Genetic mapping of the Ph gene conferring disease resistance to black shank in tobacco
- 20 Downloads
Black shank, caused by the hemibiotrophic oomycete Phytophthora parasitica var. nicotianae, is one of the most destructive tobacco diseases. Using host resistance is the most environmentally friendly and sustainable strategy for reducing potential crop losses from blue shank disease. To assist breeding for black shank resistance and to facilitate gene cloning, we genetically mapped and characterized the Ph gene that confers resistance to P. parasitica var. nicotianae race 0. The Ph gene, which originated in N. plumbaginifolia, was found to be located on the top of LG20 in a genomic region that is enriched with genes coding for receptor-like kinases. Expression analysis of pathogen-related (PR) genes revealed that the hypersensitive response (HR) was induced rapidly in resistant plants at the biotrophic infection stage, while in susceptible lines, an intensified HR-like reaction was activated during necrotrophy. The genotype race-specific resistance conditioned by the Ph gene may be triggered by recognition of a matching Avirulence (Avr) protein secreted by the pathogen during the early phase of infection. However, pathogen colonization in compatible hosts could be achieved by hijacking of resistance signaling and acquiring nutrients from the dead cells after it switches to necrotrophy.
KeywordsBlack shank Hemibiotrophic oomycete Ph Disease resistance Genetic mapping
This research was supported by British American Tobacco (to SY) and Council for Burley Tobacco (to SY).
Conceived and designed the experiments: DL, RM and SY. Performed the experiments: YB, ND, QQ, XW, NM, and DL. Analyzed the data: YB, ND, DL, DZ, and SY. Wrote the first draft: YB, ND and SY.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- Apple JL (1962) Physiological specialization within Phytophthora parasitica var.nicotianae. Phytopathology 52:351–354Google Scholar
- Arora S, Steuernagel B, Gaurav K, Chandramohan S, Long Y, Matny O, Johnson R, Enk J, Periyannan S, Singh N, Asyraf Md Hatta M, Athiyannan N, Cheema J, Yu G, Kangara N, Ghosh S, Szabo LJ, Poland J, Bariana H, Jones JDG, Bentley AR, Ayliffe M, Olson E, Xu SS, Steffenson BJ, Lagudah E, Wulff BBH (2019) Resistance gene cloning from a wild crop relative by sequence capture and association genetics. Nat Biotechnol 37(2):139–143. https://doi.org/10.1038/s41587-018-0007-9 CrossRefPubMedGoogle Scholar
- Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406. https://doi.org/10.1146/annurev.arplant.57.032905.105346 CrossRefPubMedGoogle Scholar
- Bos JI, Armstrong MR, Gilroy EM, Boevink PC, Hein I, Taylor RM, Zhendong T, Engelhardt S, Vetukuri RR, Harrower B, Dixelius C, Bryan G, Sadanandom A, Whisson SC, Kamoun S, Birch PR (2010) Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1. Proc Natl Acad Sci U S A 107(21):9909–9914. https://doi.org/10.1073/pnas.0914408107 CrossRefPubMedPubMedCentralGoogle Scholar
- Chanda B, Venugopal SC, Kulshrestha S, Navarre DA, Downie B, Vaillancourt L, Kachroo A, Kachroo P (2008) Glycerol-3-phosphate levels are associated with basal resistance to the hemibiotrophic fungus Colletotrichum higginsianum in Arabidopsis. Plant Physiol 147(4):2017–2029. https://doi.org/10.1104/pp.108.121335 CrossRefPubMedPubMedCentralGoogle Scholar
- Davis DL, Nielsen MT (1999) Tobacco: production, chemistry and technology. Blackwell Publ., BostonGoogle Scholar
- Edwards KD, Fernandez-Pozo N, Drake-Stowe K, Humphry M, Evans AD, Bombarely A, Allen F, Hurst R, White B, Kernodle SP, Bromley JR, Sanchez-Tamburrino JP, Lewis RS, Mueller LA (2017) A reference genome for Nicotiana tabacum enables map-based cloning of homeologous loci implicated in nitrogen utilization efficiency. BMC Genomics 18(1):448. https://doi.org/10.1186/s12864-017-3791-6 CrossRefPubMedPubMedCentralGoogle Scholar
- Engelhardt S, Boevink PC, Armstrong MR, Ramos MB, Hein I, Birch PR (2012) Relocalization of late blight resistance protein R3a to endosomal compartments is associated with effector recognition and required for the immune response. Plant Cell 24(12):5142–5158. https://doi.org/10.1105/tpc.112.104992 CrossRefPubMedPubMedCentralGoogle Scholar
- Evangelisti E, Govetto B, Minet-Kebdani N, Kuhn ML, Attard A, Ponchet M, Panabieres F, Gourgues M (2013) The Phytophthora parasitica RXLR effector penetration-specific effector 1 favours Arabidopsis thaliana infection by interfering with auxin physiology. New Phytol 199(2):476–489. https://doi.org/10.1111/nph.12270 CrossRefPubMedGoogle Scholar
- Gaulin E, Drame N, Lafitte C, Torto-Alalibo T, Martinez Y, Ameline-Torregrosa C, Khatib M, Mazarguil H, Villalba-Mateos F, Kamoun S, Mazars C, Dumas B, Bottin A, Esquerre-Tugaye MT, Rickauer M (2006) Cellulose binding domains of a Phytophthora cell wall protein are novel pathogen-associated molecular patterns. Plant Cell 18(7):1766–1777. https://doi.org/10.1105/tpc.105.038687 CrossRefPubMedPubMedCentralGoogle Scholar
- Janeway CA Jr, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20:197–216. https://doi.org/10.1146/annurev.immunol.20.083001.084359 CrossRefPubMedGoogle Scholar
- Larroque M, Barriot R, Bottin A, Barre A, Rougé P, Dumas B, Gaulin E, (2012) The unique architecture and function of cellulose-interacting proteins in oomycetes revealed by genomic and structural analyses. BMC Genomics 13(1):605. https://doi.org/10.1186/1471-2164-13-605 CrossRefPubMedPubMedCentralGoogle Scholar
- Litton CC, Stokes GW, Smiley JH (1966) Occurrence of race 1 of Phytophthora parasitica var. nicotianae. Tob Sci 10:73–74Google Scholar
- Mateos FV, Rickauer M, Esquerre-Tugaye MT (1997) Cloning and characterization of a cDNA encoding an elicitor of Phytophthora parasitica var. nicotianae that shows cellulose-binding and lectin-like activities. Mol Plant-Microbe Interact 10(9):1045–1053. https://doi.org/10.1094/MPMI.19220.127.116.115 CrossRefPubMedGoogle Scholar
- Shew HD, Lucas GB (1991) Compendium of tobacco diseases. American Phytopathological Society, St. PaulGoogle Scholar
- Steuernagel B, Periyannan SK, Hernandez-Pinzon I, Witek K, Rouse MN, Yu G, Hatta A, Ayliffe M, Bariana H, Jones JD, Lagudah ES, Wulff BB (2016) Rapid cloning of disease-resistance genes in plants using mutagenesis and sequence capture. Nat Biotechnol 34(6):652–655. https://doi.org/10.1038/nbt.3543 CrossRefPubMedGoogle Scholar
- Stokes GW, Litton CC (1966) Source of black shank resistance in tobacco and host reaction to races 0 and 1 of Phytophthora parasitica var. nicotianae. Phytopathology 56:678–680Google Scholar
- Valleau WD, Stokes GW, Johnson EM (1960) Nine years’ experience with the Nicotiana longiflora factor for resistance to Phytophthora parasitica var. nicotianae in the control of black shank. Tob Sci 4:92–94Google Scholar
- Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, Gilroy EM, Armstrong MR, Grouffaud S, van West P, Chapman S, Hein I, Toth IK, Pritchard L, Birch PR (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450(7166):115–118. https://doi.org/10.1038/nature06203 CrossRefPubMedGoogle Scholar