 2014. Mapping of Yr62 and a small effect QTL for high-temperature adult-plant resistance to stripe rust in spring wheat PI 192252. Theoretical and Applied Genetics, 127, 1449–1459.
Mauch F, Mauch-Mani B, Boller T. 1988. Antifungal hydrolases in pea tissue II. Inhibition of fungal growth by combinations of chitinase and β-1,3-glucanase. Plant Physiology, 88, 936–942.
Molina A, Görlach 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. Molecular Plant-Microbe Interactions, 12, 53–58.
Niu J S, Liu R, Zheng L. 2007. Expression analysis of wheat
PR-1, PR-2, PR-5 activated by Bgt and SA, and powdery mildew resistance. Journal of Triticeae Crops, 27, 1132–1137.
Odjakova M, Hadjiivanova C. 2001. The complexity of pathogen defense in plants. Bulgarian Journal of Plant Physiology, 27, 101–110.
Osmond R, Hrmova M, Fontaine F, Imberty A, Fincher G. 2001. Binding interactions between barley thaumatin-like proteins and (1-3)-β-D-glucans. European Journal of Biochemistry, 268, 4190–4199.
Park C J, Kim K J, Shin R, Park J M, Shin Y C, Paek K H. 2004. Pathogenesis-related protein 10 isolated from hot pepper functions as a ribonuclease in an antiviral pathway. Plant Journal, 37, 186–198.
Pozo M J, Van Loon L C, Pieterse C M. 2004. Jasmonates-signals in plant-microbe interactions. Plant Growth Regulation, 23, 211–222.
Pritsch C, Muehlbauer G J, Bushnell W R, Somers D A, Vance C P. 2000. Fungal development and induction of defense response genes during early infection of wheat spikes by Fusarium graminearum. Molecular Plant-Microbe Interactions, 13, 159–169.
Ray S, Anderson J M, Urmeev F I, Goodwin S B. 2003. Rapid induction of a protein disulfide isomerase and defense-related genes in wheat in response to the hemibiotrophic fungal pathogen Mycosphaerella graminicola. Plant Molecular Biology, 53, 701–714.
Rebman G, Mauch F, Dudler R. 1991. Sequence of a wheat cDNA encoding a pathogen-induced thaumatin-like protein. Plant Molecular Biology, 17, 283–285.
Ren R S, Wang M N, Chen X M, Zhang Z J. 2012. Characterization and molecular mapping of Yr52 for high-temperature adult-plant resistance to stripe rust in spring wheat germplasm PI 183527. Theoretical and Applied Genetics, 125, 847–857.
Soltanloo H, Khorzoghi E G, Ramezanpour S S, Arabi M K, Pahlavani M H. 2010. The expression profile of Chi-1, Glu-2, Glu-3 and PR1.2 genes in scab-resistant and susceptible wheat cultivars during infection by Fusarium graminearum. Plant Omics, 3, 162–166.
Takahashi H, Kanayama Y, Zheng M S, Kusano T, Hase S, Ikegami M, Shah J. 2004. Antagonistic interactions between the SA and JA signaling pathways in Arabidopsis modulate expression of defense genes and gene-for-gene resistance to cucumber mosaic virus. Plant Cell Physiology, 45, 803–809.
Tenhaken R, Levine A, Brisson L F, Dixon R A, Lamb C. 1995. Function of the oxidative burst in hypersensitive disease resistance. Proceedings of the National Academy of Sciences of the United States of America, 92, 4158–4163.
Walter S, Nicholson P, Doohan F M. 2010. Action and reaction of host and pathogen during Fusarium head blight disease. New Phytologist, 185, 54–66.
Wan A M, Chen X M. 2014. Virulence characterization of Puccinia striiformis f. sp. tritici using a new set of Yr single-gene line differentials in the United States in 2010. Plant Disease, 98, 1534–1542.
Wang H Y, Liu D Q, Yang W X, Li Y N, Zhang N, Gao Q. 2007. Cloning and characterization of pathogenesis-related protein 1 gene from TcLr35 wheat. Plant Genetic Resources, 8, 16–20. (in Chinese)
Wang X J, Liu W, Chen X M, Tang C L, Dong Y L, Ma J B, Huang X L, Wei G R, Han Q M, Huang L L, Kang Z S. 2010. Differential gene expression in incompatible interaction between wheat and stripe rust fungus revealed by cDNA-AFLP and comparison to compatible interaction. BMC Plant Biology, 10, 9.
Wellings C R. 2011. Global status of stripe rust: A review of historical and current threats. Euphytica, 179, 129–141.
Wellings C R, Singh R P, McIntosh R A, Pretorius Z A. 2004. The development and application of near isogenic lines for the stripe (yellow) rust pathosystem. In: The Proceedings of the 11th International Cereal Rusts and Powdery Mildew Conference. 22–27 August, 2004. Norwich, England. [2017-06-01]. http://www.crpmb.org/icrpmc11/abstracts.htm
Williams B, Dickman M. 2008. Plant programmed cell death: Can’t live with it; can’t live without it. Molecular Plant Pathology, 9, 531–544.
Wu J, Kim S G, Kang K Y, Kim J G, Park S R, Gupta R, Kim Y H, Wang Y, Kim S T. 2016. Overexpression of a pathogenesis-related protein 10 enhances biotic and abiotic stress tolerance in rice. Journal of Plant Pathology, 32, 552–562.
Xiang C, Feng J Y, Wang M N, Chen X M, See D R, Wan A M, Wang T. 2016. Molecular mapping of stripe rust resistance gene Yr76 in winter club wheat cultivar Tyee. Phytopathology, 106, 1186–1193.
Yin C T, Chen X M, Wang X J, Han Q M, Kang Z S, Hulbert S. 2009. Generation and analysis of expression sequence tags from haustoria of the wheat stripe rust fungus Puccinia striiformis f. sp. tritici. BMC Genomics, 10, 626.
Yoshikawa M, Yamaoka N, Rakeuchi Y. 1993. Elicitors: Their significance and primary modes of action in the induction of plant defense reactions. Plant Cell Physiology, 34, 1163–1173.
Zhang H, Wang C, Cheng Y, Chen X, Han Q, Huang L, Wei G, Kang Z. 2012. Histological and cytological characterization of adult plant resistance to wheat stripe rust. Plant Cell Reporter, 31, 2121–2137.
Zhou X L, Wang M N, Chen X M, Lu Y, Kang Z S, Jing J X. 2014. Identification of Yr59 conferring high-temperature adult-plant resistance to stripe rust in wheat germplasm PI 178759. Theoretical and Applied Genetics, 127, 935–945.
|No Suggested Reading articles found!