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Identification and molecular characterization of miRNAs and their target genes associated with seed development through small RNA sequencing in chickpea

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Abstract

Multiple studies have attempted to dissect the molecular mechanism underlying seed development in chickpea (Cicer arietinum L.). These studies highlight the need to focus on the role of miRNAs in regulating storage protein accumulation in seeds. Therefore, a total of 8,856,691 short-read sequences were generated from a small RNA library of developing chickpea seeds and were analyzed using miRDeep-P to identify 74 known and 26 novel miRNA sequences. Known miRNAs were classified into 22 miRNA families with miRNA156 family being most abundant. Of the 26 putative novel miRNAs identified, only 22 could be experimentally validated using stem loop end point PCR. Differential expression analyses led to the identification of known as well as novel miRNAs that could regulate various stages of chickpea seed development. In silico target prediction revealed several important target genes and transcription factors like SPL, mediator of RNA Polymerase II transcription subunit 12, aspartic proteinase and NACs, which were further validated by real-time PCR analysis. A comparative expression analysis in chickpea genotypes with contrasting seed protein content revealed one known (Car-miR156h) and two novel miRNA (Car-novmiR7 and Car-novmiR23) candidates to be highly expressed in the LPC (low protein content) chickpea genotypes, targets of which are known to regulate seed storage protein accumulation. Therefore, this study provides a useful resource in the form of miRNA and their targets which can be further utilized to understand and manipulate various regulatory mechanisms involved in seed development with the overall aim of improving yield and nutrition attributes in chickpea.

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Data availability

All relevant supporting data can be found within the additional files accompanying this article. The RNA-Seq reads described in the article were deposited at the Sequence Read Archive (SRA) database; BioProject PRJNA298120; Accession number SRR3103025.

Abbreviations

RPM:

reads per million

TF:

transcription factor

LPC:

low protein content

HPC:

high protein content

GO:

gene ontology

References

  • Allen RS, Li J, Stahle MI, Dubroué A, Gubler F, Millar AA (2007) Genetic analysis reveals functional redundancy and the major target genes of the Arabidopsis miR159 family. Proc Natl Acad Sci 104(41):16371–16376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bai B, Shi B, Hou N, Cao Y, Meng Y, Bian H, Zhu M, Han N (2017) microRNAs participate in gene expression regulation and phytohormone cross-talk in barley embryo during seed development and germination. BMC Plant Biol 17(1):150

    Article  PubMed  PubMed Central  Google Scholar 

  • Ballen-Taborda C, Plata G, Ayling S, Rodriguez-Zapata F, Becerra Lopez-Lavalle LA, Duitama J, Tohme J (2013) Identification of cassava MicroRNAs under abiotic stress. Int J Genomics 2013:857986–857910. https://doi.org/10.1155/2013/857986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bao W, Kojima KK, Kohany O (2015) Repbase Update, a database of repetitive elements in eukaryotic genomes. Mobile Dna 6(1):11

    Article  PubMed  PubMed Central  Google Scholar 

  • Bellieny-Rabelo D, De Oliveira EA, da Silva RE, Costa EP, Oliveira AE, Venancio TM (2016) Transcriptome analysis uncovers key regulatory and metabolic aspects of soybean embryonic axes during germination. Sci Rep 6:36009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berezikov E, Cuppen E, Plasterk RH (2006) Approaches to microRNA discovery. Nature Genet 38(6):S2–S7

    Article  CAS  PubMed  Google Scholar 

  • Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320(5880):1185–1190

    Article  CAS  PubMed  Google Scholar 

  • Cao R, Guo L, Ma M, Zhang W, Liu X, Zhao H (2019) Identification and functional characterization of Squamosa promoter binding protein-like gene TaSPL16 in wheat (Triticum aestivum L.). Front Plant Sci 10(212)

  • Cao S, Zhu QH, Shen W, Jiao X, Zhao X, Wang MB, Liu L, Singh S, Liu Q (2013) Comparative profiling of miRNA expression in developing seeds of high linoleic and high oleic safflower (Carthamus tinctorius L.) plants. Frontiers in. Plant Sci 4(489)

  • Chen D, Yan W, Fu LY, Kaufmann K (2018) Architecture of gene regulatory networks controlling flower development in Arabidopsis thaliana. Nat Commun 9(1):1–3

    Google Scholar 

  • Choudhary S, Sethy NK, Shokeen B, Bhatia S (2009) Development of chickpea EST–SSR markers and analysis of allelic variation across related species. Theor Appl Genet 118:591–608. https://doi.org/10.1007/s00122-008-0923-z

  • Creighton CJ, Reid JG, Gunaratne PH (2009) Expression profiling of microRNAs by deep sequencing. Brief Bioinform 10(5):490–497. https://doi.org/10.1093/bib/bbp019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Czech B, Hannon GJ (2011) Small RNA sorting: matchmaking for Argonautes. Nat Rev Genet 12(1):19–31

    Article  CAS  PubMed  Google Scholar 

  • Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39(suppl_2):W155–W159. https://doi.org/10.1093/nar/gkr319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duan H, Lu X, Lian C, An Y, Xia X, Yin W (2016) Genome-wide analysis of microRNA responses to the phytohormone abscisic acid in Populus euphratica. Front Plant Sci 7:1184

    Article  PubMed  PubMed Central  Google Scholar 

  • Dussert S, Serret J, Bastos-Siqueira A, Morcillo F, Déchamp E, Rofidal V, Lashermes P, Etienne H, Joët T (2018) Integrative analysis of the late maturation programme and desiccation tolerance mechanisms in intermediate coffee seeds. J Exp Bot 69(7):1583–1597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garg R, Sahoo A, Tyagi AK, Jain M (2010) Validation of internal control genes for quantitative gene expression studies in chickpea (Cicer arietinum L.). Biochem Biophys Res Commun 396(2):283–288

    Article  CAS  PubMed  Google Scholar 

  • German MA, Luo S, Schroth G, Meyers BC, Green PJ (2009) Construction of Parallel Analysis of RNA Ends (PARE) libraries for the study of cleaved miRNA targets and the RNA degradome. Nat Protoc 4(3):356–362

    Article  CAS  PubMed  Google Scholar 

  • Goetz M, Vivian-Smith A, Johnson SD, Koltunow AM (2006) AUXIN RESPONSE FACTOR8 is a negative regulator of fruit initiation in Arabidopsis. Plant Cell 18(8):1873–1886. https://doi.org/10.1105/tpc.105.037192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gomes CP, Cho JH, Hood LE, Franco OL, Pereira RW, Wang K (2013) A review of computational tools in microRNA discovery. Front Genet 4:81. https://doi.org/10.3389/fgene.2013.00081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hofacker IL (2003) Vienna RNA secondary structure server. Nucleic Acids Res 31(13):3429–3431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huijser P, Schmid M (2011) The control of developmental phase transitions in plants. Development 138(19):4117–4129

    Article  CAS  PubMed  Google Scholar 

  • Jain M, Chevala VN, Garg R (2014) Genome-wide discovery and differential regulation of conserved and novel microRNAs in chickpea via deep sequencing. J Exp Bot 65(20):5945–5958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiao Y, Song W, Zhang M, Lai J (2011) Identification of novel maize miRNAs by measuring the precision of precursor processing. BMC Plant Biol 11(1):141. https://doi.org/10.1186/1471-2229-11-141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X, Qian Q (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42(6):541–544

    Article  CAS  PubMed  Google Scholar 

  • Jin Y, Liu L, Hao X, Harry DE, Zheng Y, Huang T, Huang J (2019) Unravelling the microRNA-mediated gene regulation in developing Pongamia seeds by high-throughput small RNA profiling. Int J Mol Sci 20(14):3509

    Article  CAS  PubMed Central  Google Scholar 

  • Jin J, Tian F, Yang DC, Meng YQ, Kong L, Luo J, Gao G (2016) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res Oct 23:gkw982

  • Khandal H, Parween S, Roy R, Meena MK, Chattopadhyay D (2017) MicroRNA profiling provides insights into post-transcriptional regulation of gene expression in chickpea root apex under salinity and water deficiency. Sci Rep 7:4632. https://doi.org/10.1038/s41598-017-04906-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khemka N, Singh VK, Garg R, Jain M (2016) Genome-wide analysis of long intergenic non-coding RNAs in chickpea and their potential role in flower development. Sci Rep 6:33297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khraiwesh B, Zhu JK, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta (BBA)-Gene Regulatory Mechanisms 1819(2):137–148

    Article  CAS  Google Scholar 

  • Kohli D, Joshi G, Deokar AA, Bhardwaj AR, Agarwal M, Katiyar-Agarwal S, Srinivasan R, Jain PK (2014) Identification and characterization of wilt and salt stress-responsive microRNAs in chickpea through high-throughput sequencing. PloS one 9(10):e108851

  • Koroban NV, Kudryavtseva AV, Krasnov GS, Sadritdinova AF, Fedorova MS, Snezhkina AV, Bolsheva NL, Muravenko OV, Dmitriev AA, Melnikova NV (2016) The role of microRNA in abiotic stress response in plants. Mol Biol 50(3):337–343

    Article  CAS  Google Scholar 

  • Kozomara A, Birgaoanu M, Griffiths-Jones S (2019) miRBase: from microRNA sequences to function. Nucleic Acids Res 47(D1):D155–D162

    Article  CAS  PubMed  Google Scholar 

  • Kukurba KR, Montgomery SB (2015) RNA sequencing and analysis. Cold Spring Harbor Protocols. 2015(11):pdb-top084970.

  • Lee WC, Lu SH, Lu MH, Yang CJ, Wu SH, Chen HM (2015) Asymmetric bulges and mismatches determine 20-nt microRNA formation in plants. RNA Biol 12(9):1054–1066

    Article  PubMed  PubMed Central  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25(14):1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li T, Ma L, Geng Y, Hao C, Chen X, Zhang X (2015) Small RNA and degradome sequencing reveal complex roles of miRNAs and their targets in developing wheat grains. PloS one 10(10):e0139658

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu X, Huang J, Wang Y, Khanna K, Xie Z, Owen HA, Zhao D (2010) The role of floral organs in carpels, an Arabidopsis loss-of-function mutation in MicroRNA160a, in organogenesis and the mechanism regulating its expression. Plant J 62(3):416–428

    Article  PubMed  Google Scholar 

  • Liu H, Qin C, Chen Z, Zuo T, Yang X, Zhou H, Xu M, Cao S, Shen Y, Lin H, He X (2014) Identification of miRNAs and their target genes in developing maize ears by combined small RNA and degradome sequencing. BMC Genomics 15(1):25

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu N, Wu S, Li Z, Khan AQ, Hu H, Zhang X, Tu L (2020) Repression of microRNA 160 results in retarded seed integument growth and smaller final seed size in cotton. Crop J 8:602–612

    Article  Google Scholar 

  • Liu MY, Wu XM, Long JM, Guo WW (2017) Genomic characterization of miR156 and SQUAMOSA promoter binding protein-like genes in sweet orange (Citrus sinensis). Plant Cell, Tissue Organ Cult (PCTOC) 130(1):103–116

    Article  CAS  Google Scholar 

  • Ma X, Zhang X, Zhao K, Li F, Li K, Ning L, He J, Xin Z, Yin D (2018) Small RNA and degradome deep sequencing reveals the roles of microRNAs in seed expansion in peanut (Arachis hypogaea L.). Front Plant Sci 9(349)

  • 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(1):1–2

    Article  Google Scholar 

  • Malovichko YV, Shtark OY, Vasileva EN, Nizhnikov AA, Antonets KS (2020) Transcriptomic insights into mechanisms of early seed maturation in the garden pea (Pisum sativum L.). Cells 9(3):779

    Article  CAS  PubMed Central  Google Scholar 

  • Mao HD, Yu LJ, Li ZJ, Yan Y, Han R, Liu H, Ma M (2016) Genome-wide analysis of the SPL family transcription factors and their responses to abiotic stresses in maize. Plant Gene 6:1–2

    Article  CAS  Google Scholar 

  • Martin RC, Martínez-Andújar C, Nonogaki H (2012) Role of miRNAs in seed development. In: Sunkar R (ed) MicroRNAs in Plant Development and Stress Responses. Springer, Berlin, Heidelberg, pp 109–121. https://doi.org/10.1007/978-3-642-27384-1_6

    Chapter  Google Scholar 

  • Meyers BC, Axtell MJ (2019) MicroRNAs in plants: Key findings from the early years. Plant Cell 31(6):1206–1207. https://doi.org/10.1105/tpc.19.00310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miao C, Wang D, He R, Liu S, Zhu JK (2020) Mutations in MIR 396e and MIR 396f increase grain size and modulate shoot architecture in rice. Plant Biotechnol J 18(2):491–501

    Article  CAS  PubMed  Google Scholar 

  • Montes RA, De Paoli E, Accerbi M, Rymarquis LA, Mahalingam G, Marsch-Martínez N, Meyers BC, Green PJ, de Folter S (2014) Sample sequencing of vascular plants demonstrates widespread conservation and divergence of microRNAs. Nat Commun 5(1):1–5

    Google Scholar 

  • Nodine MD, Bartel DP (2010) MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev 24(23):2678–2692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ortiz JP, Leblanc O, Rohr C, Grisolia M, Siena LA, Podio M, Colono C, Azzaro C, Pessino SC (2019) Small RNA-seq reveals novel regulatory components for apomixis in Paspalum notatum. BMC Genomics 20(1):487

    Article  PubMed  PubMed Central  Google Scholar 

  • Pant BD, Buhtz A, Kehr J, Scheible WR (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53(5):731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patel RK, Jain M (2012) NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PloS one 7(2):e30619

  • Peng T, Sun H, Du Y, Zhang J, Li J, Liu Y, Zhao Y, Zhao Q (2013) Characterization and expression patterns of microRNAs involved in rice grain filling. PloS one 8(1):e54148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Porta H, Rocha-Sosa M (2002) Plant lipoxygenases. Physiological and molecular features. Plant Physiol 130(1):15–21

    Article  CAS  PubMed  PubMed Central  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. Frontiers in. Plant Sci 5(698)

  • 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(7):e0180469. https://doi.org/10.1371/journal.pone.0180469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raboy V, Dickinson DB (1984) Effect of phosphorus and zinc nutrition on soybean seed phytic acid and zinc. Plant Physiol 75(4):1094–1098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rogers K, Chen X (2013) Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25(7):2383–2399. https://doi.org/10.1105/tpc.113.113159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schreiber AW, Shi B-J, Huang C-Y, Langridge P, Baumann U (2011) Discovery of barley miRNAs through deep sequencing of short reads. BMC Genomics 12:129. https://doi.org/10.1186/1471-2164-12-129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen W, Yao X, Ye T, Ma S, Liu X, Yin X, Wu Y (2018) Arabidopsis Aspartic Protease ASPG1 Affects Seed Dormancy, Seed Longevity and Seed Germination. Plant Cell Physiol 59:1415–1431

    CAS  PubMed  Google Scholar 

  • Sheng L, Chai W, Gong X, Zhou L, Cai R, Li X, Zhao Y, Jiang H, Cheng B (2015) Identification and characterization of novel maize miRNAs involved in different genetic background. Int J Biol Sci 11(7):781–793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi Y, Mandal R, Singh A, Pratap Singh A (2020) Legume lipoxygenase: Strategies for application in food industry. Legum Sci 2(3):e44

    CAS  Google Scholar 

  • Shunmugam AS, Bock C, Arganosa GC, Georges F, Gray GR, Warkentin TD (2015) Accumulation of phosphorus-containing compounds in developing seeds of low-phytate pea (Pisum sativum L.) mutants. Plants 4(1):1–26

    Article  Google Scholar 

  • Si L, Chen J, Huang X, Gong H, Luo J, Hou Q, Zhou T, Lu T, Zhu J, Shangguan Y, Chen E (2016) OsSPL13 controls grain size in cultivated rice. Nature Genet 48(4):447–456

    Article  CAS  PubMed  Google Scholar 

  • Song X, Li Y, Cao X, Qi Y (2019) MicroRNAs and their regulatory roles in plant–environment interactions. Annu Rev Plant Biol 70:489–525

    Article  CAS  PubMed  Google Scholar 

  • Srivastava S, Zheng Y, Kudapa H, Jagadeeswaran G, Hivrale V, Varshney RK, Sunkar R (2015) High throughput sequencing of small RNA component of leaves and inflorescence revealed conserved and novel miRNAs as well as phasiRNA loci in chickpea. Plant Sci 235:46–57

    Article  CAS  PubMed  Google Scholar 

  • Tang M, Bai X, Niu LJ, Chai X, Chen MS, Xu ZF (2018) miR172 regulates both vegetative and reproductive development in the perennial woody plant Jatropha Curcas. Plant Cell Physiol 59(12):2549–2563

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tang X, Bian S, Tang M, Lu Q, Li S, Liu X, Tian G, Nguyen V, Tsang EW, Wang A, Rothstein SJ (2012) MicroRNA–mediated repression of the seed maturation program during vegetative development in Arabidopsis. PLoS Genet 8(11):e1003091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang J, Chu C (2017) MicroRNAs in crop improvement: fine-tuners for complex traits. Nat Plants 3(7):1–1

    Article  Google Scholar 

  • Tatematsu K, Nakabayashi K, Kamiya Y, Nambara E (2008) Transcription factor AtTCP14 regulates embryonic growth potential during seed germination in Arabidopsis thaliana. Plant J 53(1):42–52

    Article  CAS  PubMed  Google Scholar 

  • Tian B, Wang S, Todd TC, Johnson CD, Tang G, Trick HN (2017) Genome-wide identification of soybean microRNA responsive to soybean cyst nematodes infection by deep sequencing. BMC Genomics 18:572. https://doi.org/10.1186/s12864-017-3963-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Varkonyi-Gasic E, Wu R, Wood M, Walton EF, Hellens RP (2007) Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods 3(1):1–2. https://doi.org/10.1186/1746-4811-3-12

    Article  CAS  Google Scholar 

  • Verma S, Bhatia S (2019) Analysis of genes encoding seed storage proteins (SSPs) in chickpea (Cicer arietinum L.) reveals co-expressing transcription factors and a seed-specific promoter. Functional Integr Genomics 19(3):373–390

    Article  CAS  Google Scholar 

  • Wang J, Mei J, Ren G (2019) Plant microRNAs: biogenesis, homeostasis, and degradation. Front Plant Sci 10:360

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang WQ, Wang J, Wu YY, Li DW, Allan AC, Yin XR (2020) Genome-wide analysis of coding and non-coding RNA reveals a conserved miR164-NAC regulatory pathway for fruit ripening. New Phytologist 225(4):1618–1634

    Article  CAS  PubMed  Google Scholar 

  • Wei W, Li G, Jiang X, Wang Y, Ma Z, Niu Z, Wang Z, Geng X (2018) Small RNA and degradome profiling involved in seed development and oil synthesis of Brassica napus. PloS one 13(10):e0204998

    Article  PubMed  PubMed Central  Google Scholar 

  • Wollmann H, Mica E, Todesco M, Long JA, Weigel D (2010) On reconciling the interactions between APETALA2, miR172 and AGAMOUS with the ABC model of flower development. Development 137(21):3633–3642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang X, Li L (2011) miRDeep-P: a computational tool for analyzing the microRNA transcriptome in plants. Bioinformatics 27(18):2614–2615

    Article  CAS  PubMed  Google Scholar 

  • Yang T, Guo L, Ji C, Wang H, Wang J, Zheng X, Xiao Q, Wu Y (2020) The B3 domain-containing transcription factor ZmABI19 coordinates expression of key factors required for maize seed development and grain filling. The Plant Cell

  • Yang T, Wang Y, Teotia S, Zhang Z, Tang G (2018) The making of leaves: how small RNA networks modulate leaf development. Front Plant Sci 9:824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yao JL, Tomes S, Xu J, Gleave AP (2016) How microRNA172 affects fruit growth in different species is dependent on fruit type. Plant Signal Behav 11(4):417–427

    Article  Google Scholar 

  • Yu JY, Zhang ZG, Huang SY, Han X, Wang XY, Pan WJ, Qin HT, Qi HD, Yin ZG, Qu KX, Zhang ZX (2019) Analysis of miRNAs Targeted Storage Regulatory Genes during Soybean Seed Development Based on Transcriptome Sequencing. Genes 10(6):408

    Article  CAS  PubMed Central  Google Scholar 

  • Zhang Z, Dong J, Ji C, Wu Y, Messing J (2019) NAC-type transcription factors regulate accumulation of starch and protein in maize seeds. Proc Natl Acad Sci 116(23):11223–11228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Xie S, Han J, Zhou Y, Liu C, Zhou Z, Wang F, Cheng Z, Zhang J, Hu Y, Hao Z (2019) Integrated transcriptome, small RNA, and degradome analysis reveals the complex network regulating starch biosynthesis in maize. BMC Genomics 20(1):574

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang B, Zhang X, Liu G, Guo L, Qi T, Zhang M, Li X, Wang H, Tang H, Qiao X, Pei W (2018) A combined small RNA and transcriptome sequencing analysis reveal regulatory roles of miRNAs during anther development of Upland cotton carrying cytoplasmic male sterile Gossypium harknessii (D2) cytoplasm. BMC Plant Biol 18(1):242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Wang S, Wu W, Li L, Jiang T, Zheng B (2018) Clearance of maternal barriers by paternal miR159 to initiate endosperm nuclear division in Arabidopsis. Nat Commun 9(1):1–1

    Article  Google Scholar 

  • Zhou X, Khare T, Kumar V (2020) Recent trends and advances in identification and functional characterization of plant miRNAs. Acta Physiol Plantarum 42(2):25

    Article  CAS  Google Scholar 

  • Zhu H, Hu F, Wang R, Zhou X, Sze SH, Liou LW, Barefoot A, Dickman M, Zhang X (2011) Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 145(2):242–256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu QH, Upadhyaya NM, Gubler F, Helliwell CA (2009) Over-expression of miR172 causes loss of spikelet determinacy and floral organ abnormalities in rice (Oryza sativa). BMC Plant Biol 9(1):149

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

SP and SV acknowledge the award of research fellowship from the Department of Biotechnology, Govt. of India. AC acknowledges the award of a research fellowship from the CSIR, Govt. of India. The authors are thankful to DBT-eLibrary Consortium (DeLCON) for providing access to e-resources. The authors also thank Dr. Swarup Parida, NIPGR, New Delhi, India for providing the chickpea seeds for LPC and HPC genotypes.

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-PhaseII/01/2014).

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SP, SV, AC, and SB were involved in the designing and execution of the work. SP, SV, and AC conducted all the experiments, 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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Pradhan, S., Verma, S., Chakraborty, A. et al. Identification and molecular characterization of miRNAs and their target genes associated with seed development through small RNA sequencing in chickpea. Funct Integr Genomics 21, 283–298 (2021). https://doi.org/10.1007/s10142-021-00777-w

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