Skip to main content
SpringerLink
Log in

The plant LIM proteins: unlocking the hidden attractions

  • Review
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

The plant LIMs comprise two sub-families with one (DA1/DAR) and two (2LIM) LIM domains. This review comprehensively discussed the structure and potential role of this protein family in diverse area of plant biology.

The description of first eukaryote lineage-specific plant LIM domain (LIN11, ISL1, and MEC3) proteins was observed in Helianthus long back. The successive study of LIM proteins in diverse plants has shown its vital relation to development, metabolism and defence. This nascent gene family has been worked out for their role in actin dynamics, organ size determination and transcription regulation. On grounds of protein architecture, two sub-families have been delineated as DA1/DAR (one LIM domain) and 2LIMs (two LIM domains). The genomic and expression study guides to the identification of diverse sub-categories. The significance of 2LIMs in regulation of actin dynamics leading to pollen growth and development has prospects to understand the plant reproductive behaviour. Interestingly, new facet of these LIMs as a transcriptional regulator in biological pathway/biosynthesis was also reported. Recently, the cumulative contribution of these features was also recognized for obtaining good quality fibre, thus giving translational outlook to this family. The DA1/DAR proteins are orchestrated with additional domains and provide a key role in regulation of organ size and tolerance to biotic and abiotic stress. This review will focus the journey of plant LIMs till date and will cover details of its structure, type, classification and functional relevance. This will provide insight to identify the potential of this gene family in the improvement of desired crop features.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • 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 Res 14:103–116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baltz R, Evrard JL (1996) The pollen-specific LIM protein PLIM-1 from sunflower binds nucleic acids in vitro. Sex Plant Repro 9:264–268

    Article  CAS  Google Scholar 

  • Baltz R, Evrard JL, Domon C, Steinmetz A (1992) A LIM motif is present in a pollen-specific protein. Plant Cell 4:1465–1466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baltz R, Schmit AC, Kohnen M, Hentges F, Steinmetz A (1999) Differential localization of the LIM domain protein PLIM-1 in microspores and mature pollen grains from sunflower. Sex Plant Reprod 12:60–65

    Article  CAS  Google Scholar 

  • Bi D, Johnson KC, Zhu Z, Huang Y, Chen F, Zhang Y, Li X (2011) Mutations in an atypical TIR-NB-LRR-LIM resistance protein confer autoimmunity. Front Plant Sci 2:71

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 44:1055–1063

    Article  PubMed  Google Scholar 

  • Du L, Li N, Chen L, Xu Y, Li Y, Zhang Y, Li C, Li Y (2014) The ubiquitin receptor DA1 regulates seed and organ size by modulating the stability of the ubiquitin-specific protease UBP15/SOD2 in Arabidopsis. Plant Cell 26:665–677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eliasson A, Gass N, Munde C, Baltz R, Krauter R, Evrard JL, Steinmetz A (2000) Molecular and expression analysis of a LIM protein gene family from flowering plants. Mol Genet Genom 264:257–267

    Article  CAS  Google Scholar 

  • Fraser CM, Chapple C (2011) The phenylpropanoid pathway in Arabidopsis. Arabidopsis Book 9:e0152

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 344:876–879

    Article  CAS  PubMed  Google Scholar 

  • 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 25:4421–4438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han L, Li Y, Sun Y, Wang H, Kong Z, Xia G (2016) The two domains of cotton WLIM1a protein are functionally divergent. Sci Chin Life Sci 59:206–212

    Article  CAS  Google Scholar 

  • Hobert O, Westphal H (2000) Functions of LIM-homeobox genes. Trends Genet 16:75–83

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann C, Moes D, Dieterle M, Neumann K, Moreau F, Furtado AT, Dumas D, Steinmetz A, Thomas C (2014) Live cell imaging reveals actin-cytoskeleton-induced self-association of the actin-bundling protein WLIM1. J Cell Sci 127:583–598

    Article  CAS  PubMed  Google Scholar 

  • Kadrmas JL, Beckerle MC (2004) The LIM domain: from the cytoskeleton to the nucleus. Nature Rev Mol Cell Biol 5:920–931

    Article  CAS  Google Scholar 

  • Kaothien P, Kawaoka A, Ebinuma H, Yoshida K, Shinmyo A (2002) Ntlim1, a PAL-box binding factor, controls promoter activity of the horseradish wound-inducible peroxidase gene. Plant Mol Biol 49:591–599

    Article  CAS  PubMed  Google Scholar 

  • 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 344:879–882

    Article  CAS  PubMed  Google Scholar 

  • Kawaoka A, Ebinuma H (2001) Transcriptional control of lignin biosynthesis by tobacco LIM protein. Phytochemistry 57:1149–1157

    Article  CAS  PubMed  Google Scholar 

  • Kawaoka A, Kaothien P, Yoshida K, Endo S, Yamada K, Ebinuma H (2000) Functional analysis of tobacco LIM protein Ntlim1 involved in lignin biosynthesis. Plant J 22:289–301

    Article  CAS  PubMed  Google Scholar 

  • Kawaoka A, Nanto K, Ishii K, Ebinuma H (2006) Reduction of lignin content by suppression of expression of the LIM domain transcription factor in Eucalyptus camaldulensis. Sil Genet 55:269–277

    Google Scholar 

  • 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 Physiol Biochem 108:177–190

    Article  CAS  PubMed  Google Scholar 

  • Khurana P, Henty JL, Huang S, Staiger AM, Blanchoin L, Staiger CJ (2010) Arabidopsis VILLIN1 and VILLIN3 have overlapping and distinct activities in actin bundle formation and turnover. Plant Cell 22:2727–2748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li N, Li Y (2015a) Maternal control of seed size in plants. J Exp Bot 66:1087–1097

    Article  CAS  PubMed  Google Scholar 

  • Li N, Li Y (2015b) Ubiquitin-mediated control of seed size in plants. Front Plant Sci 5:332

    Google Scholar 

  • Li Y, Zheng L, Corke F, Smith C, Bevan MW (2008) Control of final seed and organ size by the DA1 gene family in Arabidopsis thaliana. Genes Dev 22:1331–1336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 Physiol Biochem 66:34–40

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Yue X, Que Y, Yan X, Ma Z, Talbot NJ, Wang Z (2014) Characterisation of four LIM protein-encoding genes involved in infection-related development and pathogenicity by the rice blast fungus Magnaporthe oryzae. PLoS Osne 9:e88246

    Article  Google Scholar 

  • Li L, Li Y, Wang NN, Lu R, Li XB (2015) Cotton LIM domain-containing protein GhPLIM1 is specifically expressed in anthers and participates in modulating F-actin. Plant Biol 17:528–534

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Osbourn A, Ma P (2015) MYB transcription factors as regulators of phenylpropanoid metabolism in plants. Mol plant 8:689–708

    Article  CAS  PubMed  Google Scholar 

  • Matthews JM, Lester K, Joseph S, Curtis DJ (2013) LIM-domain-only proteins in cancer. Nat Rev Can 13:111–122

    Article  CAS  Google Scholar 

  • 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 6:483–502

    Article  CAS  PubMed  Google Scholar 

  • Moes D, Hoffmann C, Dieterle M, Moreau F, Neumann K, Papuga J, Furtado AT, Steinmetz A, Thomas C (2015) The pH sensibility of actin-bundling LIM proteins is governed by the acidic properties of their C-terminal domain. FEBS Lett 589:2312–2319

    Article  CAS  PubMed  Google Scholar 

  • Mundel C, Baltz R, Eliasson Å, 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 42:291–302

    Article  CAS  PubMed  Google Scholar 

  • Na JK, Huh SM, Yoon IS, Byun MO, Lee YH, Lee KO, Kim DY (2014) Rice LIM protein OsPLIM2a is involved in rice seed and tiller development. Mol Breed 34:569–581

    Article  CAS  Google Scholar 

  • 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 22:3034–3052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 Genom 15:641

    Article  Google Scholar 

  • Peng Y, Ma W, Chen L, Yang L, Li S, Zhao H, Zhao Y, Jin W, Li N, Bevan MW, Li X, Tong Y, Li Y (2013) Control of root meristem size by DA1-RELATED PROTEIN2 in Arabidopsis. Plant Physiol 161:1542–1556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng Y, Chen L, Lu Y, Wu Y, Dumenil J, Zhu Z, Bevan MW, Li Y (2015) The ubiquitin receptors DA1, DAR1, and DAR2 redundantly regulate endoreduplication by modulating the stability of TCP14/15 in Arabidopsis. Plant Cell 273:649–662

    Article  Google Scholar 

  • 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 Mol Biol 1:388–398

    Article  Google Scholar 

  • Porter K, Day B (2016) From filaments to function: the role of the plant actin cytoskeleton in pathogen perception, signaling and immunity. J Integr Plant Biol 58: 299–311

    Article  CAS  PubMed  Google Scholar 

  • Sadler I, Crawford AW, Michelsen JW, Beckerle MC (1992) Zyxin and cCRP: two interactive LIM domain proteins associated with the cytoskeleton. J Cell Biol 119:1573–1587

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-García I, Rabbits TH (1994) The LIM domain: a new structural motif found in zinc-finger-like proteins. Trends Genet 10:315–320

    Article  PubMed  Google Scholar 

  • Schmeichel KL, Beckerle MC (1997) Molecular dissection of a LIM domain. Mol Biol Cell 8:219–230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skau CT, Courson DS, Bestul AJ, Winkelman JD, Rock RS, Sirotkin V, Kovar DR (2011) Actin filament bundling by fimbrin is important for endocytosis, cytokinesis, and polarization in fission yeast. J Biol Chem 286:26964–26977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srivastava V, Verma PV (2015) Genome wide identification of LIM genes in Cicer arietinum and response of Ca-2LIMs in development, hormone and pathogenic stress. PLoS One 10:e0138719

    Article  PubMed  PubMed Central  Google Scholar 

  • Sweetman J, Spurr C, Eliasson A, Gass N, Steinmetz A, Twell D (2000) Isolation and characterisation of two pollen-specific LIM domain protein cDNAs from Nicotiana tabacum. Sex Plant Reprod 12(6):339–345

    Article  CAS  Google Scholar 

  • 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 18:2194–2206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas C, Moreau F, Dieterle M, Hoffmann C, Gatti S, Hofmann C, Van Troys M, Ampe C, Steinmetz A (2007a) The LIM domains of WLIM1 define a new class of actin bundling modules. J Biol Chem 282:33599–33608

    Article  CAS  PubMed  Google Scholar 

  • Thomas C, Hoffmann C, Gatti S, Steinmetz A (2007b) LIM proteins: a novel class of actin cytoskeleton organizers in plants. Plant Signal Behav 2:99–100

    Article  PubMed  PubMed Central  Google Scholar 

  • Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3:2–20

    Article  CAS  PubMed  Google Scholar 

  • Wang HJ, Wan AR, Jauh GY (2008) An actin binding protein, LlLIM1, mediates Ca2+ and hydrogen regulation of actin dynamics in pollen tubes. Plant Physiol 147:1619–1636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Liu B, Huang C, Zhang X, Luo C, Cheng X, Yu R, Wu Z (2012) Over expression of Zmda1-1 gene increases seed mass of corn. Afr J Biotechnol 11(69):13387–13395

    Article  CAS  Google Scholar 

  • Way JC, Chalfie M (1988) Mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegans. Cell 54:5–16

    Article  CAS  PubMed  Google Scholar 

  • Weiskirchen R, Günther K (2003) The CRP/MLP/TLP family of LIM domain proteins: acting by connecting. BioEssays 25:152–162

    Article  CAS  PubMed  Google Scholar 

  • Xia T, Li N, Dumenil J, Li J, Kamenski A, Bevan MW, Gao F, Li Y (2013) The ubiquitin receptor DA1 interacts with the E3 ubiquitin ligase DA2 to regulate seed and organ size in Arabidopsis. Plant Cell 25:3347–3359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu F, Zhu C, Cevik V, Johnson K, Liu Y, Sohn K, Jones JD, Holub EB, Li X (2015) Autoimmunity conferred by chs3-2D relies on CSA1, its adjacent TNL-encoding neighbour. Sci Rep 5:8792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang H, Shi Y, Liu J, Guo L, Zhang X, Yang S (2010) A mutant CHS3 protein with TIR-NB-LRR-LIM domains modulates growth, cell death and freezing tolerance in a temperature-dependent manner in Arabidopsis. Plant J 63:283–296

    Article  CAS  PubMed  Google Scholar 

  • Yao X, Pérez-Alvarado GC, Louis HA, Pomiès P, Hatt C, Summers MF, Beckerle MC (1999) Solution structure of the chicken cysteine-rich protein, CRP1, a double-LIM protein implicated in muscle differentiation. Biochem 38:5701–5713

    Article  CAS  Google Scholar 

  • Ye J, Xu M (2012) Actin bundler PLIM2s are involved in the regulation of pollen development and tube growth in Arabidopsis. J Plant Physiol 169:516–522

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Liu CJ (2015) Multifaceted regulations of gateway enzyme phenylalanine ammonia-lyase in the biosynthesis of phenylpropanoids. Mol Plant 8:17–27

    Article  CAS  PubMed  Google Scholar 

  • 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. Genom Biol Evol 6:1000–1012

    Article  CAS  Google Scholar 

  • Zhao M, Gu Y, He L, Chen Q, He C (2015) Sequence and expression variations suggest an adaptive role for the DA1-like gene family in the evolution of soybeans. BMC Plant Biol 15:120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng Q, Zhao Y (2007) The diverse biofunctions of LIM domain proteins: determined by subcellular localization and protein–protein interaction. Bio Cell 99:489–502

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Authors acknowledge Central University of Jammu (CUJ), Jammu and National Institute of Plant Genome Research (NIPGR), New Delhi for work facility. This work is supported by the Department of Biotechnology project, Government of India (BT/AGR/CG-Phase II/01/2014) and Council of Scientific and Industrial Research (CSIR), India.

Author information

Authors and Affiliations

  1. Department of Plant Sciences, Central University of Jammu, Rahya-Suchani (Bagla), Dist. Samba, Jammu, Jammu and Kashmir, 181143, India

    Vikas Srivastava

  2. Plant Immunity Laboratory, National Institute of Plant Genome Research, Aruna Asaf Ali Marg, New Delhi, India

    Praveen Kumar Verma

Authors
  1. Vikas Srivastava
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Praveen Kumar Verma
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Praveen Kumar Verma.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Srivastava, V., Verma, P.K. The plant LIM proteins: unlocking the hidden attractions. Planta 246, 365–375 (2017). https://doi.org/10.1007/s00425-017-2715-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-017-2715-7

Keywords

Search

Navigation