Molecular diversity of phospholipase D in angiosperms

BackgroundThe phospholipase D (PLD) family has been identified in plants by recent molecular studies, fostered by the emerging importance of plant PLDs in stress physiology and signal transduction. However, the presence of multiple isoforms limits the power of conventional biochemical and pharmacological approaches, and calls for a wider application of genetic methodology.ResultsTaking advantage of sequence data available in public databases, we attempted to provide a prerequisite for such an approach. We made a complete inventory of the Arabidopsis thaliana PLD family, which was found to comprise 12 distinct genes. The current nomenclature of Arabidopsis PLDs was refined and expanded to include five newly described genes. To assess the degree of plant PLD diversity beyond Arabidopsis we explored data from rice (including the genome draft by Monsanto) as well as cDNA and EST sequences from several other plants. Our analysis revealed two major PLD subfamilies in plants. The first, designated C2-PLD, is characterised by presence of the C2 domain and comprises previously known plant PLDs as well as new isoforms with possibly unusual features-catalytically inactive or independent on Ca2+. The second subfamily (denoted PXPH-PLD) is novel in plants but is related to animal and fungal enzymes possessing the PX and PH domains.ConclusionsThe evolutionary dynamics, and inter-specific diversity, of plant PLDs inferred from our phylogenetic analysis, call for more plant species to be employed in PLD research. This will enable us to obtain generally valid conclusions.

[1]  T. Südhof,et al.  C2-domains, Structure and Function of a Universal Ca2+-binding Domain* , 1998, The Journal of Biological Chemistry.

[2]  S. Karlin,et al.  Prediction of complete gene structures in human genomic DNA. , 1997, Journal of molecular biology.

[3]  Thomas L. Madden,et al.  BLAST 2 Sequences, a new tool for comparing protein and nucleotide sequences. , 1999, FEMS microbiology letters.

[4]  G. F. Barry.  The use of the Monsanto draft rice genome sequence in research. , 2001, Plant physiology.

[5]  Xuemin Wang,et al.  A novel phospholipase D of Arabidopsis that is activated by oleic acid and associated with the plasma membrane. , 2001, Plant physiology.

[6]  K. Chapman,et al.  Emerging physiological roles for N-acylphosphatidylethanolamine metabolism in plants: signal transduction and membrane protection. , 2000, Chemistry and physics of lipids.

[7]  T. Munnik.  Phosphatidic acid: an emerging plant lipid second messenger. , 2001, Trends in plant science.

[8]  F. Salamini,et al.  Water Deficit Triggers Phospholipase D Activity in the Resurrection Plant Craterostigma plantagineum , 2000, Plant Cell.

[9]  T. Munnik,et al.  Nod factor-induced phosphatidic acid and diacylglycerol pyrophosphate formation: a role for phospholipase C and D in root hair deformation. , 2001, The Plant journal : for cell and molecular biology.

[10]  D. Hanahan,et al.  A new phospholipide-splitting enzyme specific for the ester linkage between the nitrogenous base and the phosphoric acid grouping. , 1947, The Journal of biological chemistry.

[11]  K. Pappan,et al.  Plant phospholipase Dalpha is an acidic phospholipase active at near-physiological Ca(2+) concentrations. , 1999, Archives of biochemistry and biophysics.

[12]  Xuemin Wang,et al.  Distinct Ca2+ Binding Properties of Novel C2 Domains of Plant Phospholipase Dα and β* , 2000, The Journal of Biological Chemistry.

[13]  Suqin Zheng,et al.  Antisense suppression of phospholipase D alpha retards abscisic acid- and ethylene-promoted senescence of postharvest Arabidopsis leaves. , 1997, The Plant cell.

[14]  C P Ponting,et al.  A novel family of phospholipase D homologues that includes phospholipid synthases and putative endonucleases: Identification of duplicated repeats and potential active site residues , 1996, Protein science : a publication of the Protein Society.

[15]  Xuemin Wang,et al.  Plant Phospholipase Dα Is an Acidic Phospholipase Active at Near-Physiological Ca2+ Concentrations , 1999 .

[16]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[17]  Xuemin Wang.  PLANT PHOSPHOLIPASES. , 2001, Annual review of plant physiology and plant molecular biology.

[18]  G. Saalbach,et al.  Cloning and direct G-protein regulation of phospholipase D from tobacco. , 2001, Biochimica et biophysica acta.

[19]  Peer Bork,et al.  SMART: a web-based tool for the study of genetically mobile domains , 2000, Nucleic Acids Res..

[20]  G. Fiucci,et al.  Phospholipase D: molecular and cell biology of a novel gene family. , 2000, The Biochemical journal.

[21]  X. Wang,et al.  Multiple forms of phospholipase D in plants: the gene family, catalytic and regulatory properties, and cellular functions. , 2000, Progress in lipid research.

[22]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[23]  J. Claverie,et al.  Large-scale statistical analyses of rice ESTs reveal correlated patterns of gene expression. , 1999, Genome research.

[24]  S. Naito,et al.  Molecular cloning and characterization of a cDNA Sequence encoding an ethylene receptor in potato (Solanum tuberosum L.) Plants (Accession No. AF051938). (PGR 99–081) , 1999 .

[25]  T. Munnik,et al.  Phospholipid Signaling in Plants: Holding On to Phospholipase D , 2001, Science's STKE.

[26]  J. Felsenstein.  Inferring phylogenies from protein sequences by parsimony, distance, and likelihood methods. , 1996, Methods in enzymology.

[27]  K. Shinozaki,et al.  Involvement of a novel Arabidopsis phospholipase D, AtPLDdelta, in dehydration-inducible accumulation of phosphatidic acid in stress signalling. , 2001, The Plant journal : for cell and molecular biology.

[28]  B. Whitaker,et al.  Cloning, characterization and functional expression of a phospholipase Dalpha cDNA from tomato fruit. , 2001, Physiologia plantarum.

[29]  W. Qin,et al.  Molecular Cloning and Functional Analysis of Polyphosphoinositide-dependent Phospholipase D, PLDβ, from Arabidopsis* , 1997, The Journal of Biological Chemistry.

[30]  M. Haring,et al.  Characterization of five tomato phospholipase D cDNAs: rapid and specific expression of LePLDbeta1 on elicitation with xylanase. , 2003, The Plant journal : for cell and molecular biology.

[31]  S. Ritchie,et al.  A 90-kD Phospholipase D from Tobacco Binds to Microtubules and the Plasma Membrane , 2001, The Plant Cell Online.

[32]  F. Cvrčková.  Are plant formins integral membrane proteins? , 2000, Genome Biology.

[33]  T. Komari,et al.  Purification and characterization of phospholipase D (PLD) from rice (Oryza sativa L.) and cloning of cDNA for PLD from rice and maize (Zea mays L.). , 1995, Plant & cell physiology.

[34]  T. Munnik,et al.  Phospholipid signalling in plants. , 1998, Biochimica et biophysica acta.

[35]  W. Qin,et al.  Molecular Heterogeneity of Phospholipase D (PLD) , 1997, The Journal of Biological Chemistry.

[36]  L. Zheng,et al.  Cloning and expression of phosphatidylcholine-hydrolyzing phospholipase D from Ricinus communis L. , 1994, The Journal of biological chemistry.

[37]  G. Prestwich,et al.  Identification of a phosphoinositide binding motif that mediates activation of mammalian and yeast phospholipase D isoenzymes , 1999, The EMBO journal.

[38]  C. Ponting,et al.  Phospholipase D regulation and localisation is dependent upon a phosphatidylinositol 4,5-bisphosphate-specific PH domain , 2000, Current Biology.

[39]  J. Falke,et al.  The C2 domain calcium‐binding motif: Structural and functional diversity , 1996, Protein science : a publication of the Protein Society.

[40]  The Arabidopsis Genome Initiative.  Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[41]  G D Schuler,et al.  A workbench for multiple alignment construction and analysis , 1991, Proteins.