Major QTL on LG 1 and 3 control seed filling and seed coat development, thereby affecting seed shape, size, color, composition and weight, key determinants of crop yield and quality.
A chickpea (Cicer arietinum L.) population consisting of 189 recombinant inbred lines (RILs) derived from a cross between medium-protein ICC 995 and high-protein ICC 5912 genotypes of the desi market class was analyzed for seed properties. Seed from the parental lines and RILs was produced in four different environments for determination of seed shape (SS), 100-seed weight (100-SW), protein (PRO) and starch (STA) concentration. Polymorphic genetic markers for the population were identified by Genotyping by Sequencing and assembled into a 522.5 cM genetic map. Phenotype data from the different growth environments were analyzed by QTL mapping done by single and multi-environment analyses and in addition, single marker association mapping. The analyses identified in total 11 QTL, of which the most significant (P < 0.05) loci were located on LG 1 (q-1.1), LG 2 (q-2.1), LG 3 (q-3.2, q-3.3), LG 4 (q-4.2), and LG 5 (q-5.1). STA was mostly affected by q-1.1, which explained 19.0% of the phenotypic variance for the trait. The largest QTL effects were demonstrated by q-3.2 that explained 52.5% of the phenotypic variances for 100-SW, 44.3% for PRO, and 14.6% for SS. This locus was also highly associated with flower color (COL; 95.2% explained) and showed q-3.2 alleles from the ICC 5912 parent conferred the blue flower color and production of small, round seeds with relatively high protein concentration. Genes affecting seed filling at q-1.1 and seed coat development at q-3.2, respectively, were considered to underlie differences in seed composition and morphology in the RIL population.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Abbo S, Molina C, Jungmann R, Grusak MA, Berkovitch Z, Reifen R, Kahl G, Winter P, Reifen R (2005) Quantitative trait loci governing carotenoid concentration and weight in seeds of chickpea (Cicer arietinum L.). Theor Appl Genet 111:185–195. https://doi.org/10.1007/s00122-005-1930-y
Ainsworth EA, Bush DR (2011) Carbohydrate export from the leaf: a highly regulated process and target to enhance photosynthesis and productivity. Plant Physiol 155:64–69. https://doi.org/10.1104/pp.110.167684
Alonso-Blanco C, Blankestijn-de Vries H, Hanhart CJ, Koornneef M (1999) Natural allelic variation at seed size loci in relation to other life history traits of Arabidopsis thaliana. Proc Natl Acad Sci 96:4710–4717. https://doi.org/10.1073/pnas.96.8.4710
Bajaj D, Das S, Upadhyaya HD, Ranjan R, Badoni S, Kumar V, Tripathi S, Gowda CLL, Sharma S, Singh S, Tyagi AK, Parida SK (2015) A genome-wide combinatorial strategy dissects complex genetic architecture of seed coat color in chickpea. Front Plant Sci 6:979. https://doi.org/10.3389/fpls.2015.00979
Baxter IR, Young JC, Armstrong G, Foster N, Bogenschutz N, Cordova T, Peer WA, Hazen SP, Murphy AS, Harper JF (2005) A plasma membrane H + -ATPase is required for the formation of proanthocyanidins in the seed coat endothelium of Arabidopsis thaliana. Proc Natl Acad Sci 102:2649–2654. https://doi.org/10.1073/pnas.0406377102
Berger F, Chaudhury A (2009) Parental memories shape seeds. Trends Plant Sci 14:550–556. https://doi.org/10.1016/j.tplants.2009.08.003
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Borisjuk L, Rolletschek H, Walenta S, Panitz R, Wobus U, Weber H (2003) Energy status and its control on embryogenesis of legumes: ATP distribution within Vicia faba embryos is developmentally regulated and correlated with photosynthetic capacity. Plant J 36:318–329. https://doi.org/10.1046/j.1365-313X.2003.01879.x
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 111:130–136. https://doi.org/10.1016/j.fcr.2008.11.006
Cowan RK, Hoen DR, Schoen DJ, Bureau TE (2005) MUSTANG is a novel family of domesticated transposase genes found in diverse angiosperms. Mol Biol Evol 22:2084–2089. https://doi.org/10.1093/molbev/msi202
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158. https://doi.org/10.1093/bioinformatics/btr330
Das S, Upadhyaya HD, Bajaj D, Kujur A, Badoni S, Laxmi Kumar V, Tripathi S, Gowda CLL, Sharma S, Singh S, Tyagi AK, Parida SK (2015) Deploying QTL-seq for rapid delineation of a potential candidate gene underlying major trait-associated QTL in chickpea. DNA Res 22:193–203. https://doi.org/10.1093/dnares/dsv004
Doddamani D, Katta MAVSK, Khan AW, Agarwal G, Shah TM, Varshney RK (2014) CicArMiSatDB: the chickpea microsatellite database. BMC Bioinform 15:212. https://doi.org/10.1186/1471-2105-15-212
Doughty J, Aljabri M, Scott RJ (2014) Flavonoids and the regulation of seed size in Arabidopsis. Biochem Soc Trans 42:364–369. https://doi.org/10.1042/BST20140040
Edwards D (2016) Improved desi reference genome. CyVerse Data Commons. https://doi.org/10.7946/P2KW2Q
Faraco M, Spelt C, Bliek M, Verweij W, Hoshino A, Espen L, Prinsi B, Jaarsma R, Tarhan E, DeBoer AH, Di Sansebastiano G-P, Koes R, Quattrocchio FM (2014) Hyperacidification of vacuoles by the combined action of two different P-ATPases in the tonoplast determines flower color. Cell Rep 6:32–43. https://doi.org/10.1016/j.celrep.2013.12.009
Figueiredo DD, Batista RA, Roszak PJ, Hennig L, Köhler C (2016) Auxin production in the endosperm drives seed coat development in Arabidopsis. Elife 5:e20542. https://doi.org/10.7554/eLife.20542
Folsom JJ, Begcy K, Hao X, Wang D, Walia H (2014) Rice fertilization-independent endosperm1 regulates seed size under heat stress by controlling early endosperm development. Plant Physiol 165:238–248. https://doi.org/10.1104/pp.113.232413
Garcia D, Fitz Gerald JN, Berger F (2005) Maternal control of integument cell elongation and zygotic control of endosperm growth are coordinated to determine seed size in Arabidopsis. Plant Cell 17:52–60. https://doi.org/10.1105/tpc.104.027136
Gaur PM, Singh MK, Samineni S, Sajja SB, Jukanti AK, Kamatam S, Varshney RK (2016) Inheritance of protein content and its relationships with seed size, grain yield and other traits in chickpea. Euphytica 209:253–260. https://doi.org/10.1007/s10681-016-1678-2
Glaubitz JC, Casstevens TM, Lu F, Harriman J, Elshire RJ, Sun Q, Buckler ES (2014) TASSEL-GBS: a high capacity genotyping by sequencing analysis pipeline. PLoS ONE 9:e90346. https://doi.org/10.1371/journal.pone.0090346
Hehenberger E, Kradolfer D, Köhler C (2012) Endosperm cellularization defines an important developmental transition for embryo development. Development 139:2031–2039. https://doi.org/10.1242/dev.077057
Hossain S, Ford R, McNeil D, Pittock C, Panozzo JF (2010) Inheritance of seed size in chickpea (Cicer arietinum L.) and identification of QTL based on 100-seed weight and seed size index. Aust J Crop Sci 4:126–135
Hurkman WJ, Wood DF (2011) High temperature during grain fill alters the morphology of protein and starch deposits in the starchy endosperm cells of developing wheat (Triticum aestivum L.) grain. J Agric Food Chem 59:4938–4946. https://doi.org/10.1021/jf102962t
Ingouff M, Jullien PE, Berger F (2006) The female gametophyte and the endosperm control cell proliferation and differentiation of the seed coat in Arabidopsis. Plant Cell 18:3491–3501. https://doi.org/10.1105/tpc.106.047266
Jadhav AA, Rayate SJ, Mhase LB, Thudi M, Chitikineni A, Harer PN, Jadhav AS, Varshney RK, Kulwal PL (2015) Marker-trait association study for protein content in chickpea (Cicer arietinum L.). J Genet 94:279–286
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 74:715–729. https://doi.org/10.1111/tpj.12173
Joly-Lopez Z, Forczek E, Hoen DR, Juretic N, Bureau TE (2012) A gene family derived from transposable elements during early angiosperm evolution has reproductive fitness benefits in Arabidopsis thaliana. PLoS Genet. https://doi.org/10.1371/journal.pgen.1002931
Kaushal N, Awasthi R, Gupta K, Gaur P, Siddique KHM, Nayyar H (2013) Heat-stress-induced reproductive failures in chickpea (Cicer arietinum) are associated with impaired sucrose metabolism in leaves and anthers. Funct Plant Biol 40:1334–1349. https://doi.org/10.1071/FP13082
Knights EJ, Wood JA, Harden S (2011) A gene influencing seed shape of desi type chickpea (Cicer arietinum L.). Plant Breed 130:278–280. https://doi.org/10.1111/j.1439-0523.2010.01810.x
Kujur A, Upadhyaya HD, Shree T, Bajaj D, Das S, Saxena MS, Badoni S, Kumar V, Tripathi S, Gowda CLL, Sharma S, Singh S, Tyagi AK, Parida SK (2015) Ultra-high density intra-specific genetic linkage maps accelerate identification of functionally relevant molecular tags governing important agronomic traits in chickpea. Sci Rep 5:9468. https://doi.org/10.1038/srep09468
Lafon-Placette C, Köhler C (2014) Embryo and endosperm, partners in seed development. Curr Opin Plant Biol 17:64–69. https://doi.org/10.1016/j.pbi.2013.11.008
Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25. https://doi.org/10.1186/gb-2009-10-3-r25
Lefèvre F, Boutry M (2018) Towards identification of the substrates of ATP-binding cassette transporters. Plant Physiol 178:00325. https://doi.org/10.1104/pp.18.00325
Lepiniec L, Debeaujon I, Routaboul J-M, Baudry A, Pourcel L, Nesi N, Caboche M (2006) Genetics and biochemistry of seed flavonoids. Annu Rev Plant Biol 57:405–430. https://doi.org/10.1146/annurev.arplant.57.032905.105252
Li N, Li Y (2016) Signaling pathways of seed size control in plants. Curr Opin Plant Biol 33:23–32. https://doi.org/10.1016/j.pbi.2016.05.008
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 25:2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Li Y, Ruperao P, Batley J, Edwards D, Khan T, Colmer TD, Pang J, Siddique KHM, Sutton T (2018) Investigating drought tolerance in chickpea using genome-wide association mapping and genomic selection based on whole-genome resequencing data. Front Plant Sci 9:1–12. https://doi.org/10.3389/fpls.2018.00190
Magrane M, Consortium UP (2011) UniProt Knowledgebase: a hub of integrated protein data. Database 2011, bar009. https://doi.org/10.1093/database/bar009
Mascher M, Wu S, St. Amand P, Stein N, Poland J (2013) Application of genotyping-by-sequencing on semiconductor sequencing platforms: a comparison of genetic and reference-based marker ordering in barley. PLoS ONE 8:e76925. https://doi.org/10.1371/journal.pone.0076925
Mizukami Y (2001) A matter of size: developmental control of organ size in plants. Curr Opin Plant Biol 4:533–539. https://doi.org/10.1016/S1369-5266(00)00212-0
Morley-Smith ER, Pike MJ, Findlay K, Köckenberger W, Hill LM, Smith AM, Rawsthorne S (2008) The transport of sugars to developing embryos is not via the bulk endosperm in oilseed rape seeds. Plant Physiol 147:2121–2130. https://doi.org/10.1104/pp.108.124644
Parween S, Nawaz K, Roy R, Pole AK, Suresh BV, Misra G, Jain M, Yadav G, Parida SK, Tyagi AK, Bhatia S, Chattopadhyay D (2015) An advanced draft genome assembly of a desi type chickpea (Cicer arietinum L). Sci Rep 5:12806. https://doi.org/10.1038/srep12806
Ruan Y-L, Patrick JW, Bouzayen M, Osorio S, Fernie AR (2012) Molecular regulation of seed and fruit set. Trends Plant Sci 17:656–665. https://doi.org/10.1016/j.tplants.2012.06.005
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 21:695–710. https://doi.org/10.1093/dnares/dsu031
Sonah H, Bastien M, Iquira E, Tardivel A, Légaré G, Boyle B, Normandeau É, Laroche J, Larose S, Jean M, Belzile F (2013) An improved genotyping by sequencing (GBS) approach offering increased versatility and efficiency of SNP discovery and genotyping. PLoS ONE 8:e54603. https://doi.org/10.1371/journal.pone.0054603
Sun X, Shantharaj D, Kang X, Ni M (2010) Transcriptional and hormonal signaling control of Arabidopsis seed development. Curr Opin Plant Biol 13:611–620. https://doi.org/10.1016/j.pbi.2010.08.009
Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, Kuhn M, Bork P, Jensen LJ, von Mering C (2015) STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43:D447–D452. https://doi.org/10.1093/nar/gku1003
Tondelli A, Francia E, Barabaschi D, Aprile A, Skinner JS, Stockinger EJ, Stanca AM, Pecchioni N (2006) Mapping regulatory genes as candidates for cold and drought stress tolerance in barley. Theor Appl Genet 112:445–454. https://doi.org/10.1007/s00122-005-0144-7
Upadhyaya HD, Bajaj D, Das S, Kumar V, Gowda CLL, Sharma S, Tyagi AK, Parida SK (2016a) Genetic dissection of seed-iron and zinc concentrations in chickpea. Sci Rep 6:24050. https://doi.org/10.1038/srep24050
Upadhyaya HD, Bajaj D, Narnoliya L, Das S, Kumar V, Gowda CLL, Sharma S, Tyagi AK, Parida SK (2016b) Genome-wide scans for delineation of candidate genes regulating seed-protein content in chickpea. Front Plant Sci 7:302. https://doi.org/10.3389/fpls.2016.00302
van Ooijen JW, Voorips RE (2001) JoinMap 3.0, software for the calculation of genetic linkage maps
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 Biotechnol 31:240–246. https://doi.org/10.1038/nbt.2491
Verma M, Kumar V, Patel RK, Garg R, Jain M (2015a) CTDB: an integrated chickpea transcriptome database for functional and applied genomics. PLoS ONE 10:1371. https://doi.org/10.1371/journal.pone.0136880
Verma S, Gupta S, Bandhiwal N, Kumar T, Bharadwaj C, Bhatia S (2015b) High-density linkage map construction and mapping of seed trait QTLs in chickpea (Cicer arietinum L) using genotyping-by-sequencing (GBS). Sci Rep 5:17512. https://doi.org/10.1038/srep17512
Verweij W, Spelt C, Di Sansebastiano G-P, Vermeer J, Reale L, Ferranti F, Koes R, Quattrocchio F (2008) An H + P-ATPase on the tonoplast determines vacuolar pH and flower colour. Nat Cell Biol 10:1456–1462. https://doi.org/10.1038/ncb1805
Voorrips R (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Wang R, Gangola MP, Jaiswal S, Båga M, Gaur PM, Chibbar RN (2017) Variation in seed-quality traits of chickpea and their correlation to raffinose family oligosaccharides concentrations. Crop Sci 57:1594–1602. https://doi.org/10.2135/cropsci2016.08.0710
Weber H, Borisjuk L, Wobus U (2005) Molecular physiology of legume seed development. Annu Rev Plant Biol 56:253–279. https://doi.org/10.1146/annurev.arplant.56.032604.144201
Wood JA, Grusak MA (2007) Nutritional value of chickpea. In: Yadav SS, Redden R, Chen W, Sharma B (eds) Chickpea breeding and management. CAB International, Wallingford, pp 101–142
Wood JA, Knights EJ, Campbell GM, Choct M (2014) Differences between easy- and difficult-to-mill chickpea (Cicer arietinum L.) genotypes. Part I: broad chemical composition. J Sci Food Agric 94:1437–1445. https://doi.org/10.1002/jsfa.6437
Yang J, Hu C, Hu H, Yu R, Xia Z, Ye X, Zhu J (2008) QTLNetwork: mapping and visualizing genetic architecture of complex traits in experimental populations. Bioinformatics 24:721–723. https://doi.org/10.1093/bioinformatics/btm494
Yu S-M, Lo S-F, Ho T-HD (2015) Source-sink communication: regulated by hormone, nutrient, and stress cross-signaling. Trends Plant Sci 20:844–857. https://doi.org/10.1016/j.tplants.2015.10.009
This work was financially supported by Canada Research Chairs Program, Natural Sciences and Engineering Research Council, and Agriculture and Agri-Food Canada Internationalization program. The core research grant of International Crops Research Institute for Semi-Arid Tropics (ICRISAT, Patancheru, India) is acknowledged for the development of the chickpea RIL population and field trial at ICRISAT. RW is a grateful recipient of the China Scholarship Council fellowship for Ph.D. We are very grateful to Mr. John Bennet (Biggar Saskatchewan) and Mr. Jeff Sopatyk (Aberdeen, Saskatchewan) who provided land for the field trials.
Conflict of interest
The authors declare that they have no conflict of interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Communicated by Henry T. Nguyen.
Electronic supplementary material
Below is the link to the electronic supplementary material.
About this article
Cite this article
Wang, R., Gangola, M.P., Irvine, C. et al. Co-localization of genomic regions associated with seed morphology and composition in a desi chickpea (Cicer arietinum L.) population varying in seed protein concentration. Theor Appl Genet 132, 1263–1281 (2019). https://doi.org/10.1007/s00122-019-03277-5