Photosynthetica 2010, 48(3):409-416 | DOI: 10.1007/s11099-010-0053-0

Antisense-mediated suppression of tomato zeaxanthin epoxidase alleviates photoinhibition of PSII and PSI during chilling stress under low irradiance

N. Wang1, B. Li1, H. L. Feng1, Q. Y. Zhang1, X. H. Yang1, Q. W. Meng1,*
1 College of Life Science, State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai'an, P.R. China

A tomato (Lycopersicon esculentum Mill.) zeaxanthin epoxidase gene (LeZE) was isolated and antisense transgenic tomato plants were produced. Northern, southern, and western blot analyses demonstrated that antisense LeZE was transferred into the tomato genome and the expression of LeZE was inhibited. The ratio of (A+Z)/(V+A+Z) in antisense transgenic plants was maintained at a higher level than in the wild type (WT) plants under high light and chilling stress with low irradiance. The value of non-photochemical quenching (NPQ) in WT and transgenic plants was not affected during the stresses. The oxidizable P700 and the maximal photochemical efficiency of PSII (Fv/Fm) in transgenic plants decreased more slowly at chilling temperature under low irradiance. These results suggested that suppression of LeZE caused zeaxanthin accumulation, which was helpful in alleviating photoinhibition of PSI and PSII in tomato plants under chilling stress.

Keywords: antisense transgenic plants; chilling stress under low irradiance; photoinhibition; tomato; zeaxanthin epoxidase gene.

Received: July 16, 2009; Accepted: May 18, 2010; Published: September 1, 2010Show citation

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Wang, N., Li, B., Feng, H.L., Zhang, Q.Y., Yang, X.H., & Meng, Q.W. (2010). Antisense-mediated suppression of tomato zeaxanthin epoxidase alleviates photoinhibition of PSII and PSI during chilling stress under low irradiance. Photosynthetica48(3), 409-416. doi: 10.1007/s11099-010-0053-0.
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References

  1. Adams, W.W., III, Demmig-Adams, B., Verhoeven, A.S., Barker, D.H.: Photoinhibition during winter stress: Involvement of sustained xanthophyll cycle-dependent energy dissipation. - Aust. J. Plant Physiol. 22: 261-276, 1995. Go to original source...
  2. Allen, D.J., Ort, D.R.: Impacts of chilling temperatures on photosynthesis in warm-climate plants. - Trends Plant Sci. 6: 36-42, 2001. Go to original source...
  3. Aro, E.M., Virgin, I., Andersson, B.: Photoinhibition of photosystem II: Inactivation, protein damage and turnover. - Biochim. Biophys. Acta 1143: 113-134, 1993. Go to original source...
  4. Audran, C., Borel, C., Frey, A., Sotta, B., Meyer, C., Simonneau, T., Marion-Poll, A.: Expression studies of the zeaxanthin epoxidase gene in Nicotiana plumbaginifolia. - Plant Physiol. 118: 1021-1028, 1998. Go to original source...
  5. Bertamini, M., Muthuchelian, K., Rubinigg, M., Zorer, R., Velasco, R., Nedunchezhian, N.: Low-night temperature increased the photoinhibition of photosynthesis in grapevine (Vitis vinifera L. cv. Riesling) leaves. - Environ. Exp. Bot. 57: 25-31, 2006. Go to original source...
  6. Boese, S.R., Hüner, N.P.A.: Developmental history affects the susceptibility of spinach leaves to in vivo low temperature photoinhibition. - Physiol. Plant. 99: 1141-1145, 1992. Go to original source...
  7. Bradford, M.M.: A rapid and sensitive method for the quantification of microgram quantities of protein using the principal of protein-dye binding. - Anal. Biochem. 72: 248-254, 1976. Go to original source...
  8. Bugos, R.C., Hieber, D., Yamamoto, H.Y.: Xanthophyll cycle enzymes are members of the lipocalin family, the first identified from plants. - J. Biol. Chem. 273: 15321-15324, 1998. Go to original source...
  9. Burbidge, A., Grieve, T., Terry, C., Corlett, J., Thompson, A., Taylor, I.: Structure and expression of a cDNA encoding zeaxanthin epoxidase, isolated from a wilt-related tomato (Lycopersicon esculentum Mill.) library. - J. Exp. Bot. 48: 1749-1750, 1997. Go to original source...
  10. Croce, R., Zucchelli, G., Garlaschi, F., Bassi, R., Jennings, R.C.: Excited state equilibration in the photosystem I lightharvesting I complex: P700 is almost isoenergetic with its antenna. - Biochemistry 35: 8572-8579, 1996. Go to original source...
  11. Demmig-Adams, B., Adams, W.W., III: Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species. - Planta 198: 460-470, 1996. Go to original source...
  12. Feierabend, J., Schaan, C., Hertwig, B.: Photoinactivation of catalase occurs under both high-and low-temperature stress conditions and accompanies photoinhibition of photosystem II. - Physiol. Plant. 100: 1554-1561, 1992. Go to original source...
  13. Foyer, C.H., Lelandais, M.: A comparison of the relative rate of transport of ascorbate and glucose across the thylakoid, chloroplast and plasmalemma membranes of pea leaf mesophyll cells. - J. Plant Physiol. 148: 391-398, 1996. Go to original source...
  14. Foyer, C.H., Lelandais, M., Kunert, K.J.: Photooxidative stress in plants. - Physiol Plant. 92: 696-717, 1994. Go to original source...
  15. Gruszecki, W.I., Strzałka, K.: Does the xanthophyll cycle take part in the regulation of fluidity of the membrane? - Biochim. Biophys. Acta 1060: 310-314, 1991. Go to original source...
  16. Hager, A.: The reversible, light-induced conversions of xanthophylls in the chloroplast. - In: Czygan, F.-C. (ed.): Pigments in Plants. 2nd Ed. Pp. 57-79. G.Fischer Verlag, Stuttgart - New York 1980.
  17. Havaux, M.: Carotenoids as membrane stabilizers in chloroplasts. - Trends Plant Sci. 3: 147-151, 1998. Go to original source...
  18. Havaux, M., Dall'Osto, L., Cuinè, S., Giuliano, G., Bassi, R.: The effect of zeaxanthin as the only xanthophyll on the structure and function of the photosynthetic apparatus in Arabidopsis thaliana. - J. Biol. Chem. 279: 13878-13888, 2004. Go to original source...
  19. Havaux, M., Davaud, A.: Photoinhibition of photosynthesis in chilled potato leaves is not correlated with loss of photosystem II activity. Preferential inactivation of Photosystem I. - Photosynth. Res. 40: 75-92, 1994. Go to original source...
  20. Havaux, M., Gruszecki, W.I.: Heatinduced and light-induced chlorophyll a fluorescence changes in potato leaves containing high or low levels of the carotenoid zeaxanthin: Indications of a regulatory effect of zeaxanthin on thylakoid membrane fluidity. - Photochem. Photobiol. 58: 607-614, 1993. Go to original source...
  21. Havaux, M., Niyogi, K.K.: The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. - Proc. Nat. Acad. Sci. USA 96: 8762-8767, 1999. Go to original source...
  22. Holsters, M., De Waele, D., Depicker, A., Messens, E., van Montagu, M., Schell, J.: Transfection and transformation of Agrobacterium tumefaciens. - Mol. Gen. Genet. 163: 181-187, 1978. Go to original source...
  23. Horsch, R.B., Fry, J.E., Hoffmann, N.L., Eichholtz, D., Rogers, S.G., Fraley, R.T.: A simple and general method for transferring gene into plants. - Science 227: 1229-1231, 1985.
  24. Horton, P., Ruban, A.V., Walters, R.G.: Regulation of light harvesting in green plants. - Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 655-684, 1996. Go to original source...
  25. Huner, N.P.A., Öquist, G., Sarhan, F.: Energy balance and acclimation to light and cold. - Trends Plant Sci. 3: 224-230, 1998. Go to original source...
  26. Hurry, V., Andersson, J.M., Chow, W.S., Osmond, C.B.: Accumulation of zeaxanthin in abscisic acid-deficient mutants of Arabidopsis does not affect chlorophyll fluorescence quenching or sensitivity to photoinhibition in vivo. - Plant Physiol. 113: 639-648, 1997. Go to original source...
  27. Jakob, B., Heber, U.: Photoproduction and detoxification of hydroxyl radicals in chloroplasts and leaves and relation to photoinactivation of photosystem I and II. - Plant Cell Physiol. 37: 629-635, 1996. Go to original source...
  28. Jin, É., Yokthongwattana, K., Polle, J.E.W., Melis, A.: Role of the reversible xanthophyll cycle in the photosystem II damage and repair cycle in Dunaliella salina. - Plant Physiol. 132: 352-364, 2003. Go to original source...
  29. Kratsch, H.A., Wise, R.R.: The ultrastructure of chilling stress. - Plant Cell Environ. 23: 337-350, 2000. Go to original source...
  30. Lee, A.I., Thornber, J.P.: Analysis of the pigment stoichiometry of the pigment-protein complexes from barley (Hordeum vulgare): the xanthophyll cycle intermediates occur mainly in the light-harvesting complexes of photosystem I and photosystem II. - Plant Physiol. 107: 565-574, 1995. Go to original source...
  31. Li, X.-G., Meng, Q.-W., Jiang, G.-Q., Zou, Q.: The susceptibility of cucumber and sweet pepper to chilling under low irradiance is related to energy dissipation and water-water cycle. - Photosynthetica 41: 259-265, 2003. Go to original source...
  32. Li, X.G., Duan, W., Meng, Q.W., Zou, Q., Zhao, S.J.: The function of chloroplastic NAD(P)H dehydrogenase in tobacco during chilling stress under low irradiance. - Plant Cell Physiol. 45: 103-108, 2004. Go to original source...
  33. Li, X.-G., Bi, Y.-P., Zhao, S.-J., Meng, Q.-W., Zou, Q., He, Q.-W.: Cooperation of xanthophyll cycle with water-water cycle in the protection of photosystems 1 and 2 against inactivation during chilling stress under low irradiance. - Photosynthetica 43: 261-266, 2005. Go to original source...
  34. Liu, P., Meng, Q.W., Zou, Q., Zhao, S.J., Liu, Q.Z.: Effects of cold-hardening on chilling-induced photoinhibition of photosynthesis and on xanthophyll cycle pigments in sweet pepper. - Photosynthetica 39: 467-472, 2001. Go to original source...
  35. Long, S.P., Humphries, S., Falkowski, P.G.: Photoinhibition of photosynthesis in nature. - Annu. Rev. Plant Physiol. Plant Mol. Biol. 45: 633-662, 1994. Go to original source...
  36. Murata, N., Takahashi, S., Nishiyama, Y., Allakhverdiev, S.I.: Photoinhibition of photosystem II under environmental stress. - Biochim. Biophys. Acta 1767: 414-421, 2007. Go to original source...
  37. Müller, P., Li, X.P., Niyogi, K.K.: Non-photochemical quenching. A response to excess light energy. - Plant Physiol. 125: 1558-1566, 2001. Go to original source...
  38. Niyogi, K.K., Grossman, A.R., Björkman, O.: Arabidopsisi mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. - Plant Cell 10: 1121-1134, 1998. Go to original source...
  39. Niyogi, K.K., Shih, C., Chow, W.S., Pogson, B.J., DellaPenna, D., Björkman, O.: Photoprotection in a zeaxanthin- and lutein-deficient double mutant of Arabidopsis. - Photosynth. Res. 67: 139-145, 2001. Go to original source...
  40. Pastenes, C., Pimentel, P., Lillo, J.: Leaf movements and photoinhibition in relation to water stress in field-grown beans. - J. Exp. Bot. 56: 425-433, 2005.
  41. Rock, C.D., Zeevaart, J.A.D.: The ABA mutant of Arabidopsis thaliana is impaired in epoxy-carotenoid biosynthesis. - Proc. Nat. Acad. Sci. USA 88: 7496-7499, 1991. Go to original source...
  42. Sambrook, J., Fritsch, E.F., Maniatis, T.: Molecular Cloning. A Laboratory Manual. 2nd Ed. - Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York 1989.
  43. Schansker, G., Srivastava, A., Govindjee, Strasser, R.J.: Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves. - Funct. Plant Biol. 30: 785-96, 2003. Go to original source...
  44. Schreiber, U., Bilger, W., Neubauer, C.: Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. - In: Schulze, E.-D., Caldwell, M.M. (ed.): Ecophysiology of Photosynthesis. Pp. 49-70. Springer-Verlag, Berlin 1994. Go to original source...
  45. Sonoike, K.: Photoinhibition of photosystem I: Its physiological significance in the chilling sensitivity of plants. - Plant Cell Physiol. 37: 239-247, 1996. Go to original source...
  46. Sonoike, K., Kamo, M., Hihara, Y., Hiyama, T., Enami, I.: The mechanism of the degradation of psaB gene product, one of the photosynthetic reaction center subunits of Photosystem I, upon photoinhibition. - Photosynth. Res. 53: 55-63, 1997. Go to original source...
  47. Sonoike, K., Terashima, I.: Mechanism of photosystem I photoinhibition in leaves of Cucumis sativus L. - Planta 194: 287-93, 1994. Go to original source...
  48. Tardy, F., Havaux, M.: Photosynthesis, chlorophyll fluorescence, light-harvesting system and photoinhibition resistance of a zeaxanthin-accumulating mutant of Arabidopsis thaliana. - J. Photochem. Photobiol. B: Biol. 34: 87-94, 1996. Go to original source...
  49. Telfer, A., Dhami, S., Bishop, S.M., Phillips, D., Barber, J.: Beta-carotene quenches singlet oxygen formed by isolated photosystem II reaction centers. - Biochemistry 33: 14469-14474, 1994. Go to original source...
  50. Terashima, I., Funayama, S., Sonoike, K.: The site of photoinhibition in leaves of Cucumis sativus L. at low temperatures is photosystem I, not photosystem II. - Planta 193: 300-306, 1994. Go to original source...
  51. Tjus, S.E., Moller, B.L., Scheller, H.V.: Photosystem I is an early target of photoinhibition in barley illuminated at chilling temperatures. - Plant Physiol. 116: 755-764, 1998. Go to original source...
  52. Thayer, S.S., Björkman, O.: Carotenoid distribution and deepoxidation in thylakoid pigment-protein complexes from cotton leaves and bundle-sheath cells of maize. Photosynth. Res. 33: 213-225, 1992. Go to original source...
  53. Thompson, A.J., Jackson, A.C., Parker, R.A., Morpeth, D.R., Burbidge, A., Taylor, I.B.: Abscisic acid biosynthesis in tomato: Regulation of zeaxanthin epoxidase and 9-cis-epoxycarotenoid dioxygenase mRNAs by light/dark cycles, water stress and abscisic acid. - Plant Mol. Biol. 42: 833-845, 2000. Go to original source...
  54. van Kooten, O., Snel, J.F.H.: The use of chlorophyll fluorescence nomenclature in plant stress physiology. - Photosynth. Res. 25: 147-150, 1990. Go to original source...
  55. Walker, D.A.: The Use of the Oxygen Electrode and Fluorescence Probes in Simple Measurements of Photosynthesis. - Oxygraphics Ltd., Univ. Sheffield, Sheffield 1990.
  56. Wang, N., Fang, W., Han, H., Sui, N., Li, B., Meng, Q.W.: Overexpression of zeaxanthin epoxidase gene enhances the sensitivity of tomato PSII photoinhibition to high light and chilling stress. - Physiol. Plant. 132: 384-396, 2008. Go to original source...
  57. Xu, C.C., Jeon, Y.A., Lee, C.H.: Relative contributions of photochemical and non-photochemical routes to excitation energy dissipation in rice and barley illuminated at a chilling temperature. - Physiol. Plant. 107: 447-453, 1999. Go to original source...
  58. Yamamoto, H.Y.: Biochemistry of the violaxanthin cycle in higher plants. - Pure Appl. Chem. 51: 639-648, 1979. Go to original source...
  59. Zhang, L., Paakkarinen, V., van Wijk, K.J., Aro, E.M.: Biogenesis of the chloroplast-encoded D1 protein: Regulation of translation, elongation, insertion, and assembly into photosystem II. - Plant Cell 12: 1769-1781, 2000. Go to original source...
  60. Zhao, S.J., Meng, Q.W., Xu, C.C., Han, H.Y., Zou, Q.: Analysis of xanthophyll cycle components in plant tissues by high performance liquid chromatography. - Plant Physiol. Commun. 31: 438-442, 1995.