Abstract
Target leaf spot is one of the major sorghum diseases in southern Japan and caused by a necrotrophic fungus, Bipolaris sorghicola. Sorghum resistance to target leaf spot is controlled by a single recessive gene (ds1). A high-density genetic map of the ds1 locus was constructed with simple sequence repeat markers using progeny from crosses between a sensitive variety, bmr-6, and a resistant one, SIL-05, which allowed the ds1 gene to be genetically located within a 26-kb region on the short arm of sorghum chromosome 5. The sorghum genome annotation database for BTx623, for which the whole genome sequence was recently published, indicated a candidate gene from the Leucine-Rich Repeat Receptor Kinase family in this region. The candidate protein kinase gene was expressed in susceptible plants but was not expressed or was severely reduced in resistant plants. The expression patterns of ds1 gene and the phenotype of target leaf spot resistance were clearly correlated. Genomic sequences of this region in parental varieties showed a deletion in the promoter region of SIL-05 that could cause reduction of gene expression. We also found two ds1 alleles for resistant phenotypes with a stop codon in the coding region. The results shown here strongly suggest that the loss of function or suppression of the ds1 protein kinase gene leads to resistance to target leaf spot in sorghum.
Similar content being viewed by others
References
Ali GS, Reddy A (2008) PAMP-triggered immunity: early events in the activation of FLAGELLIN SENSITIVE2. Plant Signal Behav 3:423–426
Agrawal GK, Jwa NS, Rakwal R (2000) A novel rice (Oryza sativa L.) acidic PR1 gene highly responsive to cut, phytohormones, and protein phosphatase inhibitors. Biochem Biophys Res Commun 274:157–165
Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795
Bent AF, Mackey D (2007) Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Ann Rev Phytopathol 45:399–436
Boon-Long T, Sontirat P, Wirojwatanakul K (1988) Target spot new sorghum disease in Thailand. http://agrisfaoorg/agris-search/search/displaydo?f=1995/TH/TH95007xml;TH9321755
Borges OL (1979) Herencia de la resistencia a Drechslera Sorghicola en Sorgo. Instituto de genetica informe de investigacion’ 79:32–35
Borges OL (1983) Pathogenicity of Drechslera sorghicola isolates on sorghum in Venezuela. Plant Dis 67:996–997
Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G (2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18:465–476
Chu Z, Ouyang Y, Zhang J, Yang H, Wang S (2004) Genome-wide analysis of defense-responsive genes in bacterial blight resistance of rice mediated by the recessive R gene xa13. Mol Genet Genom 271:111–120
Dalmacio SC (2000) Target leaf spot. In: Frederiksen RA, Odvody GN (eds) Compendium of sorghum diseases, 2nd edn. APS Press, the American Phytopathological Society, St. Paul, pp 16–17
Eckardt NA (2002) Plant disease susceptibility genes? Plant Cell 14:1983–1986
Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer ELL, Eddy SR, Bateman A (2010) The Pfam protein families database. Nucl Acids Res 38:D211–222
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 (New York, NY 325:998–1001
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Ann Rev Phytopathol 43:205–227
Hammond-Kosack KE, Parker JE (2003) Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding. Curr Opin Biotechnol 14:177–193
He K, Gou X, Powell RA, Yang H, Yuan T, Guo Z, Li J (2008) Receptor-like protein kinases, BAK1 and BKK1, regulate a light-dependent cell-death control pathway. Plant Signal Behav 3:813–815
Humphry M, Consonni C, Panstruga R (2006) mlo-based powdery mildew immunity: silver bullet or simply non-host resistance? Mol Plant Pathol 7:605–610
Iyer AS, McCouch SR (2004) The rice bacterial blight resistance gene xa5 encodes a novel form of disease resistance. Mol Plant Microbe Interact 17:1348–1354
Katewa R, Mathur K, Bunker RN (2005) Variability in target leaf spot pathogen Bipolaris sorghicola of Sorghum in Rajasthan, India. Int Sorghum Millets Newsl 46:32–35
Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newberg LA (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181
Lee SW, Han SW, Sririyanum M, Park CJ, Seo YS, Ronald PC (2009) A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity. Science (New York, NY 326:850–853
Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC (2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110:213–222
Macko V, Stimmel MB, Wolpert TJ, Dunkle LD, Acklin W, Banteli R, Jaun B, Arigoni D (1992) Structure of the host-specific toxins produced by the fungal pathogen Periconia circinata. Proc Natl Acad Sci USA 89:9574–9578
Mihara M, Itoh T, Izawa T (2010) SALAD database: a motif-based database of protein annotations for plant comparative genomics. Nucl Acids Res 38:D835–842
Minami E, Ozeki Y, Matsuoka M, Koizuka N, Tanaka Y (1989) Structure and some characterization of the gene for phenylalanine ammonia-lyase from rice plants. Eur J Biochem FEBS 185:19–25
Moffett P (2009) Mechanisms of recognition in dominant R gene mediated resistance. Adv Virus Res 75:1–33
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucl Acid Res 8:4321–4325
Nagy E, Lee T-C, Ramakrishna W, Xu Z, Klein P, SanMiguel P, Cheng C-P, Li J, Devos K, Schertz K, Dunkle L, Bennetzen J (2007) Fine mapping of the Pc locus of Sorghum bicolor, a gene controlling the reaction to a fungal pathogen and its host-selective toxin. TAG Theor Appl Genet 114:961–970
Nishihara N (1972) Target spot of sorghums. Bull Natl Grassl Res Inst 2:46–53 [in Japanese]
Nishizawa Y, Kawakami A, Hibi T, He DY, Shibuya N, Minami E (1999) Regulation of the chitinase gene expression in suspension-cultured rice cells by N-acetylchitooligosaccharides: differences in the signal transduction pathways leading to the activation of elicitor-responsive genes. Plant Mol Biol 39:907–914
Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob ur R, Ware D, Westhoff P, Mayer KF, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556
Pavan S, Jacobsen E, Visser R, Bai Y (2010) Loss of susceptibility as a novel breeding strategy for durable and broad-spectrum resistance. Mol Breed 25:1–12
Perriere G, Gouy M (1996) WWW-query: an on-line retrieval system for biological sequence banks. Biochimie 78:364–369
Piffanelli P, Ramsay L, Waugh R, Benabdelmouna A, D’Hont A, Hollricher K, Jorgensen JH, Schulze-Lefert P, Panstruga R (2004) A barley cultivation-associated polymorphism conveys resistance to powdery mildew. Nature 430:887–891
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sasaki T, Matsumoto T, Yamamoto K, Sakata K, Baba T, Katayose Y, Wu J, Niimura Y, Cheng Z, Nagamura Y, Antonio BA, Kanamori H, Hosokawa S, Masukawa M, Arikawa K, Chiden Y, Hayashi M, Okamoto M, Ando T, Aoki H, Arita K, Hamada M, Harada C, Hijishita S, Honda M, Ichikawa Y, Idonuma A, Iijima M, Ikeda M, Ikeno M, Ito S, Ito T, Ito Y, Ito Y, Iwabuchi A, Kamiya K, Karasawa W, Katagiri S, Kikuta A, Kobayashi N, Kono I, Machita K, Maehara T, Mizuno H, Mizubayashi T, Mukai Y, Nagasaki H, Nakashima M, Nakama Y, Nakamichi Y, Nakamura M, Namiki N, Negishi M, Ohta I, Ono N, Saji S, Sakai K, Shibata M, Shimokawa T, Shomura A, Song J, Takazaki Y, Terasawa K, Tsuji K, Waki K, Yamagata H, Yamane H, Yoshiki S, Yoshihara R, Yukawa K, Zhong H, Iwama H, Endo T, Ito H, Hahn JH, Kim HI, Eun MY, Yano M, Jiang J, Gojobori T (2002) The genome sequence and structure of rice chromosome 1. Nature 420:312–316
Simmons CR, Litts JC, Huang N, Rodriguez RL (1992) Structure of a rice beta-glucanase gene regulated by ethylene, cytokinin, wounding, salicylic acid and fungal elicitors. Plant Mol Biol 18:33–45
Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, Gardner J, Wang B, Zhai WX, Zhu LH, Fauquet C, Ronald P (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science (New York, NY 270:1804–1806
Speth EB, Lee YN, He SY (2007) Pathogen virulence factors as molecular probes of basic plant cellular functions. Curr Opin Plant Biol 10:580–586
Sweat TA, Wolpert TJ (2007) Thioredoxin h5 Is Required for Victorin Sensitivity Mediated by a CC-NBS-LLR Gene in Arabidopsis. Plant Cell 19:673–687
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680
Torii KU (2004) Leucine-rich repeat receptor kinases in plants: structure, function, and signal transduction pathways. Int Rev Cytol 234:1–46
Tsukiboshi T, Kasuga S, Kimigafukuro T (1990) Inheritance of resistance to target leaf spot caused by Bipolaris cookei (Saccardo) Shoemarker in sorghum (Sorghum bicolar Moench). J Jpn Grassl Sci 35:302–308
Tyler L, Thomas SG, Hu J, Dill A, Alonso JM, Ecker JR, Sun TP (2004) Della proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiol 135:1008–1019
Wisser RJ, Sun Q, Hulbert SH, Kresovich S, Nelson RJ (2005) Identification and characterization of regions of the rice genome associated with broad-spectrum, quantitative disease resistance. Genetics 169:2277–2293
Wolpert TJ, Dunkle LD, Ciuffetti LM (2002) Host-selective toxins and avirulence determinants: what’s in a name? Ann Rev Phytopathol 40:251–285
Wu J, Mizuno H, Hayashi-Tsugane M, Ito Y, Chiden Y, Fujisawa M, Katagiri S, Saji S, Yoshiki S, Karasawa W, Yoshihara R, Hayashi A, Kobayashi H, Ito K, Hamada M, Okamoto M, Ikeno M, Ichikawa Y, Katayose Y, Yano M, Matsumoto T, Sasaki T (2003) Physical maps and recombination frequency of six rice chromosomes. Plant J 36:720–730
Yonemaru J-i, Yamamoto T, Fukuoka S, Uga Y, Hori K, Yano M (2010) Q-TARO: QTL Annotation Rice Online Database. Rice
Yonemaru J, Ando T, Mizubayashi T, Kasuga S, Matsumoto T, Yano M (2009) Development of genome-wide simple sequence repeat markers using whole-genome shotgun sequences of sorghum (Sorghum bicolor (L.) Moench). DNA Res 16:187–193
Zipfel C (2008) Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol 20:10–16
Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–760
Acknowledgments
We thank Dr. Takao Tsukiboshi for providing Bipolaris sorghicola and for his valuable experimental suggestions for dealing with the fungi. We also thank Mr. Futa Sakakibara and Ms. Teiko Tanaka for their support in the field work. This work was supported by a grant from the Ministry of Agriculture, Forestry and Fisheries of Japan (Genomics for Agricultural Innovation, SOR-0002)
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Graner.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kawahigashi, H., Kasuga, S., Ando, T. et al. Positional cloning of ds1, the target leaf spot resistance gene against Bipolaris sorghicola in sorghum. Theor Appl Genet 123, 131–142 (2011). https://doi.org/10.1007/s00122-011-1572-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-011-1572-1