Current progress on genetic interactions of rice with rice blast and sheath blight fungi

Abstract

Analysis of genetic interactions between rice and its pathogenic fungi Magnaporthe oryzae and Rhizoctonia solani should lead to a better understanding of molecular mechanisms of host resistance, and the improvement of strategies to manage rice blast and sheath blight diseases. Currently, dozens of rice resistance (R) genes against specific races of the blast fungus have been described. Among them, ten were molecularly characterized and some were widely used for breeding for genetic resistance. The Pi-ta gene was one of the best characterized rice R genes. Following the elucidation of its molecular structure, interaction, distribution, and evolution, user friendly DNA markers were developed from portions of the cloned genes to facilitate the incorporations of the Pi-ta mediated resistance into improved rice varieties using marker assisted selection (MAS). However, rice blast is still a major threat for stable rice production because of race change mutations occurring in rice fields, which often overcome added resistance based on single R genes, and these virulent races of M. oryzae pose a continued challenge for blast control. For sheath blight, progress has been made on the exploration of novel sources of resistance from wild rice relatives and indica rice cultivars. A major quantitative trait locus (QTL), named qSB9-2, was recently verified in several mapping populations with different phenotyping methods, including greenhouse methods. The ability to identify qSB9-2 using greenhouse methods should accelerate the efforts on the qSB9-2 fine mapping and positional cloning.

Keywords

blast / Magnaporthe oryzae / Oryza sativa / Pi-ta / rice / Rhizoctonia solani / sheath blight

References

[1] Ashikawa I, Hayashi N, Yamane H, Kanamori H, Wu J, Matsumoto T, Ono K, Yano M (2008). Two adjacent nucleotide-binding site-leucine-rich repeat class genes are required to confer Pikm-specific rice blast resistance. Genetics, 180: 2267-2276

[2] Ballini E, Morel J B, Droc G, Price A, Courtois B, Notteghem J L, Tharreau D (2008). A genome-wide meta-analysis of rice blast resistance genes and quantitative trait loci provides new insights into partial and complete resistance. Mol Plant-Microbe Interact, 21: 859-868

[3] Bohnert H U, Fudal I, Dioh W, Tharreau D, Notteghem J L, Lebrun, M H (2004). A putative polyketide synthase/peptide synthetase from Magnaporthe grisea signals pathogen attack to resistant rice. Plant Cell, 16: 2499-2513

[4] Bowen P, Menzies J, Ehret D (1992). Soluble silicon sprays inhibit powdery mildew development on grape leaves. Journal of the American Society for Horticultural Science, 117: 906-912

[5] Brooks S A (2007). Sensitivity to a host-selective toxin from Rhizoctonia solani correlates with sheath blight susceptibility in rice. Phytopathology, 97: 1207-1212

[6] Bryan G T, Wu K, Farrall L, Jia Y, Hershey H P, McAdams S A, Faulk K N, Donaldson G K, Tarchini R, Valent B (2000). A single amino acid difference distinguishes resistant and susceptible alleles of rice blast resistance gene Pi-ta. Plant Cell, 12: 2033-2045

[7] Che K P, Zhan Q C, Xing Q H, Wang Z P, Jin D M, He D J, Wang B (2003). Tagging and mapping of rice sheath blight resistance gene. Theor Appl Genet, 106: 293-297

[8] Chen C Q, Belanger R R, Benhamous N, Paulitz T C (1998). Induced systemic resistance by Pseudomonas spp. impairs pre-and post-infection development of Pythium aphanidermatum on cucumber roots. Eur J Plant Pathol, 104: 877-886

[9] Chen X W, Shang J J, Chen D X, Lei C L, Zou Y, Zhai W X, Liu G Z, Xu J C, Ling Z Z, Cao G, Ma B T, Wang Y P, Zhao X F, Li S G, Zhu L H (2006). A B-lectin receptor kinase gene conferring rice blast resistance. Plant J, 46: 794-804

[10] Dann E K, Deverall B J (1995). Effectiveness of systemic resistance in bean against foliar and soilborne pathogens as induced by biological and chemical means. Plant Pathol, 44: 458-466

[11] Dioh W, Tharreau D, Notteghem J L, Orbach M, Lebrun M H (2000). Mapping of avirulence genes in the rice blast fungus, Magnaporthe grisea, with RFLP and RAPD markers. Mol Plant-Microbe Interact, 13: 217-227

[12] Eizenga G C, Agama H A, Lee F N, Jia Y (2006). Identifying novel resistance genes in newly introduced blast resistant rice germplasm. Crop Sci, 46: 1870-1878

[13] Eizenga G C, Agrama H A, Lee F N, Jia Y (2009). Exploring genetic diversity and potential novel disease resistance genes in a collection of rice wild relatives. Genet Resour Crop Evol, 56: 65-76

[14] Farman M L, Leong S A (1998). Chromosome walking to the AVR1-CO39 avirulence gene of Magnaporthe grisea: Discrepancy between the physical and genetic maps. Genetics, 150: 1049-1058

[15] Fjellstrom R G, Conaway-Bormans C A, McClung A M, Marchetti M A, Shank A R, Park W D (2004). Development of DNA markers suitable for marker assisted selection of three Pi genes conferring resistance to multiple Pyricularia grisea pathotypes. Crop Sci, 44: 1790-1798

[16] Flor H H (1971). Current status of the gene-for-gene concept. Annu Rev Phytopathol, 9: 275-296

[17] Gibbons J W, Moldenhauer K A K, Gravois K A, Lee F N, Bernhardt J L, Meullenet J F, Bryant R J, Anders M, Norman R J, Cartwright K, Taylor K, Bullock J, Blocker M M (2006). Registration of 'Cybonnet' Rice. Crop Sci, 46: 2317–2318

[18] Gravois K A, Moldenhauer K A K, Lee F N, Norman R J, Helms R S, Bernhardt J L, Wells B R, Dilday R H, Rohman P C, Blocker M M (1995). Registration of ‘Kaybonnet’ rice. Crop Sci, 35: 586-587

[19] Han Y P, Xing Y Z, Chen Z X, Gu S L, Pan X B, Chen X L, Zhang Q F (2002). Mapping QTL for horizontal resistance to sheath blight in an elite restorer line Minghui 63. Chin J Genet, 29: 622-626 (in Chinese)

[20] Hayashi K, Yoshida H (2009). Refunctionalization of the ancient rice blast disease resistance gene Pit by the recruitment of a retrotransposon as a promoter. Plant J, 57: 413-425

[21] Howard R, Ferrari J, Roach M A, Roach D H, Money N P (1991). Penetration of hard substrates by a fungus employing enormous turgor pressures. Proc Natl Acad Sci USA, 88: 11281-11284

[22] Jia Y, Bryan G, Farrall L, Valent B (2003). Natural variation at the Pi-ta rice blast resistance locus. Phytopathology, 93: 1452-1459

[23] Jia Y, Correa-Victoria F J, McClung A, Zhu L, Liu G, Wamishe Y, Xie J, Marchetti M A, Pinson S R M, Rutger J N, Correll J C (2007). Rapid determination of rice cultivar responses to the sheath blight pathogen Rhizoctonia solani using a micro-chamber screening method. Plant Dis, 91: 485-489

[24] Jia Y, Martin R (2008) Identification of a new locus, Ptr(t), required for rice blast resistance gene Pi-ta-mediated resistance. Mol Plant Microbe Interact, 21: 396-403

[25] Jia Y, McAdams S, Bryan G, Hershey H, Valent B (2000). Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J, 19: 4004-4014

[26] Jia Y, Redus M, Wang Z, Rutger J N (2004). Development of a SNLP marker from the Pi-ta blast resistance gene by tri-Primer PCR. Euphytica, 138: 97-105

[27] Jia Y, Wang Z, Singh P (2002). Development of dominant rice blast resistance Pi-ta gene markers. Crop Sci, 42: 2145-2149

[28] Jia Y, Zhou E, Winston E, Singh P, Correll J, Lee F N, Valent B (2006). Molecular co-evolution of the rice Pi-ta resistance gene and Magnaporthe oryzae avirulence gene AVR-Pita. In: Sanchez F, Quinto C, Lopez-Lara I M, Geiger O, eds. Biology of Plant-Microbe Interactions, Vol. 5, 12^th Intern Symp Plant-Microbe Interact, IS-MPMI, St. Paul, USA, 325-331

[29] Kang S, Lebrun M H, Farrall L, Valent B (2001). Gain of virulence caused by insertion of a Pot3 transposon in a Magnaporthe grisea avirulence gene. Mol Plant-Microbe Interact, 14: 671-674

[30] Kang S, Sweigard J A, Valent B (1995). The PWL host specificity gene family in the blast fungus Magnaporthe grisea. Mol Plant-Microbe Interact, 8: 939-948

[31] Kankanala P, Czymmek K, Valent B (2007). Roles for rice membrane dynamics and plasmodesmata during biotrophic invasion by the blast fungus. Plant Cell, 19: 706-724

[32] Khang C H, Park S Y, Lee Y H, Valent B, Kang S (2008). Genome organization and evolution of the AVR-Pita avirulence gene family in the Magnaporthe grisea species complex. Mol Plant-Microbe Interact, 21: 658-670

[33] Khush G, Jena K (2007). Current status and future prospects of research on blast disease in rice (Oryza sativa). Oral presentation at the 4^th international rice blast conference, Changsha, China

[34] Kunihiro Y, Qian Q, Sato H, Teng S, Zeng D L, Fujimoto K, Zhu L H (2002). QTL analysis of sheath blight resistance in rice (Oryza sativa L.). Chin J Genet, 29: 50-55 (in Chinese)

[35] Lee S K, Song M Y, Seo Y S, Kim H K, Ko S, Cao P J, Suh J P, Yi G, Roh J H, Lee S, An G, Hahn T R, Wang G L, Ronald P, Jeon J S (2009). Rice Pi5-mediated resistance to Magnaporthe oryzae requires the presence of two coiled-coil-nucleotide-binding-leucine-rich repeat genes. Genetics, 181: 1627-1638

[36] Li B, Wang J, Wu Y, Hu X, Zhang Z, Zhang Q, Zhao Q, Feng H, Zhang Z, Wang G L, Wang G, Lu B, Han Z, Wang Z, Zhou B (2009). The Magnaporthe oryzae avirulence gene AvrPiz-t encodes a predicted secreted protein that triggers the immunity in rice mediated by the blast resistance gene Piz-t. Mol Plant-Microbe Interact, 22: 411-420

[37] Li Z K, Pinson S R M, Marchetti M A, Stansel J W, Park W D (1995). Characterization of quantitative trait loci (QTL) in cultivated rice contributing to field resistance to sheath blight (Rhizoctonia solani). Theor Appl Genet, 91: 382-388

[38] Lin F, Chen S, Que Z Q, Wang L, Liu X Q, Pan Q H (2007). The blast resistance gene Pi37 encodes a nucleotide binding site-leucine-rich repeat protein and is a member of a resistance gene cluster on rice chromosome 1. Genetics, 177: 1871-1880

[39] Liu G, Jia Y, Correa-Victoria F J, Prado G A, Yeater K M, McClung A, Correll J C (2009). Mapping quantitative trait loci responsible for resistance to sheath blight in rice. Phytopathology, (in press)

[40] Liu X Q, Lin F, Wang L, Pan Q H (2007). The in silico map-based cloning of Pi36, a rice coiled-coil–nucleotide-binding site–leucine-rich repeat gene that confers race-specific resistance to the blast fungus. Genetics, 176: 2541-2549

[41] Manosalva P, Davidson R, Hulbert S, Leung H, Leach J E (2009). Germin-like protein genes contribute to rice blast disease resistance governed by quantitative trait loci. Plant Physiol, 149: 286-296

[42] Martin G B, Bogdanove A J, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annual Review of Plant Biology, 54: 23-61

[43] McClung A M, Marchetti M, Webb B, Bollich C (1999). Registration of `Madison' Rice. Crop Sci, 39: 1256

[44] Moldenhauer K A K, Gibbons J W, Anders M M, Lee F N, Bernhardt J L, Wilson C E, Cartwright R D, Norman R J, Blocker M M, Boyett V A, Talbert A C, Taylor K, Bulloch J M (2007a). Registration of ‘Spring’ Rice. Crop Sci, 47: 447-449

[45] Moldenhauer K A K, Gibbons J W, Lee F N, Bernhardt J L, Wilson C E, Cartwright R D, Anders M M, Norman R J, Blocker M M, Boyett V A, Tolbert A C, Taylor K, Bulloch J M (2007b). Registration of ‘Banks’ Rice. Crop Sci, 47: 445-446

[46] Moldenhauer K A K, Gravois K A, Lee F N, Norman R J, Bernhardt J L, Well B R, Dilday R H, Blocker M M, Rohman P C, McMinn T A (1998). Registration of ‘Drew’ Rice. Crop Sci, 38: 896-897

[47] Moldenhauer K A K, Lee F N, Gibbons J W, Bernhardt J L, Norman R J, Slaton N A, Wilson C E, Cartwright R D, Anders M M, Blocker M M, Tolbert A C, Bulloch J M (2007c). Registration of ‘Ahrent’ Rice. Crop Sci, 47: 446-447

[48] Moldenhauer K A K, Lee F N, Norman R J, Helms R S, Well R H, Dilday R H, Rohman P C, Marchetti M A (1990). Registration of ‘Katy’ Rice. Crop Sci, 30: 747-748

[49] Orbach M J, Farrall L, Sweigard J A, Chumley F G, Valent B (2000). A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta. Plant Cell, 12: 2019-2032

[50] Pan X B, Zou J H, Chen Z X, Lu J F, Yu H X, Li H T, Wang Z B, Rush M C, Zhu L H (1999). Mapping the QTLs responsible for sheath blight resistance from rice cultivar Jasmine 85. Chinese Science Bulletin, 44: 1629-1635 (in Chinese)

[51] Pinson S R M, Capdevielle F M, Oard J H (2005). Confirming QTL and finding additional loci conditioning sheath blight resistance in rice using recombinant inbred lines. Crop Sci, 45: 503-510

[52] Prasad B, Eizenga G C (2008). Rice sheath blight resistance identified in Oryza spp. accessions. Plant Dis, 92: 1503-1509

[53] Qu S H, Liu G F, Zhou B, Bellizzi M, Zeng L R, Dai L Y, Han B, Wang G L (2006). The broad-spectrum blast resistance gene Pi9 encodes a nucleotide-binding site-leucine-rich repeat protein and is a member of multigene family in rice. Genetics, 172: 1901-1914

[54] Sato H, Ideta O, Ando I, Kunihiro Y, Hirabayashi H, Iwano M, Miyasaka A, Nemoto H, Imbe T (2004). Mapping QTL for sheath blight resistance in the rice line WSS2. Breed Sci, 54: 265-271

[55] Savary S, Teng P S, Willocquet L, Nutter F W Jr (2006). Quantification and modeling of crop losses: A review of purposes. Ann Rev Phytopathol, 44: 89-112

[56] Savary S, Willocquet L, Elazegui F A, Castilla N, Teng P S (2000). Rice pest constraints in tropical Asia: Quantification of yield losses due to rice pests in a range of production situations. Plant Dis, 84: 357-369

[57] Sharma A, McClung A M, Pinson S R M, Kepiro J L, Shank A R, Tabien R E, Wang Y, Fjellstrom R G (2009) Genetic mapping of sheath blight resistance QTL within tropical japonica rice cultivars. Crop Sci, 49: 256-264

[58] Silue D, Notteghem J L, Tharreau D (1992). Evidence for a gene for gene relationship in the Oryza sativa-Magnaporthe grisea pathosystem. Phytopathology, 82: 577-582

[59] Sweigard J A, Carroll A M, Kang S, Farrall L, Chumley F G, Valent B (1995). Identification, cloning, and characterization of PWL2, a gene for host species specificity in the rice blast fungus. Plant Cell, 7: 1221-1233

[60] Tan C X, Ji X M, Yang Y, Pan X Y, Zuo S M, Zhang Y F, Zou J H, Chen Z X, Zhu L H, Pan X B (2005). Identification and marker-assisted selection of two major quantitative genes controlling rice sheath blight resistance in backcross generations. Chin J Genet, 32: 399-405 (in Chinese)

[61] Venu R C, Jia Y, Gowda M, Jia M H, Jantasuriyarat C, Stahlberg E, Li H, Rhineheart A, Boddhireddy P, Singh P, Rutger N, Kudrna D, Wing R, Nelson J C, Wang G L (2007). RL-SAGE and microarray analysis of the rice transcriptome after Rhizoctonia solani infection. Molecular Genetics and Genomics, 278: 421-431

[62] Wamishe Y A, Jia Y, Singh P, Cartwright R D (2007). Identification of field isolates of Rhizoctonia solani to detect quantitative resistance in rice under greenhouse conditions. Front Agric China, 1: 361-367

[63] Wang X, Jia Y, Shu Q Y, Wu D (2008). Haplotype diversity at the Pi-ta locus in cultivated rice and its wild relatives. Phytopathology, 98: 1305-1311

[64] Wang X, Yano M, Yamanouchi U, Iwamoto M, Monna L, Hayasaka H, Katayose Y, Sasaki T (1999). The Pi-b gene for rice blast resistance belongs to the nucleotide binding and leucine-rich repeat class of plant disease resistance genes. The Plant J, 19: 55-64

[65] Wang Z H, Jia Y L, Lin H, Valent B, Rutger J (2007a). Host active defense responses occur within 24 hours after pathogen inoculation in the rice blast system. Rice Sci, 14: 302-310

[66] Wang Z, Jia Y, Rutger J N, Xia Y (2007b). Rapid survey for presence of a blast resistance gene Pi-ta in rice cultivars using the dominant DNA markers derived from portions of the Pi-ta gene. Plant Breed, 126: 36-42

[67] Yamamoto T, Lin H X, Sasaki T, Yano M (2000) Identification of heading date quantitative trait locus Hd6 and characterization of its epistatic interactions with Hd2 in rice. Genetics, 154: 885-891

[68] Yano M, Harushima Y, Nagamura Y, Kurata N, Minobe Y, Sasaki T (1997) Identification of quantitative trait loci controlling heading date of rice using a high-density linkage map. Theor Appl Genet, 95: 1025-1032

[69] Yi M, Chi M H, Khang C H, Park S Y, Kang S, Valent B, Lee Y H (2009). The ER chaperone LHS1 is involved in asexual development and rice infection by the blast fungus Magnaporthe oryzae. Plant Cell, (www.plantcell.org/cgi/doi/10.1105/tpc.107.055988)

[70] Zhou B, Qu S H, Liu G F, Dolan M, Sakai H, Lu G D, Bellizzi M, Wang G L (2006). The eight amino acid differences within three leucine-rich repeats between Pi2 and Piz-t resistance proteins determine the resistance specificity to Magnaporthe grisea. Mol Plant-Microbe Interact, 19: 1216-1228

[71] Zhou E X, Jia Y L, Singh P, Correll J C, Lee F N (2007). Instability of the Magnaporthe oryzae avirulence gene AVR-Pita alters virulence. Fungal Genet Biol, 44: 1024-1034

[72] Zou J H, Pan X B, Chen Z X, Xu J Y, Lu J F, Zhai W X, Zhu L H (2000). Mapping quantitative trait loci controlling sheath blight resistance in two rice cultivars (Oryza sativa L.). Theor Appl Genet, 101: 569-573

[73] Zou Q (2001). Experiment Guide for Plant Physiology. Beijing: China Agricultural Press, 131-135 (in Chinese)

[74] Zuo S M, Yin Y J, Zhang L, Zhang Y F, Chen Z X, Pan X B (2007). Breeding value and further mapping of a QTL qSB-11 conferring the rice sheath blight utilized resistance. Chin J Rice Sci, 21: 136-142 (in Chinese)

Acknowledgements

We thank the staff members of Dale Bumpers National Rice Research Center for their excellent technical assistance. This work was supported in part by the USDA Cooperative State Research, Education and Extension Service–National Research Initiative–Applied Plant Genomics Program entitled “RiceCAP: A coordinated research, education, and extension project for the application of genomic discoveries to improve rice in the United States” (USDA/CSREES grant 2004-35317-14867), the National Science Foundation under Grant No. 0638820, USA and ARS NP 301 project titled “Response of Diverse Rice Germplasm to Biotic and Abiotic Stresses”.

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