Abstract
Phospholipase D (PLD) and its product phosphatidic acid play important roles in the regulation of plant growth, development, and stress responses. The genome database analysis has revealed PLD family in Arabidopsis, rice, poplar and grape. In this study, we report a genomic analysis of 18 putative soybean (Glycine max) PLD genes (GmPLDs), which exist in the 14 of 20 chromosomes. GmPLDs were grouped into six types, α(3), β(4), γ, δ(5), ε(2), and ζ(3), based on gene architectures, protein domains, evolutionary relationship, and sequence identity. These GmPLDs contained two HKD domains, PX/PH domains (for GmPLDζs), and C2 domain (for the other GmPLDs). The expression patterns analyzed by quantitative reverse transcription PCR demonstrated that GmPLDs were expressed differentially in various tissues. GmPLDα1, α2, and β2 were highly expressed in most tissues, whereas GmPLDδ5 was only expressed in flowers and GmPLDζ1 was predominantly expressed in flowers and early pods. The expression of GmPLDα1 and α2 was increased and that of GmPLDγ was decreased by salt stress. GmPLDα1 protein expressed in E. coli was active under the reaction conditions for both PLDα and PLDδ, hydrolyzing the common membrane phospholipids phosphatidylcholine, phosphatidylethanolamine, and phosphatidylglycerol. The genomic analysis for soybean PLD family provides valuable data for further identity and characterization of their functions.
Similar content being viewed by others
References
Abousalham A, Teissere M, Gardies AM, Verger R, Noat G (1995) Phospholipase D from soybean (Glycine max L.) suspension-cultured cells: purification, structural and enzymatic properties. Plant Cell Physiol 36:989–996
Cheever ML, Sato TK, de Beer T, Kutateladze TG, Emr SD, Overduin M (2001) Phox domain interaction with PtdIns(3)P targets the Vam t-SNARE to vacuole membranes. Nat Cell Biol 3:613–618
Dhonukshe P, Laxult AM, Goedhart J, Gadella TWJ, Munnik T (2003) Phospholipase D activation correlates with microtubule remorganization in living plant cells. Plant Cell 15:2666–2679
Elias M, Potocky M, Cvrckova F, Zarsky V (2002) Molecular diversity of phospholipase D in angiosperms. BMC Genomics 3:2
Hiroaki H, Ago T, Ito T, Sumimoto H, Kohda D (2001) Solution structure of the PX domain, a target of the SH3 domain. Nat Struct Biol 8:526–530
Hong Y, Pan X, Welti R, Wang X (2008) Phospholipase Dα3 is involved in the hyperosmotic response in Arabidopsis. Plant Cell 20:803–816
Hong Y, Devaiah SP, Bahn SC, Thamasandra BN, Li M, Welti R, Wang X (2009) Phospholipase Dε and phosphatidic acid enhance Arabidopsis nitrogen signaling and growth. Plant J 58:376–387
Hong Y, Zhang W, Wang X (2010) Phospholipase D and phosphatidic acid signalling in plant response to drought and salinity. Plant Cell Environ 33:627–635
Kim DU, Roh TY, Lee J, Noh JY, Jang YJ, Hoe KL, Yoo HS, Choi MU (1999) Molecular cloning and functional expression of a phospholipase D from cabbage (Brassica oleracea var capitata). Biochim Biophys Acta 1437:409–414
Laxalt AM, ter Riet B, Verdonk JC, Parigi L, Tameling WI, Vossen J, Haring M, Musgrave A, Munnik T (2001) Characterization of five tomato phospholipase D cDNAs: rapid and specific expression of LePLDbeta1 on elicitation with xylanase. Plant J 26:237–247
Lein W, Saalbach G (2001) Cloning and direct G-protein regulation of phospholipase D from tobacco. Biochim Biophys Acta 1530:172–183
Lemmon MA, Ferguson KM (2000) Signal-dependent membrane targeting by pleckstrin homology (PH) domains. Biochem J 350:1–18
Li G, Xue HW (2007) Arabidopsis PLDzeta2 regulates vesicle trafficking and is required for auxin response. Plant Cell 19:281–295
Li W, Li M, Zhang W, Welti R, Wang X (2004) The plasma membrane-bound phospholipase Ddelta enhances freezing tolerance in Arabidopsis thaliana. Nat Biotechnol 22:427–33
Li M, Welti R, Wang X (2006) Quantitative profiling of Arabidopsis polar glycerolipids in response to phosphorus starvation: role of phospholipase Dζ1 and ζ2 in phosphatidylcholine hydrolysis and digalactosyldiacylglycerol accumulation in phosphorus-starved plants. Plant Physiol 142:750–761
Li G, Lin F, Xue H (2007) Genome-wide analysis of the phospholipase D family in Oryza sativa and functional characterization of PLDβ1 in seed germination. Cell Res 17:881–894
Li M, Hong Y, Wang X (2009) Phospholipase D- and phosphatidic acid-mediated signaling in plants. Biochim Biophys Acta 1791:927–935
Li Q, Zhang C, Yang Y, Hu X (2010) Genome-wide and molecular evolution analyses of the phospholipase D gene family in poplar and grape. BMC Plant Biol 10:117–131
Libault M, Thibivilliers S, Bilgin DD, Radwan O, Benitez M, Clough SJ, Stacey G (2008) Identification of four soybean reference genes for gene expression normalization. Plant Genome 1:44–54
McGee JD, Roe JL, Sweat TA, Wang X, Guikema JA, Leach JE (2003) Rice phospholipase D isoforms show differential cellular location and gene induction. Plant Cell Physiol 44:1013–1026
Mishra G, Zhang W, Deng F, Zhao J, Wang X (2006) A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidopsis. Science 312:264–266
Munnik T (2001) Phosphatidic acid: an emerging plant lipid second messenger. Trends Plant Sci 6:227–233
Nalefski EA, Falke JJ (1996) The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci 5:2375–2390
Ohashi Y, Oka A, Rodrigues-Pousada R, Possenti M, Ruberti I, Morelli G, Aoyama T (2003) Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation. Science 300:1427–1430
Ponting CP (1996) Novel domains in NADPH oxidase subunits, sorting nexins, and PtdIns 3-kinases: binding partners of SH3 domains. Protein Sci 5:2353–2357
Qin C, Wang X (2002) The Arabidopsis phospholipase D family. Plant Physiol 128:1057–1068
Qin W, Pappan K, Wang X (1997) Molecular heterogeneity of phospholipase D (PLD). Cloning of PLDgamma and regulation of plant PLDgamma, -beta, and -alpha by polyphosphoinositides and calcium. J Biol Chem 272:28267–28273
Qin C, Li M, Qin W, Bahn SC, Wang C, Wang X (2006) Expression and characterization of Arabidopsis phospholipase Dγ2. Biochim Biophys Acta 1761:1450–1458
Rizo J, Sudhof TC (1998) C2-domain, structure and function of a universal Ca2+-binding domain. J Biol Chem 273:15879–15882
Schmutz J, Cannon SB, Jackson SA et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183
Shen P, Wang R, Jing W, Zhang W (2011) Rice phospholipase Dα is involved in salt tolerance by the mediation of H+-ATPase activity and transcription. J Integr Plant Biol 53:289–299
Shultz JL, Kurunam D et al (2006) The soybean genome database (SoyGD): a browser for display of duplicated, polyploid, regions and sequence tagged sites on the integrated physical and genetic maps of Glycine max. Nucleic Acids Res 34:D758–D765
Testerink C, Munnik T (2005) Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci 10:368–375
Ueki J, Morioka S, Komari T, Kumashiro T (1995) Purification and characterization of phospholipase D (PLD) from (Oryza sativa L.) and cloning of cDNA for PLD from rice and maize (Zea mays L.). Plant Cell Physiol 36:903–914
Wang X (2005) Regulatory functions of phospholipase D and phosphatidic acid in plant growth, development, and stress responses. Plant Physiol 139:566–573
Wang X, Dyer JH, Zheng L (1993) Purification and immunological analysis of phospholipase D from castor bean endosperm. Arch Biochem Biophys 306:486–494
Wang X, Xu L, Zheng L (1994) Cloning and expression of phosphatidylcholine-hydrolyzing phospholipase D from Ricinus communis L. J Biol Chem 269:20312–20317
Wang C, Zien CA, Afitlhile M, Welti R, Hildebrand DF, Wang X (2000) Involvement of phospholipase D in wound-induced accumulation of jasmonic acid in Arabidopsis. Plant Cell 12:2237–2246
Whitaker BD, Smith DL, Green KC (2001) Cloning, characterization and functional expression of a phospholipase D alpha cDNA from tomato fruit. Physiol Plant 112:87–94
Yamaguchi T, Kuroda M, Yamakawa H, Ashizawa T, Hirayae K, Kurimoto L, Shinya T, Shibuya N (2009) Suppression of a phospholipase D gene, OsPLDβ1, activates defense responses and increases disease resistance in rice. Plant Physiol 150:308–319
Yu L, Nie J, Cao C, Jin Y, Yan M, Wang F, Liu J, Xiao Y, Liang Y, Zhang W (2010) Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New Phytol 188:762–773
Zhang W, Wang C, Qin C, Wood T, Olafsdottir G, Welti R, Wang X (2003) The oleate-stimulated phospholipase D, PLDδ, and phosphatidic acid decrease H2O2-induced cell death in Arabidopsis. Plant Cell 15:2285–2295
Zhang W, Qin C, Zhao J, Wang X (2004) Phospholipase Dα1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling. Proc Natl Acad Sci USA 101:9508–9513
Zhang W, Wan X, Hong Y, Li W, Wang X (2010) Plant Phospholipase D. In: Munnik T (ed) Lipid signaling in plants. Plant Cell Monographs, vol 16. Springer, Berlin, pp 39–62
Zhao J, Wang X (2004) Arabidopsis phospholipase Dα1 interacts with the heterotrimeric G-protein α-subunit through a motif analogous to the DRY motif in G-protein-coupled receptors. J Biol Chem 279:1794–1800
Zheng L, Krishnamoorthi R, Zockievoshi M, Wang X (2001) Distinct Ca2+ binding properties of novel C2 domains of plant phospholipase Dα and β. J Biol Chem 275:19700–19706
Acknowledgment
The work is supported by grants from Ministry of Science and Technology in China, Ministry of Education in China (KYT201001), and Jiangsu province (200910 and PAPD) to W. Zhang.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhao, J., Zhou, D., Zhang, Q. et al. Genomic analysis of phospholipase D family and characterization of GmPLDαs in soybean (Glycine max). J Plant Res 125, 569–578 (2012). https://doi.org/10.1007/s10265-011-0468-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-011-0468-0