Suppression of phospholipase Dγs confers increased aluminum resistance in Arabidopsis thaliana

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Zhao, Jian ^a,b   Wang, Cunxi ^a,f   Bedair, Mohamed ^b   Welti, Ruth ^a   Sumner, Lloyd ^b   Baxter, Ivan ^c,d   Wang, Xuemin ^a,d,e  

^a KANSAS STATE UNIVERSITY   (United States)

^b PLANT BIOLOGY DIVISION   (United States)

^c U S DEPARTMENT OF AGRICULTURE   (United States)

^d DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

^e UNIVERSITY OF MISSOURI ST LOUIS   (United States)

^f MONSANTO COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALUMINUM; GLYCOLIPID; PHOSPHOLIPASE D; PHOSPHOLIPID; RNA; LIPID;

ARABIDOPSIS; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENZYME REPRESSION; GENE DISRUPTION; LIPID COMPOSITION; LIPID PEROXIDATION; MODULATION; MOLECULAR MECHANICS; NONHUMAN; PLANT CELL; PLANT ROOT; RNA INTERFERENCE; ROOT GROWTH; STRESS; WILD TYPE; CHEMISTRY; DRUG ANTAGONISM; DRUG RESISTANCE; ELECTROSPRAY MASS SPECTROMETRY; GENE EXPRESSION REGULATION; METABOLISM; METHODOLOGY; MUTATION; OXIDATIVE STRESS; PLANT;

ALUMINUM; ARABIDOPSIS; DRUG RESISTANCE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GLYCOLIPIDS; LIPID PEROXIDATION; LIPIDS; MUTATION; OXIDATIVE STRESS; PHOSPHOLIPASE D; PHOSPHOLIPIDS; PLANT ROOTS; PLANT SHOOTS; RNA INTERFERENCE; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

EID: 82855172148     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028086     Document Type: Article

References (57)

1. Ma JF, Ryan PR, Delhaize E, (2001) Aluminum tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6: 273-278.
2. Kochian LV, Hoekenga OA, Piñeros MA, (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol 55: 459-493.
3. Larsen PB, Degenhardt J, Tai CY, Stenzler LM, Howell SH, Kochian LV, (1998) Aluminum-resistant Arabidopsis mutants that exhibit altered patterns of aluminum accumulation and organic acid release from roots. Plant Physiol 117: 9-18.
4. Zhang G, Slaski JJ, Archambault DJ, Taylor GJ, (1996) Aluminum-induced alteration in lipid composition of microsomal membrane from an aluminum-resistant and aluminum sensitive cultivar of Triticum aestivum. Physiol Plant 96: 683-691.
5. Zhang G, Slaski JJ, Archambault DJ, Taylor GJ, (1997) Alteration of plasma membrane lipids in aluminum-resistant and aluminum-sensitive wheat genotypes in response to aluminum stress. Physiol Plant 99: 302-308.
6. Yamamoto Y, Kobayashi Y, Devi SR, Rikiishi S, Matsumoto H, (2002) Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiol 128: 63-72.
7. Ryan PR, Liu Q, Sperling P, Dong B, Franke S, et al. (2007) A higher plant delta8 sphingolipid desaturase with a preference for (Z)-isomer formation confers aluminum tolerance to yeast and plants. Plant Physiol 144: 1968-1977.
8. Rounds M, Larsen PB, (2008) Aluminum-dependent root-growth inhibition in Arabidopsis results from AtATR-regulated cell-cycle arrest. Curr Biol 18: 1495-1500.
9. Shen H, He LF, Sasaki T, Yamamoto Y, Zheng SJ, et al. (2005) Citrate secretion coupled with the modulation of soybean root tip under aluminum stress. Up-regulation of transcription, tanslation, and treonine-oriented phosphorylation of plasma membrane H+-ATPase. Plant Physiol 138: 287-296.
10. Yamaguchi M, Sasaki T, Sivaguru M, Yamamoto Y, Osawa H, et al. (2005) Evidence for the plasma membrane localization of Al-activated malate transporter (ALMT1). Plant Cell Physiol 46: 812-816.
11. Ryan PR, Raman H, Gupta S, Horst WJ, Delhaize E, (2009) A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots. Plant Physiol 149: 340-351.
12. Kobayashi Y, Hoekenga OA, Itoh H, Nakashima M, Saito S, et al. (2007) Characterization of AtALMT1 expression in aluminum-inducible malate release and its role for rhizotoxic stress tolerance in Arabidopsis. Plant Physiol 145: 843-852.
13. Stival da Silva AL, Sperling P, Horst WJ, Franke S, Ott C, et al. (2006) A possible role of sphingolipids in the aluminum resistance of yeast and maize. J Plant Physiol 163: 26-38.
14. Sarin S, Gupta V, Gill KD, (1997) Alterations in lipid composition and neuronal injury in primates following chronic aluminium exposure. Biol Trace Elem Res 59: 133-143.
15. Chaffai R, Marzouk B, El Ferjani E, (2005) Aluminum mediates compositional alterations of polar lipid classes in maize seedlings. Phytochemistry 66: 1903-1912.
16. Jones DL, Kochian LV, (1995) Aluminum inhibition of the inositol 1,4,5-trisphosphate signal transduction pathway in wheat roots: A role in aluminum toxicity? Plant Cell 7: 1913-1922.
17. Martinez-Estevez M, Racagni-Di Palma G, Munoz-Sanchez JA, Brito-Argaez L, Loyola-Vargas VM, et al. (2003) Aluminium differentially modifies lipid metabolism from the phosphoinositide pathway in Coffea arabica cells. J Plant Physiol 160: 1297-1303.
18. Ezaki B, Gardner RC, Ezaki Y, Matsumoto H, (2000) Expression of aluminium-induced genes in transgenic Arabidopsis plants can ameliorate aluminium stress and and/or oxidative stress. Plant Physiol 122: 657-665.
19. Ezaki B, Katsuhara M, Kawamura M, Matsumoto H, (2001) Different mechanisms of four aluminum (Al)-resistant transgenes for Al toxicity in Arabidopsis. Plant Physiol 127: 918-927.
20. Yamamoto Y, Kobayashi Y, Matsumoto H, (2001) Lipid peroxidation is an early symptom triggered by aluminium, but not the primary cause of elongation inhibition in pea roots. Plant Physiol 125: 199-208.
21. Vierstra R, Haug A, (1978) The effect of Al3+ on the physical properties of membrane lipids in Thermoplasma acidophilum. Biochem Biophys Res Commun 84: 138-143.
22. Zhao XJ, Sucoff E, Stadelmann EJ, (1987) Al3+ and Ca2+ alteration of membrane permeability of Quercus rubra root cortex cells. Plant Physiol 83: 159-162.
23. Gunsé B, Poschenrieder C, Barceló J, (1997) Water transport properties of roots and root cortical cells in proton- and Al-stressed maize varieties. Plant Physiol 113: 595-602.
24. Delhaize E, Hebb DM, Richards KD, Lin JM, Ryan PR, et al. (1999) Cloning and expression of a wheat (Triticum aestivum L.) phosphatidylserine synthase cDNA. Overexpression in plants alters the composition of phospholipids. J Biol Chem 274: 7082-7088.
25. Li L, Fleming N, (1999) Aluminum fluoride inhibits phospholipase D activation by a GTP-binding protein-independent mechanism. FEBS Lett 458: 419-423.
26. Ramos-Díaz A, Brito-Argáez L, Munnik T, Hernández-Sotomayor SM, (2007) Aluminum inhibits phosphatidic acid formation by blocking the phospholipase C pathway. Planta 225: 393-401.
27. Pejchar P, Pleskot R, Schwarzerová K, Martinec J, Valentová O, et al. (2008) Aluminum ions inhibit phospholipase D in a microtubule-dependent manner. Cell Biol Int 32: 554-556.
28. Quintal-Tun F, Muñoz-Sánchez JA, Ramos-Díaz A, Escamilla-Bencomo A, Martínez-Estévez M, et al. (2007) Aluminium-induced phospholipid signal transduction pathway in Coffea arabica suspension cells and its amelioration by silicic acid. J Inorg Biochem 101: 362-369.
29. Wang X, (2000) Multiple forms of phospholipase D in plants: the gene family, catalytic and regulatory properties, and cellular functions. Prog Lipid Res 39: 109-145.
30. Wang X, (2005) Regulatory functions of phospholipase D and phosphatidic acid in plant growth, development, and stress responses. Plant Physiol 39: 566-573.
31. Hong Y, Pan X, Welti R, Wang X, (2008a) Phospholipase Dα3 is involved in hyperosmotic responses in Arabidopsis. Plant Cell 20: 803-816.
32. Hong Y, Zheng S, Wang X, (2008) Dual functions of phospholipase Dα1 in plant response to drought. Molecular Plant 1: 262-269.
33. Qin W, Pappan K, Wang X, (1997) Molecular heterogeneity of phospholipase D (PLD): cloning of PLDγ and regulation of plant PLDα, β and γ by polyphosphoinositides and calcium. J Biol Chem 272: 28267-28273.
34. Qin C, Li M, Qin W, Bahn SC, Wang C, et al. (2006) Expression and characterization of Arabidopsis phospholipase Dγ 2. Biochim Biophys Acta 1761: 1450-1458.
35. Milla MAR, Butler E, Huete AR, Wilson CF, Anderson Q, et al. (2002) Expressed sequence tag-based gene expression analysis under aluminum stress in rye. Plant Physiol 130: 1706-1716.
36. Schreiner KA, Hoddinott J, Taylor GJ, (1994) Aluminum-induced deposition of (1,3)-glucans (callose) in Triticum aestivum L. Plant Soil 162: 273-280.
37. Jones DL, Blancaflor EB, Kochian LV, Gilroy S, (2006) Spatial coordination of aluminium uptake, production of reactive oxygen species, callose production and wall rigidification in maize roots. Plant Cell Environ 29: 1309-1318.
38. Ezaki B, Suzuki M, Motoda H, Kawamura M, Nakashima S, et al. (2004) Mechanism of gene expression of Arabidopsis glutathione S-transferase, AtGST1, and AtGST11 in response to aluminum stress. Plant Physiol 134: 1672-1682.
39. Welti R, Li W, Li M, Sang Y, Biesiada H, et al. (2002) Profiling membrane lipids in plant stress responses. Role of phospholipase D alpha in freezing-induced lipid changes in Arabidopsis. J Biol Chem 277: 31994-32002.
40. Li M, Welti R, Wang X, (2006) Quantitative profiling of Arabidopsis polar glycerolipids in response to phosphorus starvation. Roles of phospholipases D zeta1 and D zeta2 in phosphatidylcholine hydrolysis and digalactosyldiacylglycerol accumulation in phosphorus-starved plants. Plant Physiol 142: 750-761.
41. Noctor G, Foyer CH, (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49: 249-279.
42. Fan L, Zheng S, Cui D, Wang X, (1999) Subcellular distribution and tissue expression of phospholipase Dalpha, Dbeta, and Dgamma in Arabidopsis. Plant Physiol 119: 1371-1378.
43. Novotna Z, Linek J, Hynek R, Martinec J, Potocky M, et al. (2003) Plant PIP2-dependent phospholipase D activity is regulated by phosphorylation. FEBS Lett 554: 50-54.
44. Cruz-Ramirez A, Oropeza-Aburto A, Razo-Hernandez F, Ramirez-Chavez E, Herrera-Estrella L, (2006) Phospholipase Dζ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Proc Natl Acad Sci USA 103: 6765-6770.
45. Hernandez LE, Cooke DT, (1997) Modifications of the root plasma membrane lipid composition of cadmium-treated Pisum sativum. J Exp Bot 48: 1375-1381.
46. Quartacci MF, Cosi E, Navari-Izzo F, (2001) Lipids and NADPH-dependent superoxide production in plasma membrane vesicles from roots of wheat grown under copper deficiency or excess. J Exp Bot 52: 77-84.
47. Quartacci MF, Pinzino C, Sgherri CLM, Dalla Vecchia F, Navari-Izzo F, (2000) Growth in excess copper induces changes in the lipid composition and fluidity of PSII-enriched membranes in wheat. Physiol Plant 108: 87-93.
48. Ouariti O, Boussama N, Zarrouk M, Cherif A, Ghorbal MH, (1997) Cadmium- and copper-induced changes in tomato membrane lipids. Photochemistry 45: 1343-1350.
49. Peixoto PHP, Cambraia J, Sant'Anna R, Mosquim PR, Moreira MA, (1999) Aluminum effects on lipid peroxidation and on the activities of enzymes of oxidative metabolism in Sorghum. R Bras Fisiol Veg 11: 137-143.
50. Meriga B, Attitalla IH, Ramgopal M, Ediga A, Kavikishor PB, (2010) Differential tolerance to aluminium toxicity in rice cultivars: Involvement of antioxidative enzymes and possible role of aluminium resistant locus. Acad J Plant Sci 3: 53-63.
51. Piñeros MA, Shaff JE, Manslank HS, Alves VM, Kochian LV, (2005) Aluminum resistance in maize cannot be solely explained by root organic acid exudation. A comparative physiological study. Plant Physiol. 137: 231-241.
52. Hoekenga OA, Maron LG, Piñeros MA, Cançado GM, Shaff J, et al. (2006) AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proc Natl Acad Sci U S A 103: 9738-9743.
53. Degenhardt J, Larsen PB, Howell SH, Kochian LV, (1998) Aluminum resistance in the Arabidopsis mutant alr-104 is caused by an aluminum-induced increase in rhizosphere pH. Plant Physiol 117: 19-27.
54. Qin C, Wang X, (2002) The Arabidopsis phospholipase D family. Characterization of a calcium-independent and phosphatidylcholine-selective PLDzeta 1 with distinct regulatory domains. Plant Physiol 128: 1057-1068.
55. Wang C, Zien CA, Afitlhile M, Welti R, Hildebrand DF, et al. (2001) Involvement of phospholipase D in wound-induced accumulation of jasmonic acid in Arabidopsis. Plant Cell 12: 2237-2246.
56. Baxter I, Hosmani PS, Rus A, Lahner B, Borevitz JO, et al. (2009) Root suberin forms an extracellular barrier that affects water relations and mineral nutrition in Arabidopsis. PLoS Genet 5: e1000492.
57. Zhao J, Fujita K, Sakai K, (2005) Oxidative stress in plant cell culture: a role in production of beta-thujaplicin by Cupresssus lusitanica suspension culture. Biotechnol Bioeng 90: 621-631.