Skip to main content
Log in

Genetic mapping of a major gene in triticale conferring resistance to bacterial leaf streak

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

A major gene conferring resistance to bacterial leaf streak was mapped to chromosome 5R in triticale.

Abstract

Bacterial leaf streak (BLS), caused by Xanthomonas translucens pv. undulosa (Xtu), is an important disease of wheat and triticale around the world. Although resistance to BLS is limited in wheat, several triticale accessions have high levels of resistance. To characterize the genetic basis of this resistance, we developed triticale mapping populations using a resistant accession (Siskiyou) and two susceptible accessions (UC38 and Villax St. Jose). Bulked segregant analysis in an F2 population derived from the cross of Siskiyou × UC38 led to the identification of a simple sequence repeat (SSR) marker (XSCM138) on chromosome 5R that co-segregated with the resistance gene. The cross of Siskiyou × Villax St. Jose was advanced into an F2:5 recombinant inbred line population and evaluated for BLS reaction. Genetic linkage maps on this population were assembled with markers generated using genotyping-by-sequencing as well as several SSR markers previously identified on 5R. Quantitative trait locus (QTL) mapping revealed a single major QTL on chromosome 5R, underlined by the same SSR marker as in the Siskiyou × UC38 population. The F1 hybrids of the two crosses were highly resistant to BLS, indicating that resistance is largely dominant. This work will facilitate introgression of this rye-derived BLS resistance gene into the wheat genome by molecular marker-mediated chromosome engineering.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

BLS:

Bacterial leaf streak

BSA:

Bulked segregant analysis

GBS:

Genotyping-by-sequencing

LOD:

Log of odds ratio

QTL:

Quantitative trait locus

MIM:

Multiple interval mapping

RIL:

Recombinant inbred line

REMS:

Rye expressed microsatellite sites

SNP:

Single nucleotide polymorphism

SSD:

Single seed descent

SSR:

Simple sequence repeat

SCM:

Secale cereale microsatellite

Xtu :

Xanthomonas translucens pv. undulosa

References

  • Adhikari TB, Hansen JM, Gurung S, Bonman JM (2011) Identification of new sources of resistance in winter wheat to multiple strains of Xanthomonas translucens pv. undulosa. Plant Dis 95:582–588

    Article  Google Scholar 

  • Adhikari TB, Gurung S, Hansen JM, Bonman JM (2012a) Pathogenic and genetic diversity of Xanthomonas translucens pv. undulosa in North Dakota. Phytopathology 102:390–402

    Article  PubMed  Google Scholar 

  • Adhikari TB, Gurung S, Hansen JM, Jackson EW, Bonman JM (2012b) Association mapping of quantitative trait loci in spring wheat landraces conferring resistance to bacterial leaf streak and spot blotch. Plant Genome 5:1–16

    Article  Google Scholar 

  • Bauer E, Schmutzer T, Barilar I, Mascher M, Gundlach H, Martis MM, So Twardziok, Hackauf B, Gordillo A, Wilde P, Schmidt M, Korzun V, Mayer KF, Schmid K, Schön CC, Scholz U (2017) Towards a whole-genome sequence for rye (Secale cereale L.). Plant J 89:853–869

    Article  CAS  PubMed  Google Scholar 

  • Bragard C, Singer E, Alizadeh A, Vauterin L, Maraite H, Swings J (1997) Xanthomonas translucens from small grains: diversity and phytopathological relevance. Phytopathology 87:1111–1117

    Article  CAS  PubMed  Google Scholar 

  • Charkhabi NF, Shams-bakhsh M, Rahimian H (2015) Reaction of Iranian cereal genotype to multiple strains of Xanthomonas translucens pv. cerealis. J Agric Sci Technol 17:241–248

    Google Scholar 

  • Charkhabi NF, Booher NJ, Peng Z, Wang L, Rahimian H, Shams-Bakhsh M, Liu Z, Liu S, White FF, Bogdanove AJ (2017) Complete genome sequencing and targeted mutagenesis reveal virulence contributions of Tal2 and Tal4b of Xanthomonas translucens pv. undulosa ICMP11055 in bacterial leaf streak of wheat. Front Microbiol 8:1488. https://doi.org/10.3389/fmicb.2017.01488

    Article  Google Scholar 

  • Cunfer BM, Scolari BL (1982) Xanthomonas campestris pv. translucens on triticale and other small grains. Phytopathology 72:683–686

    Article  Google Scholar 

  • Duveiller E, van Ginkel M, Thijssen M (1993) Genetic analysis of resistance to bacterial leaf streak caused by Xanthomonas campestris pv. undulosa in bread wheat. Euphytica 66:35–43

    Article  Google Scholar 

  • Duveiller E, Bragard C, Maraite H (1997) Bacterial leaf streak and black chaff caused by Xanthomonas translucens. In: Duveiller E, Fucikovsky L, Rudolph K (eds) The bacterial diseases of wheat: concepts and methods of disease management. CIMMYT, Mexico, pp 25–47

    Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  CAS  PubMed  Google Scholar 

  • El Attari H, Sarrafi A, Alizadeh A, Dechamp-Guillaume G, Barrault G (1996) Genetic analysis of partial resistance to bacterial leaf streak (Xanthomonas campestris pv. cerealis) in wheat. Plant Pathol 45:736–741

    Article  Google Scholar 

  • Forster RL, Schaad NW (1988) Control of black chaff of wheat with seed treatment and a foundation seed health program. Plant Dis 72:935–938

    Article  Google Scholar 

  • Gardnier DM, Upadhya NM, Slitter J, Ellis JG, Dodds PN, Kazan K, Manners JM (2014) Genomic analysis of Xanthomonas translucens pathogenic on wheat and barley reveals cross-kingdom gene transfer events and diverse protein delivery systems. PLoS One 9:e84995

    Article  Google Scholar 

  • Gustafson JP, Rupert EA, Qualset CO (1973) Registration of UC-38 triticale germplasm. Crop Sci 13:586

    Article  Google Scholar 

  • Gustafson JP, Ma XF, Korzun V, Snape JW (2009) A consensus map of rye integrating mapping data from five mapping populations. Theor Appl Genet 118(4):793–800

    Article  PubMed  Google Scholar 

  • Hackauf B, Wehling P (2002) Identification of microsatellite polymorphisms in an expressed portion of the rye genome. Plant Breed 121:17–25

    Article  CAS  Google Scholar 

  • Hackauf B, Wehling P (2003) Development of microsatellite markers in rye: map construction. Plant Breed Seed Sci 48:143–151

    Google Scholar 

  • Jaenicke S, Bunk B, Wibberg D, Spröer C, Hersemann L, Blom J, Winkler A, Schatschneider S, Albaum SP, Kölliker R, Goesmann A, Pühler A, Overmann J, Vorhölter F (2016) Complete genome sequence of the barley pathogen Xanthomonas translucens pv. translucens DSM 1874T (ATCC 19319T). Genome Announc 4:e01334-16

    Article  PubMed  PubMed Central  Google Scholar 

  • Joehanes R, Nelson JC (2008) QGene 4.0, an extensible Java QTL-analysis platform. Bioinformatics 24(23):2788–2789

    Article  CAS  PubMed  Google Scholar 

  • Johnson JW, Cunfer BM, Morey DD (1987) Inheritance of resistance to Xanthomonas campestris pv. translucens in triticale. Euphytica 36:603–607

    Article  Google Scholar 

  • Johnson JW, Cunfer BM, Rothrock CS, Bruckner PL, Raymer PL, Roberts JJ (1989) Registration of GA21 and GA22 bacterial leaf streak resistant triticale germplasm line. Crop Sci 29:1585

    Article  Google Scholar 

  • Kandel YR, Glover KD, Tande CA, Osborne LE (2012) Evaluation of spring wheat germplasm for resistance to bacterial leaf streak caused by Xanthomonas campestris pv. translucens. Plant Dis 96:1743–1748

    Article  Google Scholar 

  • Kandel YR, Glover KD, Osborne LE, Gonzalez-Hernandez JL (2015) Mapping quantitative resistance loci for bacterial leaf streak disease in hard red spring wheat using an identity by descent mapping approach. Euphytica 201:53–65

    Article  Google Scholar 

  • Kariyawasam GK, Carter AH, Rasmussen JB, Faris JD, Xu SS, Mergoum M, Liu ZH (2016) Genetic relationships between race-nonspecific and race-specific interactions in the wheat–Pyrenophora tritici-repentis pathosystem. Theor Appl Genet 129:897–908

    Article  CAS  PubMed  Google Scholar 

  • Khlestkina EK, Than MH, Pestsova EG, Röder MS, Malyshev SV, Korzun V, Börner A (2004) Mapping of 99 new microsatellite-derived loci in rye (Secale cereale L.) including 39 expressed sequence tags. Theor Appl Genet 109:725–732

    Article  CAS  PubMed  Google Scholar 

  • Korzun V, Malyshev S, Voylokov AV, Börner A (2001) A genetic map of rye (Secale cereale L.) combining RFLP, isozyme, protein, microsatellite and gene loci. Theor Appl Genet 102:709–717

    Article  CAS  Google Scholar 

  • Kosambi DD (1944) The estimation of map distance from recombination values. Ann Eugen 12:592–597

    Google Scholar 

  • Kuleung C, Baenziger PS, Kachman SD, Dweikat I (2006) Evaluating the genetic diversity of triticale with wheat and rye SSR markers. Crop Sci 46:1692–1700

    Article  CAS  Google Scholar 

  • Kumar S, Kumar N, Balyan HS, Gupta PK (2003) 1BL.1RS translocation in some indian bread wheat genotypes and strategies for its use in future wheat breeding. Caryologia 56:23–30

    Article  Google Scholar 

  • Langlois PA, Snelling J, Hamilton JP, Bragard C, Koebnik R, Verdier V, Triplett LR, Blom J, Tisserat NA, Leach JE (2017) Characterization of the Xanthomonas translucens complex using draft genomes, comparative genomics, phylogenetic analysis and diagnostic LAMP assays. Phytopathology 107:519–527

    Article  PubMed  Google Scholar 

  • Long YM, Chao WS, Ma GJ, Xu SS, Qi LL (2017) An innovative SNP genotyping method adapting to multiple platforms and throughputs. Theor Appl Genet 130:597–607

    Article  CAS  PubMed  Google Scholar 

  • Lorieux M (2012) MapDisto: fast and efficient computation of genetic linkage maps. Mol Breeding 30(2):1231–1235

    Article  CAS  Google Scholar 

  • Lu F, Lipka AE, Glaubitz J, Elshire R, Cherney JH, Casler MD, Buckler ES, Costich DE (2013) Switchgrass genomic diversity, ploidy, and evolution: novel insights from a network-based SNP discovery protocol. PLoS Genet 9:e1003215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matos M, Pérez-Flores V, Camacho MV, Pernaute B, Pinto-Carnide O, Benito C (2007) Detection and mapping of SSRs in rye ESTs from aluminum-stressed roots. Mol Breed 20:103–115

    Article  CAS  Google Scholar 

  • Milus EA, Mirlohi AF (1995) Survival of Xanthomonas campestris pv. translucens between successive wheat crops in Arkansas. Plant Dis 79:263–265

    Article  Google Scholar 

  • Pallotta MA, Warner P, Fox RL, Kuchel H, Jefferies SJ, Langridge P (2003) Marker assisted wheat breeding in the southern region of Australia. In: Pogna NE (ed) Proceedings of the 10th International Wheat Genetics Symposium, Paestum, Italy, 1-6 September 2003, Istituto Sperimentale per la Cerealicoltura, Rome, Paestum, Italy, pp 789–791

    Google Scholar 

  • Peng Z, Hu Y, Xie Z, Potnis N, Akhunova A, Jones J, Liu Z, White F, Liu S (2016) Long read and single molecule DNA sequencing simplifies genome assembly and TAL effector gene analysis of Xanthomonas translucens. BMC Genom 17:21. https://doi.org/10.1186/s12864-015-2348-9

    Article  Google Scholar 

  • Pesce C, Bolot S, Cunnac S, Portier P, Fischer-Le Saux M, Jacques MA, Gagnevin L, Arlat M, Noël LD, Carrère S, Bragard C, Koebnik R (2015) High quality draft genome sequence of the Xanthomonas translucens pv. cerealis pathotype strain CFBP 2541. Genome Announc 3:e01574-14

    Article  PubMed  PubMed Central  Google Scholar 

  • Poland JA, Brown PJ, Sorrells ME, Jannink JL (2012) Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS One 7:e32253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qualset CO, Vogt HE, Gustafson JP, Zillinsky FJ, Prato JD, Beatty KD (1985) Registration of Siskiyou triticale. Crop Sci 25:887

    Article  Google Scholar 

  • Rabinovich SV (1998) Importance of wheat–rye translocations for breeding modern cultivars of Triticum aestivum L. Euphytica 100:323–340

    Article  Google Scholar 

  • Saal B, Wricke G (1999) Development of simple sequence repeat markers in rye (Secale cereale L.). Genome 42:964–972

    Article  CAS  PubMed  Google Scholar 

  • Sapkota S, Zhang Q, Mergoum M, Xu SS, Liu ZH (2017) Evaluation of triticale accessions for resistance to wheat bacterial leaf streak caused by Xanthomonas translucens pv. undulosa. Plant Pathol. https://doi.org/10.1111/ppa.12768 (in press)

  • Sears ER (1982) A wheat mutation conditioning an intermediate level of homoeologous chromosome pairing. Can J Genet Cytol 24:715–719

    Article  Google Scholar 

  • Shane WW, Baumer JS, Teng PS (1987) Crop losses caused by Xanthomonas streak on spring wheat and barley. Plant Dis 71:927–930

    Article  Google Scholar 

  • Sun H (2016) Development and application of chromosome specific markers of Secale cereale cv. Jingzhouheimai. Master’s thesis, Nanjing Agricultural University, China

  • Tenhola-Roininen T, Kalendar R, Schulman AH, Tanhuanpää P (2011) A double haploid rye linkage map with a QTL affecting α-amylase activity. J Appl Genet 52:299–304

    Article  CAS  PubMed  Google Scholar 

  • Tillman BL, Harrison SA (1996) Heritability of resistance to bacterial streak in winter wheat. Crop Sci 36:412–418

    Article  Google Scholar 

  • Tillman BL, Harrison SA, Clark CA, Milus EA, Russin JS (1996) Evaluation of bread wheat germplasm for resistance to bacterial streak. Crop Sci 36:1063–1068

    Article  Google Scholar 

  • Tillman BL, Kursell WS, Harrison SA, Russin JS (1999) Yield loss caused by bacterial streak in winter wheat. Plant Dis 83:609–614

    Article  Google Scholar 

  • Vauterin L, Yang P, Hoste B, Pot B, Swings J, Kersters K (1992) Taxonomy of xanthomonads from cereals and grasses based on SDS-PAGE of proteins, fatty acid analysis and DNA hybridization. J Gen Microbiol 138:1467–1477

    Article  CAS  Google Scholar 

  • Vauterin L, Hoste B, Kersters K, Swings J (1995) Reclassification of Xanthomonas. Int J Syst Bacteriol 45:472–489

    Article  CAS  Google Scholar 

  • Waldron LR (1929) The relationship of black chaff disease of wheat to certain physical and pathological characters. Science 70:268

    Article  CAS  PubMed  Google Scholar 

  • Wichmann F, Vorholter FJ, Hersemann L, Widmer L, Bolm J, Niehaus K, Reinhard S, Conradin C, Kolliker R (2013) The noncanonical type III secretion system of Xanthomonas translucens pv. graminis is essential for forage grass infection. Mol Plant Pathol 14:576–588

    Article  CAS  PubMed  Google Scholar 

  • Yang B, White FF (2004) Diverse members of the AvrBs3/PthA family of type III effectors are major virulence determinants in bacterial blight disease of rice. Mol Plant Microbe Interact 17(11):1192–1200

    Article  CAS  PubMed  Google Scholar 

  • Zeller FJ, Hsam SLK (1983) Broaden the genetic variability of cultivated wheat by utilizing rye chromatin. In: Proceedings of 6th international wheat genetic symposium. Kyoto, Japan, pp 161–173

  • Zhong S, Leng Y, Friesen TL, Faris JD, Szabo LJ (2009) Development and characterization of expressed sequence tag-derived microsatellite markers for the wheat stem rust fungus Puccinia graminis f. sp. tritici. Phytopathology 99:282–289

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Mr. Justin Hestead for technical support, Drs. Xiwen Cai and Tim Friesen for critical review of the manuscript, and Drs. Andreas Börner (Leibniz Institute of Plant Genetics and Crop Plant Research, Gatersleben, Germany) and Zengjun Qi (Nanjing Agricultural University, Nanjing, China) for providing the sequences of rye 5R SSR primers. This material is based upon work supported, in part, by the National Institute of Food and Agriculture, United States Department of Agriculture (USDA), under Hatch project number ND02224, the North Dakota Wheat Commission, and the US National Science Foundation research Grant 2012-1238189 (F.F.W).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Xuehui Li or Zhaohui Liu.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest for this article.

Ethical standards

All experiments complied with the ethical standards of the university.

Additional information

Communicated by Thomas Miedaner.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wen, A., Jayawardana, M., Fiedler, J. et al. Genetic mapping of a major gene in triticale conferring resistance to bacterial leaf streak. Theor Appl Genet 131, 649–658 (2018). https://doi.org/10.1007/s00122-017-3026-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-017-3026-x

Navigation