A member of the PLEIOTROPIC DRUG RESISTANCE family of ATP binding cassette transporters is required for the formation of a functional cuticle in Arabidopsis

Plant Cell

Volumn 23, Issue 5, 2011, Pages 1958-1970

  Bessire, Michael ^a   Borel, Sandra ^a   Fabre, Guillaume ^a   Carrac, Luis ^a,e   Efremova, Nadia ^b,f   Yephremov, Alexander ^b   Cao, Yan ^d   Jetter, Reinhard ^d   Jacquat, Anne Claude ^c   Métraux, Jean Pierre ^c   Nawratha, Christiane ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^c UNIVERSITY OF FRIBOURG   (Switzerland)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

^f Phytowelt Green Technologies GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 79959840394     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.111.083121     Document Type: Article

References (64)

1. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
2. Bessire, M., Chassot, C., Jacquat, A.C., Humphry, M., Borel, S., Petétot, J.M.C., Métraux, J.P., and Nawrath, C. (2007). A permeable cuticle in Arabidopsis leads to a strong resistance to Botrytis cinerea. EMBO J. 26: 2158-2168.
3. Bird, D., Beisson, F., Brigham, A., Shin, J., Greer, S., Jetter, R., Kunst, L., Wu, X.W., Yephremov, A., and Samuels, L. (2007). Characterization of Arabidopsis ABCG11/WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion. Plant J. 52: 485-498.
4. Bonaventure, G., Beisson, F., Ohlrogge, J., and Pollard, M. (2004). Analysis of the aliphatic monomer composition of polyesters associated with Arabidopsis epidermis: Occurrence of octadeca-cis-6, cis- 9-diene-1,18-dioate as the major component. Plant J. 40: 920-930.
5. Campbell, E.J., Schenk, P.M., Kazan, K., Penninckx, I.A., Anderson, J.P., Maclean, D.J., Cammue, B.P.A., Ebert, P.R., and Manners, J.M. (2003). Pathogen-responsive expression of a putative ATP binding cassette transporter gene conferring resistance to the diterpenoid sclareol is regulated by multiple defense signaling pathways in Arabidopsis. Plant Physiol. 133: 1272-1284.
6. Chassot, C., Nawrath, C., and Métraux, J.P. (2007). Cuticular defects lead to full immunity to a major plant pathogen. Plant J. 49: 972-980.
7. Crouzet, J., Trombik, T., Fraysse, A.S., and Boutry, M. (2006). Organization and function of the plant pleiotropic drug resistance ABC transporter family. FEBS Lett. 580: 1123-1130.
8. Curtis, M.D., and Grossniklaus, U. (2003). A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133: 462-469.
9. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M.K., and Scheible, W.R. (2005). Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139: 5-17.
10. Ducos, E., Fraysse, S., and Boutry, M. (2005). Nt PDR3, an iron deficiency inducible ABC transporter in Nicotiana tabacum. FEBS Lett. 579: 6791-6795.
11. Efremova, N., Schreiber, L., Bär, S., Heidmann, I., Huijser, P., Wellesen, K., Schwarz-Sommer, Z., Saedler, H., and Yephremov, A. (2004). Functional conservation and maintenance of expression pattern of FIDDLEHEAD-like genes in Arabidopsis and Antirrhinum. Plant Mol. Biol. 56: 821-837.
12. Franke, R., Briesen, I., Wojciechowski, T., Faust, A., Yephremov, A., Nawrath, C., and Schreiber, L. (2005). Apoplastic polyesters in Arabidopsis surface tissues: A typical suberin and a particular cutin. Phytochemistry 66: 2643-2658.
13. Geldner, N., Dénervaud-Tendon, V., Hyman, D.L., Mayer, U., Stierhof, Y.D., and Chory, J. (2009). Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J. 59: 169-178.
14. Golin, J., Ambudkar, S.V., and May, L. (2007). The yeast Pdr5p multidrug transporter: How does it recognize so many substrates? Biochem. Biophys. Res. Commun. 356: 1-5.
15. Greer, S., Wen, M., Bird, D., Wu, X.M., Samuels, L., Kunst, L., and Jetter, R. (2007). The cytochrome P450 enzyme CYP96A15 is the midchain alkane hydroxylase responsible for formation of secondary alcohols and ketones in stem cuticular wax of Arabidopsis. Plant Physiol. 145: 653-667.
16. Ito, H., and Gray, W.M. (2006). A gain-of-function mutation in the Arabidopsis pleiotropic drug resistance transporter PDR9 confers resistance to auxinic herbicides. Plant Physiol. 142: 63-74.
17. Jander, G., Norris, S.R., Rounsley, S.D., Bush, D.F., Levin, I.M., and Last, R.L. (2002). Arabidopsis map-based cloning in the post-genome era. Plant Physiol. 129: 440-450.
18. Jasinski, M., Ducos, E., Martinoia, E., and Boutry, M. (2003). The ATP-binding cassette transporters: Structure, function, and gene family comparison between rice and Arabidopsis. Plant Physiol. 131: 1169-1177.
19. Jeffree, C.E. (2006). The fine structure of the plant cuticle. In Biology of the Plant Cuticle, M. Riederer and C. Müller, eds (Oxford: Blackwell Publishing), pp. 11-125.
20. Jungwirth, H., and Kuchler, K. (2006). Yeast ABC transporters: A tale of sex, stress, drugs and aging. FEBS Lett. 580: 1131-1138.
21. Kang, J., Hwang, J.-U., Lee, M., and Kim, Y.-Y.M., A.S. Martnoia, E., and Lee, Y. (2010). PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc. Natl. Acad. Sci. USA 107: 2355-2360.
22. Kannangara, R., Branigan, C., Liu, Y., Penfield, T., Rao, V., Mouille, G., Höfte, H., Pauly, M., Riechmann, J.L., and Broun, P. (2007). The transcription factor WIN1/SHN1 regulates cutin biosynthesis in Arabidopsis thaliana. Plant Cell 19: 1278-1294.
23. Kim, D.Y., Bovet, L., Maeshima, M., Martinoia, E., and Lee, Y. (2007).
24. The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J. 50: 207-218.
25. Kobae, Y., Sekino, T., Yoshioka, H., Nakagawa, T., Martinoia, E., and Maeshima, M. (2006). Loss of AtPDR8, a plasma membrane ABC transporter of Arabidopsis thaliana, causes hypersensitive cell death upon pathogen infection. Plant Cell Physiol. 47: 309-318.
26. Kolattukudy, P.E. (2001). Polyesters in higher plants. Adv. Biochem. Eng. Biotechnol. 71: 1-49.
27. Krattinger, S.G., Lagudah, E.S., Spielmeyer, W., Singh, R.P., Huerta- Espino, J., McFadden, H., Bossolini, E., Selter, L.L., and Keller, B. (2009). A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323: 1360-1363.
28. Kunst, L., and Samuels, A.L. (2003). Biosynthesis and secretion of plant cuticular wax. Prog. Lipid Res. 42: 51-80.
29. Kunst, L., and Samuels, L. (2009). Plant cuticles shine: Advances in wax biosynthesis and export. Curr. Opin. Plant Biol. 12: 721-727.
30. Kurdyukov, S., Faust, A., Nawrath, C., Bär, S., Voisin, D., Efremova, N., Franke, R., Schreiber, L., Saedler, H., Métraux, J.P., and Yephremov, A. (2006). The epidermis-specific extra cellular BODYGUARD controls cuticle development and morphogenesis in Arabidopsis. Plant Cell 18: 321-339.
31. Lagarde, D., Basset, M., Lepetit, M., Conejero, G., Gaymard, F., Astruc, S., and Grignon, C. (1996). Tissue-specific expression of Arabidopsis AKT1 gene is consistent with a role in K+ nutrition. Plant J. 9: 195-203.
32. Li, H., Pinot, F., Sauveplane, V., Werck-Reichhart, D., Diehl, P., Schreiber, L., Franke, R., Zhang, P., Chen, L., Gao, Y.W., Liang, W. Q., and Zhang, D.B. (2010). Cytochrome P450 family member CYP704B2 catalyzes the omega-hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. Plant Cell 22: 173-190.
33. Li, Y.H., Beisson, F., Koo, A.J.K., Molina, I., Pollard, M., and Ohlrogge, J. (2007). Identification of acyl transferases required for cutin biosynthesis and production of cut in with suberin-like monomers. Proc. Natl. Acad. Sci. USA 104: 18339-18344.
34. Li-Beisson, Y., et al. (2010). Acyl-lipid metabolism. The Arabidopsis Book 6: e0133, doi/10.1199/tab.0133.
35. Li-Beisson, Y., Pollard, M., Sauveplane, V., Pinot, F., Ohlrogge, J., and Beisson, F. (2009). Nanoridges that characterize the surface morphology of flowers require the synthesis of cutin polyester. Proc. Natl. Acad. Sci. USA 106: 22008-22013.
36. Lü, S.Y., Song, T., Kosma, D.K., Parsons, E.P., Rowland, O., and Jenks, M.A. (2009). Arabidopsis CER8 encodes LONG-CHAINACYL-COA SYNTHETASE 1 (LACS1) that has overlapping functions with LACS2 in plant wax and cutin synthesis. Plant J. 59: 553-564.
37. Lukowitz, W., Gillmor, C.S., and Scheible, W.R. (2000). Positional cloning in Arabidopsis. Why it feels good to have a genome initiative working for you. Plant Physiol. 123: 795-805.
38. Luo, B., Xue, X.Y., Hu, W.L., Wang, L.J., and Chen, X.Y. (2007). An ABC transporter gene of Arabidopsis thaliana, AtWBC11, is involved in cuticle development and prevention of organ fusion. Plant Cell Physiol. 48: 1790-1802.
39. Martinoia, E., Klein, M., Geisler, M., Bovet, L., Forestier, C., Kolukisaoglu, U., Müller-Röber, B., and Schulz, B. (2002). Multifunctionality of plant ABC transporters: More than just detoxifiers. Planta 214: 345-355.
40. McFarlane, H.E., Shin, J.H., Bird, D.A., and Samuels, A.L. (2010). Arabidopsis ABCG transporters, which are required for export of diverse cuticular lipids, dimerize in different combinations. Plant Cell 22: 3066-3075.
41. Molina, I., Li-Beisson, Y., Beisson, F., Ohlrogge, J.B., and Pollard, M. (2009). Identification of an Arabidopsis feruloyl-coenzyme A transferase required for suberin synthesis. Plant Physiol. 151: 1317-1328.
42. Moons, A. (2003). Ospdr9, which encodes a PDR-type ABC transporter, is induced by heavy metals, hypoxic stress and redox perturbations in rice roots. FEBS Lett. 553: 370-376.
43. Nawrath, C. (2006). Unraveling the complex network of cuticular structure and function. Curr. Opin. Plant Biol. 9: 281-287.
44. Panikashvili, D., Savaldi-Goldstein, S., Mandel, T., Yifhar, T., Franke, R.B., Höfer, R., Schreiber, L., Chory, J., and Aharoni, A. (2007). The Arabidopsis DESPERADO/AtWBC11 transporter is required for cutin and wax secretion. Plant Physiol. 145: 1345-1360.
45. Panikashvili, D., Shi, J.X., Bocobza, S., Franke, R.B., Schreiber, L., and Aharoni, A. (2010). The Arabidopsis DSO/ABCG11 transporter affects cutin metabolism in reproductive organs and suberin in roots. Mol Plant 3: 563-575.
46. Panikashvili, D., Shi, J.X., Schreiber, L., and Aharoni, A. (2009). The Arabidopsis DCR encoding a soluble BAHD acyltransferase is required for cutin polyester formation and seed hydration properties. Plant Physiol. 151: 1773-1789.
47. Panikashvili, D., Shi, J.X., Schreiber, L., and Aharoni, A. (2011). The Arabidopsis ABCG13 transporter is required for flower cuticle secretion and patterning of the petal epidermis. New Phytol. 190: 113-124.
48. Pighin, J.A., Zheng, H.Q., Balakshin, L.J., Goodman, I.P., Western, T.L., Jetter, R., Kunst, L., and Samuels, A.L. (2004). Plant cuticular lipid export requires an ABC transporter. Science 306: 702-704.
49. Pollard, M., Beisson, F., Li, Y.H., and Ohlrogge, J.B. (2008). Building lipid barriers: Biosynthesis of cutin and suberin. Trends Plant Sci. 13: 236-246.
50. Poulson, M.E., Edwards, G.E., and Browse, J. (2002). Photosynthesis is limited at high leaf to air vapor pressure deficit in a mutant of Arabidopsis thaliana that lacks trienoic fatty acids. Photosynth. Res. 72: 55-63.
51. Rani, S.H., Krishna, T.H.A., Saha, S., Negi, A.S., and Rajasekharan, R. (2010). Defective in cuticular ridges (DCR) of Arabidopsis thaliana, a gene associated with surface cutin formation, encodes a soluble diacylglycerol acyltransferase. J. Biol. Chem. 285: 38337-38347.
52. Reina-Pinto, J.J., and Yephremov, A. (2009). Surface lipids and plant defenses. Plant Physiol. Biochem. 47: 540-549.
53. Riederer, M. (2006). Introduction: Biology of the plant cuticle. In Biology of the Plant Cuticle, M. Riederer and C. Müller, eds (Oxford: Blackwell Publishing), pp. 1-10.
54. Sieber, P., Schorderet, M., Ryser, U., Buchala, A., Kolattukudy, P., Métraux, J.P., and Nawrath, C. (2000). Transgenic Arabidopsis plants expressing a fungal cutinase show alterations in the structure and properties of the cuticle and postgenital organ fusions. Plant Cell 12: 721-738.
55. Stefanato, F.L., Abou-Mansour, E., Buchala, A., Kretschmer, M., Mosbach, A., Hahn, M., Bochet, C.G., Métraux, J.P., and Schoonbeek, H.J. (2009). The ABC transporter Bcatr B from Botrytis cinerea exports camalex in and is a virulence factor on Arabidopsis thaliana. Plant J. 58: 499-510.
56. Stein, M., Dittgen, J., Sánchez-Rodríguez, C., Hou, B.H., Molina, A., Schulze-Lefert, P., Lipka, V., and Somerville, S. (2006). Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18: 731-746.
57. Strader, L.C., and Bartel, B. (2009). The Arabidopsis PLEIOTROPIC DRUG RESISTANCE8/ABCG36 ATP binding cassette transporter modulates sensitivity to the auxin precursor indole-3-butyric acid. Plant Cell 21: 1992-2007.
58. Stukkens, Y., Bultreys, A., Grec, S., Trombik, T., Vanham, D., and Boutry, M. (2005). NpPDR1, a pleiotropic drug resistance-type ATP binding cassette transporter from Nicotiana plumbaginifolia, plays a major role in plant pathogen defense. Plant Physiol. 139: 341-352.
59. Ukitsu, H., et al. (2007). Cytological and biochemical analysis of COF1, an Arabidopsis mutant of an ABC transporter gene. Plant Cell Physiol. 48: 1524-1533.
60. van den Brûle, S., and Smart, C.C. (2002). The plant PDR family of ABC transporters. Planta 216: 95-106.
61. Verrier, P.J., et al. (2008). Plant ABC proteins: A unified nomenclature and updated inventory. Trends Plant Sci. 13: 151-159.
62. Voisin, D., Nawrath, C., Kurdyukov, S., Franke, R., Reina-Pinto, J.J., Efremova, N., Will, I., Schreiber, L., and Yephremov, A. (2009). Dissection of the complex phenotype in cuticle mutants of Arabidopsis reveals a role of SERRATE as a mediator. PLoS Genet. 5: e1000703.
63. Yang, W.L., Pollard, M., Li-Beisson, Y., Beisson, F., Feig, M., and Ohlrogge, J. (2010). A distinct type of glycerol-3-phosphate acyltransferase with sn-2 preference and phosphatase activity producing 2-monoacylglycerol. Proc. Natl. Acad. Sci. USA 107: 12040-12045.
64. Yeats, T.H., Howe, K.J., Matas, A.J., Buda, G.J., Thannhauser, T.W., and Rose, J.K.C. (2010). Mining the surface proteome of tomato (Solanum lycopersicum) fruit for proteins associated with cuticle biogenesis. J. Exp. Bot. 61: 3759-3771.