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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 Genome-wide analysis of polymorphisms identified domestication-associated long low diversity region carrying important rice grain size/weight QTL(John Wiley & Sons, 2020) Kumar, Angad; Daware, Anurag; Kumar, Arvind; Kumar, Vinay; Krishnan S, Gopala; Mondal, Subhasish; Patra, Bhaskar Chandra; Singh, Ashok. K.; Tyagi, Akhilesh K.; Parida, Swarup K.; Thakur, Jitendra K.Rice grain size and weight are major determinants of grain quality and yield and so have been under rigorous selection since domestication. However, genetic basis for contrasting grain size/weight trait among Indian germplasms and their association with domestication‐driven evolution is not well understood. In this study, two long (LGG) and two short grain (SGG) genotypes were resequenced. LGG (LGR and PB 1121) differentiated from SGG (Sonasal and Bindli) by 504,439 SNPs and 78,166 InDels. The LRK gene cluster was different and a truncation mutation in the LRK8 kinase domain was associated with LGG. Phylogeny with 3000 diverse rice accessions revealed that the four sequenced genotypes belonged to japonica group and were at the edge of the clades indicating them to be the potential source of genetic diversity available in Indian rice germplasm. Six SNPs were significantly associated with grain size/weight and top four of them could be validated in mapping population, suggesting this study as a valuable resource for high‐throughput genotyping. A contiguous ~ 6 Mb long low diversity region (LDR) carrying a major grain weight QTL (harbouring OsTOR gene) was identified on chromosome 5. This LDR was identified as an evolutionary important site with significant positive selection and multiple selection sweeps, and showed association with many domestication‐related traits including grain size/weight. The aus population retained more allelic variations in the LDR than japonica and indica populations, suggesting it to be one of the divergence loci. All the data and analyses can be accessed from RiceSzWtBase database.Item Integrated genomic strategies for cereal genetic enhancement: combining QTL and association mapping(Springer Nature Publishing AG, 2020) Daware, Anurag; Parida, Swarup K.; Tyagi, Akhilesh K.Identification of genetic basis for important agronomic traits is essential for marker-assisted crop improvement. Linkage mapping is one of the most popular approaches utilized for identification of major quantitative trait loci (QTLs) governing important agronomic traits in cereals. However, the identified QTLs usually span large genomic intervals and very few of these are subsequently fine mapped to single major effect gene. This hinders application of these QTLs in marker-aided breeding and crop genetic enhancement. On the contrary, association mapping, another popular approach for identification of QTLs, provides very high resolution but suffers from high level of false positives. Joint linkage-association analysis provides a way to combine advantages and avoid the pitfalls associated with both these methods. In this context, we recently developed MetaQTL specific regional association analysis and demonstrated its utility to rapidly narrow down previously identified QTL intervals to few candidate genes. Here, we describe the detailed step-by-step guide for performing MetaQTL specific regional association analysis to identify important genomic regions and underlying potential major effect genes governing traits of agronomic importance in cereals.Item Genome-wide cis-regulatory signatures for modulation of agronomic traits as exemplified by drought yield index (DYI) in chickpea(Springer Nature Publishing AG, 2019) Sharma, Akash; Basu, Udita; Malik, Naveen; Daware, Anurag; Thakro, Virevol; Narnoliya, Laxmi; Bajaj, Deepak; Tripathi, Shailesh; Hegde, V. S.; Upadhyaya, Hari D.; Tyagi, Akhilesh K.; Parida, Swarup K.Developing functional molecular tags from the cis-regulatory sequence components of genes is vital for their deployment in efficient genetic dissection of complex quantitative traits in crop plants including chickpea. The current study identified 431,194 conserved non-coding SNP (CNSNP) from the cis-regulatory element regions of genes which were annotated on a chickpea genome. These genome-wide CNSNP marker resources are made publicly accessible through a user-friendly web-database (http://www.cnsnpcicarbase.com). The CNSNP-based quantitative trait loci (QTL) and expression QTL (eQTL) mapping and genome-wide association study (GWAS) were further integrated with global gene expression landscapes, molecular haplotyping, and DNA-protein interaction study in the association panel and recombinant inbred lines (RIL) mapping population to decode complex genetic architecture of one of the vital seed yield trait under drought stress, drought yield index (DYI), in chickpea. This delineated two constituted natural haplotypes and alleles from a histone H3 protein-coding gene and its transcriptional regulator NAC transcription factor (TF) harboring the major QTLs and trans-acting eQTL governing DYI in chickpea. The effect of CNSNPs in TF-binding cis-element of a histone H3 gene in altering the binding affinity and transcriptional activity of NAC TF based on chromatin immunoprecipitationquantitative PCR (ChIP-qPCR) assay was evident. The CNSNP-led promising molecular tags scanned will essentially have functional significance to decode transcriptional gene regulatory function and thus can drive translational genomic analysis in chickpea.Item Transcriptional signatures modulating shoot apical meristem morphometric and plant architectural traits enhance yield and productivity in chickpea(John Wiley & Sons, 2019) Narnoliya, Laxmi; Basu, Udita; Bajaj, Deepak; Malik, Naveen; Thakro, Virevol; Daware, Anurag; Sharma, Akash; Tripathi, Shailesh; Hegde, V.S.; Upadhyaya, Hari D.; Singh, Ashok K.; Tyagi, Akhilesh K.; Parida, Swarup K.Plant height (PH) and plant width (PW), two of the major plant architectural traits determining the yield and productivity of a crop, are defined by diverse morphometric characteristics of the shoot apical meristem (SAM). The identification of potential molecular tags from a single gene that simultaneously modulates these plant/SAM architectural traits is thus prerequisite to achieve enhanced yield and productivity in crop plants, including chickpea. Large‐scale multi‐environment phenotyping of the association panel and mapping population have ascertained the efficacy of three vital SAM morphometric trait parameters, SAM width, SAM height and SAM area, as key indicators to unravel the genetic basis of the wide PW and PH trait variations observed in desi chickpea. The present study integrated a genome‐wide association study (GWAS); QTL/fine‐mapping and map‐based cloning with molecular haplotyping; transcript profiling; and protein‐DNA interaction assays for the dissection of plant architectural traits in chickpea. These exertions delineated natural alleles and superior haplotypes from a CabHLH121 transcription factor (TF) gene within the major QTLs governing PW, PH and SAM morphometric traits. A genome‐wide protein‐DNA interaction assay assured the direct binding of a known stem cell master regulator, CaWUS, to the WOX‐homeodomain TF binding sites of a CabHLH121 gene and its constituted haplotypes. The differential expression of CaWUS and transcriptional regulation of its target CabHLH121 gene/haplotypes were apparent, suggesting their collective role in altering SAM morphometric characteristics and plant architectural traits in the contrasting near isogenic lines (NILs). The NILs introgressed with a superior haplotype of a CabHLH121 exhibited optimal PW and desirable PH as well as enhanced yield and productivity without compromising any component of agronomic performance. These molecular signatures of the CabHLH121 TF gene have the potential to regulate both PW and PH traits through the modulation of proliferation, differentiation and maintenance of the meristematic stem cell population in the SAM; therefore, these signatures will be useful in the translational genomic study of chickpea genetic enhancement. The restructured cultivars with desirable PH (semi‐dwarf) and PW will ensure maximal planting density in a specified cultivable field area, thereby enhancing the overall yield and productivity of chickpea. This can essentially facilitate the achievement of better remunerative outputs by farmers with rational land use, thus ensuring global food security in the present scenario of an increasing population density and shrinking per capita land area.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 Genetic dissection of photosynthetic efficiency traits for enhancing seed yield in chickpea(John Wiley & Sons, 2019) Basu, Udita; Bajaj, Deepak; Sharma, Akash; Malik, Naveen; Daware, Anurag; Narnoliya, Laxmi; Thakro, Virevol; Upadhyaya, Hari D.; Kumar, Rajendra; Tripathi, Shailesh; Bharadwaj, Chellapilla; Tyagi, Akhilesh K.; Parida, Swarup K.Understanding the genetic basis of photosynthetic efficiency (PE) contributing to enhanced seed yield per plant (SYP) is vital for genomics-assisted crop improvement of chickpea. The current study employed an integrated genomic strategy involving photosynthesis pathway gene-based association mapping, genome-wide association study, QTL mapping and expression profiling. This identified 16 potential SNP loci linked to major QTLs underlying 16 candidate genes significantly associated with PE and SYP traits in chickpea. The allelic variants were tightly linked to positively interacting QTLs regulating both enhanced PE and SYP traits as exemplified by a chlorophyll A-B binding protein-coding gene. The leaf tissue-specific pronounced up-regulated expression of 16 associated genes in germplasm accessions and homozygous individuals of mapping population was evident. Such combinatorial genomic strategy coupled with gene haplotype-specific association as well as in silico protein-protein interaction study delineated natural alleles and superior haplotypes from a chlorophyll A-B binding protein-coding gene and its interacting gene, Timing of CAB Expression 1, which appear to be most-promising candidates in modulating chickpea PE and SYP traits. These functionally pertinent molecular signatures identified have efficacy to drive marker-assisted selection for developing PE-enriched cultivars with high seed yield in chickpea.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.