Abstract
DNA replication, repair, and recombination (DRRR) are the fundamental processes required for faithful transmission of genetic information within and between generations. The DRRR genes protect the cells from potential mutations and damage during the developmental phases and stress conditions. Thus, these genes indirectly regulate diverse important agronomic traits in a crop plant. A genome-wide survey of six DRRR pathway genes, namely, DNA replication, Base Excision Repair, Nucleotide Excision Repair, Homologous Recombination, Mismatch Excision Repair, and Non-Homologous End-Joining, identified 157 DRRR genes in chickpea. Phylogenetic analysis of these genes within the legume clades and model plant Arabidopsis identified 42 conserved DRRR genes exhibiting clade-specific evolutionary patterns. Integrating the gene-based association mapping with differential expression profiling identified the natural alleles of the potential DRRR genes, primarily regulating flowering and maturation time and involved in drought tolerance of chickpea. Identifying and understanding DRRR genes’ roles in regulating yield and stress tolerance traits in a vital grain legume like chickpea is requisite for its future crop improvement endeavors. Manipulation of promising functionally relevant DRRR genes will pave the way for simultaneous improvement in multiple beneficial agronomic traits in chickpea.
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References
Ambawat S, Sharma P, Yadav NR, Yadav RC (2013) MYB transcription factor genes as regulators for plant responses: an overview. Physiol Mol Biol Plants 19:307–321
Atieno J, Li Y, Langridge P, Dowling K, Brien C, Berger B, Varshney RK, Sutton T (2017) Exploring genetic variation for salinity tolerance in chickpea using image-based phenotyping. Sci Rep 7:1–11
Bajaj D, Srivastava R, Nath M, Tripathi S, Bharadwaj C, Upadhyaya HD, Tyagi AK, Parida SK (2016a) EcoTILLING-based association mapping efficiently delineates functionally relevant natural allelic variants of candidate genes governing agronomic traits in chickpea. Front Plant Sci 7:1–9
Bajaj D, Upadhyaya HD, Das S, Kumar V, Gowda CL, Sharma S, Tyagi AK, Parida SK (2016b) Identification of candidate genes for dissecting complex branch number trait in chickpea. Plant Sci 245:61–70
Bajaj D, Upadhyaya HD, Khan Y, Das S, Badoni S, Shree T, Kumar V, Tripathi S, Gowda CL, Singh S, Sharma S, Tyagi AK, Chattopdhyay D, Parida SK (2015) A combinatorial approach of comprehensive QTL-based comparative genome mapping and transcript profiling identified a seed weight-regulating candidate gene in chickpea. Sci Rep 5:1–14
Basu U, Bajaj D, Sharma A, Malik N, Daware A, Narnoliya L, Thakro V, Upadhyaya HD, Kumar R, Tripathi S, Bharadwaj C, Tyagi AK, Parida SK (2019a) Genetic dissection of photosynthetic efficiency traits for enhancing seed yield in chickpea. Plant Cell Environ 42:158–173
Basu U, Upadhyaya HD, Srivastava R, Daware A, Malik N, Sharma A, Bajaj D, Narnoliya L, Thakro V, Kujur A, Tripathi S, Bharadwaj C, Hegde VS, Pandey AK, Singh AK, Tyagi AK, Parida SK (2019b) ABC transporter-mediated transport of glutathione conjugates enhances seed yield and quality in chickpea. Plant Physiol 180:253–275
Bertioli DJ, Moretzsohn MC, Madsen LH, Sandal N, Leal-Bertioli SC, Guimarães PM, Hougaard BK, Fredslund J, Schauser L, Nielsen AM, Sato S, Tabata S, Cannon SB, Stougaard J (2009) An analysis of synteny of Arachis with Lotus and Medicago sheds new light on the structure, stability and evolution of legume genomes. BMC Genomics 10:45
Bhar A, Chatterjee M, Gupta S, Das S (2018) Salicylic acid regulates systemic defense signaling in chickpea during Fusarium oxysporum f. sp. ciceri race 1 infection. Plant Mol Biol Report 36:162–175
Chai MF, Wei PC, Chen QJ, An R, Chen J, Yang S, Wang XC (2006) NADK3, a novel cytoplasmic source of NADPH, is required under conditions of oxidative stress and modulates abscisic acid responses in Arabidopsis. Plant J 47:665–674
Deokar A, Sagi M, Daba K, Tar’an B, (2019) QTL sequencing strategy to map genomic regions associated with resistance to ascochyta blight in chickpea. Plant Biotechnol J 17:275–288
Dreni L, Zhang D (2016) Flower development: the evolutionary history and functions of the AGL6 subfamily MADS-box genes. J Exp Bot 67:1625–1638
Fulcher N, Sablowski R (2009) Hypersensitivity to DNA damage in plant stem cell niches. Proc Natl Acad Sci 106:20984–20988
Garg R, Shankar R, Thakkar B, Kudapa H, Krishnamurthy L, Mantri N, Varshney RK, Bhatia S, Jain M (2016) Transcriptome analyses reveal genotype- and developmental stage-specific molecular responses to drought and salinity stresses in chickpea. Sci Rep 6:1–15
Gaur PM, Srinivasan S, Gowda CLL, Rao BV (2007) Rapid generation advancement in chickpea. J SAT Agric Res 3:1–3
Gowda SJ, Radhika P, Mhase LB, Jamadagni BM, Gupta VS, Kadoo NY (2011) Mapping of QTLs governing agronomic and yield traits in chickpea. J Appl Genet 52:9–21
Gu C, Guo ZH, Hao PP, Wang GM, Jin ZM, Zhang SL (2017) Multiple regulatory roles of AP2/ERF transcription factor in angiosperm. Bot Stud 58:6
Gupta S, Nawaz K, Parween S, Roy R, Sahu K, Kumar Pole A, Khandal H, Srivastava R, Kumar Parida S, Chattopadhyay D (2016) Draft genome sequence of Cicer reticulatum L., the wild progenitor of chickpea provides a resource for agronomic trait improvement. DNA Res 24:1–10
Hitomi K, Arvai AS, Yamamoto J, Hitomi C, Teranishi M, Hirouchi T, Yamamoto K, Iwai S, Tainer JA, Hidema J, Getzoff ED (2012) Eukaryotic class II cyclobutane pyrimidine dimer photolyase structure reveals basis for improved ultraviolet tolerance in plants. J Biol Chem 287:12060–12069
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
Jia N, Liu X, Gao H (2016) A DNA2 homolog is required for DNA damage repair, cell cycle regulation, and meristem maintenance in plants. Plant Physiol 171:318–333
Kale SM, Jaganathan D, Ruperao P, Chen C, Punna R, Kudapa H, Thudi M, Roorkiwal M, Katta MA, Doddamani D, Garg V, Kishor PBK, Gaur PM, Nguyen HT, Batley J, Edwards D, Sutton T, Varshney RK (2015) Prioritization of candidate genes in “QTL-hotspot” region for drought tolerance in chickpea (Cicer arietinum L.). Sci Rep 5:1–14
Kudapa H, Garg V, Chitikineni A, Varshney RK (2018) The RNA-Seq-based high resolution gene expression atlas of chickpea (Cicer arietinum L.) reveals dynamic spatio-temporal changes associated with growth and development. Plant Cell Environ 41:2209–2225
Kujur A, Bajaj D, Upadhyaya HD, Das S, Ranjan R, Shree T, Saxena MS, Badoni S, Kumar V, Tripathi S, Gowda CLL, Sharma S, Singh S, Tyagi AK, Parida SK (2015a) A genome-wide SNP scan accelerates trait-regulatory genomic loci identification in chickpea. Sci Rep 5:11166
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 (2015b) Employing genome-wide SNP discovery and genotyping strategy to extrapolate the natural allelic diversity and domestication patterns in chickpea. Front Plant Sci 6:162
Kujur A, Upadhyaya HD, Bajaj D, Gowda CL, Sharma S, Tyagi AK, Parida SK (2016) Identification of candidate genes and natural allelic variants for QTLs governing plant height in chickpea. Sci Rep 6:1–9
Kujur A, Upadhyaya HD, Shree T, Bajaj D, Das S, Saxena MS, Badoni S, Kumar V, Tripathi S, Gowda CL, Sharma S, Singh S, Tyagi AK, Parida SK (2015c) 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
Li D, Zhang H, Mou M, Chen Y, Xiang S, Chen L, Yu D (2019a) Arabidopsis class II TCP transcription factors integrate with the FT-FD module to control flowering. Plant Physiol 181:97–111
Li Z, Liu C, Zhang Y, Wang B, Ran Q, Zhang J (2019b) The bHLH family member ZmPTF1 regulates drought tolerance in maize by promoting root development and abscisic acid synthesis. J Exp Bot 70:5471–5486
Lipka AE, Tian F, Wang Q, Peiffer J, Li M, Bradbury PJ, Gore MA, Buckler ES, Zhang Z (2012) GAPIT: genome association and prediction integrated tool. Bioinformatics 2:2397–2399
Liu H, Yang Y, Liu D, Wang X, Zhang L (2020) Transcription factor TabHLH49 positively regulates dehydrin WZY2 gene expression and enhances drought stress tolerance in wheat. BMC Plant Biol 20:259
Malik N, Dwivedi N, Singh AK, Parida SK, Agarwal P, Thakur JK, Tyagi AK (2016) An integrated genomic strategy delineates candidate mediator genes regulating grain size and weight in rice. Sci Rep 6:23253
Mannur DM, Babbar A, Thudi M, Sabbavarapu MM, Roorkiwal M, Yeri SB, Bansal VP, Jayalakshmi SK, Singh Yadav S, Rathore A, Chamarthi SK, Mallikarjuna BP, Gaur PM, Varshney RK (2018) Super Annigeri 1 and improved JG 74: two Fusarium wilt-resistant introgression lines developed using marker-assisted backcrossing approach in chickpea (Cicer arietinum L.). Mol Breed 39:1–13
Manova V, Gruszka D (2015) DNA damage and repair in plants—from models to crops. Front Plant Sci 6:1–26
Mathew IE, Das S, Mahto A, Agarwal P (2016) Three rice NAC transcription factors heteromerize and are associated with seed size. Front Plant Sci 7:1638
Parween S, Nawaz K, Roy R, Pole AK, Venkata Suresh B, 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 5:1–14
Purushothaman R, Lakshmanan K, Upadhyaya HD, Vadez V, Varshney RK (2016) Shoot traits and their relevance in terminal drought tolerance of chickpea (Cicer arietinum L.). Field Crops Res 197:10–27
Purushothaman R, Lakshmanan K, Upadhyaya HD, Vadez V, Varshney RK (2017) Root traits confer grain yield advantages under terminal drought in chickpea (Cicer arietinum L.). Field Crops Res 201:146–161
Rehman AU, Malhotra RS, Bett K, Tar'an B, Bueckert R, Warkentin TD (2011) Mapping QTL associated with traits affecting grain yield in chickpea (Cicer arietinum L.) under terminal drought stress. Crop Sci 51:450
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
Shim JS, Oh N, Chung PJ, Kim YS, Choi YD, Kim JK (2018) Overexpression of OsNAC14 improves drought tolerance in rice. Front Plant Sci 9:1–14
Singh SK, Roy S, Choudhury SR, Sengupta DN (2010) DNA repair and recombination in higher plants: Insights from comparative genomics of Arabidopsis and rice. BMC Genomics 11:443
Singh VK, Garg R, Jain M (2013) A global view of transcriptome dynamics during flower development in chickpea by deep sequencing. Plant Biotechnol J 11:691–701
Sivasakthi K, Thudi M, Tharanya M, Kale SM, Kholová J, Halime MH, Jaganathan D, Baddam R, Thirunalasundari T, Gaur PM, Varshney RK, Vadez V (2018) Plant vigour QTLs co-map with an earlier reported QTL hotspot for drought tolerance while water saving QTLs map in other regions of the chickpea genome. BMC Plant Biol 18:1–18
Smaczniak C, Immink RG, Angenent GC, Kaufmann K (2012) Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies. Development 139:3081–1398
Srivastava R, Bajaj D, Malik A, Singh M, Parida SK (2016) Transcriptome landscape of perennial wild Cicer microphyllum uncovers functionally relevant molecular tags regulating agronomic traits in chickpea. Sci Rep 6:33616
Tuteja N, Beven AF, Shaw PJ, Tuteja R (2001) A pea homologue of human DNA helicase I is localized within the dense fibrillar component of the nucleolus and stimulated by phosphorylation with CK2 and cdc2 protein kinases. Plant J 25:9–17
Upadhyaya HD, Furman BJ, Dwivedi SL, Upuda SM, Gowda CL, Baum M, Crouch JH, Buhariwalla HK, Singh S (2006) Development of a composite collection for mining germplasm possessing allelic variation for beneficial traits in chickpea. Plant Genet Resour Charact Util 4:13–19
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
Varshney RK, Thudi M, Nayak SN, Gaur PM, Kashiwagi J, Krishnamurthy L, Jaganathan D, Koppolu J, Bohra A, Tripathi S, Rathore A, Jukanti AK, Jayalakshmi V, Vemula A, Singh SJ, Yasin M, Sheshshayee MS, Viswanatha KP (2014) Genetic dissection of drought tolerance in chickpea (Cicer arietinum L.). Theor Appl Genet 127:445–462
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 5:1–14
Wang X, Li BB, Ma TT, Sun LY, Tai L, Hu CH, Liu WT, Li WQ, Chen KM (2020) The NAD kinase OsNADK1 affects the intracellular redox balance and enhances the tolerance of rice to drought. BMC Plant Biol 20:1–9
Waterworth WM, Drury GE, Bray CM, West CE (2011) Repairing breaks in the plant genome: the importance of keeping it together. New Phytol 192:805–822
Waterworth WM, Footitt S, Bray CM, Finch-Savage WE, West CE (2016) DNA damage checkpoint kinase ATM regulates germination and maintains genome stability in seeds. Proc Natl Acad Sci 113:9647–9652
Waterworth WM, Masnavi G, Bhardwaj RM, Jiang Q, Bray CM, West CE (2010) A plant DNA ligase is an important determinant of seed longevity. Plant J 63:848–860
Wong CE, Singh MB, Bhalla PL (2009) Molecular processes underlying the floral transition in the soybean shoot apical meristem. Plant J 57:832–845
Xing X, Jiang J, Huang Y, Zhang Z, Song A, Ding L, Wang H, Yao J, Chen S, Chen F, Fang W (2019) The constitutive expression of a Chrysanthemum ERF transcription factor influences flowering time in Arabidopsis thaliana. Mol Biotechnol 6:20–31
Yang H, Xue Q, Zhang Z, Du J, Yu D, Huang F (2018) GmMYB181, a Soybean R2R3-MYB protein, increases branch number in transgenic Arabidopsis. Front Plant Sci 9:1027
Yang S, Xu K, Chen S, Li T, Xia H, Chen L, Liu H, Luo L (2019) A stress-responsive bZIP transcription factor OsbZIP62 improves drought and oxidative tolerance in rice. BMC Plant Biol 19:260
Zhang Z, Ersoz E, Lai CQ, Todhunter RJ, Tiwari HK, Gore MA, Bradbury PJ, Yu J, Arnett DK, Ordovas JM, Buckler ES (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42:355–360
Zong X, Yan Q, Wu F, Ma Q, Zhang J (2020) Genome-wide analysis of the role of NAC family in flower development and abiotic stress responses in Cleistogenes songorica. Genes (basel) 11:927
Acknowledgements
UB acknowledges the UGC (University Grants Commission), India, for research fellowship awards.
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The financial support for this study was provided by a research grant from the Department of Biotechnology (DBT), Government of India (102/IFD/SAN/2161/2013–14).
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UB, HDU, and DB performed the field and laboratory experiments as well as drafted the manuscript. UB, DB, NM, and AS involved in genotyping and data analysis. HDU and UCJ assisted in constitution of an association panel and its field phenotyping. SKP conceived and designed the research study, guided data analysis and interpretation, and participated in drafting and correcting the manuscript critically, and all authors gave the final approval of the version to be published.
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Genome-wide survey identified 157 DNA replication repair and recombination (DRRR) genes in chickpea and their homologs within the sequenced legumes. Phylogenetic analysis deciphered clade specific evolutionary pattern of these genes within legumes. Expression profiling and association mapping delineates few crucial DRRR genes regulating yield and stress tolerance traits in chickpea
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Basu, U., Sharma, A., Bajaj, D. et al. The DNA Replication, Repair, and Recombination Pathway Genes Modulating Yield and Stress Tolerance Traits in Chickpea. Plant Mol Biol Rep 40, 119–135 (2022). https://doi.org/10.1007/s11105-021-01303-9
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DOI: https://doi.org/10.1007/s11105-021-01303-9