Abstract
Three recombinant inbred populations (RIP-1, RIP-7 and RIP-10) were used to validate and saturate the target area involved in the resistance to Fusarium oxysporum f.sp. ciceris race 0 (Foc0) in chickpeas. With the aim of physically localizing the genetic area controlling Foc0 resistance, a new genetic map of the linkage group 5 (LG5) and a physical map of the Ca5 pseudomolecule were drawn up and compared. The genetic and physical between CaGM20820 and CaGM20889 (16759541–17501349 bp) within an interval of 2 cM comprising 27 annotated genes. Only two of the annotated genes in this region could mapping results obtained were useful to refine the position of the target area be involved in resistance mechanisms. The three RIPs were used to develop three pairs of near isogenic lines (NILs) for resistance/susceptibility to Foc0. NILs are a valuable tool for fine mapping, refining the target region and selecting candidate genes for resistance to Foc0. The information reported in this paper will help develop diagnostic markers, considered useful tools for MAS in chickpea breeding programs.
Similar content being viewed by others
References
Ahmad F, Slinkard AE (1992) Genetic relationships in the genus Cicer L. as revealed by polyacrylamide gel electrophoresis of seed storage proteins. Theor Appl Genet 84:688–692
Ali L, Madrid E, Varshney RK, Azam S, Millan T, Rubio J, Gil J (2014) Mapping and identification of a Cicer arietinum NSP2 gene involved in nodulation pathway. Theor Appl Genet 127(2):481–488. doi:10.1007/s00122-013-2233-3
Ali L, Azam S, Rubio J, Kudapa H, Madrid E, Varshney RK, Castro P, Chen W, Gil J, Millan T (2015a) Detection of a new QTL/gene for growth habit in chickpea CaLG1 using wide and narrow crosses. Euphytica 204:1–13. doi:10.1007/s10681-015-1369-4
Ali L, Deokar A, Caballo C, Tar’an B, Gil J, Chen W, Millan T, Rubio J (2015b) Fine mapping for double podding gene in chickpea. Theor Appl Genet. doi:10.1007/s00122-015-2610-1
Ali-Benali MA, Badawi M, Houde Y, Houde M (2013) Identification of oxidative stress-responsive C2H2 zinc fingers associated with Al tolerance in near-isogenic wheat lines. Plant Soil 366(1–2):199–212. doi:10.1007/s11104-012-1417-y
Al-Taae AK, Hadwan HA, Al-Jobory SAE (2013) Physiological Races of Fusarium oxysporum f. sp. Ciceris in Iraq. J Life Sci 7(10):1070–1075
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(1):202–211
Brouwer DJ, St Clair DA (2004) Fine mapping of three quantitative trait loci for late blight resistance in tomato using near isogenic lines (NILs) and sub-NILs. Theor Appl Genet 108(4):628–638. doi:10.1007/s00122-003-1469-8
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(8):1519–1526. doi:10.1007/s00122-010-1407-5
Castro P, Rubio J, Madrid E, FernÁNdez-Romero MD, MillÁN T, Gil J (2013) Efficiency of marker-assisted selection for ascochyta blight in chickpea. J Agr Sci 153(01):56–67. doi:10.1017/s0021859613000865
Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138(3):963–971
Cobos MJ, Fernandez MJ, Rubio J, Kharrat M, Moreno MT, Gil J, Millan T (2005) A linkage map of chickpea (Cicer arietinum L.) based on populations from Kabuli x Desi crosses: location of genes for resistance to fusarium wilt race 0. Theor Appl Genet 110(7):1347–1353. doi:10.1007/s00122-005-1980-1
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 Crops Res 111(1–2):130–136
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(1491):557–572. doi:10.1098/rstb.2007.2170
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(1–2):169–196. doi:10.1007/s10681-005-1681-5
Craig A, Ewan R, Mesmar J, Gudipati V, Sadanandom A (2009) E3 ubiquitin ligases and plant innate immunity. J Exp Bot 60(4):1123–1132. doi:10.1093/jxb/erp059
Doddamani D, Katta M, Khan A, Agarwal G, Shah T, Varshney R (2014) CicArMiSatDB: the chickpea microsatellite database. BMC Bioinform 15(1):212
Dreher K, Callis J (2007) Ubiquitin, hormones and biotic stress in plants. Ann Bot 99(5):787–822. doi:10.1093/aob/mcl255
FAOSTAT (2016) http://faostat3.fao.org
Gaur PM, Jukanti AK, Varshney RK (2012) Impact of genomic technologies on chickpea breeding strategies. Agronomy 2(3):199–221
Gowda SJM, Radhika P, Kadoo NY, Mhase LB, Gupta VS (2009) Molecular mapping of wilt resistance genes in chickpea. Mol Breed 24(2):177–183
Graham GI, Wolff DW, Stuber CW (1997) Characterization of a yield quantitative trait locus on chromosome five of maize by fine mapping. Crop Sci 37(5):1601–1610. doi:10.2135/cropsci1997.0011183X003700050033x
Gujaria N, Kumar A, Dauthal P, Dubey A, Hiremath P, Bhanu Prakash A, Farmer A, Bhide M, Shah T, Gaur P, Upadhyaya H, Bhatia S, Cook D, May G, Varshney R (2011) Development and use of genic molecular markers (GMMs) for construction of a transcript map of chickpea (Cicer arietinum L.). Theor Appl Genet 122(8):1577–1589. doi:10.1007/s00122-011-1556-1
Gullì M, Salvatori E, Fusaro L, Pellacani C, Manes F, Marmiroli N (2015) Comparison of drought stress response and gene expression between a GMmaize variety and a near-isogenic non-GM variety. PLoS ONE 10(2):e0117073. doi:10.1371/journal.pone.0117073
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 35:67–74
Halila MH, Strange RN (1997) Screening of Kabuli chickpea germplasm for resistance to Fusarium wilt. Euphytica 96(2):273–279
Halila I, Cobos MJ, Rubio J, Millán T, Kharrat M, Marrakchi M, Gil J (2009) Tagging and mapping a second resistance gene for Fusarium wilt race 0 in chickpea. Eur J Plant Pathol 124(1):87–92. doi:10.1007/s10658-008-9395-x
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(5):563–566
Hiremath PJ, Kumar A, Penmetsa RV, Farmer A, Schlueter JA, Chamarthi SK, Whaley AM, Carrasquilla-Garcia N, Gaur PM, Upadhyaya HD, Kavi Kishor PB, Shah TM, Cook DR, Varshney RK (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(6):716–732. doi:10.1111/j.1467-7652.2012.00710.x
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(5):715–729. doi:10.1111/tpj.12173
Jiménez-Díaz RM, Castillo P, Jiménez-Gasco MdM, Landa BB, Navas-Cortés JA (2015) Fusarium wilt of chickpeas: biology, ecology and management. Crop Prot 73:16–27. doi:10.1016/j.cropro.2015.02.023
Jiménez-Fernández D, Montes-Borrego M, Navas-Cortés JA, Jiménez-Díaz RM, Landa BB (2010) Identification and quantification of Fusarium oxysporum in planta and soil by means of an improved specific and quantitative PCR assay. Appl Soil Ecol 46(3):372–382
Jiménez-Gasco MM, Jiménez-Díaz RM (2003) Development of a specific polymerase chain reaction-based assay for the identification of Fusarium oxysporum f. sp. ciceris and its pathogenic races 0, 1A, 5, and 6. Am Phytopathol Soc 93(2):200–209
Jiménez-Gasco M, Pérez-Artés E, Jiménez-Diaz RM (2001) Identification of pathogenic races 0, 1B/C, 5, and 6 of Fusarium oxysporum f. sp. ciceris with random amplified polymorphic DNA (RAPD). Eur J Plant Pathol 107(2):237–248
Johnson HW, Bernard RL (1962) Soybean genetic and breeding. Advances in agronomy, vol 14. Academic Press, London
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
Kazan K, Muehlbauer FJ (1991) Allozyme variation and phylogeny in annual species of Cicer (Leguminosae). Plant Sys Evol 175:11–21
Keurentjes JJ, Bentsink L, Alonso-Blanco C, Hanhart CJ, Blankestijn-De Vries H, Effgen S, Vreugdenhil D, Koornneef M (2007) Development of a near-isogenic line population of Arabidopsis thaliana and comparison of mapping power with a recombinant inbred line population. Genetics 175(2):891–905. doi:10.1534/genetics.106.066423
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
Kumar Y, Dholakia BB, Panigrahi P, Kadoo NY, Giri AP, Gupta VS (2015) Metabolic profiling of chickpea-Fusarium interaction identifies differential modulation of disease resistance pathways. Phytochemistry 116:120–129. doi:10.1016/j.phytochem.2015.04.001
Labdi M, Robertson LD, Singh KB, Charrier A (1996) Genetic diversity and phylogenetic relationships among the annual Cicer species as revealed by isozyme polymorphisms. Euphytica 88:181–188
Landa BB, Navas-Cortés JA, Jiménez-Gasco MM, Katan J, Retig B, Jiménez-Díaz RM (2006) Temperature response of chickpea cultivars to races of Fusarium oxysporum f.sp. ciceris, causal agent of Fusarium wilt. Plant Dis 90:365–374. doi:10.1094/PD-90-0365
Li H (2011) A quick method to calculate QTL confidence interval. J Genet 90(2):355–360. doi:10.1007/s12041-011-0077-7
Lichtenzveig J, Scheuring C, Dodge J, Abbo S, Zhang HB (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(3):492–510. doi:10.1007/s00122-004-1857-8
Madrid E, Barilli E, Gil J, Huguet T, Gentzbittel L, Rubiales D (2014a) Detection of partial resistance quantitative trait loci against Didymella pinodes in Medicago truncatula. Mol Breed 33(3):589–599. doi:10.1007/s11032-013-9976-z
Madrid E, Seoane P, Claros MG, Barro F, Rubio J, Gil J, Millán T (2014b) Genetic and physical mapping of the QTLAR3 controlling blight resistance in chickpea (Cicer arietinum L). Euphytica 198(1):69–78. doi:10.1007/s10681-014-1084-6
Martin GB, Bogdanove AJ, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 54:23–61. doi:10.1146/annurev.arplant.54.031902.135035
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(5):1625–1629
Moumeni A, Satoh K, Kondoh H, Asano T, Hosaka A, Venuprasad R, Serraj R, Kumar A, Leung H, Kikuchi S (2011) Comparative analysis of root transcriptome profiles of two pairs of drought-tolerant and susceptible rice near-isogenic lines under different drought stress. BMC Plant Biol 11:174. doi:10.1186/1471-2229-11-174
Muehlbauer GJ, Staswiek PE, Speeht JE, Graef GL, Shoemaker RC, Keim P (1991) RFLP mapping using near-isogenic lines in the soybean [Glycine max (L.) Merr.]. Theor Appl Genet 81:189–198
Nayak S, Zhu H, Varghese N, Datta S, Choi H-K, Horres R, Jüngling R, Singh J, Kavi Kishor PB, Sivaramakrishnan S, Hoisington D, Kahl G, Winter P, Cook D, Varshney R (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(7):1415–1441. doi:10.1007/s00122-010-1265-1
Patil BS, Ravikumar RL, Bhat JS, Soregaon CD (2014) Molecular mapping of QTLs for resistance to early and late Fusarium wilt in chickpea. Czech J Genet Plant Breed 50(2):171–176
Poczai P, Varga I, Laos M, Cseh A, Bell N, Valkonen J, Hyvonen J (2013) Advances in plant gene-targeted and functional markers: a review. Plant Meth 9(1):6. doi:10.1186/1746-4811-9-6
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
Rubio J, Moreno MT, Cubero JI, Gil J (1998) Effect of the gene for double pod in chickpea on yield, yield components and stability of yield. Plant Breed Seed Sci 117:585–587
Rubio J, Hajj-Moussa E, Kharrat M, Moreno MT, Millan T, Gil J (2003) Two genes and linked RAPD markers involved in resistance to Fusarium oxysporum f. sp. ciceris race 0 in chickpea. Plant Breed 122(2):188–191
Sharma KD, Muehlbauer FJ (2007) Fusarium wilt of chickpea: physiological specialization, genetics of resistance and resistance gene tagging. Euphytica 157(1–2):1–14
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(4):385–390. doi:10.1094/PD-89-0385
Thudi M, Bohra A, Nayak SN, Varghese N, Shah TM, Penmetsa RV, Thirunavukkarasu N, Gudipati S, Gaur PM, Kulwal PL, Upadhyaya HD, KaviKishor PB, Winter P, Kahl G, Town CD, Kilian A, Cook DR, Varshney RK (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(11):e27275. doi:10.1371/journal.pone.0027275
Trapero-Casas A, Jiménez-Díaz RM (1985) Fungal wilt and root rot diseases of chickpea in southern Spain. Phytopathology 75:1146–1151
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(2):83–86. doi:10.1007/BF03262930
Van Ooijen G (2004) MapQTL ® 5, software for the mapping of quantitative trait loci in experimental populations. Kyazma BV (ed), Wageningen
Varshney RK, Song C, Saxena RK, Azam S, Yu S, Sharpe AG, Cannon S, Baek J, Rosen BD, Tar’an B, Millan T, Zhang X, Ramsay LD, Iwata A, Wang Y, Nelson W, Farmer AD, Gaur PM, Soderlund C, Penmetsa RV, Xu C, Bharti AK, He W, Winter P, Zhao S, Hane JK, Carrasquilla-Garcia N, Condie JA, Upadhyaya HD, Luo M-C, Thudi M, Gowda CLL, Singh NP, Lichtenzveig J, Gali KK, Rubio J, Nadarajan N, Dolezel J, Bansal KC, Xu X, Edwards D, Zhang G, 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 Biotech 31(3):240–246. doi:10.1038/nbt.2491
Winter P, Pfaff T, Udupa SM, Huttel B, Sharma PC, Sahi S, Arreguin-Espinoza R, Weigand F, Muehlbauer FJ, Kahl G (1999) Characterization and mapping of sequence-tagged microsatellite sites in the chickpea (Cicer arietinum L.) genome. Mol Gen Genet 262(1):90–101. doi:10.1007/s004380051063
Xue S, Xu F, Li G, Zhou Y, Lin M, Gao Z, Su X, Xu X, Jiang G, Zhang S, Jia H, Kong Z, Zhang L, Ma Z (2013) Fine mapping TaFLW1, a major QTL controlling flag leaf width in bread wheat (Triticum aestivum L.). Theor Appl Genet 126(8):1941–1949. doi:10.1007/s00122-013-2108-7
Zhu Y, Cao Z, Xu F, Huang Y, Chen M, Guo W, Zhou W, Zhu J, Meng J, Zou J, Jiang L (2012) Analysis of gene expression profiles of two near-isogenic lines differing at a QTL region affecting oil content at high temperatures during seed maturation in oilseed rape (Brassica napus L.). Theor Appl Genet 124(3):515–531. doi:10.1007/s00122-011-1725-2
Acknowledgments
We wish to thank all of the technical staff who contributed to this work from the laboratory of genetics of the University of Cordoba and from the Tunisian Chickpea Program. W. Jendoubi was supported by a fellowship from the MESRT (Ministère de l’Enseignement Supérieur et de la Recherche Scientifique-Tunisie) and the Tunisian Project on Chickpeas (Efficacité de la sélection assistée par marqueurs dans la détection de génotypes de pois chiche résistants aux principales maladies fongiques en Tunisie) funded by IRESA (Institution de la Recherche et de l’Enseignement Supérieur Agricole- Ministère de l’Agriculture).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Jendoubi, W., Bouhadida, M., Millan, T. et al. Identification of the target region including the Foc0 1 /foc0 1 gene and development of near isogenic lines for resistance to Fusarium Wilt race 0 in chickpea. Euphytica 210, 119–133 (2016). https://doi.org/10.1007/s10681-016-1712-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10681-016-1712-4