SEC14 phospholipid transfer protein is involved in lipid signaling-mediated plant immune responses in Nicotiana benthamiana

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Kiba, Akinori ^a   Galis, Ivan ^b   Hojo, Yuko ^b   Ohnishi, Kouhei ^a   Yoshioka, Hirofumi ^c   Hikichi, Yasufumi ^a  

^a KOCHI UNIVERSITY   (Japan)

^b OKAYAMA UNIVERSITY   (Japan)

^c NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DIACYLGLYCEROL; DIACYLGLYCEROL KINASE; JASMONIC ACID; PHOSPHATIDIC ACID; PHOSPHOLIPASE C; PHOSPHOLIPASE D; PHOSPHOLIPID TRANSFER PROTEIN; PHYTOHORMONE; PROTEIN SEC14; UNCLASSIFIED DRUG; CYCLOPENTANE DERIVATIVE; ISOLEUCINE; JASMONOYL-ISOLEUCINE; OXYLIPIN; VEGETABLE PROTEIN;

ARTICLE; BACTERIUM ISOLATE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; GENE SILENCING; NICOTIANA BENTHAMIANA; NONHUMAN; PLANT GENE; PLANT IMMUNITY; PLASMID; PR 4 GENE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RALSTONIA SOLANACEARUM; REAL TIME POLYMERASE CHAIN REACTION; SEC14 GENE; SIGNAL TRANSDUCTION; SYNTHESIS; ANALOGS AND DERIVATIVES; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; LIPID METABOLISM; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; TOBACCO;

CYCLOPENTANES; GENE EXPRESSION REGULATION, PLANT; IMMUNITY, INNATE; ISOLEUCINE; LIPID METABOLISM; OXYLIPINS; PHOSPHOLIPID TRANSFER PROTEINS; PLANT DISEASES; PLANT PROTEINS; RALSTONIA SOLANACEARUM; SIGNAL TRANSDUCTION; TOBACCO;

EID: 84901363538     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098150     Document Type: Article

References (63)

1. Jones DA, Takemoto D (2004) Plant innate immunity - direct and indirect recognition of general and specific pathogen-associated molecules. Curr Opin Immunol 16: 48-62. (Pubitemid 38198117)
2. Gohre V, Robatzek S (2008) Breaking the barriers: Microbial effector molecules subvert plant immunity. Ann Rev Phytopathol 46: 189-215.
3. Zipfel C (2008) Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol 20: 10-16.
4. Jones JD, Dangl JL (2006) The plant immune system. Nature 444: 323-329. (Pubitemid 44764102)
5. Boller T, Felix G (2009). A renaissance of elicitors: perception of microbeasociated molecular pattern and danger signals by pattern-recognition receptors. Ann Rev Plant Bioliol 60: 379-406.
6. Nurnberger T, Brunner F, Kemmerling B, Piater L (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198: 249-266. (Pubitemid 38406948)
7. Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, et al. (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19: 1065-1080. (Pubitemid 46953247)
8. Gechev TS, Hille J (2005) Hydrogen peroxide as a signal controlling plant programmed cell death. J. Cell Science 168: 17-20. (Pubitemid 40111052)
9. Asai S, Yoshioka H (2009) Nitric oxide as a partner of reactive oxygen species participates in disease resistance to necrotrophic pathogen Botrytis cinerea in Nicotiana benthamiana. Mol Plant-Microbe Interact 22: 619-629.
10. Yoshioka H, Asai S, Yoshioka M, Kobayashi M (2009) Molecular mechanisms of generation for nitric oxide and reactive oxygen species, and role of the radical burst in plant immunity. Mol Cells 28: 321-329.
11. 2accumulation and resistance to Phytophthora infestans. Plant Cell 15: 706-718.
12. Asai S, Ohta K, Yoshioka H (2008) MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana. Plant Cell 20: 1390-1406. (Pubitemid 352844190)
13. Jin H, Liu Y, Yang KY, Kim CY, Baker B, et al. (2003) Function of mitogen-activated protein kinase pathway in N gene-mediated resistance in tobacco. Plant J 33: 719-731. (Pubitemid 36325914)
14. Ekengren SK, Liu Y, Schiff M, Dinesh-Kumar SP, Martin GB (2003) Two MAPK cascades, NPR1, and TGA transcription factors play a role in Pto-mediated disease resistance in tomato. Plant J 36: 905-917. (Pubitemid 38069776)
15. Pedley KF, Martin GB (2005) Role of mitogen activated protein kinases in plant immunity. Curr Opin Plant Biol 8: 541-547. (Pubitemid 41188190)
16. Pitzschke A, Schikora A, Hirt H (2009) MAPK cascade signaling networls in plant defense. Curr Opin Plant Biol 12: 421-426.
17. Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5: 325-331. (Pubitemid 34695970)
18. Robert-Seilaniantz A, Navarro L, Bari R, Jonathan DG (2007) Pathologocal hormone imbalances. Curr Opin Plant Biol 10: 372-379.
19. Laxalt AM, Riet BT, Verdonk JC, Parigi L, Tameling WIL, et al. (2001) Characterization of five tomato phospholipase D cDNA: rapid and specific expression of LePLD b1 on elicitation with xylanase. Plant J 26: 237-247. (Pubitemid 32623530)
20. Yamaguchi T, Minami E, Ueki J, Shibuya N (2005) Elicitor-induced activation of phospholipases plays an important role for the induction of defense responses in suspension-cultured rice cells. Plant Cell Physiol 46: 579-587. (Pubitemid 40640932)
21. Young SA, Wang X, Leach JE (1996) Changes in the plasma membrane distribution of rice phospholipase D during resistant interactions with Xanthomanas oryzae pv. oryzae. Plant Cell 8: 1079-1090. (Pubitemid 26329827)
22. Vossen JH, Abd-El-Haliem A, Fradin EF, van den Berg GC, Ekengren SK, et al. (2010) In tomato plants, two isoforms of PLC, SlPLC4 and SlPLC6 are required for Cf-4 dependent immune response, whereas SlPLC may have a role in more general immune responses. Plant J 62: 224-239.
23. van der Luit AH, Piatti T, von Doorn A, Musgrave A, Felix G, et al. (2000) Elicitation of suspension-cultured tomato cells triggers the formation of phosphatidic acid and diacylglycerol pyrophosphate. Plant Physiol 123: 1507-1515. (Pubitemid 30656706)
24. de Jong CF, Laxalt AM, Bargmann BOR, de Wit PJGM, Joosten MHA, et al. (2004) Phosphatidic acid accumulation is an early response in the Cf-4/Avr4 interaction. Plant J 39: 1-12. (Pubitemid 38893574)
25. Kiba A, Nakano M, Vincent-Pope P, Takahashi H, Sawasaki T, et al. (2012) A novel Sec14 phospholipid transfer protein from Nicotiana benthamiana is upregulated in response to Ralstonia solanacearum infection, pathogen associated molecular patterns and effector molecules and involved in plant immunity. J Plant Physiol 169: 1017-1022.
26. Bankaitis VA, Aitken JF, Cleves AE, Dowhan W (1990) An essential role for a phospholipid transfer protein in yeast Golgi function. Nature 347: 561-562.
27. Bankaitis VA, Mousley CJ, Schaaf G (2010) The Sec14 superfamily and mechanisms for crosstalk between lipid metabolism and lipid signaling. Trend Biochem Sci 35: 150-60.
28. Bankaitis VA, Vincent P, Merkulova M, Tyeryar K, Liu Y (2007) Phosphatidylinositol transfer proteins and functional specification of lipid signaling pools. Adv Enzyme Reg 47: 27-40 (Pubitemid 47302061)
29. Ohashi M, de Vries JK, Frank R, Snoek G, Bankaitis VA, et al. (1995) A role for phosphatidylinositol transfer protein in secretory vesicle formation. Nature 377: 544-547.
30. Simon JP, Morimoto T, Bankaitis VA, Gottlieb TA, Ivanov IE, et al. (1998) An essential role for phosphatidylinositol transfer protein in the scission of COPI-coated vesicles from trans-Golgi network. Proc Natl Acad Sci USA 95: 11181-11186. (Pubitemid 28450102)
31. Philips SE, Vincent P, Rizzieri KE, Schaaf G, Bankaitis VA, et al. (2006) The diverse biological functions of phosphatidylinositol transfer proteins in eukaryotes. Biochem Mol Biol 41: 21-49. (Pubitemid 43214656)
32. Maimbo M, Ohnishi K, Hikichi Y, Yoshioka H, Kiba A (2007) Induction of a small heat shock protein and its functional roles in Nicotiana Plants in the defense response against Ralstonia solanacearum. Plant Physiol 145: 1588-1599. (Pubitemid 350276778)
33. Nakano M, Nishihara M, Yoshioka H, Takahashi H, Sawasaki T, et al.(2013) Suppression of DS1 phosphatidic acid phosphatase confirms resistance to Ralstonia solanacearum in Nicotiana benthamiana. PLoS One 8, e75124.
34. Huitema E, Vleeshouwers VGAA, Cakir C, Kamoun S, Govers F (2005) Differences in intensity and specificity of hypersensitive response induction in Nicotiana spp. by INF1, INF2A, and INF2B of Phytophthora infestans. Mol Plant-Microbe Interact 18: 183-193. (Pubitemid 40263613)
35. Maimbo M, Ohnishi K, Hikichi Y, Yoshioka H, Kiba A (2010) S-glycoproteinlike protein regulates defense responses in Nicotiana plants against Ralstonia solanacearum. Plant Physiol. 152, 2023-2035.
36. Katou S, Yamamoto A, Yoshioka H, Kawakita K, Doke N (2003) Functional analysis of potato mitogen-activated protein kinase kinase, StMEK1. J Gen Plant Pathol 69: 161-168.
37. Fukumoto K, Alamgir KMd, Yamashita Y, Mori IC, Matsuura H, et al. (2013). Response of rice to insect elicitors and the role of OsJAR1 in wound and herbivory-induced JA-Ile accumulation. J Integ Plant Biol 55: 775-784.
38. Munnik T, Musgrave A, de Vrije T (1994) Rapid turnover of polyphosphoinositides in carnation flower petals. Planta 193: 89-98. (Pubitemid 2043597)
39. Munnik T, Irvine RF, Musgrave A (1994) Rapid turnover of phosphatidylinositol 3-phosphate in the green alga Chamydomopnas eugametos: signs of phosphatidylinositol 3-kinase oathway in lower plants? Biochem J 298: 269-273. (Pubitemid 24072465)
40. Munnik T, Van Himbergen JAJ, Ter Riet B, Braun FJ, Irvine RF, et al. (1998) Deatiled analysis of the turnover of polyphosphoinositides and phosphatidic acid upon activation of phospholipase C and D in Chamydomopnas cells treated with non-permeabilizing concentration of mastoparan. Planta 207: 133-145. (Pubitemid 29059826)
41. Zien CA, Wang C, Wang X, Welti R (2001) In vivo substrates and the contribution of the common phospholipase Da, to wound-induced metabolism of lipids in Arabidopsis. Biochim Biophys Acta 1530: 236-248. (Pubitemid 32182433)
42. Bligh EG, Dyer WJ (1959) A rapid method for total lipid extraction and purification. Can J Biochem Physiol 37: 911-917.
43. Munnik T, Meijer HJG, Riet B, Hirt H, Frank W, et al. (2000) Hyperosmotic stress stimulates phospholipase D activity and elevates the levels of phosphatidic acid and diacylglycerol pyrophosphate. Plant J 22: 147-154. (Pubitemid 30308407)
44. Munnik T (2001) Phosphatidic acid: an emerging plant lipid second messenger Trend Plant Sci 6: 227-233.
45. Drobak BK, Watkins PAC, Valenta R, Dove SK, Liioyd CW, et al. (1994) Inhibition of plant plasma membrane phosphoinositide phospholipase C by the actin-binding protein, profilin. Plant J 6: 389-400.
46. Testerink CT, Munnik T (2005) Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trend Plant Sci 10: 1360-1385.
47. Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: An Arabidopsis Gene Required for Jasmonate-Regulated Defense and Fertility. Science 280: 1091-1094. (Pubitemid 28234953)
48. Pejchar P, Potocky M, Novotna Z, Veselkova S, Kocourkova D, et al. (2010) Aluminium ions inhibit the formation of diacylglycerol generated by phosphatidylcholine-hydrolysing phospholipase C in tobacco cells. New Phytol 188: 150-160.
49. Helling D, Possart A, Cottier S, Klahre U, Kost B (2006) Pollen tube tip growth depends on plasma membrane polarization mediated by tobacco PLC3 activity and endocytic membrane recycling. Plant Cell 18: 3519-3534. (Pubitemid 46464909)
50. Zhang Y, Zhu H, Zhang Q, Li M, Yan M, et al. (2009) Phospholipase Dα1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21: 2357-2377.
51. 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 U S A 101: 9508-9513. (Pubitemid 38812905)
52. Laxalt AM, Raho N, ten Have A, Lamattina L (2007) Nitric oxide is critical for inducing phosphatidic acid accumulation in xylanase-elicited tomato cells. J Biol Chem 282: 21160-21168. (Pubitemid 47099956)
53. Testerink C, Larsen BP, van der Does D, van Himbergen JAJ, Munnik T (2007) Phosphatidic acid binds to and inhibits the activity of Arabidopsis CTR1. J Exp Bot 58: 3905-3914.
54. Wang C, Zien CA, Afitlhile M, Welti R, Hildebrand DF, et al. (2000) Involvement of phospholipase D in wound-induced accumulation of jasmonic acid in Arabidopsis. Plant Cell 12: 2237-2246. (Pubitemid 32053406)
55. Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nature Chem Biol5: 308-316.
56. Vincent P, Chua M, Nogue F, Fairbrother A, Mekeel H, et al. (2005) A Sec14p-nodulin domain phosphatidylinositol transfer protein polarizes membrane growth of Arabidopsis thaliana root hairs. J Cell Bioliol 168: 801-812. (Pubitemid 40328163)
57. Peterman TK, Ohol YM, McReynolds LJ, Luna EJ (2004) Patellin1, a novel Sec14-like protein, localizes to the cell plate and binds phosphoinositides. Plant Physiol 136: 3080-94. (Pubitemid 41096307)
58. Monks DE, Aghoram K, Courtney PD, DeWald DB, Dewey RE (2001) Hyperosmotic stress induces the rapid phosphorylation of a soybean phosphatidylinositol transfer protein homolog through activation of the protein kinases SPK1 and SPK2. Plant Cell 13: 1205-1219. (Pubitemid 32480652)
59. Schaaf G, Ortlund EA, Tyeryar KR, Mousley CJ, Ile KE, et al. (2008) Functional anatomy of phospholipid binding and regulation of phosphoinositide homeostasis by proteins of the sec14 superfamily. Molular Cell 29: 191-206. (Pubitemid 351172821)
60. Munnik T, Testerink C (2009) Plant phospholipid signaling: "in a nutshell". J Lipid Res S260-S265.
61. Wimalasekera R, Pejchar P, Holk A, Martinec J, Scherer GF (2010) Plant phosphatidylcholine-hydrolyzing phospholipases C NPC3 and NPC4 with roles in root development and brassinolide signaling in Arabidopsis thaliana. Molecular Plant 3: 610-25.
62. Toyoda K, Shiraishi T, Yoshioka H, Yamada T, Ichinose Y, et al. (1992) Regulation of polyphosphoinositide metabolism in peaplasma membrane by elicitor and suppressor from a pea pathogen Mycosphaerella pinodes. Plant Cell Physiol 33: 445-552.
63. Toyoda K, Shiraishi T, Yoshioka H, Yamada T, Ichinose Y, et al. (1993) Regulation of polyphosphoinositide metabolism in pea in response to fungalsignals. Plant Cell Physiol 34: 729-735.