Overexpression of Rice Sphingosine-1-Phoshpate Lyase Gene OsSPL1 in Transgenic Tobacco Reduces Salt and Oxidative Stress Tolerance

Journal of Integrative Plant Biology

Volumn 54, Issue 9, 2012, Pages 652-662

  Zhang, Huijuan ^a   Zhai, Jing ^a   Mo, Jibo ^a   Li, Dayong ^a   Song, Fengming ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

OsSPL1; Oxidative stress; Salt stress; Sphingolipids; Sphingosine 1 phosphate lyase (SPL)

Indexed keywords

ABSCISIC ACID; HYDROGEN PEROXIDE; LYASE; PARAQUAT; SODIUM CHLORIDE; SPHINGOSINE 1 PHOSPHATE LYASE (ALDOLASE); SPHINGOSINE 1-PHOSPHATE LYASE (ALDOLASE); VEGETABLE PROTEIN;

GENE EXPRESSION; PHOSPHATE; RICE; SALT; STRESS; TOBACCO; TOLERANCE;

ARTICLE; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGICAL STRESS; PLANT GENE; RICE; SALT TOLERANCE; SEEDLING; TOBACCO; TRANSGENIC PLANT;

ABSCISIC ACID; ALDEHYDE-LYASES; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HYDROGEN PEROXIDE; ORYZA SATIVA; OXIDATIVE STRESS; PARAQUAT; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; SALT-TOLERANCE; SEEDLING; SODIUM CHLORIDE; STRESS, PHYSIOLOGICAL; TOBACCO;

NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM; ORYZA SATIVA;

EID: 84866313329     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/j.1744-7909.2012.01150.x     Document Type: Article

References (64)

1. Alden KP, Dhondt-Cordelier S, McDonald KL, Reape TJ, Ng CK, McCabe PF, Leaver CJ (2011) Sphingolipid long chain base phosphates can regulate apoptotic-like programmed cell death in plants. Biochem. Biophys. Res. Comm. 20, 574-580.
2. Ashraf M (2010) Inducing drought tolerance in plants: Recent advances. Biotechnol. Adv. 28, 169-183.
3. Aubert A, Marion J, Boulogne C, Bourge M, Abreu S, Bellec Y, Faure JD, Satiat-Jeunemaitre B (2011) Sphingolipids involvement in plant endomembrane differentiation: The BY2 case. Plant J. 65, 958-971.
4. Bhatnagar-Mathur P, Vadez V, Sharma KK (2008) Transgenic approaches for abiotic stress tolerance in plants: Retrospect and prospects. Plant Cell Rep. 27, 411-424.
5. Chalfant CE, Spiegel S (2005) Sphingosine 1-phosphate and ceramide 1-phosphate: Expanding roles in cell signaling. J. Cell Sci. 118, 4605-4612.
6. Chao DY, Gable K, Chen M, Baxter I, Dietrich CR, Cahoon EB, Guerinot ML, Lahner B, Lü S, Markham JE, Morrissey J, Han G, Gupta SD, Harmon JM, Jaworski JG, Dunn TM, Salt DE (2011) Sphingolipids in the root play an important role in regulating the leaf ionome in Arabidopsis thaliana. Plant Cell 23, 1061-1081.
7. Chen M, Han G, Dietrich CR, Dunn TM, Cahoon EB (2006) The essential nature of sphingolipids in plants as revealed by the functional identification and characterization of the Arabidopsis LCB1 subunit of serine palmitoyltransferase. Plant Cell 18, 3576-3593.
8. Chen M, Markham JE, Dietrich CR, Jaworski JG, Cahoon EB (2008) Sphingolipid long-chain base hydroxylation is important for growth and regulation of sphingolipid content and composition in Arabidopsis. Plant Cell 20, 1862-1878.
9. Chen M, Markham JE, Cahoon EB (2012) Sphingolipid Δ8 unsaturation is important for glucosylceramide biosynthesis and low-temperature performance in Arabidopsis. Plant J. 69, 769-781.
10. Cong L, Zhang YX, Chai TY (2008) Arabidopsis DREB1A confers high salinity tolerance and regulates the expression of GA dioxygenases in tobacco. Plant Sci. 174, 156-164.
11. Coursol S, Fan LM, Le Stunff H, Spiegel S, Gilroy S, Assmann SM (2003) Sphingolipid signalling in Arabidopsis guard cells involves heterotrimeric G proteins. Nature 423, 651-654.
12. Coursol S, Le Stunff H, Lynch DV, Gilroy S, Assmann SM, Spiegel S (2005) Arabidopsis sphingosine kinase and the effects of phytosphingosine-1-phosphate on stomatal aperture. Plant Physiol. 137, 724-737.
13. Dietrich CR, Han G, Chen M, Berg RH, Dunn TM, Cahoon EB (2008) Loss-of-function mutations and inducible RNAi suppression of Arabidopsis LCB2 genes reveal the critical role of sphingolipids in gametophytic and sporophytic cell viability. Plant J. 54, 284-298.
14. Dunn TM, Lynch DV, Michaelson LV, Napier JA (2004) A post-genomic approach to understanding sphingolipid metabolism in Arabidopsis thaliana. Ann. Bot. 93, 483-497.
15. Dutilleul C, Benhassaine-Kesri G, Demandre C, Rézé N, Launay A, Pelletier S, Renou JP, Zachowski A, Baudouin E, Guillas I (2012) Phytosphingosine-phosphate is a signal for AtMPK6 activation and Arabidopsis response to chilling. New Phytol. 194, 181-191.
16. Espartero J, Pintor JA, Pardo JM (1994) Differential accumulation of S-adenosylmethionine synthetase transcripts in response to salt stress. Plant Mol. Biol. 25, 217-227.
17. Gechev TS, Ferwerda MA, Mehterov N, Laloi C, Qureshi MK, Hille J (2008) Arabidopsis AAL-toxin-resistant mutant atr1 shows enhanced tolerance to programmed cell death induced by reactive oxygen species. Biochem. Biophys. Res. Comm. 375, 639-644.
18. Guo L, Mishra G, Markham JE, Li M, Tawfall A, Welti R, Wang X (2012) Connections between sphingosine kinase and phospholipase D in the abscisic acid signaling pathway in Arabidopsis. J. Biol. Chem. 287, 8286-8296.
19. Guo L, Mishra G, Taylor K, Wang X (2011) Phosphatidic acid binds and stimulates Arabidopsis sphingosine kinases. J. Biol. Chem. 286, 13336-13345.
20. Imamura T, Kusano H, Kajigaya Y, Ichikawa M, Shimada H (2007) A rice dihydrosphingosine C4 hydroxylase (DSH1) gene, which is abundantly expressed in the stigmas, vascular cells and apical meristem, may be involved in fertility. Plant Cell Physiol. 48, 1108-1120.
21. Kawaguchi M, Imai H, Naoe M, Yasui Y, Ohnishi M (2000) Cerebrosides in grapevine leaves: Distinct composition of sphingoid bases among the grapevine species having different tolerances to freezing temperature. Biosci. Biotechnol. Biochem. 64, 1271-1273.
22. Li SF, Song LY, Yin WB, Chen YH, Chen L, Li JL, Wang RR, Hu ZM (2012) Isolation and functional characterization of the genes encoding Δ(8)-Sphingolipid desaturase from Brassica rapa. J. Genet. Genomics 39, 47-59.
23. Luo H, Song F, Zheng Z (2005) Overexpression in transgenic tobacco reveals different roles for the rice homeodomain gene OsBIHD1 in biotic and abiotic stress responses. J. Exp. Bot. 56, 2673-82.
24. Lynch DV, Dunn TM (2004) An introduction to plant sphingolipids and a review of recent advances in understanding their metabolism and function. New Phytol. 161, 677-702.
25. Lynch DV, Chen M, Cahoon EB (2009) Lipid signaling in Arabidopsis: No sphingosine? No problem! Trends Plant Sci. 14, 463-466.
26. Masuta C, Furuno M, Tanaka H, Yamada M, Koiwai A (1992) Molecular cloning of a cDNA clone for tobacco lipid transfer protein and expression of the functional protein in Escherichia coli. FEBS Lett. 311, 119-123.
27. Markham JE, Molino D, Gissot L, Bellec Y, Hématy K, Marion J, Belcram K, Palauqui JC, Satiat-Jeunemaître B, Faure JD (2011) Sphingolipids containing very-long-chain fatty acids define a secretory pathway for specific polar plasma membrane protein targeting in Arabidopsis. Plant Cell 23, 2362-2378.
28. Michaelson LV, Zäuner S, Markham JE, Haslam RP, Desikan R, Mugford S, Albrecht S, Warnecke D, Sperling P, Heinz E, Napier JA (2009) Functional characterization of a higher plant sphingolipid Delta4-desaturase: Defining the role of sphingosine and sphingosine-1-phosphate in Arabidopsis. Plant Physiol. 149, 487-498.
29. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) The reactive oxygen gene network of plants. Trends Plant Sci. 9, 490-498.
30. Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci. 11, 15-19.
31. Munnik T, Testerink C (2009) Plant phospholipid signaling: In a nutshell. J. Lipid Res. 50(Suppl.), S260-S265.
32. Ng CK, Carr K, McAinsh MR, Powell B, Hetherington AM (2001a) Drought-induced guard cell signal transduction involves sphingosine-1-phosphate. Nature 410, 596-599.
33. Ng CKY, Hetherington AM (2001b) Sphingolipid-mediated signalling in plants. Ann. Bot. 88, 957-965.
34. Nishikawa M, Hosokawa K, Ishiguro M, Minamioka H, Tamura K, Hara-Nishimura I, Takahashi Y, Shimazaki K, Imai H (2008) Degradation of sphingoid long-chain base 1-phosphates (LCB-1Ps): Functional characterization and expression of AtDPL1 encoding LCB-1P lyase involved in the dehydration stress response in Arabidopsis. Plant Cell Physiol. 49, 1758-1763.
35. Nishiura H, Tamura K, Morimoto Y, Imai H (2000) Characterization of sphingolipid long-chain base kinase in Arabidopsis thaliana. Biochem. Soc. Trans. 28, 747-748.
36. Niu Y, Chen KL, Wang JZ, Liu X, Qin HJ, Zhang AM, Wang DW (2007) Molecular and functional characterization of sphingosine-1-phosphate lyase homolog from higher plants. J. Integr. Plant Biol. 49, 323-335.
37. Payne SG, Milstien S, Sarah Spiegel S (2002) Sphingosine-1-phosphate: dual messenger functions. FEBS Lett. 531, 54-57.
38. Pandey S, Assmann SM (2004) The Arabidopsis putative G protein coupled receptor GCR1 interacts with the G protein a subunit GPA1 and regulates abscisic acid signaling. Plant Cell 16, 1616-1632.
39. Quist TM, Sokolchik I, Shi H, Joly RJ, Bressan RA, Maggio A, Narsimhan M, Li X (2009) HOS3, an ELO-like gene, inhibits effects of ABA and implicates a S-1-P/ceramide control system for abiotic stress responses in Arabidopsis thaliana. Mol. Plant 2, 138-151.
40. Ryan PR, Liu Q, Sperling P, Dong B, Franke S, Delhaize E (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.
41. Saucedo-García M, Guevara-García A, González-Solís A, Cruz-García F, Vázquez-Santana S, Markham JE, Lozano-Rosas MG, Dietrich CR, Ramos-Vega M, Cahoon EB, Gavilanes-Ruíz M (2011) MPK6, sphinganine and the LCB2a gene from serine palmitoyltransferase are required in the signaling pathway that mediates cell death induced by long chain bases in Arabidopsis. New Phytol. 191, 943-957.
42. Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr. Opin. Plant Biol. 10, 296-302.
43. Shi L, Bielawski J, Mu J, Dong H, Teng C, Zhang J, Yang X, Tomishige N, Hanada K, Hannun YA, Zuo J (2007) Involvement of sphingoid bases in mediating reactive oxygen intermediate production and programmed cell death in Arabidopsis. Cell Res. 17, 1030-1040.
44. Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J. Exp. Bot. 58, 221-227.
45. Sperling P, Ternes P, Moll H, Franke S, Zähringer U, Heinz E (2001) Functional characterization of sphingolipid C4-hydroxylase genes from Arabidopsis thaliana. FEBS Lett. 494, 90-94.
46. Sperling P, Heinz E (2003) Plant sphingolipids: Structural diversity, biosynthesis, first genes and functions. Biochim. Biophysi. Acta 1632, 1-15.
47. Spiegel S, Milstien S (2003) Sphingosine-1-phosphate: An enigmatic signalling lipid. Nat. Rev. Mol. Cell Biol. 4, 397-407.
48. Tamura K, Nishiura H, Mori J, Imai H (2000) Cloning and characterization of a cDNA encoding serine palmitoyltransferase in Arabidopsis thaliana. Biochem. Soc. Trans. 28, 745-747.
49. Tamura K, Mitsuhashi N, Hara-Nishimura I, Imai H (2001) Characterization of an Arabidopsis cDNA encoding a subunit of serine palmitoyltransferase, the initial enzyme in sphingolipid biosynthesis. Plant Cell Physiol. 42, 1274-1281.
50. Teng C, Dong H, Shi L, Deng Y, Mu J, Zhang J, Yang X, Zuo J (2008) Serine palmitoyltransferase, a key enzyme for de novo synthesis of sphingolipids, is essential for male gametophyte development in Arabidopsis. Plant Physiol. 146, 1322-1332.
51. Torres-Schumann S, Godoy JA, Pintor-Toro JA (1992) A probable lipid transfer protein gene is induced by NaCl in stems of tomato plants. Plant Mol. Biol. 18, 749-757.
52. Tsegaye Y, Richardson CG, Bravo JE, Mulcahy BJ, Lynch DV, Markham JE, Jaworski JG, Chen M, Cahoon EB, Dunn TM (2007) Arabidopsis mutants lacking long chain base phosphate lyase are fumonisin-sensitive and accumulate trihydroxy-18:1 long chain base phosphate. J. Biol. Chem. 282, 28195-28206.
53. Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Engineering drought tolerance in plants: Discovering and tailoring genes to unlock the future. Curr. Opin. Biotechnol. 17, 113-122.
54. Wang X, Devaiah SP, Zhang W, Welti R (2006) Signaling functions of phosphatidic acid. Prog. Lipid Res. 45, 250-278.
55. Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: Towards genetic engineering for stress tolerance. Planta 218, 1-14.
56. Wei W, Zhang Y, Han L, Guan Z, Chai T (2008) A novel WRKY transcriptional factor from Thlaspi caerulescens negatively regulates the osmotic stress tolerance of transgenic tobacco. Plant Cell Rep. 27, 795-803.
57. Worrall D, Ng CK, Hetherington AM (2003) Sphingolipids, new players in plant signaling. Trends Plant Sci. 8, 317-320.
58. Worrall D, Liang YK, Alvarez S, Holroyd GH, Spiegel S, Panagopulos M, Gray JE, Hetherington AM (2008) Involvement of sphingosine kinase in plant cell signalling. Plant J. 56, 64-72.
59. Xiong TC, Coursol S, Grat S, Ranjeva R, Mazars C (2008) Sphingolipid metabolites selectively elicit increases in nuclear calcium concentration in cell suspension cultures and in isolated nuclei of tobacco. Cell Cal. 43, 29-37.
60. Xu D, Duan X, Wang B, Hong B, Ho DT-H, Wu R (1996) Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol. 110, 249-257.
61. Yamaguchi T, Blumwald E (2005) Developing salt-tolerant crop plants: Challenges and opportunities. Trends Plant Sci. 10, 615-620.
62. Zauner S, Ternes P, Warnecke D (2010) Biosynthesis of sphingolipids in plants (and some of their functions). Adv. Exp. Med. Biol. 688, 249-263.
63. Zheng H, Rowland O, Kunst L (2005) Disruptions of the Arabidopsis enoyl-CoA reductase gene reveal an essential role for very-long-chain fatty acid synthesis in cell expansion during plant morphogenesis. Plant Cell 17, 1467-1481.
64. Zhu JK (2002) Salt and drought stress signal transduction in plants. Ann. Rev. Plant Biol. 53, 247-273.