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Analysis of genes encoding seed storage proteins (SSPs) in chickpea (Cicer arietinum L.) reveals co-expressing transcription factors and a seed-specific promoter

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Abstract

Improvement of the quality and quantity of chickpea seed protein can be greatly facilitated by an understanding of the genic organization and the genetic architecture of the genes encoding seed storage proteins (SSPs). The aim of this study was to provide a comprehensive analysis of the chickpea SSP genes, putative co-expressing transcription factors (TFs), and to identify a seed-specific SSP gene promoter. A genome-wide identification of SSP genes in chickpea led to the identification of 21 non-redundant SSP encoding genes located on 6 chromosomes. Phylogenetic analysis grouped SSP genes into 3 subgroups where members within the same clade demonstrated similar motif composition and intron-exon organization. Tandem duplications were identified to be the major contributors to the expansion of the SSP gene family in chickpea. Co-expression analysis revealed 14 TFs having expression profiles similar to the SSP genes that included members of important TF families that are known to regulate seed development. Expression analysis of SSP genes and TFs revealed significantly higher expression in late stages of seed development as well as in high seed protein content (HPC) genotypes. In silico analysis of the promoter regions of the SSP encoding genes revealed several seed-specific cis-regulatory elements such as RY repeats, ACGT motifs, CAANTG, and GCN4. A candidate promoter was analyzed for seed specificity by generating stable transgenics in Arabidopsis. Overall, this study provides a useful resource to explore the regulatory networks involved in SSP synthesis and/or accumulation for utilization in developing nutritionally improved chickpea genotypes.

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References

  • Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME suite. Nucleic Acids Res 43:W39–W49. https://doi.org/10.1093/nar/gkv416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baumlein H, Nagy I, Villarroel R, Inze D, Wobus U (1992) Cis-analysis of a seed protein gene promoter: the conservative RY repeat CATGCATG within the legumin box is essential for tissue-specific expression of a legumin gene. The Plant Journal 2:233–239

    CAS  PubMed  Google Scholar 

  • Boehm JD, Nguyen V, Tashiro RM, Anderson D, Shi C, Wu X, Woodrow L, Yu K, Cui Y, Li Z (2018) Genetic mapping and validation of the loci controlling 7S α′ and 11S A-type storage protein subunits in soybean [Glycine max (L.) Merr.]. Theor Appl Genet 131(3):659–671

    Article  CAS  PubMed  Google Scholar 

  • Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10–10. https://doi.org/10.1186/1471-2229-4-10

    Article  PubMed  PubMed Central  Google Scholar 

  • Chagas EP, Santoro LG (1997) Globulin and albumin proteins in dehulled seeds of three Phaseolus vulgaris cultivars. Plant Foods Hum Nutr 51:17–26. https://doi.org/10.1023/a:1007971329420

    Article  CAS  PubMed  Google Scholar 

  • Chavan JK, Kadam SS, Salunkhe DK (1989) Chickpea. In: Salunkhe DK, Kadam SS (eds) Handbook of world food legumes: nutritional chemistry, processing technology and utilization, vol I. CRC, Boca Raton, pp 247–288

    Google Scholar 

  • Doyle JJ, Schuler MA, Godette WD, Zenger V, Beachy RN, Slightom JL (1986) The glycosylated seed storage proteins of Glycine max and Phaseolus vulgaris. Structural homologies of genes and proteins. J Biol Chem 261(20):9228–9238

    CAS  PubMed  Google Scholar 

  • Dunwell JM, Purvis A, Khuri S (2004) Cupins: the most functionally diverse protein superfamily? Phytochemistry 65:7–17

    Article  CAS  PubMed  Google Scholar 

  • Ellerström M, Stålberg K, Ezcurra I, Rask L (1996) Functional dissection of a napin gene promoter: identification of promoter elements required for embryo and endosperm-specific transcription. Plant Mol Biol 32:1019–1027. https://doi.org/10.1007/bf00041385

    Article  PubMed  Google Scholar 

  • Ericson ML, Muren E, Gustavsson HO, Josefsson LG, Rask L (1991) Analysis of the promoter region of napin genes from Brassica napus demonstrates binding of nuclear protein in vitro to a conserved sequence motif. Eur J Biochem 197:741–746

    Article  CAS  PubMed  Google Scholar 

  • Fauteux F, Strömvik MV (2009) Seed storage protein gene promoters contain conserved DNA motifs in Brassicaceae, Fabaceae and Poaceae. BMC Plant Biol 9:126. https://doi.org/10.1186/1471-2229-9-126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fierens K, Brijs K, Courtin CM, Gebruers K, Goesaert H, Raedschelders G, Robben J, Van Campenhout S, Volckaert G, Delcour JA (2003) Molecular identification of wheat endoxylanase inhibitor TAXI-I1, member of a new class of plant proteins. FEBS Lett 540:259–263

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene <em>ABI5</em> encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609. https://doi.org/10.1105/tpc.12.4.599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujiwara T, Nambara E, Yamagishi K, Goto DB, Naito S (2002) Storage proteins. The Arabidopsis book 1:e0020. https://doi.org/10.1199/tab.0020

  • Garg R, Patel RK, Jhanwar S, Priya P, Bhattacharjee A, Yadav G, Bhatia S, Chattopadhyay D, Tyagi AK, Jain M (2011) Gene discovery and tissue-specific transcriptome analysis in chickpea with massively parallel pyrosequencing and web resource development. Plant Physiol 156:1661–1678. https://doi.org/10.1104/pp.111.178616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Higo H (1998) PLACE: A database of plant cis -acting regulatory DNA elements. Nucleic Acids Res 26:358–359. https://doi.org/10.1093/nar/26.1.358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hobo T, Kowyama Y, Hattori T (1999) A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc Natl Acad Sci 96:15348–15,353. https://doi.org/10.1073/pnas.96.26.15348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics (Oxford, England) 31:1296–1297. https://doi.org/10.1093/bioinformatics/btu817

    Article  Google Scholar 

  • Il'in MM, Semenova MG, Belyakova LE, Antipova AS, Polikarpov YN (2004) Thermodynamic and functional properties of legumin (11S globulin from Vicia faba) in the presence of small-molecule surfactants: effect of temperature and pH. J Colloid Interface Sci 278:71–80. https://doi.org/10.1016/j.jcis.2004.05.039

    Article  CAS  PubMed  Google Scholar 

  • Jadhav A, Rayate S, Mhase L, Thudi M, Chitikineni A, Harer P, Jadhav A, Varshney R, Kulwal P (2015) Marker-trait association study for protein content in chickpea (Cicer arietinum). J Genet 94:279–286

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Jeong HJ, Choi JY, Shin HY, Bae JM, Shin JS (2014) Seed-specific expression of seven Arabidopsis promoters. Gene 553:17–23. https://doi.org/10.1016/j.gene.2014.09.051

    Article  CAS  PubMed  Google Scholar 

  • Jiang H, Wu P, Zhang S, Song C, Chen Y, Li M, Jia Y, Fang X, Chen F, Wu G (2012) Global Analysis of gene expression profiles in developing physic nut (Jatropha curcas L.) seeds. PLoS One 7:e36522. https://doi.org/10.1371/journal.pone.0036522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jimenez-Lopez JC, Melser S, DeBoer K, Thatcher LF, Kamphuis LG, Foley RC, Singh KB (2016) Narrow-leafed lupin (Lupinus angustifolius) β1- and β6-conglutin proteins exhibit antifungal activity, protecting plants against necrotrophic pathogen induced damage from Sclerotinia sclerotiorum and Phytophthora nicotianae. Front Plant Sci 7:1856. https://doi.org/10.3389/fpls.2016.01856

    Article  PubMed  PubMed Central  Google Scholar 

  • Jin J, Tian F, Yang DC, Meng YQ, Kong L, Luo J, Gao G (2017) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res 45:D1040–d1045. https://doi.org/10.1093/nar/gkw982

    Article  CAS  PubMed  Google Scholar 

  • Jofuku KD, Omidyar PK, Gee Z, Okamuro JK (2005) Control of seed mass and seed yield by the floral homeotic gene APETALA2. Proc Natl Acad Sci U S A 102:3117–3122. https://doi.org/10.1073/pnas.0409893102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones SI, Vodkin LO (2013) Using RNA-Seq to profile soybean seed development from fertilization to maturity. PLoS One 8:e59270. https://doi.org/10.1371/journal.pone.0059270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawakatsu T, Yamamoto MP, Hirose S, Yano M, Takaiwa F (2008) Characterization of a new rice glutelin gene GluD-1 expressed in the starchy endosperm. J Exp Bot 59:4233–4245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krishnan HB (2005) Engineering soybean for enhanced sulfur amino acid content. Crop Sci 45:454–461. https://doi.org/10.2135/cropsci2005.0454

    Article  CAS  Google Scholar 

  • Krishnan HB, Coe EH Jr (2001) Seed storage proteins A2 - Brenner, Sydney. In: Miller JH (ed) Encyclopedia of genetics. Academic Press, New York, pp 1782–1787

    Chapter  Google Scholar 

  • Kujur A, Bajaj D, Upadhyaya HD, Das S, Ranjan R, Shree T, Saxena MS, Badoni S, Kumar V, Tripathi S, Gowda CL, Sharma S, Singh S, Tyagi AK, Parida SK (2015) Employing genome-wide SNP discovery and genotyping strategy to extrapolate the natural allelic diversity and domestication patterns in chickpea. Front Plant Sci 6:162. https://doi.org/10.3389/fpls.2015.00162

    Article  PubMed  PubMed Central  Google Scholar 

  • Le BH, Cheng C, Bui AQ, Wagmaister JA, Henry KF, Pelletier J, Kwong L, Belmonte M, Kirkbride R, Horvath S, Drews GN, Fischer RL, Okamuro JK, Harada JJ, Goldberg RB (2010) Global analysis of gene activity during <em>Arabidopsis</em> seed development and identification of seed-specific transcription factors. Proc Natl Acad Sci 107:8063–8070. https://doi.org/10.1073/pnas.1003530107

    Article  PubMed  PubMed Central  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics (Oxford, England) 25:1754–1760. https://doi.org/10.1093/bioinformatics/btp324

    Article  CAS  Google Scholar 

  • Li C, Zhang YM (2010) Molecular evolution of glycinin and β-conglycinin gene families in soybean (Glycine max L. Merr.). Heredity 106:633. https://doi.org/10.1038/hdy.2010.97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li C, Li M, Dunwell JM, Zhang YM (2012) Gene duplication and an accelerated evolutionary rate in 11S globulin genes are associated with higher protein synthesis in dicots as compared to monocots. BMC Evol Biol 12:15. https://doi.org/10.1186/1471-2148-12-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu C, Wang H, Cui Z, He X, Wang X, Zeng X, Ma H (2007) Optimization of extraction and isolation for 11S and 7S globulins of soybean seed storage protein. Food Chem 102:1310–1316

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods (San Diego, Calif) 25:402–408. https://doi.org/10.1006/meth.2001.1262

    Article  CAS  Google Scholar 

  • Mandal S, Mandal R (2000) Seed storage proteins and approaches for improvement of their nutritional quality by genetic engineering. Curr Sci 10:576–589

    Google Scholar 

  • Menkens AE, Schindler U, Cashmore AR (1995) The G-box: a ubiquitous regulatory DNA element in plants bound by the GBF family of bZIP proteins. Trends Biochem Sci 20:506–510

    Article  CAS  PubMed  Google Scholar 

  • Müntz K (1998) Globulins from legume seeds: structure and function during storage and reactivation. Plant proteins from European crops, pp 3–12. Springer, Berlin, Heidelberg

  • Müntz K, Horstmann C, Schlesier B (1999) Vicia globulins. In: Shewry PR, Casey R (eds) Seed proteins. Springer Netherlands, Dordrecht, pp 259–284

    Chapter  Google Scholar 

  • Mylne JS, Hara-Nishimura I, Rosengren KJ (2014) Seed storage albumins: biosynthesis, trafficking and structures. Funct Plant Biol 41:671–677. https://doi.org/10.1071/FP14035

    Article  CAS  PubMed  Google Scholar 

  • Nambara E, Naito S, McCourt P (1992) A mutant of Arabidopsis which is defective in seed development and storage protein accumulation is a new abi3 allele. Plant J 2:435–441

    Article  CAS  Google Scholar 

  • Nambara E, McCourt P, Naito S (1995) A regulatory role for the ABI3 gene in the establishment of embryo maturation in Arabidopsis thaliana. Development (Cambridge, England) 121:629–636

    CAS  Google Scholar 

  • Nie DM, Ouyang YD, Wang X, Zhou W, Hu CG, Yao J (2013) Genome-wide analysis of endosperm-specific genes in rice. Gene 530:236–247. https://doi.org/10.1016/j.gene.2013.07.088

    Article  CAS  PubMed  Google Scholar 

  • Oo MM, Bae HK, Nguyen TD, Moon S, Oh SA, Kim JH, Soh MS, Song JT, Jung KH, Park SK (2014) Evaluation of rice promoters conferring pollen-specific expression in a heterologous system, Arabidopsis. Plant Reprod 27:47–58. https://doi.org/10.1007/s00497-014-0239-x

  • Osborne TB (1924) The vegetable proteins. Longmans Green and Company, London, p 154

    Google Scholar 

  • Parcy F, Valon C, Kohara A, Miséra S, Giraudat J (1997) The ABSCISIC ACID-INSENSITIVE3, FUSCA3, and LEAFY COTYLEDON1 loci act in concert to control multiple aspects of Arabidopsis seed development. Plant Cell 9:1265–1277. https://doi.org/10.1105/tpc.9.8.1265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pathak V, Singh M, Sharma S, Bhardwaj K (2012) Investigation of proteins on kabuli, desi and green desi chickpea. Int J Chem Sci 10:1669–1679

  • Peng FY, Weselake RJ (2011) Gene coexpression clusters and putative regulatory elements underlying seed storage reserve accumulation in Arabidopsis. BMC Genomics 12:286. https://doi.org/10.1186/1471-2164-12-286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plietz P, Damaschun G, Zirwer D, Gast K, Schlesier B (1983) Structure of 7S seed globulin from Phaseolus vulgaris L. in solution. Int J Biol Macromol 5:356–360

    Article  CAS  Google Scholar 

  • Pradhan S, Bandhiwal N, Shah N, Kant C, Gaur R, Bhatia S (2014) Global transcriptome analysis of developing chickpea (Cicer arietinum L.) seeds. Front Plant Sci 5. https://doi.org/10.3389/fpls.2014.00698

  • Pradhan S, Kant C, Verma S, Bhatia S (2017) Genome-wide analysis of the CCCH zinc finger family identifies tissue specific and stress responsive candidates in chickpea (Cicer arietinum L.). PLoS One 12:e0180469. https://doi.org/10.1371/journal.pone.0180469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Puranik S, Sahu PP, Mandal SN, Parida SK, Prasad M (2013) Comprehensive genome-wide survey, genomic constitution and expression profiling of the NAC transcription factor family in foxtail millet (Setaria italica L.). PLoS One 8:e64594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J (2003) TM4: a free, open-source system for microarray data management and analysis. BioTechniques 34:374–378

    Article  CAS  PubMed  Google Scholar 

  • Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J (2006) TM4 microarray software suite. Methods Enzymol 411:134–193. https://doi.org/10.1016/s0076-6879(06)11009-5

    Article  CAS  PubMed  Google Scholar 

  • Sales MP, Gerhardt IR, Grossi-de-Sá MF, Xavier-Filho J (2000) Do legume storage proteins play a role in defending seeds against bruchids? Plant Physiol 124:515–522. https://doi.org/10.1104/pp.124.2.515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang X-C, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178. https://doi.org/10.1038/nature08670

    Article  CAS  PubMed  Google Scholar 

  • Shahmuradov IA, Umarov RK, Solovyev VV (2017) TSSPlant: a new tool for prediction of plant Pol II promoters. Nucleic Acids Res 45:e65. https://doi.org/10.1093/nar/gkw1353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shewry PR (1995) Plant storage proteins. Biol Rev 70(3):375–426

    Article  CAS  PubMed  Google Scholar 

  • Shewry PR, Napier JA, Tatham AS (1995) Seed storage proteins: structures and biosynthesis. Plant Cell 7:945–956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shutov AD, Kakhovskaya IA, Braun H et al (1995) J Mol Evol 41:1057. https://doi.org/10.1007/BF00173187

    Article  CAS  PubMed  Google Scholar 

  • Singh U, Jambunathan R (1982) Distribution of seed protein fractions and amino acids in different anatomical parts of chickpea (Cicer arietinum L.) and pigeonpea (Cajanus cajan L.). Plant Foods Hum Nutr 31(4):347–354

    Article  CAS  Google Scholar 

  • Sjodahl S, Rodin J, Rask L (1991) Characterization of the 12S globulin complex of Brassica napus. Evolutionary relationship to other 11-12S storage globulins. Eur J Biochem 196:617–621

    Article  CAS  PubMed  Google Scholar 

  • Stålberg K, Ellerström M, Josefsson LG, Rask L (1993) Deletion analysis of a 2S seed storage protein promoter of Brassica napus in transgenic tobacco. Plant Mol Biol 23(4):671–683

    Article  PubMed  Google Scholar 

  • Stålberg K, Ellerstöm M, Ezcurra I, Ablov S, Rask L (1996) Disruption of an overlapping E-box/ABRE motif abolished high transcription of the napA storage-protein promoter in transgenic Brassica napus seeds. Planta 199:515–519. https://doi.org/10.1007/bf00195181

    Article  PubMed  Google Scholar 

  • Sunilkumar G, Connell JP, Smith CW, Reddy AS, Rathore KS (2002) Cotton alpha-globulin promoter: isolation and functional characterization in transgenic cotton, Arabidopsis, and tobacco. Transgenic Res 11:347–359

    Article  CAS  PubMed  Google Scholar 

  • Tai SS, Wu LS, Chen EC, Tzen JT (1999) Molecular cloning of 11S globulin and 2S albumin, the two major seed storage proteins in sesame. J Agric Food Chem 47:4932–4938

    Article  CAS  PubMed  Google Scholar 

  • Takuya Y, Toshiyuki S, Mayuki Y, Misako T, Yuji N, Naoki S, Satoru U, Hisashi H, Mamoru S, Hiroshi H (2011) Crystal structure of basic 7S globulin, a xyloglucan-specific endo-β-1,4-glucanase inhibitor protein-like protein from soybean lacking inhibitory activity against endo-β-glucanase. FEBS J, 278:1944–1954. https://doi.org/10.1111/j.1742-4658.2011.08111.x

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taski-Ajdukovic K, Djordjevic V, Vidic M, Vujakovic M (2010) Subunit composition of seed storage proteins in high-protein soybean genotypes. Pesq Agrop Brasileira 45:721–729

    Article  Google Scholar 

  • Toledo-Ortiz G, Huq E, Quail PH (2003) The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15:1749–1770. https://doi.org/10.1105/tpc.013839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Upadhyaya HD, Bajaj D, Narnoliya L, Das S, Kumar V, Gowda CLL, Sharma S, Tyagi AK, Parida SK (2016) Genome-wide scans for delineation of candidate genes regulating seed-protein content in chickpea:7. https://doi.org/10.3389/fpls.2016.00302

  • 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 MC, Thudi M, Gowda CL, 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

    Article  CAS  PubMed  Google Scholar 

  • Verdier J, Thompson RD (2008) Transcriptional regulation of storage protein synthesis during dicotyledon seed filling. Plant Cell Physiol 49:1263–1271. https://doi.org/10.1093/pcp/pcn116

    Article  CAS  PubMed  Google Scholar 

  • Verdier J, Torres-Jerez I, Wang M, Andriankaja A, Allen SN, He J, Tang Y, Murray JD, Udvardi MK (2013) Establishment of the Lotus japonicus gene expression atlas (LjGEA) and its use to explore legume seed maturation. The Plant Journal 74:351–362. https://doi.org/10.1111/tpj.12119

    Article  CAS  PubMed  Google Scholar 

  • Voorrips R (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Tang H, DeBarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H, Kissinger JC, Paterson AH (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:e49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Deng D, Zhang R, Wang S, Bian Y, Yin Z (2012a) Systematic analysis of plant-specific B3 domain containing proteins based on the genome resources of 11 sequenced species. Mol Biol Rep 39:6267–6282. https://doi.org/10.1007/s11033-012-1448-8

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Li P, Yang Y, Chi Y, Fan B, Chen Z (2016) Expression and functional analysis of a novel group of legume-specific WRKY and Exo70 protein variants from soybean. Sci Rep 6:32090. https://doi.org/10.1038/srep32090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Washida H, Wu C-Y, Suzuki A, Yamanouchi U, Akihama T, Harada K, Takaiwa F (1999) Identification of cis-regulatory elements required for endosperm expression of the rice storage protein glutelin gene GluB-1. Plant Mol Biol 40:1–12. https://doi.org/10.1023/a:1026459229671

    Article  CAS  PubMed  Google Scholar 

  • Weber H, Sreenivasulu N, Weschke W (2010) Molecular physiology of seed maturation and seed storage protein biosynthesis. In: Pua EC, Davey MR (eds) Plant developmental biology - biotechnological perspectives, vol 2. Springer Berlin Heidelberg Berlin, Heidelberg, pp 83–104

    Chapter  Google Scholar 

  • Wu C-Y, Washida H, Onodera Y, Harada K, Takaiwa F (2000) Quantitative nature of the prolamin-box, ACGT and AACA motifs in a rice glutelin gene promoter: minimal cis-element requirements for endosperm-specific gene expression. Plant J 23:415–421. https://doi.org/10.1046/j.1365-313x.2000.00797.x

    Article  CAS  PubMed  Google Scholar 

  • Wu Z, Cheng J, Cui J, Xu X, Liang G, Luo X, Chen X, Tang X, Hu K, Qin C (2016) Genome-wide identification and expression profile of dof transcription factor gene family in pepper (Capsicum annuum L.). Front Plant Sci 7:574

    PubMed  PubMed Central  Google Scholar 

  • Xu J-H, Messing J (2008) Organization of the prolamin gene family provides insight into the evolution of the maize genome and gene duplications in grass species. Proc Natl Acad Sci 105:14330–14,335. https://doi.org/10.1073/pnas.0807026105

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu JH, Messing J (2009) Amplification of prolamin storage protein genes in different subfamilies of the Poaceae. Theor Appl Genet 119(8):1397

    Article  CAS  PubMed  Google Scholar 

  • Yaklich RW (2001) β-Conglycinin and glycinin in high-protein soybean seeds. J Agric Food Chem 49:729–735

    Article  CAS  PubMed  Google Scholar 

  • Yang A, Yu X, Zheng A, James AT (2016) Rebalance between 7S and 11S globulins in soybean seeds of differing protein content and 11SA4. Food Chem 210:148–155. https://doi.org/10.1016/j.foodchem.2016.04.095

    Article  CAS  PubMed  Google Scholar 

  • Yin SW, Tang CH, Wen QB, Yang XQ (2011) Conformational and thermal properties of phaseolin, the major storage protein of red kidney bean (Phaseolus vulgaris L.). J Sci Food Agric 91:94–99. https://doi.org/10.1002/jsfa.4155

    Article  CAS  PubMed  Google Scholar 

  • Young ND, Debellé F, Oldroyd GED, Geurts R, Cannon SB, Udvardi MK, Benedito VA, Mayer KFX, Gouzy J, Schoof H, Van de Peer Y, Proost S, Cook DR, Meyers BC, Spannagl M, Cheung F, De Mita S, Krishnakumar V, Gundlach H, Zhou S, Mudge J, Bharti AK, Murray JD, Naoumkina MA, Rosen B, Silverstein KAT, Tang H, Rombauts S, Zhao PX, Zhou P, Barbe V, Bardou P, Bechner M, Bellec A, Berger A, Bergès H, Bidwell S, Bisseling T, Choisne N, Couloux A, Denny R, Deshpande S, Dai X, Doyle JJ, Dudez A-M, Farmer AD, Fouteau S, Franken C, Gibelin C, Gish J, Goldstein S, González AJ, Green PJ, Hallab A, Hartog M, Hua A, Humphray SJ, Jeong D-H, Jing Y, Jöcker A, Kenton SM, Kim D-J, Klee K, Lai H, Lang C, Lin S, Macmil SL, Magdelenat G, Matthews L, McCorrison J, Monaghan EL, Mun J-H, Najar FZ, Nicholson C, Noirot C, O’Bleness M, Paule CR, Poulain J, Prion F, Qin B, Qu C, Retzel EF, Riddle C, Sallet E, Samain S, Samson N, Sanders I, Saurat O, Scarpelli C, Schiex T, Segurens B, Severin AJ, Sherrier DJ, Shi R, Sims S, Singer SR, Sinharoy S, Sterck L, Viollet A, Wang B-B, Wang K, Wang M, Wang X, Warfsmann J, Weissenbach J, White DD, White JD, Wiley GB, Wincker P, Xing Y, Yang L, Yao Z, Ying F, Zhai J, Zhou L, Zuber A, Dénarié J, Dixon RA, May GD, Schwartz DC, Rogers J, Quétier F, Town CD, Roe BA (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480:520. https://doi.org/10.1038/nature10625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zinsmeister J, Lalanne D, Terrasson E, Chatelain E, Vandecasteele C, Vu BL, Dubois-Laurent C, Geoffriau E, Signor CL, Dalmais M, Gutbrod K, Dörmann P, Gallardo K, Bendahmane A, Buitink J, Leprince O (2016) ABI5 Is a regulator of seed maturation and longevity in legumes. Plant Cell 28:2735–2754. https://doi.org/10.1105/tpc.16.00470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgment

SV acknowledges the award of research fellowship from the Department of Biotechnology, Govt. of India. Authors thank Mr. Sandeep Yadav and Dr. Anand Sarkar for helping in microscopy, and Dr. Chandra Kant for helping in in silico expression profiling. Authors thank Dr. Swarup K Parida for the kind gift of HPC, LPC chickpea accessions. The authors are thankful to DBT-eLibrary Consortium (DeLCON) for providing access to e-resources.

Funding

This work was funded by the Department of Biotechnology, Government of India, under the Challenge Programme on Chickpea Functional Genomics (grant number: BT/ AGR/CG-Phase II/01/2014).

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SV and SB were involved in the designing and execution of the work. SV majorly conducted all the experiments, lab work, analyzed data, and prepared the manuscript draft. SB corrected the manuscript and gave the final approval for the version to be published.

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Correspondence to Sabhyata Bhatia.

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Verma, S., Bhatia, S. Analysis of genes encoding seed storage proteins (SSPs) in chickpea (Cicer arietinum L.) reveals co-expressing transcription factors and a seed-specific promoter. Funct Integr Genomics 19, 373–390 (2019). https://doi.org/10.1007/s10142-018-0650-8

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