Skip to main content
Log in

Genetic and physical mapping of the QTLAR3 controlling blight resistance in chickpea (Cicer arietinum L)

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

Physical and genetic maps of chickpea a QTL related to Ascochyta blight resistance and located in LG2 (QTLAR3) have been constructed. Single-copy markers based on candidate genes located in the Ca2 pseudomolecule were for the first time obtained and found to be useful for refining the QTL position. The location of the QTLAR3 peak was linked to an ethylene insensitive 3-like gene (Ein3). The Ein3 gene explained the highest percentage of the total phenotypic variation for resistance to blight (44.3 %) with a confidence interval of 16.3 cM. This genomic region was predicted to be at the Ca2 physical position 32–33 Mb, comprising 42 genes. Candidate genes located in this region include Ein3, Avr9/Cf9 and Argonaute 4, directly involved in disease resistance mechanisms. However, there are other genes outside the confidence interval that may play a role in the blight resistance pathway. The information reported in this paper will facilitate the development of functional markers to be used in the screening of germplasm collections or breeding materials, improving the efficiency and effectiveness of conventional breeding methods.

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.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Adie B, Chico J, Rubio-Somoza I, Solano R (2007) Modulation of Plant Defenses by Ethylene. J Plant Growth Regul 26:160–177. doi:10.1007/s00344-007-0012-6

    Article  CAS  Google Scholar 

  • Agorio A, Vera P (2007) ARGONAUTE4 Is Required for Resistance to Pseudomonas syringae in Arabidopsis. Plant Cell 19:3778–3790. doi:10.1105/tpc.107.054494

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Alonso JM, Stepanova AN, Solano R, Wisman E, Ferrari S, Ausubel FM et al (2003) Five components of the ethylene-response pathway identified in a screen for weak ethylene-insensitive mutants in Arabidopsis. Proc Natl Acad Sci 100:2992–2997. doi:10.1073/pnas.0438070100

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Anbessa Y, Taran B, Warkentin TD, Tullu A, Vandenberg A (2009) Genetic analyses and conservation of QTL for ascochyta blight resistance in chickpea (Cicer arietinum L.). Theor Appl Genet 119:757–765. doi:10.1007/s00122-009-1086-2

    Article  CAS  PubMed  Google Scholar 

  • Aryamanesh N, Nelson MN, Yan G, Clarke HJ, Siddique KHM (2010) Mapping a major gene for growth habit and QTLs for ascochyta blight resistance and flowering time in a population between chickpea and Cicer reticulatum. Euphytica 173:307–319. doi:10.1007/s10681-009-0086-2

    Article  Google Scholar 

  • Atik O, Baum M, El-Ahmed A, Ahmed S, Abang MM, Yabrak MM et al (2011) Chickpea Ascochyta Blight: Disease Status and Pathogen Mating Type Distribution in Syria. J Phytopathol 159:443–449. doi:10.1111/j.1439-0434.2011.01788.x

    CAS  Google Scholar 

  • Berrada AF, Shivakumar BG, Yaburaju NT (2007) Chickpea in cropping systems. In: Yadav SSS, Redden R, Chen W, Sharma B (eds) Chickpea Breeding and Management. CABI Publishing, Wallingford, pp 193–212

    Chapter  Google Scholar 

  • Bouhadida M, Benjannet R, Madrid E, Amri M, Kharrat M (2013) Efficiency of marker-assisted selection in detection of ascochyta blight resistance in Tunisian chickpea breeding lines. Phytopathol Mediterr 52:202–211

    CAS  Google Scholar 

  • Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, Ecker JR (1997) Activation of the Ethylene Gas Response Pathway in Arabidopsis by the Nuclear Protein ETHYLENE-INSENSITIVE3 and Related Proteins. Cell 89:1133–1144. doi:10.1016/S0092-8674(00)80300-1

    Article  CAS  PubMed  Google Scholar 

  • Cho S, Muehlbauer FJ (2004) Genetic effect of differentially regulated fungal response genes on resistance to necrotrophic fungal pathogens in chickpea (Cicer arietinum L.). Physiol Mol Plant Pathol 64:57–66. doi:10.1016/j.pmpp.2004.07.003

    Article  CAS  Google Scholar 

  • Cho S, Chen W, Muehlbauer FJ (2004) Pathotype-specific genetic factors in chickpea (Cicer arietinum L.) for quantitative resistance to ascochyta blight. Theor Appl Genet 109:733–739. doi:10.1007/s00122-004-1693-x

    Article  PubMed  Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cobos MJ, Rubio J, Strange RN, Moreno MT, Gil J, Millan T (2006) A new QTL for Ascochyta blight resistance in an RIL population derived from an interspecific cross in chickpea. Euphytica 149:105–111. doi:10.1007/s10681-005-9058-3

    Article  Google Scholar 

  • Collard BCY, Mackill DJ (2008) Marker-assisted selection: An approach for precision plant breeding in the twenty-first century. Phil Trans R Soc B 363:557–572. doi:10.1098/rstb 2007.2170

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Collard BCY, Jahufer MZZ, Brouwer JB, Pang ECK (2005) An introduction to markers, quantitative trait loci (QTL) mapping and marker-assisted selection for crop improvement: The basic concepts. Euphytica 142:169–196. doi:10.1007/s10681-005-1681-5

    Article  CAS  Google Scholar 

  • Coram TE, Pang ECK (2005a) Isolation and analysis of candidate ascochyta blight defence genes in chickpea. Part I. Generation and analysis of an expressed sequence tag (EST) library. Physiol Mol Plant Pathol 66:192–200. doi:10.1016/j.pmpp.2005.08.003

    Article  CAS  Google Scholar 

  • Coram TE, Pang ECK (2005b) Isolation and analysis of candidate ascochyta blight defence genes in chickpea. Part II. Microarray expression analysis of putative defence-related ESTs. Physiol Mol Plant Pathol 66:201–210. doi:10.1016/j.pmpp.2005.08.002

    Article  CAS  Google Scholar 

  • Cubillos FA, Coustham V, Loudet O (2012) Lessons from eQTL mapping studies: non-coding regions and their role behind natural phenotypic variation in plants. Curr Opin Plant Biol 15:192–198. doi:10.1016/j.pbi.2012.01.005

    Article  CAS  PubMed  Google Scholar 

  • Flandez-Galvez H, Ades PK, Ford R, Pang ECK, Taylor PWJ (2003) QTL analysis for ascochyta blight resistance in an intraspecific population of chickpea (Cicer arietinum L.). Theor Appl Genet 107:1257–1265. doi:10.1007/s00122-003-1371-4

    Article  CAS  PubMed  Google Scholar 

  • Gan X, Stegle O, Behr J, Steffen JG, Drewe P, Hildebrand KL et al (2011) Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477:419–423. doi:10.1038/nature10414

    Article  CAS  PubMed  Google Scholar 

  • Gujaria N, Kumar A, Dauthal P, Dubey A, Hiremath P, Bhanu Prakash A et al (2011) Development and use of genic molecular markers (GMMs) for construction of a transcript map of chickpea (Cicer arietinum L.). Theor Appl Genet 122:1577–1589. doi:10.1007/s00122-011-1556-1

    Article  PubMed Central  PubMed  Google Scholar 

  • Hammond-Kosack KE, Tang S, Harrison K, Jones JDG (1998) The Tomato Cf-9 Disease Resistance Gene Functions in Tobacco and Potato to Confer Responsiveness to the Fungal Avirulence Gene Product Avr9. Plant Cell 10:1251–1266. doi:10.1105/tpc.10.8.1251

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hiremath PJ, Kumar A, Penmetsa RV, Farmer A, Schlueter JA, Chamarthi SK et al (2012) Large-scale development of cost-effective SNP marker assays for diversity assessment and genetic mapping in chickpea and comparative mapping in legumes. Plant Biotechnol J 10:716–732. doi:10.1111/j.1467-7652.2012.00710.x

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Honée G, Buitink J, Jabs T, De Kloe J, Sijbolts F, Apotheker M et al (1998) Induction of Defense-Related Responses in Cf9 Tomato Cells by the AVR9 Elicitor Peptide of Cladosporium fulvum Is Developmentally Regulated. Plant Physiol 117:809–820. doi:10.1104/pp.117.3.809

    Article  PubMed Central  PubMed  Google Scholar 

  • Imtiaz M, Materne M, Hobson K, Van Ginkel M, Malhotra RS (2008) Molecular genetic diversity and linked resistance to ascochyta blight in Australian chickpea breeding materials and their wild relatives. Aust J Agric Res 59:554–560. doi:10.1071/AR07386

    Article  CAS  Google Scholar 

  • Iruela M, Rubio J, Barro F, Cubero JI, Millán T, Gil J (2006) Detection of two quantitative trait loci for resistance to ascochyta blight in an intra-specific cross of chickpea (Cicer arietinum L.): Development of SCAR markers associated with resistance. Theor Appl Genet 112:278–287. doi:10.1007/s00122-005-0126-9

    Article  CAS  PubMed  Google Scholar 

  • Iruela M, Castro P, Rubio J, Cubero JI, Jacinto C, Millán T et al (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 119:29–37. doi:10.1007/s10658-007-9121-0

    Article  Google Scholar 

  • Jain M, Misra G, Patel RK, Priya P, Jhanwar S, Khan AW et al (2013) A draft genome sequence of the pulse crop chickpea (Cicer arietinum L.). Plant J 74:715–729. doi:10.1111/tpj.12173

    Article  CAS  PubMed  Google Scholar 

  • Jones L, Keining T, Eamens A, Vaistij FE (2006) Virus-Induced Gene Silencing of Argonaute Genes in Nicotiana benthamiana Demonstrates That Extensive Systemic Silencing Requires Argonaute1-Like and Argonaute4-Like Genes. Plant Physiol 141:598–606. doi:10.1104/pp.105.076109

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kalendar R, Lee D, Schulman AH (2009) FastPCR software for PCR primer and probe design and repeat search. In: Mansour A (ed) Focus on bioinformatics. Genes, genomes and genomics. 3(Special Issue 1): pp. 1–14

  • Kosambi DD (1944) The estimation of map distance from recombination values. Ann Eugen 12:172–175. doi:10.1111/j.1469-1809.1943.tb02321.x

    Article  Google Scholar 

  • Kumar J, Choudhary AK, Solanki RK, Pratap A (2011) Towards marker-assisted selection in pulses: a review. Plant Breed 130:297–313. doi:10.1111/j.1439-0523.2011.01851.x

    Article  CAS  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE et al (1987) MAPMAKER: An interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181. doi:http://dx.doi.org/10.1016/0888-7543(87)90010-3

  • Li H (2011) A quick method to calculate QTL confidence interval. J Genet 90:355–360. doi:10.1007/s12041-011-0077-7

    Article  PubMed  Google Scholar 

  • Lichtenzveig J, Bonfil DJ, Zhang HB, Shtienberg D, Abbo S (2006) Mapping quantitative trait loci in chickpea associated with time to flowering and resistance to Didymella rabiei the causal agent of Ascochyta blight. Theor Appl Genet 113:1357–1369. doi:10.1007/s00122-006-0390-3

    Article  PubMed  Google Scholar 

  • Luthra JC, Sittar A, B KS (1935) Life-history of gram blight [Ascochyta rabiei (Pass.) Lab. = Phyllosticta rabiei (Pass.) Trot.] on gram (Cicer arietinum L.) and its control in the Punjab. Agriculture and Livestock in India 5:489–498

    Google Scholar 

  • Madrid E, Rajesh PN, Rubio J, Gil J, Millán T, Chen W (2012) Characterization and genetic analysis of an EIN4-like sequence (CaETR-1) located in QTLAR1 implicated in ascochyta blight resistance in chickpea. Plant Cell Rep 31:1033–1042. doi:10.1007/s00299-011-1221-9

    Article  CAS  PubMed  Google Scholar 

  • Madrid E, Chen W, Rajesh PN, Castro P, Millán T, Gil J (2013) Allele-specific amplification for the detection of ascochyta blight resistance in chickpea. Euphytica 189:183–190. doi:10.1007/s10681-012-0753-6

    Article  CAS  Google Scholar 

  • Millan T, Rubio J, Iruela M, Daly K, Cubero JI, Gil J (2003) Markers associated with Ascochyta blight resistance in chickpea and their potential in marker-assisted selection. Field Crops Res 84:373–384. doi:10.1016/S0378-4290(03)00103-5

    Article  Google Scholar 

  • Millan T, Clarke HJ, Siddique KHM, Buhariwalla HK, Gaur PM, Kumar J et al (2006) Chickpea molecular breeding: New tools and concepts. Euphytica 147:81–103. doi:10.1007/s10681-006-4261-4

    Article  Google Scholar 

  • Millan T, Winter P, Jüngling R, Gil J, Rubio J, Cho S et al (2010) A consensus genetic map of chickpea (Cicer arietinum L.) based on 10 mapping populations. Euphytica 175:175–189. doi:10.1007/s10681-010-0157-4

    Article  CAS  Google Scholar 

  • Nayak S, Zhu H, Varghese N, Datta S, Choi H-K, Horres R et al (2010) Integration of novel SSR and gene-based SNP marker loci in the chickpea genetic map and establishment of new anchor points with Medicago truncatula genome. Theor Appl Genet 120:1415–1441. doi:10.1007/s00122-010-1265-1

    Google Scholar 

  • Nene YL (1982) A review of Ascochyta blight of chickpea. Trop Pest Manag 28:61–70. doi:10.1080/09670878209370675

    Article  Google Scholar 

  • Poczai P, Varga I, Laos M, Cseh A, Bell N, Valkonen J et al (2013) Advances in plant gene-targeted and functional markers: a review. Plant Methods 9:6. doi:10.1186/1746-4811-9-6

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rakshit S, Winter P, Tekeoglu M, Juarez Muñoz J, Pfaff T, Benko-Iseppon AM et al (2003) DAF marker tightly linked to a major locus for Ascochyta blight resistance in chickpea (Cicer arietinum L.). Euphytica 132:23–30. doi:10.1023/A:1024681422799

    Article  CAS  Google Scholar 

  • Rowland O, Ludwig AA, Merrick CJ, Baillieul F, Tracy FE, Durrant WE et al (2005) Functional Analysis of Avr9/Cf-9 Rapidly Elicited Genes Identifies a Protein Kinase, ACIK1, That Is Essential for Full Cf-9–Dependent Disease Resistance in Tomato. Plant Cell 17:295–310. doi:10.1105/tpc.104.026013

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rozen S, Skaletsky H (1999) Primer3 on the WWW for general users and for biologist programmers. In: Misener S, Krawetz S (eds) Bioinformatics methods and protocols, vol 132. Methods in molecular biology™. Humana Press, pp 365–386. doi:10.1385/1-59259-192-2:365

  • Santra DK, Tekeoglu M, Ratnaparkhe M, Kaiser WJ, Muehlbauer FJ (2000) Identification and mapping of QTLs conferring resistance to Ascochyta blight in chickpea. Crop Sci 40:1606–1612. doi:10.2135/cropsci2000.4061606x

    Article  CAS  Google Scholar 

  • Shakeel SN, Wang X, Binder BM, Schaller GE (2013) Mechanisms of signal transduction by ethylene: overlapping and non-overlapping signalling roles in a receptor family. AoB Plants 5. doi:10.1093/aobpla/plt010

  • Stein LD, Mungall C, Shu S, Caudy M, Mangone M, Day A et al (2002) The Generic Genome Browser: A Building Block for a Model Organism System Database. Genome Res 12:1599–1610. doi:10.1101/gr.403602

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tar’an B, Warkentin TD, Tullu A, Vandenberg A (2007) Genetic mapping of ascochyta blight resistance in chickpea (Cicer arietinum L.) using a simple sequence repeat linkage map. Genome 50:26–34. doi:10.1139/g06-137

    Article  PubMed  Google Scholar 

  • Tekeoglu M, Rajesh PN, Muehlbauer FJ (2002) Integration of sequence tagged microsatellite sites to the chickpea genetic map. Theor Appl Genet 105:847–854. doi:10.1007/s00122-002-0993-2

    Article  CAS  PubMed  Google Scholar 

  • Thudi M, Bohra A, Nayak SN, Varghese N, Shah TM, Penmetsa RV et al (2011) Novel SSR Markers from BAC-End Sequences, DArT Arrays and a Comprehensive Genetic Map with 1,291 Marker Loci for Chickpea (Cicer arietinum L.). PLoS ONE 6:e27275. doi:10.1371/journal.pone.0027275

  • Udupa SM, Baum M (2003) Genetic dissection of pathotype-specific resistance to ascochyta blight disease in chickpea (Cicer arietinum L.) using microsatellite markers. Theor Appl Genet 106:1196–1202. doi:10.1007/s00122-002-1168-x

    CAS  PubMed  Google Scholar 

  • Udupa SM, Sharma A, Sharma RP, Pai RA (1993) Narrow genetic variability in Cicer arietinum L. as revealed by RFLP analysis. J Plant Biochem Biotechnol 2:83–86. doi:10.1007/BF03262930

    Article  CAS  Google Scholar 

  • Van Ooijen G (2004) MapQTL ® 5, Software for the mapping of quantitative trait loci in experimental populations. Kyazma BV, Wageningen

  • Varshney RK, Mohan SM, Gaur PM, Gangarao NVPR, Pandey MK, Bohra A et al (2013a) Achievements and prospects of genomics-assisted breeding in three legume crops of the semi-arid tropics. Biotechnol Adv 31:1120–1134. doi:10.1016/j.biotechadv.2013.01.001

    Article  PubMed  Google Scholar 

  • Varshney RK, Song C, Saxena RK, Azam S, Yu S, Sharpe AG et al (2013b) Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nat Biotech 31:240–246. doi:10.1038/nbt.2491

    Article  CAS  Google Scholar 

  • Winter P, Pfaff T, Udupa SM, Huttel B, Sharma PC, Sahi S et al (1999) Characterization and mapping of sequence-tagged microsatellite sites in the chickpea (Cicer arietinum L.) genome. Mol Gen Genet 262:90–101. doi:10.1007/s004380051063

    Article  CAS  PubMed  Google Scholar 

  • Winter P, Benko-Iseppon AM, Hüttel B, Ratnaparkhe M, Tullu A, Sonnante G et al (2000) A linkage map of the chickpea (Cicer arietinum L.) genome based on recombinant inbred lines from a C. arietinum x C. reticulatum cross: Localization of resistance genes for fusarium wilt races 4 and 5. Theor Appl Genet 101:1155–1163. doi:10.1007/s001220051592

    Article  CAS  Google Scholar 

  • Zilberman D, Cao X, Jacobsen SE (2003) ARGONAUTE4 Control of Locus-Specific siRNA Accumulation and DNA and Histone Methylation. Science 299:716–719. doi:10.1126/science.1079695

    Article  CAS  PubMed  Google Scholar 

  • Zilberman D, Cao X, Johansen LK, Xie Z, Carrington JC, Jacobsen SE (2004) Role of Arabidopsis ARGONAUTE4 in RNA-directed DNA methylation triggered by inverted repeats. Curr Biol 14:1214–1220

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by the Spanish Ministry of Science and Innovation (MICINN; project RTA2010-00059), co-financed with European Regional Development Fund (FEDER). The authors also thankfully acknowledge to FJ Esteban from the Informatics Service at Córdoba University and the computer resources and the technical support provided by the Plataforma Andaluza de Bioinformática of the University of Málaga particularly to Rocío Bautista for her support. E. Madrid was financed by ‘Juan de la Cierva’ grant.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. Madrid.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 10 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Madrid, E., Seoane, P., Claros, M.G. et al. Genetic and physical mapping of the QTLAR3 controlling blight resistance in chickpea (Cicer arietinum L). Euphytica 198, 69–78 (2014). https://doi.org/10.1007/s10681-014-1084-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10681-014-1084-6

Keywords

Navigation