Summary
Plants have diverse defense mechanisms against high light stress. Plants can reduce absorption of light energy through chloroplast avoidance and antenna size reduction. However, the capacity of the avoidance and the antenna size reduction for protection is limited, so that plants often absorb more energy than they can use. Therefore, plants need mechanisms to deal with this excess absorbed light energy, such as harmless thermal dissipation by feedback de-excitation. The transthylakoid pH gradient, xanthophyll cycle, PsbS, and other light-harvesting complex proteins are required for this thermal dissipation. In addition, alternative electron transport allows electrons to pass to acceptors other than CO2, thereby relieving overreduction of electron transport components in high light conditions. To detoxify reactive oxygen species that are inevitably produced during high light stress, plants have antioxidants including carotenoids, ascorbate, and tocopherols. In spite of these photoprotective mechanisms, photodamage may still occur, and efficient repair of damaged systems could be a photoprotective mechanism. In this chapter, recently published molecular genetics studies on each step of photoprotection have been reviewed. Genes required for each defense mechanism that have been identified thus far are introduced, and cloned genes that can possibly be related to photoprotection are discussed.
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References
Adam Z, Adamska I, Nakabayashi K, OstersetzerO, Haussuhl K, Manuell A, ZhengB,VallonO, Rodermel SR, ShinozakiKand Clarke AK (2001) Chloroplast and mitochondrial proteases in Arabidopsis. A proposed nomenclature. Plant Physiol 125: 1912–1918
Adams WW III, Demmig-Adams B, Winter K and Schreiber U (1990) The ratio of variable to maximum chlorophyll fluorescence from photosystem II, measured in leaves at ambient temperature and at 77 K, as an indicator of the photon yield of photosynthesis. Planta 180: 166–174
Adams WW III, Zarter CR, Ebbert V and Demmig-Adams B (2004) Photoprotective strategies of overwintering evergreens. BioScience 54: 41–49
Adamska I, Ohad I and Kloppstech K (1992) Synthesis of the early light-inducible protein is controlled by blue light and related to light stress. Proc Natl Acad Sci USA 89: 2610–2613
Anderson JM (1986) Photoregulation of the composition, function, and structure of thylakoid membranes. Annu Rev Plant Physiol 37: 93–136
Andersson J, Walters RG, Horton P and Jansson S (2001) Antisense inhibition of the photosynthetic antenna proteins CP29 and CP26: implications for the mechanism of protective energy dissipation. Plant Cell 13: 1193–1204
Andersson J, Wentworth M, Walters RG, Howard CA, RubanAV, Horton P and Jansson S (2003a) 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
Andersson U, Heddad M and Adamska I (2003b) Light stressinduced one-helix protein of the chlorophyll a/b-binding family associated with photosystem I. Plant Physiol 132: 811–820
Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50: 601–639
Aspinall-O’Dea M, Wentworth M, Pascal A, Robert B, Ruban A and Horton P (2002) In vitro reconstitution of the activated zeaxanthin state associated with energy dissipation in plants. Proc Natl Acad Sci USA 99: 16331–16335
Bailey S, Walters RG, Jansson S and Horton P (2001) Acclimation of Arabidopsis thaliana to the light environment: the existence of separate lowlight and high light responses. Planta 213: 794–801
Bailey S, Thompson E, Nixon PJ, Horton P, Mullineaux CW, Robinson C and Mann NH (2002) A critical role for the Var2 FtsH homologue of Arabidopsis thaliana in the photosystem II repair cycle in vivo. J Biol Chem 277: 2006–2011
Barber J and Andersson B (1992) Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci 17: 61–66
Baroli I and Melis A (1998) Photoinhibitory damage is modulated by the rate of photosynthesis and by the photosystem II light-harvesting chlorophyll antenna size. Planta 205: 288– 296
Baroli I and Niyogi KK (2000) Molecular genetics and xanthophyll-dependent photoprotection in green algae and plants. Phil Trans R Soc Lond B 355: 1385–1394
Baroli I, Do AD, Yamane T and Niyogi, KK (2003) Zeaxanthin accumulation in the absence of a functional xanthophyll cycle protects Chlamydomonas reinhardtii from photooxidative stress. Plant Cell 15: 992–1008
Bartley GE and Scolnik PA (1995) Plant carotenoids: pigments for photoprotection, visual attraction, and human health. Plant Cell 7: 1027–1038
Bassi R, Sandonà D and Croce R (1997) Novel aspects of chlorophyll a/b-binding proteins. Physiol Plant 100: 769–779
Bendall DS and Manasse RS (1995) Cyclic photophosphorylation and electron transport. Biochim Biophys Acta 1229: 23–38
Bilger W and Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of lightinduced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res 25: 173—185
Björkman O and Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170: 489–504
Burrows PA, Sazanov LA, Svab Z, Maliga P and Nixon PJ (1998) Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J 17: 868–876
Chen M, Choi YD, Voytas DF and Rodermel S (2000) Mutations in the Arabidopsis VAR2 locus cause leaf variegation due to the loss of a chloroplast FtsH protease. Plant J 22: 303–313
Cheng Z, Sattler S, Maeda H, Sakuragi Y, Bryant DA and DellaPenna D (2003) Highly divergent methyltransferases catalyze a conserved reaction in tocopherol and plastoquinone synthesis in cyanobacteria and photosynthetic eukaryotes. Plant Cell 15: 2343–2356
Collakova E and DellaPenna D (2001) Isolation and functional analysis of homogentisate phytyltransferase from Synechocystis sp. PCC 6803 and Arabidopsis. Plant Physiol 127: 1113– 1124
Collakova E and DellaPenna D (2003) Homogentisate phytyltransferase activity is limiting for tocopherol biosynthesis in Arabidopsis. Plant Physiol 131: 632–642
Conklin PL (2001) Recent advances in the role and biosynthesis of ascorbic acid in plants. Plant Cell Environ 24: 383–394
Conklin PL, Williams EH and Last RL (1996) Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant. Proc Natl Acad Sci USA 93: 9970–9974
Conklin PL, Saracco SA, Norris SR and Last RL (2000) Identification of ascorbic acid-deficient Arabidopsis thaliana mutants. Genetics 154: 847–856
Davison PA, Hunter CN and Horton P (2002) Overexpression of β-carotene hydroxylase enhances stress tolerance in Arabidopsis. Nature 418: 203–206
Demmig-Adams B, Adams WW, Heber U, Neimanis S, Winter K, Krüger A, Czygan F-C, Bilger W and Björkman O (1990) Inhibition of zeaxanthin formation and of rapid changes in radiationless energy dissipation by dithiothreitol in spinach leaves and chloroplasts. Plant Physiol 92: 293–301
Dunaeva M and Adamska I (2001) Identification of genes expressed in response to light stress in leaves of Arabidopsis thaliana using RNA differential display. Eur J Biochem 268: 5521–5529
Elrad D, Niyogi KK and Grossman AR (2002) A major lightharvesting polypeptide of photosystem II functions in thermal dissipation. Plant Cell 14: 1801–1816
Endo T, Shikanai T, Takabayashi A, Asada K and Sato F (1999) The role of chloroplastic NAD(P)H dehydrogenase in photoprotection. FEBS Lett 457: 5–8
Escoubas J-M, Lomas M, LaRoche J and Falkowski PG (1995) Light Intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. Proc Natl Acad Sci USA 92: 10237–10241
Foyer CH and Harbinson J (1999) Relationships between antioxidant metabolism and carotenoids in the regulation of photosynthesis. In: Frank HA, Young AJ, Britton G and Cogdell RJ (eds) The Photochemistry of Carotenoids, pp 305–325. Kluwer Academic Publishers, Dordrecht
Frank HA and Cogdell RJ (1993) The photochemistry and function of carotenoids in photosynthesis. In: Young A and Britton G (eds) Carotenoids in Photosynthesis, pp 252–326. Champman & Hall, London
Fryer MJ (1992) The antioxidant effects of thylakoid vitamin E (α-tocoherol). Plant Cell Environ 15: 381–392
Golan T, Li X-P, Müller-Moulé P and Niyogi KK (2004) Using mutants to understand light stress acclimation in plants. In: Papageorgiou C and Govindjee (eds) Chlorophyll a Fluorescence: A Signature of Photosynthesis, pp 525–554. Kluwer Academic Publishers, Dordrecht, Dordrecht
Heddad M and Adamska I (2000) Light stress-regulated twohelix proteins in Arabidopsis thaliana related to the chlorophyll a/b-binding gene family. Proc Natl Acad Sci USA 97: 3741–3746
HiharaY, Kamei A, Kanehisa M, Kaplan A and Ikeuchi M (2001) DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. Plant Cell 13: 793–806
Huala E, Oeller PW, Liscum E, Han I-S, Larsen E and Briggs WR (1997) Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain. Science 278: 2120–2123
Hutin C, Nussaume L, Moise N, Moya I, Kloppstech K and Havaux M (2003) Early light-induced proteins protect Arabidopsis from photooxidative stress. Proc Natl Acad Sci USA 100: 4921–4926
Jahns P and Krause GH (1994) Xanthophyll cycle and energydependent fluorescence quenching in leaves from pea plants grown under intermittent light. Planta 192: 176–182
Jahns P and Schweig S (1995) Energy-dependent fluorescence quenching in thylakoids from intermittent light grown pea plants: evidence for an interaction of zeaxanthin and the chlorophyll a/b binding protein CP26. Plant Physiol Biochem 33: 683–687
Jansson S, Anderson J, Kim SJ and Jackowski G (2000) An Arabidopsis thaliana protein homologous to cyanobacterial high-light-inducible proteins. Plant Mol Biol 42: 345–351
Jarillo JA, Gabrys H, Capel J, Alonso JM, Ecker JR and Cashmore AR (2001) Phototropin-related NPL1 controls chloroplast relocation induced by blue light. Nature 410: 952–954
Joët T, Cournac L, Horvath EM, Medgyesy P and Peltier G (2001) Increased sensitivity of photosynthesis to antimycin A induced by inactivation of the chloroplast ndhB gene. Evidence for a participation of the NADH-dehydrogenase complex to cyclic electron flow around photosystem I. Plant Physiol 125: 1919–1929
Kagawa T and Wada M (1999) Chloroplast-avoidance response induced by high-fluence blue light in prothallial cells of the fern Adiantum capillus-veneris as analyzed by microbeam irradiation. Plant Physiol 119: 917–923
Kagawa T and Wada M (2000) Blue light-induced chloroplast relocation in Arabidopsis thaliana as analyzed by microbeam irradiation. Plant Cell Physiol 41: 84–93
Kagawa T and Wada M (2002) Blue light-induced chloroplast relocation. Plant Cell Physiol 43: 367–371
Kagawa T, Sakai T, Suetsugu N, Oikawa K, Ishiguro S, Kato T, Tabata S, Okada K and Wada M (2001) Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291: 2138–2141
Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M and Wada M (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420: 829–832
Kim S, Pichersky E and Yocum CF (1994) Topological studies of spinach 22 kDa protein of photosystem II. Biochim Biophys Acta 1188: 339–348
Kimura M, Yamamoto YY, Seki M, Sakurai T, Sato M, Abe T, Yoshida S, Manabe K, Shinozaki K and Matsui M (2003) Identification of Arabidopsis genes regulated by high light-stress using cDNA microarray. Photochem Photobiol 77: 226–233
Larkin RM, Alonso JM, Ecker JR and Chory J (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299: 902–906
Li X-P, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S and Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403: 391–395
Li X-P, Phippard A, Pasari J and Niyogi KK (2002) Structure– function analysis of photosystem II subunit S (PsbS) in vivo. Func Plant Biol 29: 1131–1139
Lindahl M, Tabak S, Cseke L, Pichersky E, Andersson B and Adam Z (1996) Identification, characterization, and molecular cloning of a homologue of the bacterial FtsH protease in chloroplasts of higher plants. J Biol Chem 271: 29329–29334
Lindahl M, Spetea C, Hundal T, Oppenheim AB, Adam Z and Andersson B (2000) The thylakoid FtsH protease plays a role in the light-induced turnover of the photosystem II D1 protein. Plant Cell 12: 419–432
Long SP, Humphries S and Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45: 633–662
Ma Y-Z, Holt NE, Li X-P, Niyogi KK and Fleming GR (2003) Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting. Proc Natl Acad Sci USA 100: 4377–4382
Maxwell DP, Laudenbach DE and Huner N (1995) Redox regulation of light-harvesting complex II and cab mRNA abundance in Dunaliella salina. Plant Physiol 109: 787–795
Maxwell K and Johnson GN (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51: 659–668
Melis A (1999) Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? Trends Plant Sci 4: 130–135
Mochizuki N, Brusslan JA, Larkin R, Nagatani A and Chory J (2001) Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Natl Acad Sci USA 98: 2053–2058
Montané M-H and Kloppstech K (2000) The family of lightharvesting- related proteins (LHCs, ELIPs, HLIPs): was the harvesting of light their primary function? Gene 258: 1–8
Müller P, Li X-P and Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125: 1558–1566
Müller-Moulé P, Conklin PL and Niyogi KK (2002) Ascorbate deficiency can limit violaxanthin de-epoxidase activity in vivo. Plant Physiol 128: 970–977
Müller-Moulé P, Havaux M and Niyogi KK (2003) Zeaxanthin deficiency enhances the high light sensitivity of an ascorbatedeficient mutant of Arabidopsis. Plant Physiol 133: 748–760
Munekage Y, Takeda S, Endo T, Jahns P, Hashimoto T and Shikanai T (2001) Cytochrome b6 f mutation specifically affects thermal dissipation of absorbed light energy in Arabidopsis. Plant J 28: 351–359
Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M and Shikanai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110: 361–371
Munné-Bosch S and Alegre L (2002) The function of tocopherols and tocotrienols in plants. Crit Rev Plant Sci 21: 31–57
Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50: 333–359
Niyogi KK (2000) Safety valves for photosynthesis. Curr Op Plant Biol 3: 455–460
Niyogi KK, Björkman O and Grossman AR (1997) Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenching. Plant Cell 9: 1369–1380
Niyogi KK, Grossman AR and Björkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10: 1121–1134
Noguchi T (2002) Dual role of triplet localization on the accessory chlorophyll in the photosystem II reaction center: photoprotection and photodamage of the D1 protein. Plant Cell Physiol. 43: 1112–1116
Ort DR (2001) When there is too much light. Plant Physiol 125: 29–32
Ort DR and Baker NR (2002) A photoprotective role for O2 as an alternative electron sink in photosynthesis? Curr Op Plant Biol 5: 193–198
Oswald O, Martin T, Dominy PJ and Graham IA (2001) Plastid redox state and sugars: interactive regulators of nuclear-encoded photosynthetic gene expression. Proc Natl Acad Sci USA 98: 2047–2052
Palatnik JF, Tognetti VB, Poli HO, Rodriguez RE, Blanco N, Gattuso M, Hajirezaei M-R, Sonnewald U, Valle EM and Carrillo N (2003) Transgenic tobacco plants expressing antisense ferredoxin-NADP(H) reductase transcripts display increased susceptibility to photo-oxidative damage. Plant J 35: 332–341
Park Y, Chow WS and Anderson JM (1997) Antenna size dependency of photoinactivation of photosystem II in light-acclimated pea leaves. Plant Physiol 115: 151–157
Pfannschmidt T, Schütze K, Fey V, Sherameti I and Oelmüller R (2003) Chloroplast redox control of nuclear gene expression-a new class of plastid signals in interorganellar communication. Antioxid Redox Signal 5: 95–101
Porfirova S, Bergmüller E, Tropf S, Lemke R and Dörmann P (2002) Isolation of an Arabidopsis mutant lacking vitamin E and identification of a cyclase essential for all tocopherol biosynthesis. Proc Natl Acad Sci USA 99: 12495–12500
Rossel JB, Wilson IW and Pogson BJ (2002) Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol 130: 1109–1120
Ruban AV, Pesaresi P, Wacker U, Irrgang KD, Bassi R and Horton P (1998) The relationship between the binding of dicyclohexylcarbodiimide and quenching of chlorophyll fluorescence in the light-harvesting proteins of photosystem II. Biochemistry 37: 11586–11591
Sakai T, Kagawa T, Kasahara M, Swartz TE, Christie JM, Briggs WR, Wada M and Okada K (2001) Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Proc Natl Acad Sci USA 98: 6969–6974
Sakamoto W, Tamura T, Hanba-Tomita Y, Sodmergen and Murata M (2002) The VAR1 locus of Arabidopsis encodes a chloroplastic FtsH and is responsible for leaf variegation in the mutant alleles. Genes Cells 7: 769–780
Sattler SE, Cahoon EB, Coughlan SJ and DellaPenna D (2003) Characterization of tocopherol cyclases from higher plants and cyanobacteria. Evolutionary implications for tocopherol synthesis and function. Plant Physiol 132: 2184–2195
Savidge B, Weiss JD, Wong Y-H H, Lassner MW, Mitsky TA, Shewmaker CK, Post-Beittenmiller D and Valentin HE (2002) Isolation and characterization of homogentisate phytyltransferase genes from Synechocystis sp. PCC 6803 and Arabidopsis. Plant Physiol 129: 321–332
Schreiber U, Schliwa U and Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10: 51–62
Shikanai T, Endo T, Hashimoto T, Yamada Y, Asada K and Yokota A (1998) Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc Natl Acad Sci USA 95: 9705–9709
Shikanai T, Munekage Y, Shimizu K, Endo T and Hashimoto T (1999) Identification and characterization of Arabidopsis mutants with reduced quenching of chlorophyll fluorescence. Plant Cell Physiol 40: 1134–1142
Silva P, Thompson E, Bailey S, Kruse O, Mullineaux CW, Robinson C, Mann NH and Nixon PJ (2003) FtsH is involved in the early stages of repair of photosystem II in Synechocystis sp. PCC 6803. Plant Cell 15: 2152–2164
Smirnoff N (2000) Ascorbate biosynthesis and function in photoprotection. Phil Trans R Soc Lond B 355: 1455–1464
Strand Â, Asami T, Alonso J, Ecker JR and Chory J (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 421: 79–83
Surpin M, Larkin RM and Chory J (2002) Signal transduction between the chloroplast and the nucleus. Plant Cell 14: S327–338
Susek RE, Ausubel FM and Chory J (1993) Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74: 787– 799
Takechi K, Sodmergen, Murata M, Motoyoshi F and Sakamoto W (2000) The YELLOW VARIEGATED (VAR2) locus encodes a homologue of FtsH, an ATP-dependent protease in Arabidopsis. Plant Cell Physiol 41: 1334–1346
Wada M, Kagawa T and Sato Y (2003) Chloroplast Movement. Annu Rev Plant Biol 54: 455–468
Walters RG, Ruban AV and Horton P (1996) Identification of proton-active residues in a higher plant light-harvesting complex. Proc Natl Acad Sci USA 93: 14204–14209
Walters RG, Shephard F, Rogers JJM, Rolfe SA and Horton P (2003) Identification of mutants of Arabidopsis defective in acclimation of photosynthesis to the light environment. Plant Physiol 131: 472–481
Wollman F-A, Minai L and Nechushtai R (1999) The biogenesis and assembly of photosynthetic proteins in thylakoid membranes. Biochim Biophys Acta 1411: 21– 85
Yamamoto HY, Nakayama TO and Chichester CO (1962) Studies on the light and dark interconversions of leaf xanthophylls. Arch Biochem Biophys 97: 168–173
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Jung, HS., Niyogi, K.K. (2008). Molecular Analysis of Photoprotection of Photosynthesis. In: Demmig-Adams, B., Adams, W.W., Mattoo, A.K. (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment. Advances in Photosynthesis and Respiration, vol 21. Springer, Dordrecht. https://doi.org/10.1007/1-4020-3579-9_9
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