Abstract
The LIM gene (an acronym for Lin-11, Isl-1, and Mec-3 domain) is a transcription factor family widely distributed in plants. LIM proteins in plants regulate various biological processes, including cytoskeletal organization, secondary cell wall development, and cellular differentiation. They have been identified and characterized in many plant species. However, a comprehensive genome-wide study of the LIM gene family and their associated transcription factors in various important fruit species, such as grapevine (Vitis vinifera), has not been investigated. In this study, we conducted an extensive in silico genome-wide identification and characterization of LIM genes in grapevine using integrated bioinformatics tools. We analyzed the expression of identified LIM genes during early bud development in grapevines using RNA-seq samples. The analysis predicted six VvLIM genes in V. vinifera, corresponding to the LIM genes in the model plant Arabidopsis. Phylogenetic tree analysis revealed that the LIM genes in grapevine could be classified into four subfamilies: αLIM, βLIM, δLIM, and γLIM. A study of conserved motifs, domains, and gene structures (exon length and intron numbers) of VvLIM genes showed a higher similarity within the same gene family. Gene ontology analysis demonstrated that the predicted VvLIM genes are associated with various biological and molecular functions. Network analysis between transcription factors (TFs) and identified VvLIM genes revealed several important TF families, including MYB, NAC, ERF, bZIP, bHLH, C2H2, MIKC_MADS, and TCP. Furthermore, cis-acting regulatory elements related to light-responsive (LR), hormone-responsive (HR), stress-responsive (SR), and other (OT) functions were detected in the predicted VvLIM genes. In addition, we examined the expression changes of the six candidate VvLIM genes during early bud development in grapevines using RNA-seq samples. Differential expression patterns were observed for VvLIM genes involved in bud development, with specific timing coinciding with key developmental stages. Moreover, the expression of VvLIM genes associated with inflorescence primordia and endodormancy provided insights into the molecular mechanisms underlying bud development in grapevines, thus enhancing our understanding at the molecular level. This study will provide valuable information on grapevine LIM genes, laying a solid foundation for subsequent wet-lab characterization of the functional mechanisms of the identified VvLIM genes and their regulatory elements.
Key Message
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Firstly, identify the LIM gene families in the grapevine (Vitis vinifera) genome.
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Subsequently, an integrated bioinformatics approach was employed to analyze the LIM gene family.
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Additionally, the transcript levels of the six selected VvLIM gene candidates were assessed during the early stages of bud development in grapevines, utilizing pre-existing RNA-seq data.
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Finally, this study establishes an in silico foundation for the functional characterization of the LIM gene family and offers valuable insights for subsequent wet-lab investigations to further elucidate the properties of this gene family.
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Availability of Data and Materials
All relevant data are fully available without restriction within the manuscript and its supplementary information files.
References
Aguilar-Martínez JA, Poza-Carrión C, Cubas P (2007) Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 19(2):458–472. https://doi.org/10.1105/tpc.106.048934
Arnaud D, Déjardin A, Leplé JC, Lesage-Descauses MC, Boizot N, Villar M, Bénédetti H, Pilate G (2012) Expression analysis of LIM gene family in poplar, toward an updated phylogenetic classification. BMC Res Notes 5:102. https://doi.org/10.1186/1756-0500-5-102
Arnaud D, Déjardin A, Leplé JC, Lesage-Descauses MC, Pilate G (2007) Genome-wide analysis of LIM gene family in Populus trichocarpa, Arabidopsis thaliana, and Oryza sativa. DNA Research: an International Journal for Rapid Publication of Reports on Genes and Genomes 14(3):103–116. https://doi.org/10.1093/dnares/dsm013
Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME Suite. Nucleic Acids Res 43(W1):W39–49. https://doi.org/10.1093/nar/gkv416
Baltz R, Evrard JL, Domon C, Steinmetz A (1992) A LIM motif is present in a pollen-specific protein. Plant Cell 4(12):1465–1466. https://doi.org/10.1105/tpc.4.12.1465
Bogs J, Jaffé FW, Takos AM, Walker AR, Robinson SP (2007) The grapevine transcription factor VvMYBPA1 regulates proanthocyanidin synthesis during fruit development. 143(3):1347–1361
Brière C, Bordel AC, Barthou H, Jauneau A, Steinmetz A, Alibert G, Petitprez M (2003) Is the LIM-domain protein HaWLIM1 associated with cortical microtubules in sunflower protoplasts? Plant Cell Physiol 44(10):1055–1063. https://doi.org/10.1093/pcp/pcg126
Cao H, Huang P, Zhang L, Shi Y, Sun D, Yan Y, Liu X, Dong B, Chen G, Snyder JH, Lin F, Lu J (2016) Characterization of 47 Cys2 -His2 zinc finger proteins required for the development and pathogenicity of the rice blast fungus Magnaporthe oryzae. New Phytol 211(3):1035–1051. https://doi.org/10.1111/nph.13948
Carmona MJ, Chaïb J, Martínez-Zapater JM, Thomas MR (2008) A molecular genetic perspective of reproductive development in grapevine. 59(10):2579–2596
Castle WE (1903) Mendel’s law of heredity. Science (new York, NY) 18(456):396–406. https://doi.org/10.1126/science.18.456.396
Chao J, Li Z, Sun Y, Aluko OO, Wu X, Wang Q, Liu G (2021) MG2C: a user-friendly online tool for drawing genetic maps. Molecular Horticulture 1(1):16. https://doi.org/10.1186/s43897-021-00020-x
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13(8):1194–1202. https://doi.org/10.1016/j.molp.2020.06.009
Chen XL, Song RT, Yu MY, Sui JM, Wang JS, Qiao LX (2015) Cloning and functional analysis of the chitinase gene promoter in peanut. Genetics and Molecular Research: GMR 14(4):12710–12722. https://doi.org/10.4238/2015.October.19.15
Cheng X, Li G, Muhammad A, Zhang J, Jiang T, Jin Q, Zhao H, Cai Y, Lin Y (2019) Molecular identification, phylogenomic characterization and expression patterns analysis of the LIM (LIN-11, Isl1 and MEC-3 domains) gene family in pear (Pyrus bretschneideri) reveal its potential role in lignin metabolism. Gene 686:237–249. https://doi.org/10.1016/j.gene.2018.11.064
Dawid IB, Breen JJ, Toyama R (1998) LIM domains: multiple roles as adapters and functional modifiers in protein interactions. Trends in Genetics: TIG 14(4):156–162. https://doi.org/10.1016/s0168-9525(98)01424-3
Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15(10):573–581. https://doi.org/10.1016/j.tplants.2010.06.005
Ehrlich JS, Hansen MD, Nelson WJ (2002) Spatio-temporal regulation of Rac1 localization and lamellipodia dynamics during epithelial cell-cell adhesion. Dev Cell 3(2):259–270. https://doi.org/10.1016/s1534-5807(02)00216-2
Eliasson A, Gass N, Mundel C, Baltz R, Kräuter R, Evrard JL, Steinmetz A (2000) Molecular and expression analysis of a LIM protein gene family from flowering plants. Mol Gen Genet MGG 264(3):257–267. https://doi.org/10.1007/s004380000312
Freyd G, Kim SK, Horvitz HR (1990) Novel cysteine-rich motif and homeodomain in the product of the Caenorhabditis elegans cell lineage gene lin-11. Nature 344(6269):876–879. https://doi.org/10.1038/344876a0
Gill GN (1995) The enigma of LIM domains. Structure (London, England: 1993) 3(12):1285–1289. https://doi.org/10.1016/s0969-2126(01)00265-9
Glory E, Murphy RF (2007) Automated subcellular location determination and high-throughput microscopy. Dev Cell 12(1):7–16. https://doi.org/10.1016/j.devcel.2006.12.007
Gray WM (2004) Hormonal regulation of plant growth and development. PLoS Biol 2(9):E311. https://doi.org/10.1371/journal.pbio.0020311
Han LB, Li YB, Wang HY, Wu XM, Li CL, Luo M, Wu SJ, Kong ZS, Pei Y, Jiao GL, Xia GX (2013) The dual functions of WLIM1a in cell elongation and secondary wall formation in developing cotton fibers. Plant Cell 25(11):4421–4438. https://doi.org/10.1105/tpc.113.116970
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27(1):297–300. https://doi.org/10.1093/nar/27.1.297
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(8):1296–1297. https://doi.org/10.1093/bioinformatics/btu817
Iuchi S, Kuldell N (2007) Zinc finger proteins: from atomic contact to cellular function. Springer Science & Business Media
Jakoby M, Weisshaar B, Dröge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7(3):106–111. https://doi.org/10.1016/s1360-1385(01)02223-3
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(D1):D1040-d1045. https://doi.org/10.1093/nar/gkw982
Kadrmas JL, Beckerle MC (2004) The LIM domain: from the cytoskeleton to the nucleus. Nat Rev Mol Cell Biol 5(11):920–931. https://doi.org/10.1038/nrm1499
Karlsson O, Thor S, Norberg T, Ohlsson H, Edlund T (1990) Insulin gene enhancer binding protein Isl-1 is a member of a novel class of proteins containing both a homeo- and a Cys-His domain. Nature 344(6269):879–882. https://doi.org/10.1038/344879a0
Kaur A, Pati PK, Pati AM, Nagpal AK (2017) In-silico analysis of cis-acting regulatory elements of pathogenesis-related proteins of Arabidopsis thaliana and Oryza sativa. PLoS ONE 12(9):e0184523. https://doi.org/10.1371/journal.pone.0184523
Kawaoka A, Ebinuma H (2001) Transcriptional control of lignin biosynthesis by tobacco LIM protein. Phytochemistry 57(7):1149–1157. https://doi.org/10.1016/s0031-9422(01)00054-1
Kawaoka A, Kaothien P, Yoshida K, Endo S, Yamada K, Ebinuma H (2000) Functional analysis of tobacco LIM protein Ntlim1 involved in lignin biosynthesis. The Plant Journal: for Cell and Molecular Biology 22(4):289–301. https://doi.org/10.1046/j.1365-313x.2000.00737.x
Khatun K, Robin AHK, Park JI, Ahmed NU, Kim CK, Lim KB, Kim MB, Lee DJ, Nou IS, Chung MY (2016) Genome-wide identification, characterization and expression profiling of LIM family genes in Solanum lycopersicum L. Plant Physiology and Biochemistry: PPB 108:177–190. https://doi.org/10.1016/j.plaphy.2016.07.006
Kim JS, Mizoi J, Yoshida T, Fujita Y, Nakajima J, Ohori T, Todaka D, Nakashima K, Hirayama T, Shinozaki K, Yamaguchi-Shinozaki K (2011) An ABRE promoter sequence is involved in osmotic stress-responsive expression of the DREB2A gene, which encodes a transcription factor regulating drought-inducible genes in Arabidopsis. Plant Cell Physiol 52(12):2136–2146. https://doi.org/10.1093/pcp/pcr143
Latchman DS (1997) Transcription factors: an overview. Int J Biochem Cell Biol 29(12):1305–1312. https://doi.org/10.1016/s1357-2725(97)00085-x
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30(1):325–327. https://doi.org/10.1093/nar/30.1.325
Li L, Li Y, Wang NN, Li Y, Lu R, Li XB (2015) Cotton LIM domain-containing protein GhPLIM1 is specifically expressed in anthers and participates in modulating F-actin. Plant Biol (stuttg) 17(2):528–534. https://doi.org/10.1111/plb.12243
Li-Mallet A, Rabot A, Geny LJB (2016) Factors controlling inflorescence primordia formation of grapevine: their role in latent bud fruitfulness? A Review 94(3):147–163
Li R, Zhu F, Duan D (2020) Function analysis and stress-mediated cis-element identification in the promoter region of VqMYB15. Plant Signal Behav 15(7):1773664. https://doi.org/10.1080/15592324.2020.1773664
Li Y, Jiang J, Li L, Wang XL, Wang NN, Li DD, Li XB (2013) A cotton LIM domain-containing protein (GhWLIM5) is involved in bundling actin filaments. Plant Physiology and Biochemistry: PPB 66:34–40. https://doi.org/10.1016/j.plaphy.2013.01.018
Liu L, Zhang Z, Mei Q, Chen M (2013) PSI: a comprehensive and integrative approach for accurate plant subcellular localization prediction. PLoS ONE 8(10):e75826. https://doi.org/10.1371/journal.pone.0075826
Lucero LE, Uberti-Manassero NG, Arce AL, Colombatti F, Alemano SG, Gonzalez DH (2015) TCP15 modulates cytokinin and auxin responses during gynoecium development in Arabidopsis. The Plant Journal: for Cell and Molecular Biology 84(2):267–282. https://doi.org/10.1111/tpj.12992
Lutova LA, Dodueva IE, Lebedeva MA, Tvorogova VE (2015) Transcription factors in developmental genetics and the evolution of higher plants. Genetika 51(5):539–557
Magadum S, Banerjee U, Murugan P, Gangapur D, Ravikesavan R (2013) Gene duplication as a major force in evolution. J Genet 92(1):155–161. https://doi.org/10.1007/s12041-013-0212-8
Maul RS, Song Y, Amann KJ, Gerbin SC, Pollard TD, Chang DD (2003) EPLIN regulates actin dynamics by cross-linking and stabilizing filaments. J Cell Biol 160(3):399–407. https://doi.org/10.1083/jcb.200212057
Mengiste T, Chen X, Salmeron J, Dietrich R (2003) The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell 15(11):2551–2565. https://doi.org/10.1105/tpc.014167
Moes D, Gatti S, Hoffmann C, Dieterle M, Moreau F, Neumann K, Schumacher M, Diederich M, Grill E, Shen WH, Steinmetz A, Thomas C (2013) A LIM domain protein from tobacco involved in actin-bundling and histone gene transcription. Mol Plant 6(2):483–502. https://doi.org/10.1093/mp/sss075
Mundel C, Baltz R, Eliasson A, Bronner R, Grass N, Kräuter R, Evrard JL, Steinmetz A (2000) A LIM-domain protein from sunflower is localized to the cytoplasm and/or nucleus in a wide variety of tissues and is associated with the phragmoplast in dividing cells. Plant Mol Biol 42(2):291–302. https://doi.org/10.1023/a:1006333611189
Ng M, Yanofsky MF (2001) Function and evolution of the plant MADS-box gene family. Nat Rev Genet 2(3):186–195. https://doi.org/10.1038/35056041
Nian L, Liu X, Yang Y, Zhu X, Yi X, Haider FU (2021) Genome-wide identification, phylogenetic, and expression analysis under abiotic stress conditions of LIM gene family in Medicago sativa L. PLoS ONE 16(6):e0252213. https://doi.org/10.1371/journal.pone.0252213
Nicolas M, Cubas P (2016) TCP factors: new kids on the signaling block. Curr Opin Plant Biol 33:33–41. https://doi.org/10.1016/j.pbi.2016.05.006
Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15(7):1591–1604. https://doi.org/10.1105/tpc.011650
Papuga J, Hoffmann C, Dieterle M, Moes D, Moreau F, Tholl S, Steinmetz A, Thomas C (2010) Arabidopsis LIM proteins: a family of actin bundlers with distinct expression patterns and modes of regulation. Plant Cell 22(9):3034–3052. https://doi.org/10.1105/tpc.110.075960
Park JI, Ahmed NU, Jung HJ, Arasan SK, Chung MY, Cho YG, Watanabe M, Nou IS (2014) Identification and characterization of LIM gene family in Brassica rapa. BMC Genomics 15(1):641. https://doi.org/10.1186/1471-2164-15-641
Pérez-Alvarado GC, Miles C, Michelsen JW, Louis HA, Winge DR, Beckerle MC, Summers MF (1994) Structure of the carboxy-terminal LIM domain from the cysteine rich protein CRP. Nat Struct Biol 1(6):388–398. https://doi.org/10.1038/nsb0694-388
Pruneda-Paz JL, Breton G, Para A, Kay SA (2009) A functional genomics approach reveals CHE as a component of the Arabidopsis circadian clock. Science (new York, NY) 323(5920):1481–1485. https://doi.org/10.1126/science.1167206
Pucker B, Schwandner A, Becker S, Hausmann L, Viehöver P, Töpfer R, Weisshaar B, Holtgräwe D (2020) RNA-Seq time series of vitis vinifera bud development reveals correlation of expression patterns with the local temperature profile. Plants (Basel, Switzerland) 9(11). https://doi.org/10.3390/plants9111548
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Sánchez-García I, Rabbitts TH (1994) The LIM domain: a new structural motif found in zinc-finger-like proteins. Trends in Genetics: TIG 10(9):315–320. https://doi.org/10.1016/0168-9525(94)90034-5
Seo PJ, Park CM (2010) MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis. New Phytol 186(2):471–483. https://doi.org/10.1111/j.1469-8137.2010.03183.x
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11):2498–2504. https://doi.org/10.1101/gr.1239303
Shao H, Wang H, Tang X (2015) NAC transcription factors in plant multiple abiotic stress responses: progress and prospects. Front Plant Sci 6:902. https://doi.org/10.3389/fpls.2015.00902
Shariatipour N, Heidari B (2018) Investigation of drought and salinity tolerance related genes and their regulatory mechanisms in Arabidopsis (). 11(1)
Shaul O (2017) How introns enhance gene expression. Int J Biochem Cell Biol 91(Pt B):145–155. https://doi.org/10.1016/j.biocel.2017.06.016
Shen XX, Salichos L, Rokas A (2016) A genome-scale investigation of how sequence, function, and tree-based gene properties influence phylogenetic inference. Genome Biol Evol 8(8):2565–2580. https://doi.org/10.1093/gbe/evw179
Shu Y, Liu Y, Zhang J, Song L, Guo C (2015) Genome-wide analysis of the AP2/ERF superfamily genes and their responses to abiotic stress in Medicago truncatula. Front Plant Sci 6:1247. https://doi.org/10.3389/fpls.2015.01247
Smith MA, Hoffman LM, Beckerle MC (2014) LIM proteins in actin cytoskeleton mechanoresponse. Trends Cell Biol 24(10):575–583. https://doi.org/10.1016/j.tcb.2014.04.009
Srivastava V, Verma PK (2017) The plant LIM proteins: unlocking the hidden attractions. Planta 246(3):365–375. https://doi.org/10.1007/s00425-017-2715-7
Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4(5):447–456. https://doi.org/10.1016/s1369-5266(00)00199-0
Sun W, Jin X, Ma Z, Chen H, Liu M (2020a) Basic helix-loop-helix (bHLH) gene family in Tartary buckwheat (Fagopyrum tataricum): genome-wide identification, phylogeny, evolutionary expansion and expression analyses. Int J Biol Macromol 155:1478–1490. https://doi.org/10.1016/j.ijbiomac.2019.11.126
Sun X, Phua DYZ, Axiotakis L Jr, Smith MA, Blankman E, Gong R, Cail RC, de Los E, Reyes S, Beckerle MC, Waterman CM, Alushin GM (2020b) Mechanosensing through direct binding of tensed F-actin by LIM domains. Dev Cell 55(4):468-482.e467. https://doi.org/10.1016/j.devcel.2020.09.022
Tajima F, Nei M (1984) Estimation of evolutionary distance between nucleotide sequences. Mol Biol Evol 1(3):269–285. https://doi.org/10.1093/oxfordjournals.molbev.a040317
Takeda T, Suwa Y, Suzuki M, Kitano H, Ueguchi-Tanaka M, Ashikari M, Matsuoka M, Ueguchi C (2003) The OsTB1 gene negatively regulates lateral branching in rice. The Plant Journal: for Cell and Molecular Biology 33(3):513–520. https://doi.org/10.1046/j.1365-313x.2003.01648.x
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38(7):3022–3027. https://doi.org/10.1093/molbev/msab120
Tatematsu K, Nakabayashi K, Kamiya Y, Nambara E (2008) Transcription factor AtTCP14 regulates embryonic growth potential during seed germination in Arabidopsis thaliana. The Plant Journal: for Cell and Molecular Biology 53(1):42–52. https://doi.org/10.1111/j.1365-313X.2007.03308.x
Thaler JP, Lee SK, Jurata LW, Gill GN, Pfaff SL (2002) LIM factor Lhx3 contributes to the specification of motor neuron and interneuron identity through cell-type-specific protein-protein interactions. Cell 110(2):237–249. https://doi.org/10.1016/s0092-8674(02)00823-1
Thomas C, Dieterle M, Gatti S, Hoffmann C, Moreau F, Papuga J, Steinmetz A (2008) Actin bundling via LIM domains. Plant Signal Behav 3(5):320–321. https://doi.org/10.4161/psb.3.5.5310
Thomas C, Hoffmann C, Dieterle M, Van Troys M, Ampe C, Steinmetz A (2006) Tobacco WLIM1 is a novel F-actin binding protein involved in actin cytoskeleton remodeling. Plant Cell 18(9):2194–2206. https://doi.org/10.1105/tpc.106.040956
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25(24):4876–4882. https://doi.org/10.1093/nar/25.24.4876
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680. https://doi.org/10.1093/nar/22.22.4673
Tohge T, Fernie AR (2010) Combining genetic diversity, informatics and metabolomics to facilitate annotation of plant gene function. Nat Protoc 5(6):1210–1227. https://doi.org/10.1038/nprot.2010.82
Tran TC, Singleton C, Fraley TS, Greenwood JA (2005) Cysteine-rich protein 1 (CRP1) regulates actin filament bundling. BMC Cell Biol 6:45. https://doi.org/10.1186/1471-2121-6-45
Vasconcelos MC, Greven M, Winefield CS, Trought MC, Raw V (2009) The flowering process of Vitis vinifera: a review. 60(4):411–434
Wang C, Zhang LJ, Huang RD (2011a) Cytoskeleton and plant salt stress tolerance. Plant Signal Behav 6(1):29–31. https://doi.org/10.4161/psb.6.1.14202
Wang HJ, Wan AR, Jauh GY (2008) An actin-binding protein, LlLIM1, mediates calcium and hydrogen regulation of actin dynamics in pollen tubes. Plant Physiol 147(4):1619–1636. https://doi.org/10.1104/pp.108.118604
Wang Y, Liu GJ, Yan XF, Wei ZG, Xu ZR (2011b) MeJA-inducible expression of the heterologous JAZ2 promoter from Arabidopsis in Populus trichocarpa protoplasts. 118:69–74
Wang Y, Wang C, Rajaofera MJN, Zhu L, Liu W, Zheng F, Miao W (2020) WY7 is a newly identified promoter from the rubber powdery mildew pathogen that regulates exogenous gene expression in both monocots and dicots. PLoS ONE 15(6):e0233911. https://doi.org/10.1371/journal.pone.0233911
Way JC, Chalfie M (1988) mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegans. Cell 54(1):5–16. https://doi.org/10.1016/0092-8674(88)90174-2
Wei K, Chen J, Wang Y, Chen Y, Chen S, Lin Y, Pan S, Zhong X, Xie D (2012) Genome-wide analysis of bZIP-encoding genes in maize. DNA Research: an International Journal for Rapid Publication of Reports on Genes and Genomes 19(6):463–476. https://doi.org/10.1093/dnares/dss026
Winkelman JD, Anderson CA, Suarez C, Kovar DR, Gardel ML (2020) Evolutionarily diverse LIM domain-containing proteins bind stressed actin filaments through a conserved mechanism. Proc Natl Acad Sci USA 117(41):25532–25542. https://doi.org/10.1073/pnas.2004656117
Wittkopp PJ, Kalay G (2011) Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat Rev Genet 13(1):59–69. https://doi.org/10.1038/nrg3095
Xin H, Zhu W, Wang L, Xiang Y, Fang L, Li J, Sun X, Wang N, Londo JP, Li S (2013) Genome wide transcriptional profile analysis of Vitis amurensis and Vitis vinifera in response to cold stress. PLoS ONE 8(3):e58740. https://doi.org/10.1371/journal.pone.0058740
Xu Z-S, Chen M, Li L-C, Ma Y-ZJB (2008) Functions of the ERF transcription factor family in plants. 86(9):969–977
Yang R, Chen M, Sun JC, Yu Y, Min DH, Chen J, Xu ZS, Zhou YB, Ma YZ, Zhang XH (2019) Genome-wide analysis of LIM family genes in foxtail millet (Setaria italica L.) and characterization of the role of SiWLIM2b in drought tolerance. Intern J Mole Sci 20(6). https://doi.org/10.3390/ijms20061303
Yang X, Bu Y, Niu F, Cun Y, Zhang L, Song X (2022) Comprehensive analysis of LIM gene family in wheat reveals the involvement of TaLIM2 in pollen development. Plant Science : An International Journal of Experimental Plant Biology 314:111101. https://doi.org/10.1016/j.plantsci.2021.111101
Zhao M, He L, Gu Y, Wang Y, Chen Q, He C (2014) Genome-wide analyses of a plant-specific LIM-domain gene family implicate its evolutionary role in plant diversification. Genome Biol Evol 6(4):1000–1012. https://doi.org/10.1093/gbe/evu076
Zhao R, Song X, Yang N, Chen L, Xiang L, Liu XQ, Zhao K (2020) Expression of the subgroup IIIf bHLH transcription factor CpbHLH1 from Chimonanthus praecox (L.) in transgenic model plants inhibits anthocyanin accumulation. Plant cell reports 39 (7):891–907. https://doi.org/10.1007/s00299-020-02537-9
Zhou Y, Hu L, Wu H, Jiang L, Liu S (2017) Genome-wide identification and transcriptional expression analysis of cucumber superoxide dismutase (SOD) family in response to various abiotic stresses. International Journal of Genomics 2017:7243973. https://doi.org/10.1155/2017/7243973
Zhu X, Wang B, Wang X, Zhang C, Wei X (2021) Genome-wide identification, characterization and expression analysis of the LIM transcription factor family in quinoa. Physiology and Molecular Biology of Plants: an International Journal of Functional Plant Biology 27(4):787–800. https://doi.org/10.1007/s12298-021-00988-2
Acknowledgements
The authors are very grateful to the Department of Genetic Engineering and Biotechnology, Faculty of Biological Science and Technology, Jashore University of Science and Technology, Jashore 7408, Bangladesh, for providing the opportunity to conduct this research. The authors acknowledge and appreciate the reviewers and the editorial panel members for their valuable comments and critical suggestions for improving the quality of this manuscript.
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Conceptualization: MARS, SMR, Supervision, project administration, resources: MARS, SMR, Investigation:, MARS, MSUI, FTZ, Methodology: MARS, MSUI, FTZ, Formal analysis: MARS, MSUI, Visualization: MARS, MSUI, Writing—original draft: MARS, SS, FTZ, Writing—review and editing: MARS, SS, FTZ.
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Sarkar, M.R., Sarkar, S., Islam, M.U. et al. Genome-Wide Identification and Characterization of LIM Gene Family in Grapevine (Vitis vinifera L.) and Their Expression Analysis at Early Bud Developmental Stages. Plant Mol Biol Rep (2023). https://doi.org/10.1007/s11105-023-01416-3
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DOI: https://doi.org/10.1007/s11105-023-01416-3