Arabidopsis acyl-CoA-binding protein ACBP3 participates in plant response to hypoxia by modulating very-long-chain fatty acid metabolism

Plant Journal

Volumn 81, Issue 1, 2015, Pages 53-67

  Xie, Li Juan ^a   Yu, Lu Jun ^a   Chen, Qin Fang ^a   Wang, Feng Zhu ^a   Huang, Li ^a   Xia, Fan Nv ^a   Zhu, Tian Ren ^a   Wu, Jian Xin ^a   Yin, Jian ^a   Liao, Bin ^a   Yao, Nan ^a   Shu, Wensheng ^a   Xiao, Shi ^a  

^a SUN YAT SEN UNIVERSITY   (China)

Author keywords

acyl CoA binding proteins; Arabidopsis thaliana; hypoxic tolerance; sphingolipids; very long chain fatty acids

Indexed keywords

BIOCHEMISTRY; CHAINS; ETHYLENE; GENES; METABOLISM; PHYSIOLOGY; PROTEINS; RECOMBINANT PROTEINS; TRANSCRIPTION;

ACYL-COA BINDING PROTEINS; ARABIDOPSIS THALIANA; CELLULAR ACTIVITIES; ENHANCED SENSITIVITY; ETHYLENE RESPONSIVE FACTORS; MEDIATED SIGNALING PATHWAYS; SPHINGOLIPIDS; VERY LONG-CHAIN FATTY ACIDS;

FATTY ACIDS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ACBP3 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; CARRIER PROTEIN; FATTY ACID;

ARABIDOPSIS; CELL HYPOXIA; CHEMISTRY; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARRIER PROTEINS; CELL HYPOXIA; FATTY ACIDS; STRESS, PHYSIOLOGICAL;

EID: 84920140749     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12692     Document Type: Article

References (58)

1. Apel, K., and, Hirt, H., (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373-399.
2. Bailey-Serres, J., and, Voesenek, L.A.C.J., (2008) Flooding stress: acclimations and genetic diversity. Annu. Rev. Plant Biol. 59, 313-339.
3. Bailey-Serres, J., and, Voesenek, L.A.C.J., (2010) Life in the balance: a signaling network controlling survival of flooding. Curr. Opin. Plant Biol. 13, 489-494.
4. Bailey-Serres, J., Fukao, T., Gibbs, D.J., Holdsworth, M.J., Lee, S.C., Licausi, F., Perata, P., Voesenek, L.A.C.J., and, van Dongen, J.T., (2012) Making sense of low oxygen sensing. Trends Plant Sci. 17, 129-138.
5. Baxter-Burrell, A., Yang, Z., Springer, P.S., and, Bailey-Serres, J., (2002) RopGAP4-dependent Rop GTPase rheostat control of Arabidopsis oxygen deprivation tolerance. Science, 296, 2026-2028.
6. Burton, M., Rose, T.M., Faergeman, N.J., and, Knudsen, J., (2005) Evolution of the acyl-CoA binding protein (ACBP). Biochem. J. 392, 299-307.
7. Chang, W.W., Huang, L., Shen, M., Webster, C., Burlingame, A.L., and, Roberts, J.K., (2000) Patterns of protein synthesis and tolerance of anoxia in root tips of maize seedlings acclimated to a low-oxygen environment, and identification of proteins by mass spectrometry. Plant Physiol. 122, 295-318.
8. Chao, Q., Rothenberg, M., Solano, R., Roman, G., Terzaghi, W., and, Ecker, J.R., (1997) Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell, 89, 1133-1144.
9. Chen, Q.F., Xiao, S., and, Chye, M.L., (2008) Overexpression of the Arabidopsis 10-kilodalton acyl-coenzyme A-binding protein ACBP6 enhances freezing tolerance. Plant Physiol. 148, 304-315.
10. Chen, M., Saucedo-García, M., Gavilanes-Ruíz, M., Plascencia, J., and, Cahoon, E. B., (2009) Plant sphingolipids: structure, synthesis and function. In Lipids in Photosynthesis: Essential and Regulatory Functions, Advances in Photosynthesis and Respiration (, Wada, H., and, Murata, N., ed). Dordrecht: Springer, pp. 77 ? 115.
11. Devaiah, S.P., Roth, M.R., Baughman, E., Li, M., Tamura, P., Jeannotte, R., Welti, R., and, Wang, X., (2006) Quantitative profiling of polar glycerolipid species from organs of wild type Arabidopsis and a PHOSPHOLIPASE Dα1 knockout mutant. Phytochemistry, 67, 1907-1924.
12. Du, Z.Y., and, Chye, M.L., (2013) Interactions between Arabidopsis acyl-CoA-binding proteins and their protein partners. Planta, 238, 239-245.
13. Du, Z.Y., Chen, M.X., Chen, Q.F., Xiao, S., and, Chye, M.L., (2013) Arabidopsis acyl-CoA-binding protein ACBP1 participates in the regulation of seed germination and seedling development. Plant J. 74, 294-309.
14. Fan, J., Liu, J., Culty, M., and, Papadopoulos, V., (2010) Acyl-coenzyme A binding domain containing 3 (ACBD3; PAP7; GCP60): an emerging signaling molecule. Prog. Lipid Res. 49, 218-234.
15. Gaigg, B., Neergaard, T.B., Schneiter, R., et al. (2001) Depletion of acyl-coenzyme A-binding protein affects sphingolipid synthesis and causes vesicle accumulation and membrane defects in Saccharomyces cerevisiae. Mol. Biol. Cell, 12, 1147-1160.
16. Gao, W., Xiao, S., Li, H.Y., Tsao, S.W., and, Chye, M.L., (2009) Arabidopsis thaliana acyl-CoA-binding protein ACBP2 interacts with heavy-metal-binding farnesylated protein AtFP6. New Phytol. 181, 89-102.
17. Gao, W., Li, H.Y., Xiao, S., and, Chye, M.L., (2010) Acyl-CoA-binding protein 2 binds lysophospholipase 2 and lysoPC to promote tolerance to cadmium-induced oxidative stress in transgenic Arabidopsis. Plant J. 62, 989-1003.
18. Geigenberger, P., (2003) Response of plant metabolism to too little oxygen. Curr. Opin. Plant Biol. 6, 247-256.
19. Gibbs, D.J., Lee, S.C., Isa, N.M., et al. (2011) Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature, 479, 415-418.
20. Hinz, M., Wilson, I.W., Yang, J., Buerstenbinder, K., Llewellyn, D., Dennis, E.S., Sauter, M., and, Dolferus, R., (2010) Arabidopsis RAP2.2: an ethylene response transcription factor that is important for hypoxia survival. Plant Physiol. 153, 757-772.
21. Hsu, F.C., Chou, M.Y., Chou, S.J., Li, Y.R., Peng, H.P., and, Shih, M.C., (2013) Submergence confers immunity mediated by the WRKY22 transcription factor in Arabidopsis. Plant Cell, 25, 2699-2713.
22. Kieber, J.J., Rothenberg, M., Roman, G., Feldmann, K.A., and, Ecker, J.R., (1993) CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the Raf family of protein kinases. Cell, 72, 427-441.
23. Klok, E.J., Wilson, I.W., Wilson, D., Chapman, S.C., Ewing, R.M., Somerville, S.C., Peacock, W.J., Dolferus, R., and, Dennis, E.S., (2002) Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. Plant Cell, 14, 2481-2494.
24. Leung, K.C., Li, H.Y., Xiao, S., Tse, M.H., and, Chye, M.L., (2006) Arabidopsis ACBP3 is an extracellularly targeted acyl-CoA-binding protein. Planta, 223, 871-881.
25. Li, H.Y., and, Chye, M.L., (2004) Arabidopsis acyl-CoA-binding protein ACBP2 interacts with an ethylene-responsive element-binding protein, AtEBP, via its ankyrin repeats. Plant Mol. Biol. 54, 233-243.
26. Li, H.Y., Xiao, S., and, Chye, M.L., (2008) Ethylene- and pathogen-inducible Arabidopsis acyl-CoA-binding protein 4 interacts with an ethylene-responsive element binding protein. J. Exp. Bot. 59, 3997-4006.
27. Li-Beisson, Y., Shorrosh, B., Beisson, F., et al. (2013) Acyl-lipid metabolism. Arabidopsis Book, 11, e0161.
28. Licausi, F., van Dongen, J.T., Giuntoli, B., Novi, G., Santaniello, A., Geigenberger, P., and, Perata, P., (2010) HRE1 and HRE2, two hypoxia-inducible ethylene response factors, affect anaerobic responses in Arabidopsis thaliana. Plant J. 62, 302-315.
29. Licausi, F., Kosmacz, M., Weits, D.A., Giuntoli, B., Giorgi, F.M., Voesenek, L.A.C.J., Perata, P., and, van Dongen, J.T., (2011a) Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. Nature, 479, 419-422.
30. Licausi, F., Weits, D.A., Pant, B.D., Scheible, W.R., Geigenberger, P., and, van Dongen, J.T., (2011b) Hypoxia responsive gene expression is mediated by various subsets of transcription factors and miRNAs that are determined by the actual oxygen availability. New Phytol. 190, 442-456.
31. Lynch, D.V., and, Dunn, T.M., (2004) An introduction to plant sphingolipids and a review of recent advances in understanding their metabolism and function. New Phytol. 161, 677-702.
32. Markham, J.E., and, Jaworski, J.G., (2007) Rapid measurement of sphingolipids from Arabidopsis thaliana by reversed-phase high-performance liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Rapid Commun. Mass Spectrom. 21, 1304-1314.
33. Markham, J.E., Li, J., Cahoon, E.B., and, Jaworski, J.G., (2006) Separation and identification of major plant sphingolipid classes from leaves. J. Biol. Chem. 281, 22684-22694.
34. Markham, J.E., Molino, D., Gissot, L., Bellec, Y., Hématy, K., Marion, J., Belcram, K., Palauqui, J.C., Satiat-Jeunemaître, B., and, Faure, J.D., (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.
35. Mithran, M., Paparelli, E., Novi, G., Perata, P., and, Loreti, E., (2013) Analysis of the role of the pyruvate decarboxylase gene family in Arabidopsis thaliana under low-oxygen conditions. Plant Biol. (Stuttg) 16, 28-34.
36. Mortimer, J.C., Yu, X., Albrecht, S., et al. (2013) Abnormal glycosphingolipid mannosylation triggers salicylic acid-mediated responses in Arabidopsis. Plant Cell, 25, 1881-1894.
37. Murashige, T., and, Skoog, F., (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15, 473-497.
38. Ohlrogge, J.B., and, Browse, J., (1995) Lipid biosynthesis. Plant Cell, 7, 957-970.
39. Perata, P., and, Voesenek, L.A.C.J., (2007) Submergence tolerance in rice requires Sub1A, an ethylene-response-factor-like gene. Trends Plant Sci. 12, 43-46.
40. Pucciariello, C., Parlanti, S., Banti, V., Novi, G., and, Perata, P., (2012) Reactive oxygen species-driven transcription in Arabidopsis under oxygen deprivation. Plant Physiol. 159, 184-196.
41. Raffaele, S., Vailleau, F., Léger, A., Joubès, J., Miersch, O., Huard, C., Blée, E., Mongrand, S., Domergue, F., and, Roby, D., (2008) A MYB transcription factor regulates very-long-chain fatty acid biosynthesis for activation of the hypersensitive cell death response in Arabidopsis. Plant Cell, 20, 752-767.
42. Ternes, P., Feussner, K., Werner, S., Lerche, J., Iven, T., Heilmann, I., Riezman, H., and, Feussner, I., (2011) Disruption of the ceramide synthase LOH1 causes spontaneous cell death in Arabidopsis thaliana. New Phytol. 192, 841-854.
43. Vailleau, F., Daniel, X., Tronchet, M., Montillet, J.L., Triantaphylidès, C., and, Roby, D., (2002) A R2R3-MYB gene, AtMYB30, acts as a positive regulator of the hypersensitive cell death program in plants in response to pathogen attack. Proc. Natl Acad. Sci. USA, 99, 10179-10184.
44. 2 sensing and survival strategies. Curr. Opin. Plant Biol. 16, 647-653.
45. Wang, X., (2004) Lipid signaling. Curr. Opin. Plant Biol. 7, 329-336.
46. Wang, W., Yang, X., Tangchaiburana, S., et al. (2008) An inositolphosphorylceramide synthase is involved in regulation of plant programmed cell death associated with defense in Arabidopsis. Plant Cell, 20, 3163-3179.
47. Welti, R., Li, W., Li, M., Sang, Y., Biesiada, H., Zhou, H.E., Rajashekar, C.B., Williams, T.D., and, Wang, X., (2002) Profiling membrane lipids in plant stress responses. Role of phospholipase Dα in freezing-induced lipid changes in Arabidopsis. J. Biol. Chem. 277, 31994-32002.
48. Xia, Y., Yu, K., Gao, Q.M., Wilson, E.V., Navarre, D., Kachroo, P., and, Kachroo, A., (2012) Acyl CoA binding proteins are required for cuticle formation and plant responses to microbes. Front. Plant Sci. 3, 224.
49. Xiao, S., and, Chye, M.L., (2009) An Arabidopsis family of six acyl-CoA-binding proteins has three cytosolic members. Plant Physiol. Biochem. 47, 479-484.
50. Xiao, S., and, Chye, M.L., (2011a) New roles for acyl-CoA-binding proteins (ACBPs) in plant development, stress responses and lipid metabolism. Prog. Lipid Res. 50, 141-151.
51. Xiao, S., and, Chye, M.L., (2011b) Overexpression of Arabidopsis ACBP3 enhances NPR1-dependent plant resistance to Pseudomonas syringe pv tomato DC3000. Plant Physiol. 156, 2069-2081.
52. Xiao, S., Gao, W., Chen, Q.F., Chan, S.W., Zheng, S.X., Ma, J., Wang, M., Welti, R., and, Chye, M.L., (2010) Overexpression of Arabidopsis acyl-CoA binding protein ACBP3 promotes starvation-induced and age-dependent leaf senescence. Plant Cell, 22, 1463-1482.
53. Xue, Y., Xiao, S., Kim, J., Lung, S.C., Chen, L., Tanner, J.A., Suh, M.C., and, Chye, M.L., (2014) Arabidopsis membrane-associated acyl-CoA-binding protein ACBP1 is involved in stem cuticle formation. J. Exp. Bot. 65, 5473-5483.
54. Yang, C.Y., (2014) Hydrogen peroxide controls transcriptional responses of ERF73/HRE1 and ADH1 via modulation of ethylene signaling during hypoxic stress. Planta, 239, 877-885.
55. Yang, C.Y., Hsu, F.C., Li, J.P., Wang, N.N., and, Shih, M.C., (2011) The AP2/ERF transcription factor AtERF73/HRE1 modulates ethylene responses during hypoxia in Arabidopsis. Plant Physiol. 156, 202-212.
56. Yurchenko, O.P., and, Weselake, R.J., (2011) Involvement of low molecular mass soluble acyl-CoA-binding protein in seed oil biosynthesis. New Biotechnol. 28, 97-109.
57. Zheng, S.X., Xiao, S., and, Chye, M.L., (2012a) The gene encoding Arabidopsis acyl-CoA-binding protein 3 is pathogen inducible and subject to circadian regulation. J. Exp. Bot. 63, 2985-3000.
58. Zheng, Y., Schumaker, K.S., and, Guo, Y., (2012b) Sumoylation of transcription factor MYB30 by the small ubiquitin-like modifier E3 ligase SIZ1 mediates abscisic acid response in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 109, 12822-12827.