Photosynthetica, 2016 (vol. 54), issue 3

Photosynthetica 2016, 54(3):446-458 | DOI: 10.1007/s11099-016-0189-7

Molecular characterization of 5-chlorophyll a/b-binding protein genes from Panax ginseng Meyer and their expression analysis during abiotic stresses

J. Silva1, Y. J. Kim2,*, J. Sukweenadhi1, S. Rahimi1, W. S. Kwon2, D. C. Yang1,2
1 Graduate School of Biotechnology and Ginseng Bank, College of Life Science, Kyung Hee University, Yongin, Korea
2 Department of Oriental Medicinal Biotechnology, College of Life Science, Kyung Hee University, Yongin, Korea

The chlorophyll a/b-binding protein (CAB) serves in both photosystems (PS), I and II, as a coordinator of antenna pigments in the light-harvesting complex (LHC). The CABs constitute abundant and important proteins in the thylakoid membrane of higher plants. In our study, five CAB genes, which contained full-length cDNA sequences from the 4-year-old ginseng leaves (Panax ginseng Meyer), were isolated and named PgCAB. Phylogenetic comparison of the members of the subfamily between ginseng and higher plants, including Arabidopsis, revealed that the putative functions of these ginseng CAB proteins were clustered into the different family of Arabidopsis CABs; two PgCABs in LHCII family and three PgCABs in LHCI family. The expression analysis of PgCABs consistently showed dark-dependent inhibition in leaves. Expression analysis during abiotic stress identified that PgCAB genes responded to heavy metal, salinity, chilling, and UV stresses differently, suggesting their specific function during photosynthesis. This is the first comprehensive study of the CAB gene family in P. ginseng.

Keywords: gene expression; gene isolation

Received: July 7, 2015; Accepted: November 11, 2015; Published: September 1, 2016Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Silva, J., Kim, Y.J., Sukweenadhi, J., Rahimi, S., Kwon, W.S., & Yang, D.C. (2016). Molecular characterization of 5-chlorophyll a/b-binding protein genes from Panax ginseng Meyer and their expression analysis during abiotic stresses. Photosynthetica54(3), 446-458. doi: 10.1007/s11099-016-0189-7.
Download citation

Supplementary files

Download filephs-201603-0018_S1.pdf

File size: 2.48 MB

Download filephs-201603-0018_S2.pdf

File size: 361.1 kB

Download filephs-201603-0018_S3.pdf

File size: 231.66 kB

Download filephs-201603-0018_S4.pdf

File size: 120.1 kB

References

  1. Allen J.F., De Paula W.B.M., Puthiyaveetil S., Nield J.: A structural map for chloroplast photosynthesis.-Trends Plant Sci. 16: 645-655, 2011. Go to original source...
  2. Andersson J., Wentworth M., Walters R.G. et al.: Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of photosystem II-effects on photosynthesis, grana stacking and fitness.-Plant J. 35: 350-361, 2003.
  3. Arnold J., Bordoli L., Kopp J., Schwede T.: The SWISS-MODEL Workspace. A web-based environment for protein structure homology modeling.-Bioinformatics 22: 195-201, 2006. Go to original source...
  4. Bailey T.L., Boden M., Buske F.A. et al.: MEME SUITE: tools for motif discovery and searching.-Nucl. Acids Res. 37: 202-208, 2009. Go to original source...
  5. Bedbrook J.R., Smith S.M., Ellis J.: Molecular cloning and sequencing of cDNA encoding the precursor to the small subunit of chloroplast ribulose-1,5-biphosphate carboxylase.-Nature 287: 692-697, 1980. Go to original source...
  6. Baker N.R.: A possible role for photosystem II in environmental perturbations of photosynthesis.-Physiol. Plantarum 81: 563-570, 1991. Go to original source...
  7. Bannai H., Tamada Y., Maruyama O. et al.: Extensive feature detection of N-terminal protein sorting signals.-Bioinformatics 18: 298-305, 2002. Go to original source...
  8. Bassett C.L., Callahan A.M.: Characterization of a type II chlorophyll a/b-binding protein gene (Lhcb2*Pp1) in peach. II. mRNA abundance in developing leaves exposed to sun or shade.-Tree Physiol. 23: 473-480, 2003. Go to original source...
  9. Bassett C.L., Callahan A.M., Artlip T.S. et al.: A minimal peach type II chlorophyll a/b binding protein promoter retains tissue specificity and light regulation in tomato.-BCM Biotechnol. 7: 47-58, 2007. Go to original source...
  10. Bassi R., Sandonà D., Croce R.: Novel aspects of chlorophyll a/b-binding proteins.-Physiol. Plantarum 100: 769-779, 1997. Go to original source...
  11. Belkhodja R., Morales F., Abadia A. et al.: Chlorophyll fluorescence as a possible tool for salinity tolerance screening in barley (Hordeum vulgare L.).-Plant Physiol. 104: 667-673, 1994. Go to original source...
  12. Bergantino E., Dainese P., Cerovic Z. et al.: A post-translational modification of the photosystem II subunit CP29 protects maize from cold stress.-J. Biol. Chem. 270: 8474-8481, 1995 Go to original source...
  13. Bongi G., Loreto F.: Gas-exchange properties of salt-stressed olive (Olea europea L.) leaves.-Plant Physiol. 90: 1408-1416, 1989. Go to original source...
  14. Boyer J.S.: Plant productivity and environment.-Science 218: 443-448, 1982. Go to original source...
  15. Brösche M., Strid A.: Molecular events following perception of ultraviolet-B radiation by plants.-Physiol. Plantarum 117: 1-10, 2003. Go to original source...
  16. Capel J., Jarillo J.A., Madueño F. et al.: Low temperature regulates Arabidopsis Lhcb gene expression in a lightindependent manner.-Plant J. 13: 411-418, 1998.
  17. de Montaigu A., Toth R., Coupland G.: Plant development goes like clockwork.-Trends Genet. 26: 296-306, 2010. Go to original source...
  18. El Rabey H.A., Al-Malki A.L., Abulnaja K.O., Rohde W.: Proteome analysis for understanding abiotic stress (salinity and drought) tolerance in Date Palm (Phoenix dactylifera L.).-Int. J. Genomics. 2015: 1-11, 2015. Go to original source...
  19. Engelken J., Brinkmann H., Adamska I.: Taxonomic distribution and origins of the extended LHC (light-harvesting complex) antenna protein superfamily.-BMC Evol. Biol. 10: 233, 2010.
  20. Engelken J., Funk C., Adamska I.: The extended light-harvesting complex (Lhc) protein superfamily: Classification and evolutionary dynamics.-In: Burnap R.L., Vermaas W.F.J. (ed.): Functional Genomics and Evolution of Photosynthetic Systems. Pp. 265-284, Springer, Dordrecht 2012. Go to original source...
  21. Everard J.D., Gucci R., Kann S.C. et al.: Gas exchange and carbon partitioning in the leaves of celery (Apium graveolens L.) at various levels of root zone salinity.-Plant Physiol. 106: 281-292, 1994. Go to original source...
  22. Fischer N., Boudreau E., Hippler M. et al.: A large fraction of PsaF is nonfunctional in photosystem I complexes lacking the PsaJ subunit.-Biochemistry 38: 5546-5552, 1999. Go to original source...
  23. Foyer C.H., Noctor G.: Leaves in the dark see the light.-Science 284: 599-601, 1999. Go to original source...
  24. Galvez-Valdivieso G., Mullineaux P.M.: The role of reactive oxygen species in signaling from chloroplasts to the nucleus.-Physiol. Plantarum 138: 430-439, 2010. Go to original source...
  25. Gasteiger E., Hoogland C., Gattiker A. et al.: Protein identification and analysis tools on the ExPASy server.-In: Walker J.M. (ed.), The Proteomics Protocols Handbook. Pp. 571-607. Humana Press, Totowa 2005. Go to original source...
  26. Geourjon C., Deleage G.: SOPMA: significant improvements in protein secondary structure prediction by consensus prediction form multiple alignments.-Comput. Appl. Biosci. 11: 681-684, 1995. Go to original source...
  27. Gobets B., van Grondelle R.: Energy transfer and trapping in photosystem I.-BBA-Bioenergetics 1507: 80-99, 2001. Go to original source...
  28. Green B.R., Durnford D.G.: The chlorophyll-carotenoid proteins of oxygenic photosynthesis.-Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 685-714, 1996. Go to original source...
  29. Green B.R., Pichersky E., Kloppstech K.: Chlorophyll a/bbinding proteins: an extended family.-Trends Biochem. Sci. 16: 181-186, 1991. Go to original source...
  30. Greenberg B.M., Gaba V., Canaani O. et al.: Separate photosensitizers mediate degradation of the 32 kDa photosystem II reaction centre protein in the visible and UV spectral regions.-P. Natl. Acad. Sci. USA 86: 6617-6620, 1989. Go to original source...
  31. Harding A.R.: Ginseng and Other Medicinal Plants. Pp. 367. Emporium Publications, Boston 1972.
  32. Henrysson T., Schröder W.P., Spangfort M., Akerlund H.E.: Isolation and characterization of the chlorophyll a/b protein complex CP29 from spinach.-BBA-Bioenergetics 977: 301-308, 1989. Go to original source...
  33. Hoffman N.E., Pichersky E., Malik V.S. et al.: A cDNA clone encoding a photosystem I protein with homology to photosystem II chlorophyll a/b-binding polypeptides.-P. Natl. Acad. Sci. USA 84: 8844-8848, 1987. Go to original source...
  34. Horton P., Ruban A.: Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection.-J. Exp. Bot. 56: 365-373, 2005.
  35. Humbeck K., Krupinska K.: The abundance of minor chlorophyll a/b -binding proteins CP29 and LHCI of barley (Hordeum vulgare L.) during leaf senescence is controlled by light.-J. Exp. Bot. 54: 375-383, 2003. Go to original source...
  36. Chitnis P.R.: Photosystem I: function and physiology.-Annu. Rev. Plant Phys. 52: 593-626, 2001. Go to original source...
  37. In J.G., Kim M.K., Lee O.R. et al.: Molecular identification of Korean mountain ginseng using an Amplification Refractory Mutation System (ARMS).-J. Ginseng Res. 34: 41-46, 2010. Go to original source...
  38. In J.G., Lee B.S., Youn J.H. et al.: Molecular characterization of a cDNA encoding chlorophyll a/b binding protein (cab) form Panax ginseng C. A. Meyer.-Korean J. Plant Res. 18: 441-449, 2005.
  39. Jansson S., Green B., Grossman A.R., Hiller R.: A proposal for extending the nomenclature of light-harvesting proteins of the three transmembrane helix type.-Plant Mol. Biol. Rep. 17: 221-224, 1999. Go to original source...
  40. Jansson S., Pichersky E., Bassi R. et al.: A nomenclature for the genes encoding the chlorophyll a/b -binding proteins of higher plants.-Plant Mol. Biol. Rep. 10: 242-253, 1992. Go to original source...
  41. Jansson S.: A guide to the identification of the Lhc genes and their relatives in Arabidopsis.-Trends Plant. Sci. 4: 236-240, 1999. Go to original source...
  42. Jansson S.: A protein family saga: From photoprotection to lightharvesting (and back).-In: Demmig-Adams B, Adams W.W.III., and Mattoo A.K. (ed.): Photoprotection, Photoinhibition, Gene Regulation and Environment. Pp. 145-153. Springer, Dordrecht 2006. Go to original source...
  43. Jensen P.E., Bassi R., Boekema E.J. et al.: Structure, function and regulation of plant photosystem I.-Biochim. Biophys. Acta 1767: 335-352, 2007. Go to original source...
  44. Jordan B.R.: Molecular response of plant cells to UV-B stress.-Funct. Plant Biol. 29: 909-918, 2002.
  45. Jordan B.R.: The effects of UV-B radiation on plants: a molecular perspective.-Adv. Bot. Res. 22: 97-162, 1996. Go to original source...
  46. Joshi P.N., Biswal B., Kulandaivelu G., Biswal U.C.: Response of senescing wheat leaves to ultraviolet-A light: changes in energy transfer efficiency and PSII photochemistry.-Radiat. Environ. Biophys. 33: 167-176, 1994. Go to original source...
  47. Joshi P.N., Gartia S., Pradhan M.K., Biswal B.: Photosynthetic response of clusterbean chloroplasts to UV-B radiation: energy imbalance and loss in redox homeostasis between QA and QB of photosystem II.-Plant. Sci. 181: 90-95, 2011. Go to original source...
  48. Joshi P.N., Misra A.N., Nayak L., Biswal B.: Response of mature, developing and senescing chloroplast to environmental stress.-In: Biswal B., Krupinska K., Biswal U.C. (ed.). Plastid Development in Leaves during Growth and Senescence. Pp. 641-668, Springer, Dordrecht 2013. Go to original source...
  49. Joshi P.N., Ramaswamy N.K., Raval M.K. et al.: Response of senescing leaves of wheat seedlings to UV-A radiation: inhibition of PSII activity in light and darkness.-Environ. Exp. Bot. 38: 237-242, 1997. Go to original source...
  50. Kim C., Choo G.C., Cho H.S., Lim J.T.: Soil properties of cultivation sites for mountain-cultivated ginseng at local level.-J. Ginseng Res. 39: 76-80, 2015. Go to original source...
  51. Kim M.K., Lee B.S., In J.G. et al.: Comparative analysis of expressed sequence tags (ESTs) of ginseng leaf.-Plant Cell Rep. 25: 599-606, 2006. Go to original source...
  52. Kim Y.H., Lim S., Han S.H. et al.: Differential expression of 10 sweetpotato peroxidades in response to sulfur dioxide, ozone, and ultraviolet radiation.-Plant Physiol. Biochem. 45: 908-914, 2007. Go to original source...
  53. Kim Y.J., Jeon J.N., Jang M.G. et al.: Ginsenoside profiles and related gene expression during foliation in Panax ginseng Meyer.-J. Ginseng Res. 38: 66-72, 2014a. Go to original source...
  54. Kim Y.J., Lee O.R., Oh J.Y. et al.: Functional analysis of HMGRs in biosynthesizing triterpene saponin in Panax ginseng.-Plant Physiol. 165: 1-16, 2014b.
  55. Kim Y.J., Shim J.S., Krishna P.R. et al.: Isolation and characterization of a glutaredoxin gene from Panax ginseng C. A. Meyer.-Plant Mol. Biol. Rep. 26: 335-349, 2008. Go to original source...
  56. Klimmek F., Sjödin A., Noutsos C. et al.: Abundantly and rarely expressed Lhc protein genes exhibit distinct regulation patterns in plants.-Plant Physiol. 140: 793-804, 2006. Go to original source...
  57. Kovacs E., Keresztes A.: Effect of gamma and UV-B/C radiation on plant cells.-Micron 33: 199-210, 2002. Go to original source...
  58. Krasensky J., Jonak C.: Drought, salt, and temperature stressinduced metabolic rearrangements and regulatory networks.-J. Exp. Bot. 63: 1593-1608, 2012. Go to original source...
  59. Kühlbrandt W., Wang D.N., Fujiyoshi Y.: Atomic model of plant light-harvesting complex by electron crystallography.-Nature 367: 614-621, 1994. Go to original source...
  60. Küpper H., Setlík I, Spiller M. et al.: Heavy metal-induced inhibition of photosynthesis: targets of in vivo metal chlorophyll formation.-J. Phycol. 38: 429-441, 2002. Go to original source...
  61. Kuttkat A. Hartmann A., Hobe S., Paulsen H.: The C-terminal domain of light-harvesting chlorophyll a/b -binding protein is involved in the stabilization of trimeric light-harvesting complex.-Eur. J. Biochem. 242: 288-292, 1996.
  62. Kwak J.M., Nguyen V., Schroeder J.I.: The role of reactive oxygen species in hormonal responses.-Plant Physiol. 141: 323-329, 2006. Go to original source...
  63. Kyte J., Doolittle R.F.: A simple method for displaying the hydropathic character of a protein.-J. Mol. Biol. 157: 105-132, 1982. Go to original source...
  64. Larbi A., Abadía A., Abadía J., Morales F.: Down co-regulation of light absorption, photochemistry, and carboxylation in Fedeficient plants growing in different environments.-Photosynth. Res. 89: 113-126, 2006. Go to original source...
  65. Lidon F.J.C., Reboredo F.H., Leitão A.E. et al.: Impact of UV-B radiation on photosynthesis-an overview.-Emir. J. Food Agric. 24: 546-556, 2012.
  66. Liu X.D., Shen Y.G.: NaCl-induced phosphorylation of light harvesting chlorophyll a/b proteins in thylakoid membranes from the halotolerant green alga, Dunaliella salina.-FEBS Lett. 569: 337-340, 2004. Go to original source...
  67. Livak K.J., Schmittgen T.D.: Analysis of relative gene expression data using realtime quantitative PCR and the 2(-delta delta C(T)) methods.-Methods 25: 402-408, 2001. Go to original source...
  68. Long S.P., Baker N.R.: Saline terrestrial environments.-In: Baker N.R., Long S.P. (ed.): Photosynthesis in Contrasting Environments. Pp. 63-102, Elsevier, New York 1986.
  69. Lu C., Jiang G., Wang B., Kuang T.: Photosystem II photochemistry and photosynthetic pigment composition in salt-adapted halophyte Artimisia anethifolia grown under outdoor conditions.-J. Plant Physiol. 160: 403-408, 2003. Go to original source...
  70. Lu C., Qiu N., Lu Q. et al.: Does salt stress lead to increased susceptibility of photosystem II to photoinhibition and changes in photosynthetic pigment composition in halophyte Suaeda salsa grown outdoors?-Plant Sci. 163: 1063-1068, 2002. Go to original source...
  71. Matsuoka M.: Classification and characterization of cDNA that encodes the light harvesting chlorophyll a/b -binding protein of photosystem II from Rice.-Plant Cell Physiol. 31: 519-526, 1990.
  72. Melkozernov A.N.: Excitation energy transfer in photosystem I from oxygenic organisms.-Photosynth. Res. 70: 129-153, 2001. Go to original source...
  73. Melkozernov A.N., Blankenship R.E.: Structural and functional organization of the peripheral light-harvesting system in photosystem I.-Photosynth. Res. 85: 33-50, 2005. Go to original source...
  74. Millar A.J., Kay S.: Integration of circadian and phototransduction pathways in the network controlling CAB gene transcription in Arabidopsis.-P. Natl. Acad. Sci. USA 93: 15491-15494, 1996. Go to original source...
  75. Munns R., Termaat A.: Whole plant responses to salinity.-Aust. J. Plant Physiol. 13: 143-160, 1986.
  76. Munns R.: Genes and salt tolerance: bringing them together.-New. Phytol. 167: 645-663, 2005. Go to original source...
  77. Nield J., Redding K., Hippler M.: Remodeling of light-harvesting protein complexes in Chlamydomonas in response to environmental changes.-Eucaryot. Cell 3: 1370-1380, 2004. Go to original source...
  78. Nott A., Jung H.S., Koussevitzky S., Chory J.: Plastid-to-nucleus retrograde signaling.-Annu. Rev. Plant Biol. 57: 739-759, 2006. Go to original source...
  79. Palomares R., Herrmann R.G., Oelmüller R.: Different blue-light requirement for the accumulation of transcripts from nuclear genes for thylakoid proteins in Nicotiana tabacum and Lycopersicon esculentum.-J. Photochem. Photobio. B. 11: 151-162, 1991. Go to original source...
  80. Parmenter G., Littlejohn R.: Effect of shade on growth and photosynthesis of Panax ginseng.-New Zeal. J. Crop Hort. Sci. 28: 255-269, 2000. Go to original source...
  81. Pätsikkä E., Kairavuo M., Šeršen F. et al.: Excess copper predisposes photosystem II to photoinhibition in vivo by outcompeting iron and causing decrease in leaf chlorophyll.-Plant Physiol. 129: 1359-1367, 2002. Go to original source...
  82. Peer W., Silverthorne J., Peters J.: Developmental and lightregulated expression of individual members of the lightharvesting complex b gene family in Pinus palustris.-Plant Physiol. 111: 627-634, 1996. Go to original source...
  83. Peng H., Kroneck P.M., Küpper H.: Toxicity and deficiency of copper in Elsholtzia splendens affect photosynthesis biophysics, pigments and metal accumulation.-Environ. Sci. Technol. 47: 6120-6128, 2013. Go to original source...
  84. Pichersky E., Bernatzky R., Tanksley S.D. et al.: Molecular characterization and genetic mapping of two clusters of genes encoding chlorophyll a/b -binding proteins in Lycopersicon esculentum (tomato).-Gene 40: 247-258, 1985. Go to original source...
  85. Pichersky E., Brock T.G., Nguyen D. et al.: A new member of the CAB gene family: structure, expression and chromosomal location of Cab-8, the tomato gene encoding the Type III chlorophyll a/b -binding polypeptide of photosystem I.-Plant Mol. Biol. 12: 257-270, 1989. Go to original source...
  86. Pichersky E., Hoffman N.E., Malik V.S. et al.: The tomato Cab-4 and Cab-5 genes encode a second type of CAB polypeptides localized in photosystem II.-Plant Mol. Biol. 9: 109-120, 1987. Go to original source...
  87. Pichersky E., Subramaniam R., White M.J. et al.: Chlorophyll a/b binding (CAB) polypeptides of CP29, the internal chlorophyll a/b complex of PSII: characterization of the tomato gene encoding the 26 kDa (type I) polypeptide, and evidence for a second CP29 polypeptide.-Mol. Gen. Genet. 227: 277-284, 1991. Go to original source...
  88. Pichersky E., Tanksley S.D., Piechulla B. et al.: Nucleotide sequence and chromosomal location of Cab-7, the tomato gene encoding the type II chlorophyll a/b-binding polypeptide of photosystem I.-Plant Mol. Biol. 11: 69-71, 1988. Go to original source...
  89. Pruneda-Paz J.L., Kay S.A.: An expanding universe of circadian networks in high plants.-Trends Plant Sci. 15: 259-265, 2010. Go to original source...
  90. Ruban A.V., Berera R., Ilioaia C. et al.: Identification of a mechanism of photoprotective energy dissipation in higher plants.-Nature 450: 575-578, 2007. Go to original source...
  91. Schwartz E., Pichersky E.: Sequence of two tomato nuclear genes encoding chlorophyll a/b -binding proteins of CP24, a PSII antenna component.-Plant Mol. Biol. 15: 157-160, 1990. Go to original source...
  92. Schwartz E., Shen D., Aebersold R. et al.: Nucleotide sequence and chromosomal location of Cab11 and Cab12, the genes for the fourth polypeptide of the photosystem I light-harvesting antenna (LHCI).-FEBS Lett. 280: 229-234, 1991. Go to original source...
  93. Schwartz E., Stasys R., Aebersold R. et al.: Sequence of a tomato gene encoding a third type of LHCII chlorophyll a/b -binding polypeptide.-Plant Mol. Biol. 17: 923-925, 1991. Go to original source...
  94. Silverthorne J., Tobin E.M.: Demonstration of transcriptional regulation of specific genes by phytochrome action.-P. Natl. Acad. Sci. USA 81: 1112-1116, 1984. Go to original source...
  95. Spangfort M., Larsson U.K., Ljungberg U. et al.: The 20 kDa apo-polypeptide of the chlorophyll a/b protein complex CP24 -Characterization and complete primary amino sequence.-In: Baltscheffsky M (ed.): Current Research in Photosynthesis. Vol. 2. Pp. 253-256. Kluwer Acad. Publ., Dordrecht 1990. Go to original source...
  96. Stahl D.J, Kloos D.U., Hehl R.: A sugar beet chlorophyll a/b binding protein promoter void of G-box like elements confers strong and leaf specific reporter gene expression in transgenic sugar beet.-BMC Biotech. 4: 31, 2004. Go to original source...
  97. Staneloni R.T., Rodriguez-Batiller M.J., Casal J.J.: Abscisic acid, high-light, and oxidative stress down-regulate a photosynthetic gene via a promoter motif not involved in phytochromemediated transcriptional regulation.-Mol. Plant. 1: 75-83, 2008. Go to original source...
  98. Sun L., Tobin E.M.: Phytochrome-regulated expression of genes encoding light-harvesting chlorophyll a/b-binding protein in two long hypocotyls mutants and wild type plants of Arabidopsis thaliana.-Photochem. Photobiol. 52: 51-56, 1990. Go to original source...
  99. Tao L., Zeba N., Ashrafuzzaman M., Hong C.B.: Heavy metal stress-inducible early light-inducible gene CaELIP from hot pepper (Capsicum annuum) shows broad expression patterns under various abiotic stresses and circadian rhythmicity.-Environ. Exp. Bot. 72: 297-303, 2011. Go to original source...
  100. 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...
  101. Thines B., Harmon F.G.: Four easy pieces: mechanisms underlying circadian regulation of growth and development.-Curr. Opin. Plant Biol. 14: 31-37, 2011. Go to original source...
  102. Vass I., Turcsányi E., Touloupakis E. et al.: The mechanism of UV-A radiation induced inhibition of photosystem II electron transport studied by EPR and Chl fluorescence.-Biochemistry 41: 10200-10208, 2002. Go to original source...
  103. Weatherwax S.C., Ong M.S., Degenhardt J. et al.: The interaction of light and abscisic acid in the regulation of plant gene expression.-Plant Physiol. 111: 363-370, 1996. Go to original source...
  104. Wientjes E., Van Amerongen H., Croce R: LHCII is an antenna of both photosystems after long-term acclimation.-Biochim. Biophys. Acta. 1827: 420-426, 2013.
  105. Wollman F.A.: State transitions reveal the dynamics and flexibility of the photosynthetic apparatus.-EMBO J. 20: 3623-3630, 2001. Go to original source...
  106. Xu Y.H., Liu R., Yan L. et al.: Light-harvesting chlorophyll a/b -binding proteins are required for stomatal response to abscisic acid in Arabidopsis.-J. Exp. Bot. 63: 1095-1106, 2012. Go to original source...
  107. Yang D.H., Webster J., Adam Z. et al.: Induction of acclimative proteolysis of the light-harvesting chlorophyll a/b protein of photosystem II in response to elevated light intensities.-Plant Physiol. 118: 827-834, 1998. Go to original source...