Loss of abaxial leaf epicuticular wax in Medicago truncatula irg1/palm Mutants results in reduced spore differentiation of anthracnose and nonhost rust pathogens

Plant Cell

Volumn 24, Issue 1, 2012, Pages 353-370

  Uppalapati, Srinivasa Rao ^a   Ishiga, Yasuhiro ^a   Doraiswamy, Vanthana ^a   Bedair, Mohamed ^a   Mittal, Shipra ^a   Chen, Jianghua ^a   Nakashima, Jin ^a   Tang, Yuhong ^a   Tadege, Million ^a   Ratet, Pascal ^b   Chen, Rujin ^a   Schultheiss, Holger ^c   Mysore, Kirankumar S ^a  

^a PLANT BIOLOGY DIVISION   (United States)

^b CNRS   (France)

^c BASF SE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COLLETOTRICHUM TRIFOLII; MEDICAGO TRUNCATULA; PHAKOPSORA PACHYRHIZI; PUCCINIA;

EID: 84863272761     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.111.093104     Document Type: Article

References (71)

1. Aarts, M.G., Keijzer, C.J., Stiekema, W.J., and Pereira, A. (1995). Molecular characterization of the CER1 gene of Arabidopsis involved in epicuticular wax biosynthesis and pollen fertility. Plant Cell 7: 2115-2127.
2. Aharoni, A., Dixit, S., Jetter, R., Thoenes, E., van Arkel, G., and Pereira, A. (2004). The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. Plant Cell 16: 2463-2480.
3. Ayliffe, M., Singh, R., and Lagudah, E. (2008). Durable resistance to wheat stem rust needed. Curr. Opin. Plant Biol. 11: 187-192.
4. Bessire, M., Chassot, C., Jacquat, A.C., Humphry, M., Borel, S., Petétot, J.M., 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.
5. Bourdenx, B., Bernard, A., Domergue, F., Pascal, S., Léger, A., Roby, D., Pervent, M., Vile, D., Haslam, R.P., Napier, J.A., Lessire, R., and Joubès, J. (2011). Overexpression of Arabidopsis ECERIFERUM1 promotes wax very-long-chain alkane biosynthesis and influences plant response to biotic and abiotic stresses. Plant Physiol. 156: 29-45.
6. Bouton, J.H. (2007). Molecular breeding of switchgrass for use as a biofuel crop. Curr. Opin. Genet. Dev. 17: 553-558.
7. Broun, P., Poindexter, P., Osborne, E., Jiang, C.Z., and Riechmann, J.L. (2004). WIN1, a transcriptional activator of epidermal wax accumulation in Arabidopsis. Proc. Natl. Acad. Sci. USA 101: 4706-4711.
8. Carver, T.L.W., Thomas, B.J., Ingerson-Morris, S.M., and Roderick, H.W. (1990). The role of the abaxial leaf surface waxes of Lolium spp. in resistance to Erysiphe graminis. Plant Pathol. 39: 573-583.
9. 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.
10. Chassot, C., Nawrath, C., and Métraux, J.P. (2008). The cuticle: Not only a barrier for plant defence: A novel defence syndrome in plants with cuticular defects. Plant Signal. Behav. 3: 142-144.
11. Chen, J., et al. (2010). Control of dissected leaf morphology by a Cys(2) His(2) zinc finger transcription factor in the model legume Medicago truncatula. Proc. Natl. Acad. Sci. USA 107: 10754-10759.
12. Chen, X., Goodwin, S.M., Liu, X., Chen, X., Bressan, R.A., and Jenks, M.A. (2005). Mutation of the RESURRECTION1 locus of Arabidopsis reveals an association of cuticular wax with embryo development. Plant Physiol. 139: 909-919.
13. Church, G.M., and Gilbert, W. (1984). Genomic sequencing. Proc. Natl. Acad. Sci. USA 81: 1991-1995.
14. Curvers, K., Seifi, H., Mouille, G., de Rycke, R., Asselbergh, B., Van Hecke, A., Vanderschaeghe, D., Höfte, H., Callewaert, N., Van Breusegem, F., and Höfte, M. (2010). Abscisic acid deficiency causes changes in cuticle permeability and pectin composition that influence tomato resistance to Botrytis cinerea. Plant Physiol. 154: 847-860.
15. Debono, A., Yeats, T.H., Rose, J.K., Bird, D., Jetter, R., Kunst, L., and Samuels, L. (2009). Arabidopsis LTPG is a glycosylphosphatidylinositol- anchored lipid transfer protein required for export of lipids to the plant surface. Plant Cell 21: 1230-1238.
16. d'Erfurth, I., Cosson, V., Eschstruth, A., Lucas, H., Kondorosi, A., and Ratet, P. (2003). Efficient transposition of the Tnt1 tobacco retrotransposon in the model legume Medicago truncatula. Plant J. 34: 95-106.
17. Dozmorov, I., and Centola, M. (2003). An associative analysis of gene expression array data. Bioinformatics 19: 204-211.
18. Fiebig, A., Mayfield, J.A., Miley, N.L., Chau, S., Fischer, R.L., and Preuss, D. (2000). Alterations in CER6, a gene identical to CUT1, differentially affect long-chain lipid content on the surface of pollen and stems. Plant Cell 12: 2001-2008.
19. Garcia, A., Calvo, E.S., de Souza Kiihl, R.A., Harada, A., Hiromoto, D.M., and Vieira, L.G.E. (2008). Molecular mapping of soybean rust (Phakopsora pachyrhizi) resistance genes: Discovery of a novel locus and alleles. Theor. Appl. Genet. 117: 545-553.
20. Gniwotta, F., Vogg, G., Gartmann, V., Carver, T.L.W., Riederer, M., and Jetter, R. (2005). What do microbes encounter at the plant surface? Chemical composition of pea leaf cuticular waxes. Plant Physiol. 139: 519-530.
21. Goellner, K., Loehrer, M., Langenbach, C., Conrath, U., Koch, E., and Schaffrath, U. (2010). Phakopsora pachyrhizi, the causal agent of Asian soybean rust. Mol. Plant Pathol. 11: 169-177.
22. Hansjakob, A., Bischof, S., Bringmann, G., Riederer, M., and Hildebrandt, U. (2010). Very-long-chain aldehydes promote in vitro prepenetration processes of Blumeria graminis in a dose- and chain length-dependent manner. New Phytol. 188: 1039-1054.
23. Hansjakob, A., Riederer, M., and Hildebrandt, U. (2011). Wax matters: Absence of very-long-chain aldehydes from the leaf cuticular wax of the glossy11 mutant of maize compromises the prepenetration processes of Blumeria graminis. Plant Pathol. 60: 1151-1161.
24. Heath, M.C. (1977). A comparative study of non-host interactions with rust fungi. Physiol. Plant Pathol. 1: 73-76.
25. Heath, M.C. (2000). Nonhost resistance and nonspecific plant defenses. Curr. Opin. Plant Biol. 3: 315-319.
26. Hoch, H.C., Staples, R.C., Whitehead, B., Comeau, J., and Wolf, E.D. (1987). Signaling for growth orientation and cell differentiation by surface topography in uromyces. Science 235: 1659-1662.
27. Hyten, D.L., Hartman, G.L., Nelson, R.L., Frederick, R.D., Concibido, V.C., Narvel, J.M., and Cregan, P.B. (2007). Map location of the locus that confers resistance to soybean rust in soybean. Crop Sci. 47: 837-838.
28. Irizarry, R.A., Bolstad, B.M., Collin, F., Cope, L.M., Hobbs, B., and Speed, T.P. (2003). Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31: e15.
29. Javelle, M., Vernoud, V., Depège-Fargeix, N., Arnould, C., Oursel, D., Domergue, F., Sarda, X., and Rogowsky, P.M. (2010). Overexpression of the epidermis-specific homeodomain-leucine zipper IV transcription factor Outer Cell Layer1 in maize identifies target genes involved in lipid metabolism and cuticle biosynthesis. Plant Physiol. 154: 273-286.
30. Jenks, M.A., Tuttle, H.A., Eigenbrode, S.D., and Feldmann, K.A. (1995). Leaf epicuticular waxes of the eceriferum mutants in Arabidopsis. Plant Physiol. 108: 369-377.
31. Kader, J.C. (1996). Lipid-transfer proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 627-654.
32. Koch, E., and Hoppe, H.H. (1988). Development of infection structures by the direct-penetrating soybean rust fungus (Phakopsora pachyrhizi Syd.) on artificial membranes. J. Phytopathol. 122: 232-244.
33. Kolattukudy, P.E., Rogers, L.M., Li, D., Hwang, C.S., and Flaishman, M.A. (1995). Surface signaling in pathogenesis. Proc. Natl. Acad. Sci. USA 92: 4080-4087.
34. Kunst, L., and Samuels, A.L. (2003). Biosynthesis and secretion of plant cuticular wax. Prog. Lipid Res. 42: 51-80.
35. Kunst, L., and Samuels, L. (2009). Plant cuticles shine: Advances in wax biosynthesis and export. Curr. Opin. Plant Biol. 12: 721-727.
36. Lee, S.B., Go, Y.S., Bae, H.-J., Park, J.H., Cho, S.H., Cho, H.J., Lee, D.S., Park, O.K., Hwang, I., and Suh, M.C. (2009). Disruption of glycosylphosphatidylinositol-anchored lipid transfer protein gene altered cuticular lipid composition, increased plastoglobules, and enhanced susceptibility to infection by the fungal pathogen Alternaria brassicicola. Plant Physiol. 150: 42-54.
37. Lee, Y.-H., and Dean, R.A. (1994). Hydrophobicity of contact surface induces appressorium formation in Magnaporthe grisea. FEMS Microbiol. Lett. 115: 71-75.
38. Li, Y., Beisson, F., Koo, A.J., Molina, I., Pollard, M., and Ohlrogge, J. (2007). Identification of acyltransferases required for cutin biosynthesis and production of cutin with suberin-like monomers. Proc. Natl. Acad. Sci. USA 104: 18339-18344.
39. Lü, S., Song, T., Kosma, D.K., Parsons, E.P., Rowland, O., and Jenks, M.A. (2009). Arabidopsis CER8 encodes LONG-CHAIN ACYLCOA SYNTHETASE 1 (LACS1) that has overlapping functions with LACS2 in plant wax and cutin synthesis. Plant J. 59: 553-564.
40. Mang, H.G., et al. (2009). The Arabidopsis RESURRECTION1 gene regulates a novel antagonistic interaction in plant defense to biotrophs and necrotrophs. Plant Physiol. 151: 290-305.
41. Mao, B., et al. (2012). Wax crystal-sparse leaf2, a rice homologue of WAX2/GL1, is involved in synthesis of leaf cuticular wax. Planta 235: 39-52.
42. Millar, A.A., Clemens, S., Zachgo, S., Giblin, E.M., Taylor, D.C., and Kunst, L. (1999). CUT1, an Arabidopsis gene required for cuticular wax biosynthesis and pollen fertility, encodes a very-long-chain fatty acid condensing enzyme. Plant Cell 11: 825-838.
43. Monteros, M., Ha, B.-K., Phillips, D., and Boerma, H. (2010). SNP assay to detect the 'Hyuuga' red-brown lesion resistance gene for Asian soybean rust. Theor. Appl. Genet. 121: 1023-1032.
44. Müller, C., and Riederer, M. (2005). Plant surface properties in chemical ecology. J. Chem. Ecol. 31: 2621-2651.
45. Mysore, K.S., and Ryu, C.M. (2004). Nonhost resistance: How much do we know? Trends Plant Sci. 9: 97-104.
46. Pighin, J.A., Zheng, H., 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.
47. Podila, G.K., Rogers, L.M., and Kolattukudy, P.E. (1993). Chemical signals from avocado surface wax trigger germination and appressorium formation in Colletotrichum gloeosporioides. Plant Physiol. 103: 267-272.
48. Posada-Buitrago, M.L., and Frederick, R.D. (2005). Expressed sequence tag analysis of the soybean rust pathogen Phakopsora pachyrhizi. Fungal Genet. Biol. 42: 949-962.
49. Reisige, K., Gorzelanny, C., Daniels, U., and Moerschbacher, B.M. (2006). The C28 aldehyde octacosanal is a morphogenetically active component involved in host plant recognition and infection structure differentiation in the wheat stem rust fungus. Physiol. Mol. Plant Pathol. 68: 33-40.
50. Riederer, M., and Schreiber, L. (2001). Protecting against water loss: Analysis of the barrier properties of plant cuticles. J. Exp. Bot. 52: 2023-2032.
51. Ringelmann, A., Riedel, M., Riederer, M., and Hildebrandt, U. (2009). Two sides of a leaf blade: Blumeria graminis needs chemical cues in cuticular waxes of Lolium perenne for germination and differentiation. Planta 230: 95-105.
52. Rowland, O., Lee, R., Franke, R., Schreiber, L., and Kunst, L. (2007). The CER3 wax biosynthetic gene from Arabidopsis thaliana is allelic to WAX2/YRE/FLP1. FEBS Lett. 581: 3538-3544.
53. Rowland, O., Zheng, H., Hepworth, S.R., Lam, P., Jetter, R., and Kunst, L. (2006). CER4 encodes an alcohol-forming fatty acyl-coenzyme A reductase involved in cuticular wax production in Arabidopsis. Plant Physiol. 142: 866-877.
54. Samuels, L., Kunst, L., and Jetter, R. (2008). Sealing plant surfaces: Cuticular wax formation by epidermal cells. Annu. Rev. Plant Biol. 59: 683-707.
55. Segura, A., Moreno, M., and García-Olmedo, F. (1993). Purification and antipathogenic activity of lipid transfer proteins (LTPs) from the leaves of Arabidopsis and spinach. FEBS Lett. 332: 243-246.
56. Seo, P.J., Lee, S.B., Suh, M.C., Park, M.J., Go, Y.S., and Park, C.M. (2011). The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. Plant Cell 23: 1138-1152.
57. Silva, D.C., Yamanaka, N., Brogin, R.L., Arias, C.A., Nepomuceno, A.L., Di Mauro, A.O., Pereira, S.S., Nogueira, L.M., Passianotto, A. L., and Abdelnoor, R.V. (2008). Molecular mapping of two loci that confer resistance to Asian rust in soybean. Theor. Appl. Genet. 117: 57-63.
58. Tadege, M., Wen, J., He, J., Tu, H., Kwak, Y., Eschstruth, A., Cayrel, A., Endre, G., Zhao, P.X., Chabaud, M., Ratet, P., and Mysore, K.S. (2008). Large-scale insertional mutagenesis using the Tnt1 retrotransposon in the model legume Medicago truncatula. Plant J. 54: 335-347.
59. Tang, D., Simonich, M.T., and Innes, R.W. (2007). Mutations in LACS2, a long-chain acyl-coenzyme A synthetase, enhance susceptibility to avirulent Pseudomonas syringae but confer resistance to Botrytis cinerea in Arabidopsis. Plant Physiol. 144: 1093-1103.
60. Uppalapati, S.R., and Fujita, Y. (2000). Carbohydrate regulation of attachment, encystment, and appressorium formation by Pythium porphyrae (Oomycota) zoospores on Porphyra yezoensis (Rhodophyta). J. Phycol. 36: 359-366.
61. Uppalapati, S.R., Marek, S.M., Lee, H.K., Nakashima, J., Tang, Y., Sledge, M.K., Dixon, R.A., and Mysore, K.S. (2009). Global gene expression profiling during Medicago truncatula-Phymatotrichopsis omnivora interaction reveals a role for jasmonic acid, ethylene, and the flavonoid pathway in disease development. Mol. Plant Microbe Interact. 22: 7-17.
62. van de Mortel, M., Recknor, J.C., Graham, M.A., Nettleton, D., Dittman, J.D., Nelson, R.T., Godoy, C.V., Abdelnoor, R.V., Almeida, A.M.R., Baum, T.J., and Whitham, S.A. (2007). Distinct biphasic mRNA changes in response to Asian soybean rust infection. Mol. Plant Microbe Interact. 20: 887-899.
63. Xia, Y., Gao, Q.M., Yu, K., Lapchyk, L., Navarre, D., Hildebrand, D., Kachroo, A., and Kachroo, P. (2009). An intact cuticle in distal tissues is essential for the induction of systemic acquired resistance in plants. Cell Host Microbe 5: 151-165.
64. Xia, Y., Nikolau, B.J., and Schnable, P.S. (1997). Developmental and hormonal regulation of the Arabidopsis CER2 gene that codes for a nuclear-localized protein required for the normal accumulation of cuticular waxes. Plant Physiol. 115: 925-937.
65. Xia, Y., Yu, K., Navarre, D., Seebold, K., Kachroo, A., and Kachroo, P. (2010). The glabra1 mutation affects cuticle formation and plant responses to microbes. Plant Physiol. 154: 833-846.
66. Xiao, F., Goodwin, S.M., Xiao, Y., Sun, Z., Baker, D., Tang, X., Jenks, M.A., and Zhou, J.M. (2004). Arabidopsis CYP86A2 represses Pseudomonas syringae type III genes and is required for cuticle development. EMBO J. 23: 2903-2913.
67. Yeats, T.H., Howe, K.J., Matas, A.J., Buda, G.J., Thannhauser, T.W., and Rose, J.K. (2010). Mining the surface proteome of tomato (Solanum lycopersicum) fruit for proteins associated with cuticle biogenesis. J. Exp. Bot. 61: 3759-3771.
68. Young, N.D., and Udvardi, M. (2009). Translating Medicago truncatula genomics to crop legumes. Curr. Opin. Plant Biol. 12: 193-201.
69. Zabka, V., Stangl, M., Bringmann, G., Vogg, G., Riederer, M., and Hildebrandt, U. (2008). Host surface properties affect prepenetration processes in the barley powdery mildew fungus. New Phytol. 177: 251-263.
70. Zhang, J.Y., Broeckling, C.D., Blancaflor, E.B., Sledge, M.K., Sumner, L.W., and Wang, Z.Y. (2005). Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). Plant J. 42: 689-707.
71. Zhang, J.Y., Broeckling, C.D., Sumner, L.W., and Wang, Z.Y. (2007). Heterologous expression of two Medicago truncatula putative ERF transcription factor genes, WXP1 and WXP2, in Arabidopsis led to increased leaf wax accumulation and improved drought tolerance, but differential response in freezing tolerance. Plant Mol. Biol. 64: 265-278.