Inhibition of cutin deficient 2 causes defects in cuticle function and structure and metabolite changes in tomato fruit

Plant and Cell Physiology

Volumn 54, Issue 9, 2013, Pages 1535-1548

  Kimbara, Junji ^a,b   Yoshida, Miho ^a   Ito, Hirotaka ^a   Kitagawa, Mamiko ^a   Takada, Wataru ^a   Hayashi, Kayoko ^a   Shibutani, Yusuke ^a   Kusano, Miyako ^c   Okazaki, Yozo ^c   Nakabayashi, Ryo ^c   Mori, Tetsuya ^c   Saito, Kazuki ^c,d   Ariizumi, Tohru ^b   Ezura, Hiroshi ^b  

^a KAGOME CO   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

^c RIKEN Center for Sustainable Resource Science   (Japan)

^d CHIBA UNIVERSITY   (Japan)

Author keywords

Cuticle; Fine mapping; Metabolomics; Tomato; Transpiration; Water permeability

Indexed keywords

ALKALOID; CUTINE; FLAVONOID; LIPID; MEMBRANE LIPID; VEGETABLE PROTEIN; WATER; WAX;

ARTICLE; CARBOHYDRATE METABOLISM; CHEMISTRY; CUTICLE; FINE MAPPING; FRUIT; GENE EXPRESSION REGULATION; GENETICS; LIPID METABOLISM; MASS FRAGMENTOGRAPHY; METABOLISM; METABOLOMICS; METHODOLOGY; MUTATION; PLANT EPIDERMIS; PLANT LEAF; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SWEATING; TOMATO; WATER PERMEABILITY;

CUTICLE; FINE MAPPING; METABOLOMICS; TOMATO; TRANSPIRATION; WATER PERMEABILITY;

ALKALOIDS; CARBOHYDRATE METABOLISM; FLAVONOIDS; FRUIT; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GENE EXPRESSION REGULATION, PLANT; LIPID METABOLISM; LIPIDS; LYCOPERSICON ESCULENTUM; MEMBRANE LIPIDS; METABOLOMICS; MUTATION; PLANT EPIDERMIS; PLANT LEAVES; PLANT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; WATER; WAXES;

EID: 84887930969     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pct100     Document Type: Article

References (43)

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. An, G., Ebert, R., Mitra, A. and Ha, S. (1988) Binary vectors. In Plant Molecular Biology Manual. Edited by Gelvin, S.B. and Schilpeoort, R.A. pp. 1-19. Kluwer, Dordrecht, The Netherlands.
3. Bargel, H. and Neinhuis, C. (2005) Tomato (Lycopersicon esculentum Mill.) fruit growth and ripening as related to the biomechanical properties of fruit skin and isolated cuticle. J. Exp. Bot. 56: 1049-1060.
4. Bessire, M., Chassot, C., Jacquat, A.C., Humphry, M., Borel, S., Petétot, J.M.D.C. et al. (2007) A permeable cuticle in Arabidopsis leads to a strong resistance to Botrytis cinerea. EMBO J. 26: 2158-2168.
5. Bovy, A., de Vos, R., Kemper, M., Schijlen, E., Pertejo, M.A., Muir, S. et al. (2002) High-flavonol tomatoes resulting from the heterologous expression of the maize transcription factor genes LC and C1. Plant Cell 14: 2509-2526.
6. Buda, G.J., Isaacson, T., Matas, A.J., Paolillo, D.J. and Rose, J.K.C. (2009) Three-dimensional imaging of plant cuticle architecture using con-focal scanning laser microscopy. Plant J. 60: 378-385.
7. Butler, L. (1952) Sticky peel (pe), a new character in the seventh linkage group. TGC Report 2: 2-3.
8. Curvers, K., Seifi, H., Mouille, G., de Rycke, R., Asselbergh, B., Hecke, A.V. et al. (2010) Abscisic acid deficiency causes changes in cuticle permeability and pectin composition that influence tomato resistance to Botrytis cinerea. Plant Physiol. 154: 847-860.
9. Heredia, A. (2003) Biophysical and biochemical characteristics of cutin, a plant barrier biopolymer. Biochim. Biophys. Acta 1620: 1-7.
10. Hovav, R., Chehanovsky, N., Moy, M., Jetter, R. and Schaffer, A.A. (2007) The identification of a gene (Cwp1), silenced during Solanum evolution, which causes cuticle microfissuring and dehydration when expressed in tomato fruit. Plant J. 52: 627-639.
11. Isaacson, T., Kosma, D.K., Matas, A.J., Buda, G.J., He, Y., Yu, B. et al. (2009) Cutin deficiency in the tomato fruit cuticle consistently affects resistance to microbial infection and biomechanical properties, but not transpirational water loss. Plant J. 60: 363-377.
12. Jetter, R. and Kunst, L. (2008) Plant surface lipid biosynthetic pathways and their utility for metabolic engineering of waxes and hydrocarbon biofuels. Plant J. 54: 670-683.
13. Jetter, R., Schäffer, S. and Riederer, M. (2001) Leaf cuticular waxes are arranged in chemically and mechanically distinct layers: evidence from Prunus laurocerasus L. Plant Cell Environ. 23: 619-628.
14. Kerr, E. (1982) New residents on chromosome 1: rvt, vi, lg, pe, dp, Nr-2, tmf, cjf. TGC Report 32: 16-17.
15. Kimbara, J., Yoshida, M., Ito, H., Hosoi, K., Kusano, M., Kobayashi, M. et al. (2012) A novel class of sticky peel and light green mutations causes cuticle deficiency in leaves and fruits of tomato (Solanum lycopersicum). Planta 236: 1559-1570.
16. Kosma, D.K., Bourdenx, B., Bernard, A., Parsons, E.P., Lü, S., Joubès, J. et al. (2009) The impact of water deficiency on leaf cuticle lipids of Arabidopsis. Plant Physiol. 151: 1918-1929.
17. Kubo, H. and Hayashi, K. (2011) Characterization of root cells of anl2 mutant in Arabidopsis thaliana. Plant Sci. 180: 679-685.
18. Kubo, H., Peeters, A.J.M., Aarts, M.G.M., Pereira, A. and Koornneef, M. (1999) ANTHOCYANINLESS2, a homeobox gene affecting anthocya-nin distribution and root development in Arabidopsis. Plant Cell 11: 1217-1226.
19. Kunst, L. and Samuels, A. (2003) Biosynthesis and secretion of plant cuticular wax. Prog. Lipid Res. 42: 51-80.
20. Leide, J., Hildebrandt, U., Vogg, G. and Riederer, M. (2011) The positional sterile (ps) mutation affects cuticular transpiration and wax biosynthesis of tomato fruits. J. Plant Physiol. 168: 871-877.
21. Li, Y. and Beisson, F. (2009) The biosynthesis of cutin and suberin as an alternative source of enzymes for the production of bio-based chemicals and materials. Biochimie 91: 685-691.
22. Li, Y., Beisson, F., Koo, A.J.K., 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.
23. Lolle, S.J., Hsu, W. and Pruitt, R.E. (1998) Genetic analysis of organ fusion in Arabidopsis thaliana. Genetics 149: 607-619.
24. 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.
25. Mintz-Oron, S., Mandel, T., Rogachev, I., Feldberg, L., Lotan, O., Yativ, M. et al. (2008) Gene expression and metabolism in tomato fruit surface tissues. Plant Physiol. 147: 823-851.
26. Muir, S.R., Collins, G.J., Robinson, S., Hughes, S., Bovy, A., Ric De Vos, C.H. et al. (2001) Overexpression of petunia chalcone isomer-ase in tomato results in fruit containing increased levels of flavonols. Nat. Biotechnol 19: 470-474.
27. Nadakuduti, S.S., Pollard, M., Kosma, D.K., Allen, C., Ohlrogge, J.B. and Barry, C.S. (2012) Pleiotropic phenotypes of the sticky peel mutant provide new insight into the role of CUTIN DEFICIENT2 in epidermal cell function in tomato. Plant Physiol. 159: 945-960.
28. Panikashvili, D., Savaldi-Goldstein, S., Mandel, T., Yifhar, T., Franke, R.B., Höfer, R. et al. (2007) The Arabidopsis DESPERADO/AtWBC11 transporter is required for cutin and wax secretion. Plant Physiol. 145: 1345-1360.
29. Pollard, M., Beisson, F., Li, Y. and Ohlrogge, J.B. (2008) Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci. 13: 236-246.
30. Porra, R.J., Thompson, W.A. and Kriedemann, P.E. (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta 975: 384-394.
31. Riederer, M. (2007) Introduction: biology of the plant cuticle. In Biology of the Plant Cuticle. Edited by Riederer, M. and Müller, C. pp. 1-10. Blackwell, Oxford.
32. Samuels, L., Kunst, L. and Jetter, R. (2008) Sealing plant surfaces: cu-ticular wax formation by epidermal cells. Annu. Rev. Plant Biol. 59: 683-707.
33. Schnurr, J., Shockey, J. and Browse, J. (2004) The acyl-CoA synthetase encoded by LACS2 is essential for normal cuticle development in Arabidopsis. Plant Cell 16: 629-642.
34. Slimestad, R. and Verheul, M. (2009) Review of flavonoids and other phenolics from fruits of different tomato (Lycopersicon esculentum Mill.) cultivars. J. Sci. Food Agric. 89: 1255-1270.
35. Stakhova, L.N., Ladygin, V.G. and Stakhov, L.F. (2001) The effect of quercetin on the accumulation of carbohydrates and amino acids in tomato fruits. Russ. J. Plant Physiol. 48: 191-195.
36. Sun, H.-J., Uchii, S., Watanabe, S. and Ezura, H. (2006) A highly efficient transformation protocol for Micro-Tom, a model cultivar for tomato functional genomics. Plant Cell Physiol. 47: 426-431.
37. Tanaka, T., Tanaka, H., Machida, C., Watanabe, M. and Machida, Y. (2004) A new method for rapid visualization of defects in leaf cuticle reveals five intrinsic patterns of surface defects in Arabidopsis. Plant J. 37: 139-146.
38. Verhoeyen, M.E., Bovy, A., Collins, G., Muir, S., Robinson, S., de Vos, C.H.R. et al. (2002) Increasing antioxidant levels in tomatoes through modification of the flavonoid biosynthetic pathway. J. Exp. Bot. 53: 2099-2106.
39. Vogg, G., Fischer, S., Leide, J., Emmanuel, E., Jetter, R., Levy, A.A. et al. (2004) Tomato fruit cuticular waxes and their effects on transpiration barrier properties: functional characterization of a mutant deficient in a very-long-chain fatty acid beta-ketoacyl-CoA synthase. J. Exp. Bot. 55: 1401-1410.
40. Xiao, F., Goodwin, S.M., Xiao, Y., Sun, Z., Baker, D., Tang, X. et al. (2004) Arabidopsis CYP86A2 represses Pseudomonas syringae type III genes and is required for cuticle development. EMBO J. 23: 2903-2913.
41. Yeats, T.H., Martin, L.B.B., Viart, H.M.F., Isaacson, T., He, Y., Zhao, L. et al. (2012) The identification of cutin synthase: formation of the plant polyester cutin. Nat. Chem. Biol. 8: 609-611.
42. Yephremov, A. and Schreiber, L. (2005) The dark side of the cell wall: molecular genetics of plant cuticle. Plant Biosyst. 139: 74-79.
43. Zou, L., Sun, X., Zhang, Z., Liu, P., Wu, J., Tian, C. et al. (2011) Leaf rolling controlled by the homeodomain leucine zipper class IV gene Roc5 in rice. Plant Physiol. 156: 1589-1602.