Abstract
Rice cultivars exhibiting durable resistance to blast, the most important rice fungal disease provoking up to 30 % of rice losses, are very rare and searching for sources of such a resistance represents a priority for rice-breeding programs. To this aim we analyzed Gigante Vercelli (GV) and Vialone Nano (VN), two temperate japonica rice cultivars in Italy displaying contrasting response to blast, with GV showing a durable and broad-spectrum resistance, whereas VN being highly susceptible. An SSR-based genetic map developed using a GV × VN population segregating for blast resistance identified two blast resistance loci, localized to the long arm of chromosomes 1 and 4 explaining more than 78 % of the observed phenotypic variation for blast resistance. The pyramiding of two blast resistance QTLs was therefore involved in the observed durable resistance in GV. Mapping data were integrated with information obtained from RNA-seq expression profiling of all classes of resistance protein genes (resistance gene analogs, RGAs) and with the map position of known cloned or mapped blast resistance genes to search candidates for the GV resistant response. A co-localization of RGAs with the LOD peak or the marker interval of the chromosome 1 QTL was highlighted and a valuable tool for selecting the resistance gene during breeding programs was developed. Comparative analysis with known blast resistance genes revealed co-positional relationships between the chromosome 1 QTL with the Pi35/Pish blast resistance alleles and showed that the chromosome 4 QTL represents a newly identified blast resistance gene. The present genetic analysis has therefore allowed the identification of two blast resistance loci in the durable blast-resistant rice cultivar GV and tools for molecular selection of these resistance genes.
Similar content being viewed by others
References
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
Bagnaresi P, Biselli C, Orrù L, Urso S, Crispino L, Abbruscato P, Piffanelli P, Lupotto E, Cattivelli L, Valè G (2012) Comparative transcriptome profiling of the early response to Magnaporthe oryzae in durable resistant vs susceptible rice (Oryza sativa L.) genotypes. PLoS One 7:e51609
Ballini E, Morel JB, Droc G, Price A, Courtois B, Notteghem JL, 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
Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890
Chen XW, Shang J, Chen D, Lei C, Zou Y, Zhai W, Liu G, Xu J, Ling Z, Cao G, Ma B, Wang Y, Zhao X, Li S, Zhu L (2006) A B-lectin receptor kinase gene conferring rice blast resistance. Plant J 46:794–804
Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971
Couch BC, Kohn LM (2002) A multilocus gene genealogy concordant with host preference indicates segregation of a new species, Magnaporthe oryzae, from M. grisea. Mycologia 94:683–693
Dean R, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, Orbach MJ, Thon M, Kulkarni R, Xu JR, Pan H, Read ND, Lee YH, Carbone I, Brown D, Oh YY, Donofrio N, Jeong JS, Soanes DM, Djonovic S, Kolomiets E, Rehmeyer C, Li W, Harding M, Kim S, Lebrun MH, Bohnert H, Coughlan S, Butler J, Calvo S, Ma LJ, Nicol R, Purcell S, Nusbaum C, Galagan J, Birren BW (2005) The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434:980–986
Devanna NB, Vijayan J, Sharma TR (2014) The blast resistance gene Pi54of cloned from Oryza officinalis interacts with Avr-Pi54 through its novel non-LRR domains. PLoS One 9:e104840
Faivre-Rampant O, Bruschi G, Abbruscato P, Cavigliolo S, Borgo L, Lupotto E, Piffanelli P (2011) Assessment of genetic diversity in Italian rice germplasm related to agronomic traits and blast resistance (Magnaporthe oryzae). Mol Breed 27:233–246
Fukuoka S, Saka N, Koga H, Ono K, Shimizu T, Ebana K, Hayashi N, Takahashi A, Hirochika H, Okuno K, Yano M (2009) Loss of function of a proline-containing protein confers durable disease resistance in rice. Science 325:998–1001
Fukuoka S, Mizobuchi R, Saka N, Ivan S, Matsumoto T, Okuno K, Yano M (2012) A multiple gene complex on rice chromosome 4 is involved in durable resistance to rice blast. Theor Appl Genet 125:551–559
Fukuoka S, Yamamoto SI, Mizobuchi R, Yamanouchi U, Ono K, Kitazawa N, Yasuda N, Fujita Y, Nguyen TTT, Koizumi S, Sugimoto K, Matsumoto T, Yano M (2014) Multiple functional polymorphisms in a single disease resistance gene in rice enhance durable resistance to blast. Scientific Reports 4:4550
Fukuoka S, Saka N, Mizukami Y, Koga H, Yamanouchi U, Yoshioka Y, Hayashi N, Ebana K, Mizobuchi R, Yano M (2015) Gene pyramiding enhances durable blast disease resistance in rice. Scientific Reports 5:7773
Goto I (1988) Genetic studies on resistance of rice plant to blast fungus (VII). Blast resistance genes of Kuroka. Ann Phytopathol Soc Jpn 54:460–465
Gururani MA, Venkatesh J, Upadhyaya CP, Nookaraju A, Pandey SK, Park SW (2012) Plant disease resistance genes: current status and future directions. Physiol Mol Plant Pathol 78:51–65
Haegi A, Bonardi V, Dall’Aglio E, Glissant D, Tumino G, Collins NC, Bulgarelli D, Infantino A, Stanca AM, Delledonne M, Valè G (2008) Histological and molecular analysis of barley resistance to leaf stripe. Mol Plant Pathol 9:463–478
Hammond-Kosack KE, Parker JE (2003) Deciphering plant–pathogen communication: fresh perspectives for molecular resistance breeding. Curr Opin Biotechnol 14:177–193
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
Hayashi N, Inoue H, Kato T, Funao T, Shirota M, Shimizu T, Kanamori H, Yamane H, Hayano-Saito Y, Matsumoto T, Yano M, Takatsuji H (2010) Durable panicle blast-resistance gene Pb1 encodes an atypical CC-NBS-LRR protein and was generated by acquiring a promoter through local genome duplication. Plant J 64:498–510
Hittalmani S, Parco A, Mew TV, Zeigler RS, Huang N (2000) Fine mapping and DNA marker-assisted pyramiding of the three major genes for blast resistance in rice. Theor Appl Genet 100:1121–1128
Jain M, Nijhawan A, Tyagi AK, Khurana JP (2006) Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochem Biophys Res Commun 345:646–651
Kawahara Y, de la Bastide M, Hamilton JP, Kanamori H, McCombie WR, Ouyang S, Schwartz DC, Tanaka T, Wu J, Zhou S, Childs KL, Davidson RM, Lin H, Quesada-Ocampo L, Vaillancourt B, Sakai H, Lee SS, Kim J, Numa H, Itoh T, Buell CR, Matsumoto T (2013) Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice 6:4
Kim K, Choi D, Kim S, Kwak D, Choi J, Lee S, Lee B, Hwang D, Hwang I (2012) A systems approach for identifying resistance factors to rice stripe virus. Mol Plant Microbe Interact 25:534–545
Koide Y, Kawasaki A, Telebanco-Yanorial MJ, Hairmansis A, Nguyet NTM, Bigirimana J, Fujita D, Kobayashi N, Fukuta Y (2010) Development of pyramided lines with two resistance genes, Pish and Pib, for blast disease (Magnaporthe oryzae B. Couch) in rice (Oryza sativa L.). Plant Breed 129:670–675
Kosambi DD (1944) The estimation of map distance from recombination values. Ann Eugen 12:172–175
Kou Y, Wang S (2010) Broad-spectrum and durability: understanding of quantitative disease resistance. Curr Opin Plant Biol 13:181–185
Lander E, Botstein D (1989) Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199
Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25
Lee S, Song M, Seo Y, Kim H, Ko S, Cao P, Suh J, Yi G, Roh J, Lee S, An G, Hahn T, Wang G, Ronald P, Jeon J (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
Li J, Xie Y, Dai A, Liu L, Li Z (2009) Root and shoot traits responses to phosphorus deficiency and QTL analysis at seedling stage using introgression lines of rice. J Genet Genomics 36:173–183
Li Y, Xia Q, Kou H, Wang D, Lin X, Wu Y, Xu C, Xing S, Liu B (2011) Induced Pib expression and resistance to Magnaporthe grisea are compromised by cytosine demethylation at critical promoter regions in rice. J Integrative Plant Biol 53:814–823
Lin F, Chen S, Que Z, Wang L, Liu X, Pan Q (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
Liu J, Wang X, Mitchell T, Hu Y, Liu X, Dai L, Wang G (2010) Recent progress and understanding of the molecular mechanisms of the rice—Magnaporthe oryzae interaction. Mol Plant Pathol 11:419–427
Luo S, Peng J, Li K, Wang M, Kuang H (2011) Contrasting evolutionary patterns of the Rp1 resistance gene family in different species of Poaceae. Mol Biol Evol 28:313–325
Luo S, Zhang Y, Hu Q, Chen J, Li K, Lu C, Liu H, Wang W, Kuang H (2012) Dynamic nucleotide-binding site and leucine-rich repeat-encoding genes in the grass family. Plant Physiol 159:197–210
McClung AM, Marchetti MA, Webb BD, Bollich CN (1997) Registration of ‘Jefferson’ rice. Crop Sci 37:629–630
McCouch SR (2008) Gene nomenclature system for rice. Rice 1:72–84
McCouch SR, Teytelman L, Xu Y, Lobos KB, Clare K, Walton M, Fu B, Maghirang R, Li Z, Xing Y, Zhang Q, Kono I, Yano M, Fjellstrom R, DeClerck G, Schneider D, Cartinhour S, Ware D, Stein L (2002) Development and mapping of 2240 new SSR markers for rice (Oryza sativa L.). DNA Res 9:257–279
Meyers BC, Kaushik S, Nandety RS (2005) Evolving disease resistance genes. Curr Opin Plant Biol 8:129–134
Nguyen TT, Koizumi S, La TN, Zenbayashi KS, Ashizawa T, Yasuda N, Imazaki I, Miyasaka A (2006) Pi35(t), a new gene conferring partial resistance to leaf blast in the rice cultivar Hokkai 188. Theor Appl Genet 113:697–704
Nyquist WE (1991) Estimation of heritability and prediction of selection response in plant populations. Crit Rev Plant Sci 10:235–322
Rai AK, Kumar SP, Gupta SK, Gautam N, Singh NK, Sharma TR (2011) Functional complementation of rice blast resistance gene Pi-kh (Pi54) conferring resistance to diverse strains of Magnaporthe oryzae. J Plant Biochem Biotech 20:55–65
Rao Y, Dong G, Zeng D, Hu J, Zeng L, Gao Z, Zhang G, Guo L, Qian Q (2010) Genetic analysis of leaffolder resistance in rice. J Genet Genomics 37:325–331
Roumen E, Levy M, Notteghem JL (1997) Characterisation of the European pathogen population of Magnaporthe grisea by DNA fingerprinting and pathotype analysis. Eur J Plant Pathol 103:363–371
Sato H, Takeuchi Y, Hirabayashi H, Nemoto H, Hirayama M, Kato H, Imbe T, Ando I (2006) Mapping QTLs for field resistance to rice blast in the Japanese upland rice variety Norin 12. Breed Sci 56:415–418
Sen S, Churchill GA (2001) A statistical framework for quantitative trait mapping. Genetics 159:371–387
Sharma TR, Rai AK, Gupta SK, Vijayan J, Devanna BN, Ray S (2012) Rice blast management through host-plant resistance: retrospect and prospects. Agric Res 1:37–52
Skamnioti P, Gurr SJ (2009) Against the grain: safeguarding rice from rice blast disease. Trends Biotechnol 27:141–150
Tacconi G, Baldassarre V, Lanzanova C, Faivre-Rampant O, Cavigiolo S, Urso S, Lupotto E, Valè G (2010) Haplotype analysis of genomic regions associated to broad effective blast resistance genes for marker development in rice. Mol Breed 26:595–617
Takahashi A, Hayashi N, Miyao A, Hirochika H (2010) Unique features of the rice blast resistance Pish locus revealed by large scale retrotransposon-tagging. BMC Plant Biol 10:175
Thorvaldsdóttir H, Robinson JT, Mesirov JP (2012) Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14:178–192
Valent B, Khang CH (2010) Recent advances in rice blast effector research. Curr Opin Plant Biol 13:434–441
Van Ooijen JW (2006) JoinMap 4, software for the calculation of genetic linkage maps in experimental populations. Wageningen, Kyazma BV
Wang X, Lee S, Wang J, Ma J, Bianco T, Jia Y (2014) Current advances on genetic resistance to rice blast disease. In: Yan W, Bao J (eds) Rice—germplasm, genetics and improvement, InTech, pp 195–217
Xu X, Hayashi N, Wang C-T, Fukuoka S, Kawasaki S, Takatsuji H, Jang C-J (2014) Rice blast resistance gene Pikahei-1(t), a member of a resistance gene cluster on chromosome 4, encodes a nucleotide-binding site and luecine-rich repeat protein. Mol Breed 34:691–700
Yoshimura S, Yamanouchi U, Katayose Y, Toki S, Wang ZX, Kono I, Kuruta N, Yano M, Iwata N, Sasaki T (1998) Expressionof Xa1, a bacterial blight resistance gene in rice, is induced by bacterial inoculation. Proc Natl Acad Sci USA 95:1663–1668
Zeigler RS, Leong SA, Teng PS (1994) Rice Blast Disease. CAB International, Wallingford, pp 1–626
Zhou Y, Bui T, Auckland LD, Illiams CG (2002) Direct fluorescent primers are superior to M13-tailed primers for Pinus taeda microsatellites. Biotechniques 31:24–28
Acknowledgments
This research was supported by the Project “AGER RISINNOVA” (AGER grant no 2010-2369) and by the Project “ESPLORA” (MiPAAF DM 14658-7303). The authors wish to thank Gabriele Orasen and Ivana Tagliaferri for plants management.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare any conflict of interest in relation to this work.
Ethical standards
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Communicated by B. Yang.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Urso, S., Desiderio, F., Biselli, C. et al. Genetic analysis of durable resistance to Magnaporthe oryzae in the rice accession Gigante Vercelli identified two blast resistance loci. Mol Genet Genomics 291, 17–32 (2016). https://doi.org/10.1007/s00438-015-1085-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-015-1085-8