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Molecular Breeding

, 39:16 | Cite as

Saturation of genomic region implicated in resistance to Fusarium oxysporum f. sp. ciceris race 5 in chickpea

  • C. CaballoEmail author
  • E. Madrid
  • J. Gil
  • W. Chen
  • J. Rubio
  • T. Millan
Article
  • 20 Downloads

Abstract

Fusarium oxysporum f. sp. ciceris (Foc) is the major soilborne fungus affecting chickpea and race 5 (Foc5) is the most important in the Mediterranean basin. A gene controlling resistant reaction to Foc5 has been located on LG2 of the chickpea genetic map forming a cluster with resistance genes to other Foc races. The sequence-tagged microsatellite site (STMS) marker TA59 is tightly linked to this genomic region. In the current study, our aim was to look for candidate genes related to resistance to Foc5 starting from the physical position of TA59 and taking advantage of the whole chickpea genome sequence information. We selected a set of markers, covering a region of around 25 Mbp that were genotyped in near-isogenic lines and recombinant inbred lines. Joining data of different plant materials, it was possible to define an area of approximately 820 Kbp. One of the 26 genes annotated in the selected region (LOC101511605) could be considered a candidate gene for its possible implication in resistance reactions. Single-nucleotide polymorphism (SNP) markers selected in the target region were used to screen a collection of 32 genotypes differing in their reactions to Foc5. A cluster analysis showed four main groups, three of them grouping the resistant genotypes and the fourth one, the susceptible lines. The comparison between the haplotypes of representative accessions for each cluster allowed the identification of six SNPs coincident among resistant lines and different from the susceptible lines. These SNPs could be used in marker-assisted selection.

Keywords

Chickpea Fusarium wilt STMS SNPs Candidate genes Marker-assisted selection 

Notes

Acknowledgements

Caballo C. acknowledges her Ph.D. fellowship INIA-CCAA. The author thankfully acknowledges the computer resources, technical expertise, and assistance provided by the SCBI (Supercomputing and Bioinformatics) center of the University of Malaga.

Author contribution statement

GJ, RJ, and MT conceived and designed the experiment. CC and ME performed the experiments. WC provided re-sequencing data and analysis. RJ and MT contributed materials and phenotypic analysis. JG designed the statistical analysis performed by CC. CC, ME, GJ, RJ, and MT wrote the manuscript that was reviewed by WC.

Funding information

This work has been supported by INIA project RTA2017-00041-00-00 (co-financed by the European Union through the ERDF2014–2020 “Programa Operativo de Crecimiento Inteligente”) and PP.AVA.AVA201601.17.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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Supplementary file 4 (DOCX 22 kb)

References

  1. Ali L, Madrid E, Varshney RK, Azam S, Millán T, Rubio J, Gil J (2014) Mapping and identification of a Cicer arietinum NSP2 gene involved in nodulation pathway. Theor Appl Genet 127:481–488CrossRefGoogle Scholar
  2. Ali L, Deokar A, Caballo C, Tar’an B, Gil J, Chen W, Millan T, Rubio J (2016) Fine mapping for double podding gene in chickpea. Theor Appl Genet 129:77–86CrossRefGoogle Scholar
  3. Bayer PE, Ruperao P, Mason AS, Stiller J, Chan C-KK, Hayashi S, Long Y, Meng J, Sutton T, Visendi P, Varshney RK, Batley J, Edwards D (2015) High-resolution skim genotyping by sequencing reveals the distribution of crossovers and gene conversions in Cicer arietinum and Brassica napus. Theor Appl Genet 128:1039–1047CrossRefGoogle Scholar
  4. Benko-Iseppon AM, Winter P, Huettel B, Staginnus C, Muehlbauer FJ, Kahl G (2003) Molecular markers closely linked to fusarium resistance genes in chickpea show significant alignments to pathogenesis-related genes located on Arabidopsis chromosomes 1 and 5. Theor Appl Genet 107:379–386CrossRefGoogle Scholar
  5. Bhatti MA (1990) The effects of inoculum density and environmental factors on wilt and root rot of chickpea (Cicer arietinum L.). Ph.D. Dissertation, Department of Plant Pathology, Washington State University, Pullman, Washington, 132 ppGoogle Scholar
  6. Castillo P, Vovlas N, Jiménez-Díaz R (1998) Pathogenicity and histopathology of Pratylenchus thornei populations on selected chickpea genotypes. Plant Pathol 47:370–376CrossRefGoogle Scholar
  7. Castro P, Piston F, Madrid E, Millan T, Gil J, Rubio J (2010) Development of chickpea near-isogenic lines for Fusarium wilt. Theor Appl Genet 121:1519–1526CrossRefGoogle Scholar
  8. Castro P, Rubio J, Millán T, Gil J, Cobos MJ (2012) Fusarium wilt in chickpea: general aspect and molecular breeding. In: Rios TF, Ortega ER (eds) Fusarium: epidemiology, environmental sources and prevention. Nova Science Publishers, New York, pp 101–122Google Scholar
  9. Castro P, Rubio J, Madrid E, Fernandez-Romero M, Millan T, Gil J (2015) Efficiency of marker-assisted selection for ascochyta blight in chickpea. J Agric Sci 153:56–67CrossRefGoogle Scholar
  10. Cobos MJ, Fernández MJ, Rubio J, Kharrat M, Moreno MT, Gil J, Millán T (2005) A linkage map of chickpea (Cicer arietinum L.) based on populations from Kabuli × desi crosses: location of genes for resistance to fusarium wilt race 0. Theor Appl Genet 110:1347–1353CrossRefGoogle Scholar
  11. Cobos MJ, Winter P, Kharrat M, Cubero JI, Gil J, Millan T, Rubio J (2009) Genetic analysis of agronomic traits in a wide cross of chickpea. Field Crop Res 111:130–136CrossRefGoogle Scholar
  12. Deokar A, Tar’an B (2017) Classical genetics and gene mapping. In: Varshney R, Thudi M, Muehlbauer F (eds) The Chickpea Genome. Compendium of Plant Genomes. Springer, Cham, pp 69–81CrossRefGoogle Scholar
  13. Deokar AA, Ramsay L, Sharpe AG, Diapari M, Sindhu A, Bett K, Warkentin TD, Tar’an B (2014) Genome wide SNP identification in chickpea for use in development of a high density genetic map and improvement of chickpea reference genome assembly. BMC Genomics 15:708CrossRefGoogle Scholar
  14. FAOSTAT (2016) Retrieved July 15, 2018 fromhttp://faostat.fao.org/
  15. Gaur R, Azam S, Jeena G, Khan AW, Choudhary S, Jain M, Yadav G, Tyagi AK, Chattopadhyay D, Bhatia S (2012) High-throughput SNP discovery and genotyping for constructing a saturated linkage map of chickpea (Cicer arietinum L.). DNA Res 19:357–373CrossRefGoogle Scholar
  16. Gaur R, Jeena G, Shah N, Gupta S, Pradhan S, Tyagi AK, Jain M, Chattopadhyay D, Bhatia S (2015) High density linkage mapping of genomic and transcriptomic SNPs for synteny analysis and anchoring the genome sequence of chickpea. Sci Rep 5:13387CrossRefGoogle Scholar
  17. Gowda SJM, Radhika P, Kadoo NY, Mhase LB, Gupta VS (2009) Molecular mapping of wilt resistance genes in chickpea. Mol Breed 24:177–183CrossRefGoogle Scholar
  18. Gujaria N, Kumar A, Dauthal P, Dubey A, Hiremath P, Prakash AB, Farmer A, Bhide M, Shah T, Gaur PM, Upadhyaya HD, Bhatia S, Cook DR, May GD, Varshney RK (2011) Development and use of genic molecular markers (GMMs) for construction of a transcript map of chickpea (Cicer arietinum L.). Theor Appl Genet 122:1577–1589CrossRefGoogle Scholar
  19. Gupta S, Bhar A, Chatterjee M, Das S (2013) Fusarium oxysporum f.sp. ciceri race 1 induced redox state alterations are coupled to downstream defense signaling in root tissues of chickpea (Cicer arietinum L.). PLoS One 8:e73163CrossRefGoogle Scholar
  20. Halila MH, Strange RN (1996) Identification of the causal agent of wilt of chickpea in Tunisia as Fusarium oxysporum f. sp. ciceri race 0. Phytopathol Mediterr 35:67–74Google Scholar
  21. Halila I, Rubio J, Millán T, Gil J, Kharrat M, Marrakchi M (2010) Resistance in chickpea (Cicer arietinum) to Fusarium wilt race ‘0’. Plant Breed 129:563–566Google Scholar
  22. Haware MP, Nene YL (1982) Races of Fusarium oxysporum f. sp. ciceri. Plant Dis 66:809–810CrossRefGoogle Scholar
  23. Honnareddy N, Dubey S (2006) Pathogenic and molecular characterization of Indian isolates of Fusarium oxysporum f.sp ciceris causing chickpea wilt. Curr Sci 91:661–666Google Scholar
  24. Iruela M, Castro P, Rubio J, Cubero JI, Jacinto C, Millán T, Gil J (2007) Validation of a QTL for resistance to ascochyta blight linked to resistance to fusarium wilt race 5 in chickpea (Cicer arietinum L.). Eur J Plant Pathol 119:29–37CrossRefGoogle Scholar
  25. Jain M, Misra G, Patel RK, Priya P, Jhanwar S, Khan AW, Shah N, Singh VK, Garg R, Jeena G, Yadav M, Kant C, Sharma P, Yadav G, Bhatia S, Tyagi AK, Chattopadhyay D (2013) A draft genome sequence of the pulse crop chickpea (Cicer arietinum L.). Plant J 74:715–729CrossRefGoogle Scholar
  26. Jendoubi W, Bouhadida M, Boukteb A, Béji M, Kharrat M (2017) Fusarium wilt affecting chickpea crop. Agriculture 7:23CrossRefGoogle Scholar
  27. Jiménez-Díaz RM, Basallote-Ureba MJ, Rapoport H (1989) Colonization and pathogenesis in chickpeas infected by races of Fusarium oxysporum F. Sp. ciceri. In: Tjamos EC, Beckman CH (eds) Vascular wilt diseases of plants, vol 28. Springer, Berlin, pp 113–121CrossRefGoogle Scholar
  28. Jiménez-Díaz RM, Castillo P, Jiménez-Gasco MM, Landa BB, Navas-Cortés JA (2015) Fusarium wilt of chickpeas: biology, ecology and management. Crop Prot 73:16–27CrossRefGoogle Scholar
  29. Kaiser W, Alcala-Jimenez A, Hervas-Vargas A, Trapero-Casas J, Jiménez-Díaz R (1994) Screening of wild Cicer species for resistance to races 0 to 5 of Fusarium oxysporum f. sp ciceris. Plant Dis 78:962–967CrossRefGoogle Scholar
  30. Langmead B (2010) Aligning short sequencing reads with Bowtie. Curr Protoc Bioinformatics. Chapter 11, Unit 11.7Google Scholar
  31. Lassner MW, Peterson P, Yoder JI (1989) Simultaneous amplification of multiple DNA fragments by polymerase chain reaction in the analysis of transgenic plants and their progeny. Plant Mol Biol Report 7:116–128CrossRefGoogle Scholar
  32. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079CrossRefGoogle Scholar
  33. Lichtenzveig J, Scheuring C, Dodge J, Abbo S, Zhang H (2005) Construction of BAC and BIBAC libraries and their applications for generation of SSR markers for genome analysis of chickpea, Cicer arietinum L. Theor Appl Genet 110:492–510CrossRefGoogle Scholar
  34. Madrid E, Seoane P, Claros M, Barro F, Rubio J, Gil J, Millán T (2014) Genetic and physical mapping of the QTL AR3 controlling blight resistance in chickpea (Cicer arietinum L). Euphytica 198:69–78CrossRefGoogle Scholar
  35. Mayer MS, Tullu A, Simon CJ, Kumar J, Kaiser WJ, Kraft JM, Muehlbauer FJ (1997) Development of a DNA marker for Fusarium wilt resistance in chickpea. Crop Sci 37:1625–1629CrossRefGoogle Scholar
  36. Millan T, Winter P, Jüngling R, Gil J, Rubio J, Cho S, Cobos MJ, Iruela M, Rajesh PN, Tekeoglu M, Kahl G, Muehlbauer FJ (2010) A consensus genetic map of chickpea (Cicer arietinum L.) based on 10 mapping populations. Euphytica 175:175–189CrossRefGoogle Scholar
  37. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP (2011) Integrative genomics viewer. Nat Biotechnol 29:24–26CrossRefGoogle Scholar
  38. Ruperao P, Chan CKK, Azam S, Karafiátová M, Hayashi S, Čížková J, Saxena RK, Šimková H, Song C, Vrána J (2014) A chromosomal genomics approach to assess and validate the desi and kabuli draft chickpea genome assemblies. Plant Biotechnol J 12:778–786CrossRefGoogle Scholar
  39. Saxena MS, Bajaj D, Das S, Kujur A, Kumar V, Singh M, Bansal KC, Tyagi AK, Parida SK (2014) An integrated genomic approach for rapid delineation of candidate genes regulating agro-morphological traits in chickpea. DNA Res 21:695–710CrossRefGoogle Scholar
  40. Sharma KD, Muehlbauer F (2007) Fusarium wilt of chickpea: physiological specialization, genetics of resistance and resistance gene tagging. Euphytica 157:1–14CrossRefGoogle Scholar
  41. Sharma KD, Winter P, Kahl G, Muehlbauer FJ (2003) Molecular mapping of Fusarium oxysporum f. sp. ciceris race 3 resistance gene in chickpea. Theor Appl Genet 108:1243–1248CrossRefGoogle Scholar
  42. Sharma KD, Chen W, Muehlbauer FJ (2005) Genetics of chickpea resistance to five races of Fusarium wilt and a concise set of race differentials for Fusarium oxysporum f. sp. ciceris. Plant Dis 89:385–390CrossRefGoogle Scholar
  43. Tekeoglu M, Tullu A, Kaiser WJ, Muehlbauer FJ (2000) Inheritance and linkage of two genes that confer resistance to fusarium wilt in chickpea. Crop Sci 40:1247–1251CrossRefGoogle Scholar
  44. Thudi M, Khan AW, Kumar V, Gaur PM, Katta K, Garg V, Roorkiwal M, Samineni S, Varshney RK (2016) Whole genome re-sequencing reveals genome-wide variations among parental lines of 16 mapping populations in chickpea (Cicer arietinum L.). BMC Plant Biol 16:10CrossRefGoogle Scholar
  45. Torres A, Weeden N, Martin A (1993) Linkage among isozyme, RFLP and RAPD markers in Vicia faba. Theor Appl Genet 85:937–945CrossRefGoogle Scholar
  46. Tullu A, Kaiser WJ, Kraft JM, Muehlbauer FJ (1999) A second gene for resistance to race 4 of Fusarium wilt in chickpea and linkage with a RAPD marker. Euphytica 109:43–50CrossRefGoogle Scholar
  47. Varshney RK, Song C, Saxena RK, Azam S, Yu S, Sharpe AG, Cannon S, Baek J, Rosen BD, Tar'an B, Millan T, Zhang XD, Ramsay LD, Iwata A, Wang Y, Nelson W, Farmer AD, Gaur PM, Soderlund C, Penmetsa RV, Xu CY, Bharti AK, He WM, Winter P, Zhao SC, Hane JK, Carrasquilla-Garcia N, Condie JA, Upadhyaya HD, Luo MC, Thudi M, Gowda CLL, Singh NP, Lichtenzveig J, Gali KK, Rubio J, Nadarajan N, Dolezel J, Bansal KC, Xu X, Edwards D, Zhang GY, Kahl G, Gil J, Singh KB, Datta SK, Jackson SA, Wang J, Cook DR (2013) Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nat Biotechnol 31:240–246CrossRefGoogle Scholar
  48. Verma S, Gupta S, Bandhiwal N, Kumar T, Bharadwaj C, Bhatia S (2015) High-density linkage map construction and mapping of seed trait QTLs in chickpea (Cicer arietinum L.) using genotyping-by-sequencing (GBS). Sci Rep 5:17512CrossRefGoogle Scholar
  49. Winter P, Benko-Iseppon A-M, Hüttel B, Ratnaparkhe M, Tullu A, Sonnante G, Pfaff T, Tekeoglu M, Santra D, Sant JV, Rajesh NP, Kahl G, Muehlbauer JF (2000) A linkage map of the chickpea (Cicer arietinum L.) genome based on recombinant inbred lines from a C. arietinum×C. reticulatum cross: localization of resistance genes for fusarium wilt races 4 and 5. Theor Appl Genet 101:1155–1163CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Área de Genómica y BiotecnologíaIFAPACórdobaSpain
  2. 2.Department of Plant Developmental BiologyMax Planck Institute for Plant Breeding ResearchCologneGermany
  3. 3.ETSIAM-Dpto. GenéticaUniversidad de CórdobaCórdobaSpain
  4. 4.Grain Legume Genetics and Physiology Research Unit, USDA-ARSWashington State UniversityPullmanUSA

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