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Expressional diversity of wheat nsLTP genes: evidence of subfunctionalization via cis-regulatory divergence

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Abstract

Previously, the wheat non-specific lipid transfer proteins (TaLTP), members of a small multigene family, were reported to evidence a complex pattern of expression regulation. In order to assess further the expression diversity of the TaLTP genes, we have attempted to evaluate their expression profiles in responses to abiotic stresses, using semi-quantitative RT-PCR. The expression profiles generated herein revealed that the TaLTP genes in group A evidenced highly similar responses against abiotic stresses, whereas differential expression patterns among genes in each group were also observed. A total of seven promoters were fused to a GUS reporter gene and the recombinants were introduced into Arabidopsis, while three promoters evidenced non-detectible GUS activity. The promoters of TaLTP1, TaLTP7, and TaLTP10 included in group A drove strong expressions during plant development with overlapping patterns, in large part, but also exhibited distinct expression pattern, thereby suggesting subfunctionalization processing over evolutionary time. However, only trace expression in cotyledons, young emerged leaves, and epidermal cell layers of flower ovaries was driven by the promoter of TaLTP3 of group B. These results indicate that their distinct physiological functions appear to be accomplished by a subfunctionalization process involving degenerative mutations in regulatory regions.

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References

  • Blanchette M, Tompa M (2003) FootPrinter: a program designed for phylogenetic footprinting. Nucleic Acids Res 31:3840–3842. doi:10.1093/nar/gkg606

    Article  CAS  PubMed  Google Scholar 

  • Botton A, Begheldo M, Rasori A, Bonghi C, Tonutti P (2002) Differential expression of two lipid transfer protein genes in reproductive organs of peach (Prunus persica L. Batsch). Plant Sci 163:993–1000. doi:10.1016/s0168-9452(02)00271-6

    Article  CAS  Google Scholar 

  • Boutrot F, Guirao A, Alary R, Joudrier P, Gautier MF (2005) Wheat non-specifc lipid transfer protein genes display a complex pattern of expression in developing seeds. Biochim Biophys Acta, Gene Struct Exp 1730:114–125

    CAS  Google Scholar 

  • Boutrot F, Meynard D, Guiderdoni E, Joudrier P, Gautier MF (2007) The Triticum aestivum non-specific lipid transfer protein (TaLtp) gene family: comparative promoter activity of six TaLtp genes in transgenic rice. Planta 225:843–862. doi:10.1007/s00425-006-0397-7

    Article  CAS  PubMed  Google Scholar 

  • Boutrot F, Chantret N, Gautier ME (2008) Genome-wide analysis of the rice and arabidopsis non-specific lipid transfer protein (nsLtp) gene families and identification of wheat nsLtp genes by EST data mining. BMC Genomics 9:86. doi:10.1186/1471-2164-9-86

    Article  PubMed  Google Scholar 

  • Buhot N, Douliez JP, Jacquemard A, Marion D, Tran V, Maume BF, Milat ML, Ponchet M, Mikès V, Kader JP, Blein JP (2001) A lipid transfer protein binds to a receptor involved in the control of plant defence responses. FEBS Lett 509:27–30. doi:10.1016/s0014-5793(01)03116-7

    Article  CAS  PubMed  Google Scholar 

  • Cammue BPA, De Bolle MGC, Terras FRG, Proost P, Van Damme J, Rees SB, Vanderleyden J, Broekaert WF (1992) Isolation and characterization of a novel class of plant antimicrobial peptides from Mirabilis jalapa L. seeds. J Biol Chem 267:2228–2233

    CAS  PubMed  Google Scholar 

  • Carvalho AO, Machado OLT, Da Cunha M, Santos IS, Gomes VM (2001) Antimicrobial peptides and immunolocalization of a LTP in Vigna unguiculata seeds. Plant Physiol Biochem 39:137–146. doi:10.1016/s0981-9428(00)01230-4

    Article  CAS  Google Scholar 

  • Castro MS, Fontes W (2005) Plant defense and antimicrobial peptides. Pro Pept Lett 12:11–16. doi:10.2174/0929866053405832

    Article  Google Scholar 

  • Clough S, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Federico ML, Kaeppler HF, Skadsen RW (2005) The complex developmental expression of a novel stress-responsive barley Ltp gene is determined by a shortened promoter sequence. Plant Mol Biol 57:35–51. doi:10.1007/s11103-004-6769-0

    Article  CAS  PubMed  Google Scholar 

  • Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545

    CAS  PubMed  Google Scholar 

  • Gaudet DA, Laroche A, Frick M, Huel R, Puchalski B (2003) Cold induced expression of plant defensin and lipid transfer protein transcripts in winter wheat. Physiol Plant 117:195–205. doi:10.1034/j.1399-3054.2003.00041.x

    Article  CAS  Google Scholar 

  • Gowik U, Burscheidt J, Akyildiz M, Schlue U, Koczor M, Streubel M, Westhoff P (2004) cis-Regulatory elements for mesophyll-specific gene expression in the C4 plant Flaveria trinervia, the promoter of the C4 phosphoenolpyruvate carboxylase gene. Plant Cell 16:1077–1090

    Article  CAS  PubMed  Google Scholar 

  • Guiderdoni E, Cordero MJ, Vignols F, Garcia-Garrido JM, Lescot M, Tharreau D, Meynard D, FerrieÁre N, Notteghem JL, Delseny M (2002) Inducibility by pathogen attack and developmental regulation of the rice Ltp1 gene. Plant Mol Biol 49:683–699

    Article  CAS  PubMed  Google Scholar 

  • Han GW, Lee JY, Song HK, Chang C, Min K, Moon J, Shin DH, Kopka ML, Sawaya MR, Yuan HS, Kim TD, Choe J, Lim D, Moon HJ, Suh SW (2001) Structural basis of non-specific lipid binding in maize lipid transfer protein complexes revealed by high-resolution X-ray crystallography. J Mol Biol 308:263–278. doi:10.1006/jmbi.2001.4559

    Article  CAS  PubMed  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300

    Article  CAS  PubMed  Google Scholar 

  • Höfgen R, Willmitzer L (1988) Storage of competent cells for Agrobacterium transformation. Nucleic Acids Res 16:9877

    Article  PubMed  Google Scholar 

  • James VA, Avart C, Worland B, Snape JW, Vain P (2002) The relationship between homozygous and hemizygous transgene expression levels over generations in populations of transgenic rice plants. Theor Appl Genet 104:553–561

    Article  CAS  PubMed  Google Scholar 

  • Jang CS, Kim DS, Bu SY, Kim JB, Lee SS, Kim JY, Johnson JW, Seo YW (2002) Isolation and characterization of lipid transfer protein genes from a wheat-rye translocation. Plant Cell Rep 20:961–966

    Article  CAS  Google Scholar 

  • Jang CS, Lee HJ, Chang SJ, Seo YW (2004) Expression and promoter analysis of the TaLTP1 gene induced by drought and salt stress in wheat (Triticum aestivum L.). Plant Sci 167:995–1001

    Article  CAS  Google Scholar 

  • Jang CS, Johnson JW, Seo YW (2005) Differential expression of TaLTP3 and TaCOMT1 induced by Hessian fly larval infestation in a wheat line possessing H21 resistance gene. Plant Sci 168:1319–1326

    Article  CAS  Google Scholar 

  • Jang CS, Jung JH, Yim WC, Lee BM, Seo YW, Kim W (2007) Divergence of genes encoding non-specific lipid transfer proteins in the Poaceae family. Mol Cells 24:215–223

    CAS  PubMed  Google Scholar 

  • Jang CS, Yim WC, Moon JC, Hung JH, Lee TG, Lim SD, Cho SH, Lee KK, Kim W, Seo YW, Lee BM (2008) Evolution of non-specific lipid transfer protein (nsLTP) genes in the Poaceae family: their duplication and diversity. Mol Genet Genomics 279:481–497. doi:10.1007/s00438-008-0327-4

    Article  CAS  PubMed  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    CAS  PubMed  Google Scholar 

  • Jung HW, Kim WB, Hwang BK (2003) Three pathogen-inducible genes encoding lipid transfer protein from pepper are differentially activated by pathogens, abiotic, and environmental stresses. Plant Cell Environ 26:915–928. doi:10.1046/j.1365-3040.2003.01024.x

    Article  CAS  PubMed  Google Scholar 

  • Kader JC (1996) Lipid-transfer proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 47:627–654

    Article  CAS  PubMed  Google Scholar 

  • Kagaya Y, Ohmiya K, Hattori T (1999) RAV1, a novel DNA-binding protein, binds to bipartite recognition sequence through two distinct DNA-binding domains uniquely found in higher plants. Nucleic Acids Res 27:470–478

    Article  CAS  PubMed  Google Scholar 

  • Kellis M, Birren BW, Lander ES (2004) Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428:617–624

    Article  CAS  PubMed  Google Scholar 

  • Kramer EM, Jaramillo MA, Di Stilio VS (2004) Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms. Genetics 166:1011–1023

    Article  CAS  PubMed  Google Scholar 

  • Kristensen AK, Brunstedt J, Nielsen KK, Roepstorff P, Mikkelsen JD (2000) Characterization of a new antifungal non-specific lipid transfer protein (NsLTP) from sugar beet leaves. Plant Sci 155:31–40. doi:10.1016/s0168-9452(00)00190-4

    Article  CAS  PubMed  Google Scholar 

  • Lee TG, Jang CS, Kim JY, Kim DS, Park JH, Kim DY, Seo YW (2007) A Myb transcription factor (TaMyb1) from wheat roots is expressed during hypoxia: roles in response to the oxygen concentration in root environment and abiotic stresses. Physiol Plant 129:375–385. doi:10.1111/j/1399-3054.2006.00828.x

    Article  CAS  Google Scholar 

  • Liu K, Jiang H, Moore S, Watkins C, Jahn M (2006) Isolation and characterization of a lipid transfer protein expressed in ripening fruit of Capsicum chinense. Planta 223:672–683

    Article  CAS  PubMed  Google Scholar 

  • Lu ZX, Gaudet DA, Frick M, Puchalski B, Genswein B, Laroche A (2005) Identification and characterization of genes differentially expressed in the resistance reaction in wheat infected with Tilletia tritici, the common bunt pathogen. J Biochem Mol Biol 38:420–431

    CAS  PubMed  Google Scholar 

  • Maldonado AM, Doerner P, Dixonk RA, Lamb CJ, Cameron RK (2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419:399–403

    Article  CAS  PubMed  Google Scholar 

  • Moore RC, Purugganan MD (2005) The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol 8:122–128

    Article  CAS  PubMed  Google Scholar 

  • Nam J, dePamphilis CW, Ma H, Nei M (2003) Antiquity and evolution of the MADS-box gene family controlling flower development in plants. Mol Biol Evol 20:1435–1447

    Article  CAS  PubMed  Google Scholar 

  • Ohno S (1970) Evolution by gene and genome duplication. Springer, Heidelberg

    Google Scholar 

  • Opsahl-Sorteberg HG, Divon HH, Nielsen PS, Kalla R, Hammond-Kosack M, Shimamoto K, Kohli A (2004) Identification of a 49-bp fragment of the HvLTP2 promoter directing aleurone cell specific expression. Gene 341:49–58

    Article  CAS  PubMed  Google Scholar 

  • Paterson AH, Bowers JE, Chapman BA (2004) Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci USA 101:9903–9908

    Article  CAS  PubMed  Google Scholar 

  • Pyee J, Yu H, Kolattukudy PE (1994) Identification of a lipid transfer protein as the major protein in the surface wax of broccoli (Brassica oleracea) leaves. Arch Biochem Biophys 311:460–468

    Article  CAS  PubMed  Google Scholar 

  • Sakai H, Aoyama T, Oka A (2000) Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators. Plant J 24:703–711

    Article  CAS  PubMed  Google Scholar 

  • Salse J, Bolot S, Throude M, Jouffe V, Piegu B, Masood Quraishi U, Calcagno T, Cooke R, Delseny M, Feuillet C (2008) Identification and characterization of shared duplications between rice and wheat provide new insight into grass genome evolution. Plant Cell 20:11–24

    Article  CAS  PubMed  Google Scholar 

  • Sohal AK, Pallas JA, Jenkins GI (1999) The promoter of a Brassica napus lipid transfer protein gene is active in a range of tissues and stimulated by light and viral infection in transgenic Arabidopsis. Plant Mol Biol 41:75–87

    Article  CAS  PubMed  Google Scholar 

  • Sterk P, Booij H, Schellekens GA, Van Kammen A, De Vries SC (1991) Cell-specific expression of the carrot EP2 lipid transfer protein gene. Plant Cell 3:907–921

    Article  CAS  PubMed  Google Scholar 

  • Thoma SL, Kaneko Y, Somerville C (1993) A non-specific Arabidopsis lipid transfer protein is a cell wall protein. Plant J 3:27–37

    Article  Google Scholar 

  • Tsuboi S, Osafune T, Tsugeki R, Nishimura M, Yamada M (1992) Nonspecific lipid transfer protein in castor bean cotyledons cells: subcellular localization and a possible role in lipid metabolism. J Biochem 111:500–508

    CAS  PubMed  Google Scholar 

  • van Ree R (2002) Clinical importance of non-specific lipid transfer proteins as food allergens. Biochem Soc Trans 30:910–913

    Article  PubMed  Google Scholar 

  • Woolfe A, Elgar G (2007) Comparative genomics using Fugu reveals insights into regulatory subfunctionalization. Genome Biol 8:R53

    Article  PubMed  Google Scholar 

  • Zahn LM, Leebens-Mack JH, Arrington JM, Hu Y, Landherr LL, dePamphilis CW, Becker A, Theissen G, Ma H (2006) Conservation and divergence in the AGAMOUS subfamily of MADS-box genes: evidence of independent sub- and neofunctionalization events. Evol Dev 8:30–45. doi:10.1111/j.1525-142X.2006.05073.x

    Article  CAS  PubMed  Google Scholar 

  • Zhu Q, Louis I, Dabi T, Beachy RN, Lamb C (2002) Rice TATA binding protein functionally interacts with transcript factor IIB and the RF2a bZIP transcriptional activator in an enhanced plant in vitro transcription system. Plant Cell 14:795–803

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (2009-0064150) and 2008 Research Grant from Kangwon National University to CSJ.

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Correspondence to Wook Kim or Cheol Seong Jang.

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Wang, H.W., Kwon, H.J., Yim, W.C. et al. Expressional diversity of wheat nsLTP genes: evidence of subfunctionalization via cis-regulatory divergence. Genetica 138, 843–852 (2010). https://doi.org/10.1007/s10709-010-9467-7

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