Haplotype divergence and multiple candidate genes at Rphq2, a partial resistance QTL of barley to Puccinia hordei

Jazyk angličtina Země Německo Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid26542283
Odkazy

PubMed 26542283
PubMed Central PMC4733143
DOI 10.1007/s00122-015-2627-5
PII: 10.1007/s00122-015-2627-5
Knihovny.cz E-zdroje

KEY MESSAGE: Rphq2, a minor gene for partial resistance to Puccinia hordei , was physically mapped in a 188 kbp introgression with suppressed recombination between haplotypes of rphq2 and Rphq2 barley cultivars. ABSTRACT: Partial and non-host resistances to rust fungi in barley (Hordeum vulgare) may be based on pathogen-associated molecular pattern (PAMP)-triggered immunity. Understanding partial resistance may help to understand non-host resistance, and vice versa. We constructed two non-gridded BAC libraries from cultivar Vada and line SusPtrit. Vada is immune to non-adapted Puccinia rust fungi, and partially resistant to P. hordei. SusPtrit is susceptible to several non-adapted rust fungi, and has been used for mapping QTLs for non-host and partial resistance. The BAC libraries help to identify genes determining the natural variation for partial and non-host resistances of barley to rust fungi. A major-effect QTL, Rphq2, for partial resistance to P. hordei was mapped in a complete Vada and an incomplete SusPtrit contig. The physical distance between the markers flanking Rphq2 was 195 Kbp in Vada and at least 226 Kbp in SusPtrit. This marker interval was predicted to contain 12 genes in either accession, of which only five genes were in common. The haplotypes represented by Vada and SusPtrit were found in 57 and 43%, respectively, of a 194 barley accessions panel. The lack of homology between the two haplotypes probably explains the suppression of recombination in the Rphq2 area and limit further genetic resolution in fine mapping. The possible candidate genes for Rphq2 encode peroxidases, kinases and a member of seven-in-absentia protein family. This result suggests that Rphq2 does not belong to the NB-LRR gene family and does not resemble any of the partial resistance genes cloned previously.

Zobrazit více v PubMed

Allouis S, Moore G, Bellec A, Sharp R, Rampant PF, Mortimer K, Pateyron S, Foote TN, Griffiths S, Caboche M. Construction and characterisation of a hexaploid wheat (Triticum aestivum L.) BAC library from the reference germplasm’Chinese Spring’. Cereal Res Commun. 2003;31:331–338.

Almagro L, Gómez Ros LV, Belchi-Navarro S, Bru R, Ros Barceló A, Pedreño MA. Class III peroxidases in plant defence reactions. J Exp Bot. 2009;60:377–390. doi: 10.1093/jxb/ern277. PubMed DOI

Antolín-Llovera M, Ried MK, Binder A, Parniske M. Receptor kinase signaling pathways in plant-microbe interactions. Annu Rev Phytopathol. 2012;50:451–473. doi: 10.1146/annurev-phyto-081211-173002. PubMed DOI

Arru L, Francia E, Pecchioni N. Isolate-specific QTLs of resistance to leaf stripe (Pyrenophora graminea) in the ‘Steptoe’ × ’Morex’ spring barley cross. Theor Appl Genet. 2003;106:668–675. PubMed

Atienza S, Jafary H, Niks RE. Accumulation of genes for susceptibility to rust fungi for which barley is nearly a nonhost results in two barley lines with extreme multiple susceptibility. Planta. 2004;220:71–79. doi: 10.1007/s00425-004-1319-1. PubMed DOI

Brugmans B, van der Hulst RGM, Visser RGF, Lindhout P, van Eck HJ. A new and versatile method for the successful conversion of AFLP™ markers into simple single locus markers. Nucleic Acids Res. 2003;31:e55. doi: 10.1093/nar/gng055. PubMed DOI PMC

Brugmans B, Hutten RGB, Rookmaker ANO, Visser RGF, Eck HJ. Exploitation of a marker dense linkage map of potato for positional cloning of a wart disease resistance gene. Theor Appl Genet. 2006;112:269–277. doi: 10.1007/s00122-005-0125-x. PubMed DOI

Chalhoub B, Belcram H, Caboche M. Efficient cloning of plant genomes into bacterial artificial chromosome (BAC) libraries with larger and more uniform insert size. Plant Biotechnol J. 2004;2:181–188. doi: 10.1111/j.1467-7652.2004.00065.x. PubMed DOI

Chen X, Niks R, Hedley P, Morris J, Druka A, Marcel T, Vels A, Waugh R. Differential gene expression in nearly isogenic lines with QTL for partial resistance to Puccinia hordei in barley. BMC Genom. 2010;11:629. doi: 10.1186/1471-2164-11-629. PubMed DOI PMC

Clarke L, Carbon J. A colony bank containing synthetic CoI EI hybrid plasmids representative of the entire E. coli genome. Cell. 1976;9:91–99. doi: 10.1016/0092-8674(76)90055-6. PubMed DOI

Den Herder G, Yoshida S, Antolín-Llovera M, Ried MK, Parniske M. Lotus japonicus E3 ligase SEVEN IN ABSENTIA4 destabilizes the symbiosis receptor-like kinase SYMRK and negatively regulates rhizobial infection. Plant Cell. 2012;24:1691–1707. doi: 10.1105/tpc.110.082248. PubMed DOI PMC

Dros J. The creation and maintenance of two spring barley varieties. Euphytica. 1957;6:45–48. doi: 10.1007/BF00179516. DOI

Faris JD, Liu Z, Xu SS. Genetics of tan spot resistance in wheat. Theor Appl Genet. 2013;126:2197–2217. doi: 10.1007/s00122-013-2157-y. PubMed DOI

Fu H, Dooner HK. Intraspecific violation of genetic colinearity and its implications in maize. Proc Natl Acad Sci USA. 2002;99:9573–9578. doi: 10.1073/pnas.132259199. PubMed DOI PMC

Fu D, Uauy C, Distelfeld A, Blechl A, Epstein L, Chen X, Sela H, Fahima T, Dubcovsky J. A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science. 2009;323:1357–1360. doi: 10.1126/science.1166289. PubMed DOI PMC

Fukuoka S, Saka N, Koga H, Ono K, Shimizu T, Ebana K, Hayashi N, Takahashi A, Hirochika H, Okuno K, Yano M. Loss of function of a proline-containing protein confers durable disease resistance in rice. Science. 2009;325:998–1001. doi: 10.1126/science.1175550. PubMed DOI

Giese H, Holm-Jensen AG, Jensen HP, Jensen J. Localization of the Laevigatum powdery mildew resistance gene to barley chromosome 2 by the use of RFLP markers. Theor Appl Genet. 1993;85:897–900. PubMed

González AM, Marcel TC, Kohutova Z, Stam P, van der Linden CG, Niks RE. Peroxidase profiling reveals genetic linkage between peroxidase gene clusters and basal host and non-host resistance to rusts and mildew in barley. PLoS One. 2010;5:e10495. doi: 10.1371/journal.pone.0010495. PubMed DOI PMC

Gore MA, Chia J, Elshire RJ, Sun Q, Ersoz ES, Hurwitz BL, Peiffer JA, McMullen MD, Grills GS, Ross-Ibarra J, Ware DH, Buckler ES. A first-generation haplotype map of maize. Science. 2009;326:1115–1117. doi: 10.1126/science.1177837. PubMed DOI

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. 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. 2010;64:498–510. doi: 10.1111/j.1365-313X.2010.04348.x. PubMed DOI

Hickey LT, Lawson W, Platz GJ, Dieters M, Franckowiak J. Origin of leaf rust adult plant resistance gene Rph20 in barley. Genome. 2012;55:396–399. doi: 10.1139/g2012-022. PubMed DOI

Hu G, Fearon ER. Siah-1 N-terminal RING domain is required for proteolysis function, and C-terminal sequences regulate oligomerization and binding to target proteins. Mol Cell Biol. 1999;19:724–732. doi: 10.1128/MCB.19.1.724. PubMed DOI PMC

Hückelhoven R, Kogel K-H. Reactive oxygen intermediates in plant-microbe interactions: who is who in powdery mildew resistance? Planta. 2003;216:891–902. PubMed

Isidore E, Scherrer B, Bellec A, Budin K, Faivre P, Waugh R, Keller B, Caboche M, Feuillet C, Chalhoub B. Direct targeting and rapid isolation of BAC clones spanning a defined chromosome region. Funct Integr Genom. 2005;5:97–103. doi: 10.1007/s10142-004-0127-9. PubMed DOI

Jafary H, Szabo LJ, Niks RE. Innate nonhost immunity in barley to different heterologous rust fungi is controlled by sets of resistance genes with different and overlapping specificities. Mol Plant Microbe Interact. 2006;19:1270–1279. doi: 10.1094/MPMI-19-1270. PubMed DOI

Jafary H, Albertazzi G, Marcel TC, Niks RE. High diversity of genes for nonhost resistance of barley to heterologous rust fungi. Genetics. 2008;178:2327–2339. doi: 10.1534/genetics.107.077552. PubMed DOI PMC

Janda J, Bartoš J, Šafář J, Kubaláková M, Valárik M, Číhalíková J, Šimková H, Caboche M, Sourdille P, Bernard M, Chalhoub B, Doležel J. Construction of a subgenomic BAC library specific for chromosomes 1D, 4D and 6D of hexaploid wheat. Theor Appl Genet. 2004;109:1337–1345. doi: 10.1007/s00122-004-1768-8. PubMed DOI

Johnston PA, Niks RE, Meiyalaghan V, Blanchet E, Pickering R. Rph22: mapping of a novel leaf rust resistance gene introgressed from the non-host Hordeum bulbosum L. into cultivated barley (Hordeum vulgare L.) Theor Appl Genet. 2013;126:1613–1625. doi: 10.1007/s00122-013-2078-9. PubMed DOI

Jones JDG, Dangl JL. The plant immune system. Nature. 2006;444:323–329. doi: 10.1038/nature05286. PubMed DOI

Kraakman ATW, Martínez F, Mussiraliev B, Eeuwijk FA, Niks RE. Linkage disequilibrium mapping of morphological, resistance, and other agronomically relevant traits in modern spring barley cultivars. Mol Breed. 2006;17:41–58. doi: 10.1007/s11032-005-1119-8. DOI

Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science. 2009;323:1360–1363. doi: 10.1126/science.1166453. PubMed DOI

Kurtz S, Phillippy A, Delcher A, Smoot M, Shumway M, Antonescu C, Salzberg S. Versatile and open software for comparing large genomes. Genome Biol. 2004;5:R12. doi: 10.1186/gb-2004-5-2-r12. PubMed DOI PMC

Leroy P, Guilhot N, Sakai H, Bernard A, Choulet F, Theil S, Reboux S, Amano N, Flutre T, Pelegrin C, Ohyanagi H, Seidel M, Giacomoni F, Reichstadt M, Alaux M, Gicquello E, Legeai F, Cerutti L, Numa H, Tanaka T, Mayer K, Itoh T, Quesneville H, Feuillet C. TriAnnot: a versatile and high performance pipeline for the automated annotation of plant genomes. Front Plant Sci. 2012;3:5. doi: 10.3389/fpls.2012.00005. PubMed DOI PMC

Ma Z, Weining S, Sharp PJ, Liu C. Non-gridded library: a new approach for BAC (bacterial artificial chromosome) exploitation in hexaploid wheat (Triticum aestivum) Nucleic Acids Res. 2000;28:e106. doi: 10.1093/nar/28.24.e106. PubMed DOI PMC

Mago R, Tabe L, Vautrin S, Šimková H, Kubaláková M, Upadhyaya N, Berges H, Kong X, Breen J, Doležel J, Appels R, Ellis JG, Spielmeyer W. Major haplotype divergence including multiple germin-like protein genes, at the wheat Sr2 adult plant stem rust resistance locus. BMC Plant Biol. 2014;14:379. doi: 10.1186/s12870-014-0379-z. PubMed DOI PMC

Manosalva PM, Davidson RM, Liu B, Zhu X, Hulbert SH, Leung H, Leach JE. A germin-like protein gene family functions as a complex quantitative trait locus conferring broad-spectrum disease resistance in rice. Plant Physiol. 2009;149:286–296. doi: 10.1104/pp.108.128348. PubMed DOI PMC

Marcel TC, Aghnoum R, Durand J, Varshney RK, Niks RE. Dissection of the barley 2L1. 0 region carrying the ‘Laevigatum’ quantitative resistance gene to leaf rust using near-isogenic lines (NIL) and subNIL. Mol Plant Microbe Interact. 2007;20:1604–1615. doi: 10.1094/MPMI-20-12-1604. PubMed DOI

Marcel TC, Varshney RK, Barbieri M, Jafary H, de Kock MJD, Graner A, Niks RE. A high-density consensus map of barley to compare the distribution of QTLs for partial resistance to Puccinia hordei and of defence gene homologues. Theor Appl Genet. 2007;114:487–500. doi: 10.1007/s00122-006-0448-2. PubMed DOI

Marcel TC, Gorguet B, Ta MT, Kohutova Z, Vels A, Niks RE. Isolate specificity of quantitative trait loci for partial resistance of barley to Puccinia hordei confirmed in mapping populations and near-isogenic lines. New Phytol. 2008;177:743–755. doi: 10.1111/j.1469-8137.2007.02298.x. PubMed DOI

Mayer KFX, Martis M, Hedley PE, Šimková H, Liu H, Morris JA, Steuernagel B, Taudien S, Roessner S, Gundlach H, Kubaláková M, Suchánková P, Murat F, Felder M, Nussbaumer T, Graner A, Salse J, Endo T, Sakai H, Tanaka T, Itoh T, Sato K, Platzer M, Matsumoto T, Scholz U, Doležel J, Waugh R, Stein N. Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell. 2011;23:1249–1263. doi: 10.1105/tpc.110.082537. PubMed DOI PMC

Mbengue M, Camut S, de Carvalho-Niebel F, Deslandes L, Froidure S, Klaus-Heisen D, Moreau S, Rivas S, Timmers T, Hervé C, Cullimore J, Lefebvre B. The Medicago truncatula E3 ubiquitin ligase PUB1 interacts with the LYK3 symbiotic receptor and negatively regulates infection and nodulation. Plant Cell. 2010;22:3474–3488. doi: 10.1105/tpc.110.075861. PubMed DOI PMC

Meyers BC, Kaushik S, Nandety RS. Evolving disease resistance genes. Curr Opin Plant Biol. 2005;8:129–134. doi: 10.1016/j.pbi.2005.01.002. PubMed DOI

Niks RE. Comparative histology of partial resistance and the nonhost reaction to leaf rust pathogens in barley and wheat seedlings. Phytopathology. 1983;73:60–64. doi: 10.1094/Phyto-73-60. DOI

Niks RE. Haustorium formation by Puccinia hordei in leaves of hypersensitive, partially resistant, and nonhost plant genotypes. Phytopathology. 1983;73:64–66. doi: 10.1094/Phyto-73-64. DOI

Niks RE. Nonhost plant species as donors for resistance to pathogens with narrow host range I. Determination of nonhost status. Euphytica. 1987;36:841–852. doi: 10.1007/BF00051868. DOI

Niks RE, Marcel TC. Nonhost and basal resistance: how to explain specificity? New Phytol. 2009;182:817–828. doi: 10.1111/j.1469-8137.2009.02849.x. PubMed DOI

Niks RE, Fernandez E, Bv Haperen, Bekele Aleye B, Martinez F. Specificity of QTLs for partial and non-host resistance of barley to leaf rust fungi. Acta Phytopathol Entomol Hun. 2000;35:13–21.

Niks RE, Parlevliet JE, Lindhout P, Bai Y (2011) Breeding crops with resistance to diseases and pests. Wageningen Academic Publishers, Wageningen, p 198

Nilmalgoda SD, Cloutier S, Walichnowski AZ. Construction and characterization of a bacterial artificial chromosome (BAC) library of hexaploid wheat (Triticum aestivum L.) and validation of genome coverage using locus-specific primers. Genome. 2003;46:870–878. doi: 10.1139/g03-067. PubMed DOI

Noël L, Moores TL, van der Biezen EA, Parniske M, Daniels MJ, Parker JE, Jones JDG. Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant Cell. 1999;11:2099–2111. doi: 10.1105/tpc.11.11.2099. PubMed DOI PMC

Parlevliet JE, van Ommeren A. Partial resistance of barley to leaf rust, Puccinia hordei. II. Relationship between field trials, micro plot tests and latent period. Euphytica. 1975;24:293–303. doi: 10.1007/BF00028194. DOI

Peterson DG, Tomkins JP, Frisch DA, Wing RA, Paterson AH. Construction of plant bacterial artificial chromosome (BAC) libraries: an illustrated guide. J Agric Genom. 2000;5:1–100.

Qi X, Niks RE, Stam P, Lindhout P. Identification of QTLs for partial resistance to leaf rust (Puccinia hordei) in barley. Theor Appl Genet. 1998;96:1205–1215. doi: 10.1007/s001220050858. DOI

Qi X, Jiang G, Chen W, Niks RE, Stam P, Lindhout P. Isolate-specific QTLs for partial resistance to Puccinia hordei in barley. Theor Appl Genet. 1999;99:877–884. doi: 10.1007/s001220051308. DOI

Rodriguez MCS, Petersen M, Mundy J. Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol. 2010;61:621–649. doi: 10.1146/annurev-arplant-042809-112252. PubMed DOI

Saisho D, Myoraku E, Kawasaki S, Sato K, Takeda K. Construction and characterization of a bacterial artificial chromosome (BAC) library from the Japanese malting barley variety ‘Haruna Nijo’. Breed Sci. 2007;57:29–38. doi: 10.1270/jsbbs.57.29. DOI

Sakata K, Nagamura Y, Numa H, Antonio BA, Nagasaki H, Idonuma A, Watanabe W, Shimizu Y, Horiuchi I, Matsumoto T, Sasaki T, Higo K. RiceGAAS: an automated annotation system and database for rice genome sequence. Nucleic Acids Res. 2002;30:98–102. doi: 10.1093/nar/30.1.98. PubMed DOI PMC

Salvaudon L, Giraud T, Shykoff JA. Genetic diversity in natural populations: a fundamental component of plant–microbe interactions. Curr Opin Plant Biol. 2008;11:135–143. doi: 10.1016/j.pbi.2008.02.002. PubMed DOI

Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, p 626

Scherrer B, Isidore E, Klein P, Kim J-S, Bellec A, Chalhoub B, Keller B, Feuillet C. Large intraspecific haplotype variability at the Rph7 locus results from rapid and recent divergence in the barley genome. Plant Cell. 2005;17:361–374. doi: 10.1105/tpc.104.028225. PubMed DOI PMC

Schulte D, Ariyadasa R, Shi B, Fleury D, Saski C, Atkins M, Wu C, Graner A, Langridge P, Stein N. BAC library resources for map-based cloning and physical map construction in barley (Hordeum vulgare L.) BMC Genom. 2011;12:247. doi: 10.1186/1471-2164-12-247. PubMed DOI PMC

Shen J, Araki H, Chen L, Chen J, Tian D. Unique evolutionary mechanism in R-genes under the presence/absence polymorphism in Arabidopsis thaliana. Genetics. 2006;172:1243–1250. doi: 10.1534/genetics.105.047290. PubMed DOI PMC

Shi BJ, Sutton T, Collins NC, Pallotta M, Langridge P. Construction of a barley bacterial artificial chromosome library suitable for cloning genes for boron tolerance, sodium exclusion and high grain zinc content. Plant Breed. 2010;129:291–296. doi: 10.1111/j.1439-0523.2009.01762.x. DOI

The International Barley Genome Sequencing Consortium A physical, genetic and functional sequence assembly of the barley genome. Nature. 2012;491:711–716. PubMed

Thiel T, Michalek W, Varshney R, Graner A. Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.) Theor Appl Genet. 2003;106:411–422. PubMed

Trujillo M, Troeger M, Niks RE, Kogel K, Hückelhoven R. Mechanistic and genetic overlap of barley host and non-host resistance to Blumeria graminis. Mol Plant Pathol. 2004;5:389–396. doi: 10.1111/j.1364-3703.2004.00238.x. PubMed DOI

van Berloo R, Aalbers H, Werkman A, Niks R. Resistance QTL confirmed through development of QTL-NILs for barley leaf rust resistance. Mol Breed. 2001;8:187–195. doi: 10.1023/A:1013722008561. DOI

Varshney R, Marcel TC, Ramsay L, Russell J, Röder MS, Stein N, Waugh R, Langridge P, Niks RE, Graner A. A high density barley microsatellite consensus map with 775 SSR loci. Theor Appl Genet. 2007;114:1091–1103. doi: 10.1007/s00122-007-0503-7. PubMed DOI

Xia Z, Wu H, Watanabe S, Harada K. Construction and targeted retrieval of specific clone from a non-gridded soybean bacterial artificial chromosome library. Anal Biochem. 2014;444:38–40. doi: 10.1016/j.ab.2013.09.026. PubMed DOI

Yeo FKS, Hensel G, Vozábová T, Martin-Sanz A, Marcel TC, Kumlehn J, Niks RE. Golden SusPtrit: a genetically well transformable barley line for studies on the resistance to rust fungi. Theor Appl Genet. 2014;127:325–337. doi: 10.1007/s00122-013-2221-7. PubMed DOI

Yu Y, Tomkins JP, Waugh R, Frisch DA, Kudrna D, Kleinhofs A, Brueggeman RS, Muehlbauer GJ, Wise RP, Wing RA. A bacterial artificial chromosome library for barley (Hordeum vulgare L.) and the identification of clones containing putative resistance genes. Theor Appl Genet. 2000;101:1093–1099. doi: 10.1007/s001220051584. DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...