Publications of NIPGR Scientists
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Item Functional allele of a MATE gene selected during domestication modulates seed color in chickpea(John Wiley & Sons, 2024) Thakro, Virevol; Varshney, Nidhi; Malik, Naveen; Daware, Anurag; Srivastava, Rishi; Mohanty, Jitendra K; Basu, Udita; Narnoliya, Laxmi; Jha, Uday Chand; Tripathi, Shailesh; Tyagi, Akhilesh K.; Parida, Swarup K.Seed color is one of the key target traits of domestication and artificial selection in chickpeas due to its implications on consumer preference and market value. The complex seed color trait has been well dissected in several crop species; however, the genetic mechanism underlying seed color variation in chickpea remains poorly understood. Here, we employed an integrated genomics strategy involving QTL mapping, high-density mapping, map-based cloning, association analysis, and molecular haplotyping in an inter-specific RIL mapping population, association panel, wild accessions, and introgression lines (ILs) of Cicer gene pool. This delineated a MATE gene, CaMATE23, encoding a Transparent Testa (TT) and its natural allele (8-bp insertion) and haplotype underlying a major QTL governing seed color on chickpea chromosome 4. Signatures of selective sweep and a strong purifying selection reflected that CaMATE23, especially its 8-bp insertion natural allelic variant, underwent selection during chickpea domestication. Functional investigations revealed that the 8-bp insertion containing the third cis-regulatory RY-motif element in the CaMATE23 promoter is critical for enhanced binding of CaFUSCA3 transcription factor, a key regulator of seed development and flavonoid biosynthesis, thereby affecting CaMATE23 expression and proanthocyanidin (PA) accumulation in the seed coat to impart varied seed color in chickpea. Consequently, overexpression of CaMATE23 in Arabidopsis tt12 mutant partially restored the seed color phenotype to brown pigmentation, ascertaining its functional role in PA accumulation in the seed coat. These findings shed new light on the seed color regulation and evolutionary history, and highlight the transcriptional regulation of CaMATE23 by CaFUSCA3 in modulating seed color in chickpea. The functionally relevant InDel variation, natural allele, and haplotype from CaMATE23 are vital for translational genomic research, including marker-assisted breeding, for developing chickpea cultivars with desirable seed color that appeal to consumers and meet global market demand.Item Natural alleles of Mediator subunit genes modulate plant height in chickpea(John Wiley & Sons, 2023) Malik, Naveen; Basu, Udita; Srivastava, Rishi; Daware, Anurag; Ranjan, Rajeev; Sharma, Akash; Thakro, Virevol; Mohanty, Jitendra K.; Jha, Uday Chand; Tripathi, Shailesh; Tyagi, Akhilesh K.; Parida, Swarup K.Plant height (PH) is an important plant architectural trait targeted during Green Revolution to enhance crop yields. Identification of genes and natural alleles governing plant height without compromising agronomic performance can fill the lacuna of knowledge connecting ideal plant architecture with maximum achievable yield in chickpea. Through coherent strategy involving genome-wide association study, QTL/fine mapping, map-based cloning, molecular haplotyping, and downstream functional genomics, the current study identified two Mediator subunit genes namely, CaMED23 and CaMED5b and their derived natural alleles/haplotypes underlying the major QTLs and trans-acting eQTLs regulating plant height in chickpea. Differential accumulation of haplotype-specific transcripts of these two Mediator genes in corresponding haplotype-introgressed near-isogenic lines (NILs) correlates negatively with the plant height trait. Quantitative as well as qualitative estimation based on histology, scanning electron microscopy, and histochemical assay unraveled the reduced lengths and cell sizes of internodes along with compromised lignin levels in dwarf/semi-dwarf chickpea NILs introgressed with superior CaMED23 and CaMED5b gene haplotypes. This observation, supported by global transcriptome profiling-based diminished expression of various phenylpropanoid pathway genes upstream of lignin biosynthesis in dwarf/semi-dwarf NILs, essentially links plant height with lignin accumulation. The identified molecular signatures in the Mediator subunit genes can be efficiently utilized to develop desirable dwarf/semi-dwarf-type chickpea cultivars without affecting their yield per plant via modulating lignin/phenylpropanoid biosynthesis.Item A superior gene allele involved in abscisic acid signaling enhances drought tolerance and yield in chickpea(Oxford University Press, 2023) Thakro, Virevol; Malik, Naveen; Basu, Udita; Srivastava, Rishi; Narnoliya, Laxmi; Daware, Anurag; Varshney, Nidhi; Mohanty, Jitendra K; Bajaj, Deepak; Dwivedi, Vikas; Tripathi, Shailesh; Jha, Uday Chand; Dixit, Girish Prasad; Singh, Ashok K; Tyagi, Akhilesh K.; Upadhyaya, Hari D; Parida, Swarup K.Identifying potential molecular tags for drought tolerance is essential for achieving higher crop productivity under drought stress. We employed an integrated genomics-assisted breeding and functional genomics strategy involving association mapping, fine mapping, map-based cloning, molecular haplotyping and transcript profiling in the introgression lines (ILs)- and near isogenic lines (NILs)-based association panel and mapping population of chickpea (Cicer arietinum). This combinatorial approach delineated a bHLH (basic helix-loop-helix) transcription factor, CabHLH10 (Cicer arietinum bHLH10) underlying a major QTL, along with its derived natural alleles/haplotypes governing yield traits under drought stress in chickpea. CabHLH10 binds to a cis-regulatory G-box promoter element to modulate the expression of RD22 (responsive to desiccation 22), a drought/ABA-responsive gene (via a trans-expression QTL), and two strong yield-enhancement photosynthetic efficiency (PE) genes. This, in turn, upregulates other downstream drought-responsive and abscisic acid signaling genes, as well as yield-enhancing PE genes, thus increasing plant adaptation to drought with reduced yield penalty. We showed that a superior allele of CabHLH10 introgressed into the NILs improved root and shoot biomass and PE, thereby enhancing yield and productivity during drought without compromising agronomic performance. Furthermore, overexpression of CabHLH10 in chickpea and Arabidopsis (Arabidopsis thaliana) conferred enhanced drought tolerance by improving root and shoot agro-morphological traits. These findings facilitate translational genomics for crop improvement and the development of genetically-tailored, climate-resilient, high-yielding chickpea cultivars.Item CLAVATA signaling pathway genes modulating flowering time and flower number in chickpea(Springer Nature, 2019) Basu, Udita; Narnoliya, Laxmi; Srivastava, Rishi; Sharma, Akash; Bajaj, Deepak; Daware, Anurag; Thakro, Virevol; Malik, Naveen; Upadhyaya, Hari D.; Tripathi, Shailesh; Hegde, V. S.; Tyagi, Akhilesh K.; Parida, Swarup K.Unraveling the genetic components involved in CLAVATA (CLV) signaling is crucial for modulating important shoot apical meristem (SAM) characteristics and ultimately regulating diverse SAM-regulated agromorphological traits in crop plants. A genome-wide scan identifed 142 CLV1-, 28 CLV2- and 6 CLV3-like genes, and their comprehensive genomic constitution and phylogenetic relationships were deciphered in chickpea. The QTL/fne mapping and map-based cloning integrated with high-resolution association analysis identifed SNP loci from CaCLV3_01 gene within a major CaqDTF1.1/ CaqFN1.1 QTL associated with DTF (days to 50% fowering) and FN (fower number) traits in chickpea, which was further ascertained by quantitative expression profling. Molecular haplotyping of CaCLV3_01 gene, expressed specifcally in SAM, constituted two major haplotypes that diferentiated the early-DTF and high-FN chickpea accessions from late-DTF and low-FN. Enhanced accumulation of transcripts of superior CaCLV3_01 gene haplotype and known fowering promoting genes was observed in the corresponding haplotype-introgressed early-DTF and high-FN near-isogenic lines (NILs) with narrow SAM width. The superior haplotype-introgressed NILs exhibited early-fowering, high-FN and enhanced seed yield/ productivity without compromising agronomic performance. These delineated molecular signatures can regulate DTF and FN traits through SAM proliferation and diferentiation and thereby will be useful for translational genomic study to develop early-fowering cultivars with enhanced yield/productivity.Item ABC transporter-mediated transport of glutathione conjugates enhances seed yield and quality in chickpea(American Society of Plant Biologists, 2019) Basu, Udita; Upadhyaya, Hari D.; Srivastava, Rishi; Daware, Anurag; Malik, Naveen; Sharma, Akash; Bajaj, Deepak; Narnoliya, Laxmi; Thakro, Virevol; Kujur, Alice; Tripathi, Shailesh; Bharadwaj, Chellapilla; Hegde, V. S.; Pandey, Ajay K.; Singh, Ashok K.; Tyagi, Akhilesh K.; Parida, Swarup K.The identification of functionally relevant molecular tags is vital for genomics-assisted crop improvement and enhancing the seed yield, quality and productivity in chickpea. The simultaneous improvement of yield/productivity as well as quality traits often requires pyramiding of multiple genes, which remains a major hurdle given various associated epistatic and pleotropic effects. Unfortunately, no single gene that can improve yield/productivity along with quality and other desirable agromorphological traits is known, hampering the genetic enhancement of chickpea. Using a combinatorial genomics-assisted breeding and functional genomics strategy, this study identified natural alleles and haplotypes of an ABCC3-type transporter gene that regulates seed weight, an important domestication trait, by transcriptional regulation and modulating the transport of glutathione conjugates in seeds of desi and kabuli chickpea. The superior allele/haplotype of this gene introgressed in desi and kabuli near-isogenic lines enhances the seed weight, yield, productivity and multiple desirable plant architecture and seed-quality traits without compromising the agronomic performance. These salient findings can expedite crop improvement endeavors and the development of nutritionally enriched high-yielding cultivars in chickpea.Item Genome-wide generation and genotyping of informative SNPs to scan molecular signatures for seed yield in chickpea(Springer Nature Limited, 2018) Basu, Udita; Srivastava, Rishi; Bajaj, Deepak; Thakro, Virevol; Daware, Anurag; Malik, Naveen; Upadhyaya, Hari D.; Parida, Swarup K.We discovered 2150 desi and 2199 kabuli accessions-derived SNPs by cultivar-wise individual assembling of sequence-reads generated through genotyping-by-sequencing of 92 chickpea accessions. Subsequent large-scale validation and genotyping of these SNPs discovered 619 desi accessions-derived (DAD) SNPs, 531 kabuli accessions-derived (KAD) SNPs, 884 multiple accessions-derived (MAD) SNPs and 1083 two accessions (desi ICC 4958 and kabuli CDC Frontier)-derived (TAD) SNPs that were mapped on eight chromosomes. These informative SNPs were annotated in coding/non-coding regulatory sequence components of genes. The MAD-SNPs were efcient to detect high intra-specifc polymorphic potential and wide natural allelic diversity level including high-resolution admixed-population genetic structure and precise phylogenetic relationship among 291 desi and kabuli accessions. This signifes their efectiveness in introgression breeding and varietal improvement studies targeting useful agronomic traits of chickpea. Six trait-associated genes with SNPs including quantitative trait nucleotides (QTNs) in combination explained 27.5% phenotypic variation for seed yield per plant (SYP). A pentatricopeptide repeat (PPR) gene with a synonymous-coding SNP/QTN signifcantly associated with SYP trait was found most-promising in chickpea. The essential information delineated can be of immense utility in genomics-assisted breeding applications to develop high-yielding chickpea cultivars.Item A multiple QTL-Seq strategy delineates potential genomic loci governing flowering time in chickpea(Frontiers Media S.A., 2017) Srivastava, Rishi; Upadhyaya, Hari D.; Kumar, Rajendra; Daware, Anurag; Basu, Udita; Shimray, Philanim W.; Tripathi, Shailesh; Bharadwaj, Chellapilla; Tyagi, Akhilesh K.; Parida, Swarup K.Identification of functionally relevant potential genomic loci using an economical, simpler and user-friendly genomics-assisted breeding strategy is vital for rapid genetic dissection of complex flowering time quantitative trait in chickpea. A high-throughput multiple QTL-seq strategy was employed in two inter (Cicer arietinum desi accession ICC 4958 × C reticulatum wild accession ICC 17160)- and intra (ICC 4958 × C. arietinum kabuli accession ICC 8261)-specific RIL mapping populations to identify the major QTL genomic regions governing flowering time in chickpea. The whole genome resequencing discovered 1635117 and 592486 SNPs exhibiting differentiation between early- and late-flowering mapping parents and bulks, constituted by pooling the homozygous individuals of extreme flowering time phenotypic trait from each of two aforesaid RIL populations. The multiple QTL-seq analysis using these mined SNPs in two RIL mapping populations narrowed-down two longer (907.1 kb and 1.99 Mb) major flowering time QTL genomic regions into the high-resolution shorter (757.7 kb and 1.39 Mb) QTL intervals on chickpea chromosome 4. This essentially identified regulatory as well as coding (non-synonymous/synonymous) novel SNP allelic variants from two efl1 (early flowering 1) and GI (GIGANTEA) genes regulating flowering time in chickpea. Interestingly, strong natural allelic diversity reduction (88-91%) of two known flowering genes especially mapped at major QTL intervals as compared to that of background genomic regions (where no flowering time QTLs were mapped; 61.8%) in cultivated vis-à-vis wild Cicer gene pools was evident inferring the significant impact of evolutionary bottlenecks on these loci during chickpea domestication. Higher association potential of coding non-synonymous and regulatory SNP alleles mined from efl1 (36-49%) and GI (33-42%) flowering genes for early and late flowering time differentiation among chickpea accessions was evident. The robustness and validity of two functional allelic variants-containing genes localized at major flowering time QTLs was apparent by their identification from multiple intra-/inter-specific mapping populations of chickpea. The functionally relevant molecular tags delineated can be of immense use for deciphering the natural allelic diversity-based domestication pattern of flowering time and expediting genomics-aided crop improvement to develop early flowering cultivars of chickpea.Item A high-resolution InDel (Insertion-Deletion) markers-anchored consensus genetic map identifies major QTLs governing pod number and seed yield in chickpea(Frontiers Media S.A., 2016) Srivastava, Rishi; Singh, Mohar; Bajaj, Deepak; Parida, Swarup K.Development and large-scale genotyping of user-friendly informative genome/gene-derived InDel markers in natural and mapping populations is vital for accelerating genomics-assisted breeding applications of chickpea with minimal resource expenses. The present investigation employed a high-throughput whole genome next-generation resequencing strategy in low and high pod number parental accessions and homozygous individuals constituting the bulks from each of two inter-specific mapping populations [(Pusa 1103 × ILWC 46) and (Pusa 256 × ILWC 46)] to develop non-erroneous InDel markers at a genome-wide scale. Comparing these high-quality genomic sequences, 82,360 InDel markers with reference to kabuli genome and 13,891 InDel markers exhibiting differentiation between low and high pod number parental accessions and bulks of aforementioned mapping populations were developed. These informative markers were structurally and functionally annotated in diverse coding and non-coding sequence components of genome/genes of kabuli chickpea. The functional significance of regulatory and coding (frameshift and large-effect mutations) InDel markers for establishing marker-trait linkages through association/genetic mapping was apparent. The markers detected a greater amplification (97%) and intra-specific polymorphic potential (58–87%) among a diverse panel of cultivated desi, kabuli, and wild accessions even by using a simpler cost-efficient agarose gel-based assay implicating their utility in large-scale genetic analysis especially in domesticated chickpea with narrow genetic base. Two high-density inter-specific genetic linkage maps generated using aforesaid mapping populations were integrated to construct a consensus 1479 InDel markers-anchored high-resolution (inter-marker distance: 0.66 cM) genetic map for efficient molecular mapping of major QTLs governing pod number and seed yield per plant in chickpea. Utilizing these high-density genetic maps as anchors, three major genomic regions harboring each of pod number and seed yield robust QTLs (15–28% phenotypic variation explained) were identified on chromosomes 2, 4, and 6. The integration of genetic and physical maps at these QTLs mapped on chromosomes scaled-down the long major QTL intervals into high-resolution short pod number and seed yield robust QTL physical intervals (0.89–2.94 Mb) which were essentially got validated in multiple genetic backgrounds of two chickpea mapping populations. The genome-wide InDel markers including natural allelic variants and genomic loci/genes delineated at major six especially in one colocalized novel congruent robust pod number and seed yield robust QTLs mapped on a high-density consensus genetic map were found most promising in chickpea. These functionally relevant molecular tags can drive marker-assisted genetic enhancement to develop high-yielding cultivars with increased seed/pod number and yield in chickpea.Item Eco TILLING-based association mapping efficiently delineates functionally relevant natural allelic variants of candidate genes governing agronomic traits in chickpea(Frontiers Media S.A., 2016) Bajaj, Deepak; Srivastava, Rishi; Nath, Manoj; Tripathi, Shailesh; Bharadwaj, Chellapilla; Upadhyaya, Hari D.; Tyagi, Akhilesh K.; Parida, Swarup K.The large-scale mining and high-throughput genotyping of novel gene-based allelic variants in natural mapping population are essential for association mapping to identify functionally relevant molecular tags governing useful agronomic traits in chickpea. The present study employs an alternative time-saving, non-laborious and economical pool-based EcoTILLING approach coupled with agarose gel detection assay to discover 1133 novel SNP allelic variants from diverse coding and regulatory sequence components of 1133 transcription factor (TF) genes by genotyping in 192 diverse desi and kabuli chickpea accessions constituting a seed weight association panel. Integrating these SNP genotyping data with seed weight field phenotypic information of 192 structured association panel identified eight SNP alleles in the eight TF genes regulating seed weight of chickpea. The associated individual and combination of all SNPs explained 10-15 and 31% phenotypic variation for seed weight, respectively. The EcoTILLING-based large-scale allele mining and genotyping strategy implemented for association mapping is found much effective for a diploid genome crop species like chickpea with narrow genetic base and low genetic polymorphism. This optimized approach thus can be deployed for various genomics-assisted breeding applications with optimal expense of resources in domesticated chickpea. The seed weight-associated natural allelic variants and candidate TF genes delineated have potential to accelerate marker-assisted genetic improvement of chickpea.Item mQTL-seq delineates functionally relevant candidate gene harbouring a major QTL regulating pod number in chickpea(Oxford University Press, 2016) Das, Shouvik; Singh, Mohar; Srivastava, Rishi; Bajaj, Deepak; Saxena, Maneesha S.; Rana, Jai C.; Bansal, Kailash C.; Tyagi, Akhilesh K.; Parida, Swarup K.The present study used a whole-genome, NGS resequencing-based mQTL-seq (multiple QTL-seq) strategy in two inter-specific mapping populations (Pusa 1103 × ILWC 46 and Pusa 256 × ILWC 46) to scan the major genomic region(s) underlying QTL(s) governing pod number trait in chickpea. Essentially, the whole-genome resequencing of low and high pod number-containing parental accessions and homozygous individuals (constituting bulks) from each of these two mapping populations discovered >8 million high-quality homozygous SNPs with respect to the reference kabuli chickpea. The functional significance of the physically mapped SNPs was apparent from the identified 2,264 non-synonymous and 23,550 regulatory SNPs, with 8-10% of these SNPs-carrying genes corresponding to transcription factors and disease resistance-related proteins. The utilization of these mined SNPs in Δ (SNP index)-led QTL-seq analysis and their correlation between two mapping populations based on mQTL-seq, narrowed down two (CaqaPN4.1: 867.8 kb and CaqaPN4.2: 1.8 Mb) major genomic regions harbouring robust pod number QTLs into the high-resolution short QTL intervals (CaqbPN4.1: 637.5 kb and CaqbPN4.2: 1.28 Mb) on chickpea chromosome 4. The integration of mQTL-seq-derived one novel robust QTL with QTL region-specific association analysis delineated the regulatory (C/T) and coding (C/A) SNPs-containing one pentatricopeptide repeat (PPR) gene at a major QTL region regulating pod number in chickpea. This target gene exhibited anther, mature pollen and pod-specific expression, including pronounced higher up-regulated (∼3.5-folds) transcript expression in high pod number-containing parental accessions and homozygous individuals of two mapping populations especially during pollen and pod development. The proposed mQTL-seq-driven combinatorial strategy has profound efficacy in rapid genome-wide scanning of potential candidate gene(s) underlying trait-associated high-resolution robust QTL(s), thereby expediting genomics-assisted breeding and genetic enhancement of crop plants, including chickpea.