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Molecular Genetics and Genomics

, Volume 288, Issue 10, pp 519–533 | Cite as

Molecular characterisation of two homoeologous elicitor-responsive lipin genes in cotton

  • Sonia M. Phillips
  • Ian A. DuberyEmail author
  • Henriette van Heerden
Original Paper
  • 297 Downloads

Abstract

The identification and molecular characterisation of two lipin-like gene copies (GhLIPN) in cotton, Gossypium hirsutum, an allotetraploid derived from two progenitor diploid Gossypium species, is described. Sequence analyses of the GhLIPN copies, designated GhLIPN-1 and -2, revealed that they contain 11 exons, separated by ten introns. They each have a 2,643 bp open reading frame that encodes 880 aa proteins, and share a 97.7 and 95.5 % sequence similarity at the translated nucleotide and amino acid level, respectively. The GhLIPN genes have a distinct domain architecture consisting of an archetypical N-terminal lipin domain, followed by a haloacid dehalogenase (HAD) domain towards the C-terminus. A Southern blot did not distinguish between the two gene copies, which suggests that they may be homoeologs rather than paralogs. GhLIPN-2 is more similar to a homoeologous sequence from G. raimondii, representing the ancestral D-genome, compared to GhLIPN-1 that matches G. herbaceum and that represents the A-genome. Our data indicate that GhLIPN-1 and GhLIPN-2 are homoeologs that derive from the A- and the D-diploid genomes, respectively. The promoter sequences of GhLIPN-1 and -2 differ by 56 %, as a result of multiple indels. In silico analysis of the promoter regions revealed that both genes contain numerous putative defence-related and elicitor-responsive cis-elements that support a role for GhLIPN in defence responses. Relative quantification real-time PCR confirmed the up-regulation in response to a cell-wall-derived V. dahliae elicitor, which supported the association of GhLIPN with defence signalling. The results add a new dimension to the proposed roles of lipins in plants by suggesting that lipins may have a role in defence signalling.

Keywords

Allotetraploid Gossypium hirsutum Haloacid dehalogenase Homoeologs Lipin Phosphatidate phosphatase Verticillium dahliae 

Notes

Acknowledgments

This work was supported by the South African National Research Foundation and the University of Johannesburg.

Supplementary material

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References

  1. Adams K, Wendel J (2005) Novel patterns of gene expression in polyploid plants. Trends Genet 21:539–543PubMedCrossRefGoogle Scholar
  2. Adams K, Flagel L, Wendel J (2009) Responses of the cotton genome to polyploidy. In: Paterson A (ed) Genetics and genomics of cotton. Springer, New York, pp 419–429CrossRefGoogle Scholar
  3. Aguado A, de Los Santos B, Gamane D, García del Moral L, Romero F (2010) Gene effects for cotton-fiber traits in cotton plant (Gossypium hirsutum L.) under Verticillium conditions. Field Crop Res 116:209–217CrossRefGoogle Scholar
  4. Ainouche M, Jenczewski E (2010) Focus on polyploidy. New Phytol 186:1–4PubMedCrossRefGoogle Scholar
  5. Bolek Y, El-Zik K, Pepper A, Bell A, Magill C, Thaxton P, Reddy O (2005) Mapping of verticillium wilt resistance genes in cotton. Plant Sci 168:1581–1590CrossRefGoogle Scholar
  6. Breathnach R, Chambon P (1981) Organization and expression of eukaryotic split genes coding for proteins. Annu Rev Biochem 50:349–383PubMedCrossRefGoogle Scholar
  7. Burroughs A, Allen K, Dunaway-Mariano D, Aravind L (2006) Evolutionary genomics of the HAD superfamily: understanding the structural adaptations and catalytic diversity in a superfamily of phosphoesterases and allied enzymes. J Mol Biol 361:1003–1034PubMedCrossRefGoogle Scholar
  8. Carman G, Han G-S (2009) Phosphatidic acid phosphatase, a key enzyme in the regulation of lipid synthesis. J Biol Chem 284:2593–2597PubMedCrossRefGoogle Scholar
  9. Chaudhary B, Flagel L, Stupar R, Udall J, Verma N, Springer N, Wendel J (2009) Reciprocal silencing, transcriptional bias and functional divergence of homoeologs in polyploid cotton (Gossypium). Genetics 182:503–517PubMedCrossRefGoogle Scholar
  10. Chee P, Rong J, Williams-Coplin D, Schulze S, Paterson A (2004) EST derived PCR-based markers for functional gene homologues in cotton. Genome 47:449–462PubMedCrossRefGoogle Scholar
  11. Cheong Y, Chang H-S, Gupta R, Wang X, Zhu T, Luan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129:661–677PubMedCrossRefGoogle Scholar
  12. Cronn R, Small R, Wendel J (1999) Duplicated genes evolve independently after polyploid formation in cotton. Proc Natl Acad Sci USA 96:14406–14411PubMedCrossRefGoogle Scholar
  13. Csaki LS, Reue K (2010) Lipins: multifunctional lipid metabolism proteins. Annu Rev Nutrition 30:257–272PubMedCrossRefGoogle Scholar
  14. de Torres Zabella M, Fernandez-Delmond I, Niittyla T, Sanchez P, Grant M (2002) Differential expression of genes encoding Arabidopsis phospholipases after challenge with virulent or avirulent Pseudomonas isolates. Mol Plant Microbe Interact 15:808–816CrossRefGoogle Scholar
  15. den Hartog M, Verhoef N, Munnik T (2003) Nod factor and elicitors activate different phospholipid signaling pathways in suspension-cultured alfalfa cells. Plant Physiol 132:311–317CrossRefGoogle Scholar
  16. Dong S, Adams KL (2011) Differential contributions to the transcriptome of duplicated genes in response to abiotic stresses in natural and synthetic polyploids. New Phytol 190:1045–1057PubMedCrossRefGoogle Scholar
  17. Donkor J, Zhang P, Wong S, O’Loughlin L, Dewald J, Kok B, Brindley D, Reue K (2009) A conserved serine residue is required for the phosphatidate phosphatase activity but not the transcriptional coactivator functions of lipin-1 and lipin-2. J Biol Chem 284:29968–29978PubMedCrossRefGoogle Scholar
  18. Dubery I, Slater V (1997) Induced defence responses in cotton leaf discs by elicitors from Verticillium dahliae. Phytochemistry 44:1429–1434CrossRefGoogle Scholar
  19. Eastmond PJ, Quettier A-L, Kroon JTM, Craddock C, Adams N, Slabas AR (2010) Phosphatidic acid phosphoryhydrolase 1 and 2 regulate phospholipid synthesis at the endoplasmic reticulum in Arabidposis. Plant Cell 22:2796–2811PubMedCrossRefGoogle Scholar
  20. Eulgem T (2005) Regulation of the Arabidopsis defence transcriptome. Trends Plant Sci 10:71–78PubMedCrossRefGoogle Scholar
  21. Fan L, Zheng S, Wang X (1997) Antisense suppression of phospholipase Dα retards abscisic acid- and ethylene-promoted senescence of postharvest Arabidopsis leaves. Plant Cell 9:2183–2196PubMedGoogle Scholar
  22. Flagel L, Wendel J (2009) Gene duplication and evolutionary novelty in plants. New Phytol 183:557–564PubMedCrossRefGoogle Scholar
  23. Flagel L, Wendel J (2010) Evolutionary rate variation, genomic dominance and duplicate gene expression evolution during allotetraploid cotton speciation. New Phytol 186:184–193PubMedCrossRefGoogle Scholar
  24. Flagel L, Chen L, Chaudhary B, Wendel J (2009) Coordinated and fine-scale control of homoeologous gene expression in allotetraploid cotton. J Hered 100:487–490PubMedCrossRefGoogle Scholar
  25. Göre M, Caner O, Altin N, Aydin M, Erdogan O, Filizer F, Büyükdögerlioglu A (2009) Evaluation of cotton cultivars for resistance to pathotypes of Verticillium dahliae. Crop Prot 28:215–219CrossRefGoogle Scholar
  26. Gorjánácz M, Mattaj IW (2009) Lipin is required for efficient breakdown of the nuclear envelope in Caenorhabditis elegans. J Cell Sci 122:1963–1969PubMedCrossRefGoogle Scholar
  27. Han G-S, Siniossoglou S, Carman G (2007) The cellular functions of the yeast lipin homologue Pah1p are dependent on its phosphatidate phosphatase activity. J Biol Chem 51:37026–37035CrossRefGoogle Scholar
  28. Huang J-C, Piater LA, Dubery IA (2012) Identification and characterization of a differentially expressed NAC transcription factor gene in MAMP-treated Arabidopsis thaliana. Physiol Molec Plant Pathol 80:19–27CrossRefGoogle Scholar
  29. Jackson S, Chen Z (2009) Genomic and expression plasticity of polyploidy. Curr Opin Plant Biol 13:1–7CrossRefGoogle Scholar
  30. Jacob T, Ritchie S, Assmann S, Gilroy S (1999) Abscisic acid signal transduction in guard cells is mediated by phospholipase D activity. Proc Natl Acad Sci USA 96:12192–12197PubMedCrossRefGoogle Scholar
  31. Jalali B, Bhargava S, Kamble A (2006) Signal transduction and transcriptional regulation of plant defence responses. Phytopathology 154:65–74CrossRefGoogle Scholar
  32. Klosterman S, Atallah Z, Vallad G, Subbarao K (2009) Diversity, pathogenicity, and management of Verticillium species. Annu Rev Phytopathol 47:39–62PubMedCrossRefGoogle Scholar
  33. Koorneef A, Pieterse C (2008) Cross talk in defence signaling. Plant Physiol 146:839–844CrossRefGoogle Scholar
  34. Larionov A, Krause A, Miller W (2005) A standard curve based method for relative real time PCR data processing. BMC Bioinform 6:62–77CrossRefGoogle Scholar
  35. Leon-Reyes A, Spoel S, de Lange E, Abe H, Kobayashi M, Tsuda S, Millenaar F, Welschen R, Ritsema T, Pieterse C (2009) Ethylene modulates the role of nonexpressor of pathogenesis-related genes1 in cross talk between salicylate and jasmonate signaling. Plant Physiol 149:1797–1809PubMedCrossRefGoogle Scholar
  36. Li M, Hong Y, Wang X (2009) Phospholipase D- and phosphatidic acid-mediated signaling in plants. Biochim Biophys Acta 1791:927–935PubMedCrossRefGoogle Scholar
  37. Liu G-H, Gerace L (2009) Sumoylation regulates nuclear localization of lipin-1α in neuronal cells. PLoS One 4:e7031. doi: 10.1371/journal.pone.0007031 PubMedCrossRefGoogle Scholar
  38. Lorenzo O, Solano R (2005) Molecular players regulating the jasmonate signalling network. Curr Opin Plant Biol 8:532–540PubMedCrossRefGoogle Scholar
  39. Maleck K, Levine A, Eulgem T, Morgan A, Schmidt J, Lawton K, Dangl J, Dietrich R (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nature 26:403–410Google Scholar
  40. Mietkiewska E, Siloto RMP, Dewald J, Shah S, Brindley DN, Weselake RJ (2011) Lipins from plants are phosphatidate phosphatases that restore lipid synthesis in a pah1Δ mutant strain of Saccharomyces cerevisiae. FEBS J 278:764–775PubMedCrossRefGoogle Scholar
  41. Moore R, Purugganan M (2005) The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol 8:122–128PubMedCrossRefGoogle Scholar
  42. Munnik T (2001) Phosphatidic acid an emerging plant lipid second messenger. Trends Plant Sci 6:227–233PubMedCrossRefGoogle Scholar
  43. Murray M, Thompson W (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325PubMedCrossRefGoogle Scholar
  44. Nakamura Y, Koizumi R, Shui G, Shimojima M, Wenk M, Ito T, Ohta H (2009) Arabidopsis lipins mediate eukaryotic pathway of lipid metabolism and cope critically with phosphate starvation. Proc Natl Acad Sci USA 106:20978–20983PubMedCrossRefGoogle Scholar
  45. Ohme-Takagi M, Suzuki K, Shinshi H (2000) Regulation of ethylene-induced transcription of defence genes. Plant Cell Physiol 41:1187–1192PubMedCrossRefGoogle Scholar
  46. Péterfy M, Phan J, Xu P, Reue K (2001) Lipodystrophy in the fld mouse results from mutation of a new gene encoding a nuclear protein, lipin. Nature Genet 27:121–124PubMedCrossRefGoogle Scholar
  47. Péterfy M, Phan J, Reue K (2005) Alternatively spliced lipin isoforms exhibit distinct expression pattern, subcellular localization, and role in adipogenesis. J Biol Chem 280:32883–32889PubMedCrossRefGoogle Scholar
  48. Péterfy M, Harris T, Fujita N, Reue K (2010) Insulin-stimulated interaction with 14-3-3 promotes cytoplasmic localization of lipin-1 in adipocytes. J Biol Chem 285:3857–3864PubMedCrossRefGoogle Scholar
  49. Phillips SM, Dubery IA, van Heerden H (2012) Molecular characterization of an elicitor- responsive Armadillo repeat gene from cotton. Mol Biol Rep 39:8513–8523PubMedCrossRefGoogle Scholar
  50. Phillips SM, Dubery IA, van Heerden H (2013) Molecular characterization of an elicitor-responsive lectin receptor-like kinase gene (GhLec-RK2) from cotton, Gossypium hirsutum. Plant Mol Biol Rep 31:9–20CrossRefGoogle Scholar
  51. Reue K, Zhang P (2008) The lipin family: dual roles in lipid biosynthesis and gene expression. FEBS Lett 582:90–96PubMedCrossRefGoogle Scholar
  52. Rushton P, Reinstädler A, Lipka V, Lippok B, Somssich I (2002) Synthetic plant promoters containing defined regulatory elements provide novel insights into pathogen- and wound-induced signalling. Plant Cell 14:749–762PubMedCrossRefGoogle Scholar
  53. Salmon A, Flagel L, Ying B, Udall J, Wendel J (2010) Homoeologous nonreciprocal recombination in polyploid cotton. New Phytol 186:123–134PubMedCrossRefGoogle Scholar
  54. Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbour Laboratory Press, Cold Spring HarbourGoogle Scholar
  55. Senchina D, Alvarez I, Cronn R, Liu B, Rong J, Noyes R, Paterson A, Wing R, Wilkins T, Wendel J (2003) Rate variation among nuclear genes and the age of polyploidy in Gossypium. Mol Biol Evol 20:633–643PubMedCrossRefGoogle Scholar
  56. Small R, Wendel J (2002) Differential evolutionary dynamics of duplicated paralogous Adh loci in allotetraploid cotton (Gossypium). Mol Biol Evol 19:597–607PubMedCrossRefGoogle Scholar
  57. Small R, Ryburn J, Wendel J (1999) Low levels of nucleotide diversity at homoeologous Adh loci in allotetraploid cotton (Gossypium L.). Mol Biol Evol 16:491–501PubMedCrossRefGoogle Scholar
  58. Tamura K, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular Evolutionary Genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCrossRefGoogle Scholar
  59. Testerink C, Munnik T (2005) Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci 10:368–375PubMedCrossRefGoogle Scholar
  60. Udall J (2008) The Gossypium transcriptome. In: Paterson A (ed) Genetics and genomics of cotton. Springer, New York, pp 157–186Google Scholar
  61. Udall J, Swanson J, Nettleton D, Percifield R, Wendel J (2006) A novel approach for characterizing expression levels of genes duplicated by polyploidy. Genetics 173:1823–1827PubMedCrossRefGoogle Scholar
  62. van den Burg H, Takken F (2009) Does chromatin remodeling mark systemic acquired resistance? Trends Plant Sci 14:286–294PubMedCrossRefGoogle Scholar
  63. van Deynze A, Stoffel K, Lee M, Wilkins T, Kozik A, Cantrell R, Yu J, Kohel R, Stelly D (2009) Sampling nucleotide diversity in cotton. BMC Plant Biol 9:125PubMedCrossRefGoogle Scholar
  64. Walther D, Brunnemann R, Selbig J (2007) The regulatory code for transcriptional response diversity and its relation to genome structural properties in A. thaliana. PLoS Genet 3:e11PubMedCrossRefGoogle Scholar
  65. Wendel J (2000) Genome evolution in polyploids. Plant Mol Biol 42:225–249PubMedCrossRefGoogle Scholar
  66. Wendel J, Cronn R (2003) Polyploidy and the evolutionary history of cotton. Adv Agron 78:139–186CrossRefGoogle Scholar
  67. Wong M, Medrano J (2005) Real-time PCR for mRNA quantification. Biotech 39:75–85CrossRefGoogle Scholar
  68. Wyrick J, Young R (2002) Deciphering gene expression regulatory networks. Curr Opin Genet Dev 12:130–136PubMedCrossRefGoogle Scholar
  69. Yamaguchi T, Minami E, Ueki J, Shibuya N (2005) Elicitor-induced activation of phospholipases plays an important role for the induction of defence responses in suspension-cultured rice cells. Plant Cell Physiol 46:579–587PubMedCrossRefGoogle Scholar
  70. Yoo M-J, Szadkowski E, Wendel JH (2013) Homeoelog expression bias and expression level dominance in allopolyploid cotton. Heredity 110:171–180PubMedCrossRefGoogle Scholar
  71. Zwiegelaar M (2003) DDRT-PCR analysis of defence-related gene induction in cotton. RAU University, DissertationGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Sonia M. Phillips
    • 1
    • 2
  • Ian A. Dubery
    • 1
    Email author
  • Henriette van Heerden
    • 1
    • 3
  1. 1.Department of BiochemistryUniversity of JohannesburgAuckland ParkSouth Africa
  2. 2.Department of Plant ScienceUniversity of PretoriaPretoriaSouth Africa
  3. 3.Department of Veterinary Tropical DiseasesUniversity of PretoriaOnderstepoortSouth Africa

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