Photosynthetic light reactions - An adjustable hub in basic production and plant immunity signaling

Plant Physiology and Biochemistry

Volumn 81, Issue , 2014, Pages 128-134

  Kangasjärvi, Saijaliisa ^a   Tikkanen, Mikko ^a   Durian, Guido ^a   Aro, Eva Mari ^a  

^a UNIVERSITY OF TURKU   (Finland)

Author keywords

Cyclic electron flow; Light stress; Linear electron flow; Photoprotection; Photosynthetic light reactions; Plant immunity

Indexed keywords

LIGHT HARVESTING SYSTEM; OXYGEN; PHOTOSYNTHESIS; PHOTOSYSTEM II;

CHLOROPLAST; ELECTRON TRANSPORT; IMMUNOLOGY; LIGHT; LIGHT HARVESTING SYSTEM; METABOLISM; PHOTOSYNTHESIS; PHOTOSYSTEM II; PHYSIOLOGICAL STRESS; PLANT; PLANT IMMUNITY; RADIATION RESPONSE; SIGNAL TRANSDUCTION; THYLAKOID;

CHLOROPLASTS; ELECTRON TRANSPORT; LIGHT; LIGHT-HARVESTING PROTEIN COMPLEXES; OXYGEN; PHOTOSYNTHESIS; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT IMMUNITY; PLANTS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; THYLAKOIDS;

EID: 84904213164     PISSN: 09819428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plaphy.2013.12.004     Document Type: Review

References (92)

1. Amunts A., Toporik H., Borovikova A., Nelson N. Structure determination and improved model of plant photosystem I. J.Biol. Chem. 2010, 285:3478-3486.
2. Anderson J.M., Aro E.M. Grana stacking and protection of photosystem-II in thylakoid membranes of higher-plant leaves under sustained high irradiance - a hypothesis. Photosynth. Res. 1994, 41:315-326.
3. Anderson J.M., Horton P., Kim E.H., Chow W.S. Towards elucidation of dynamic structural changes of plant thylakoid architecture. Philos. Trans. R Soc. Lond. B Biol. Sci. 2012, 367:3515-3524. 10.1098/rstb.2012.0373.
4. Aro E.M., Virgin I., Andersson B. Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim. Biophys. Acta 1993, 1143:113-134.
5. Badger M.R., von Caemmerer S., Ruuska S., Nakano H. Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase. Philos. Trans. R Soc. Lond. B Biol. Sci. 2000, 355:1433-1446.
6. Bailey S., Horton P., Walters R.G. Acclimation of Arabidopsis thaliana to the light environment: the relationship between photosynthetic function and chloroplast composition. Planta 2004, 218:793-802.
7. Barber J., Andersson B. Too much of a good thing: light can be bad for photosynthesis. Trends Biochem. Sci. 1992, 17:61-66. 10.1016/0968-0004(92)90503-2.
8. Barber J., Horton P. Integrating current knowledge in various aspects of thylakoid membrane structure and dynamics. Philos. Trans. R Soc. Lond. B Biol. Sci. 2012, 367:3381-3383. 10.1098/rstb.2012.0329.
9. Bellafiore S., Bameche F., Peltier G., Rochaix J.D. State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 2005, 433:892-895.
10. Bendall D.S. Photosynthetic cytochromes of oxygenic organisms. Biochim. Biophys. Acta 1982, 683:119-151.
11. Bernoux M., Ellis J.G., Dodds P.N. New insights in plant immunity signaling activation. Curr. Opin. Plant Biol. 2011, 14:512-518. 10.1016/j.pbi.2011.05.005.
12. Bonardi V., Pesaresi P., Becker T., Schleiff E., Wagner R., Pfannschmidt T., Jahns P., Leister D. Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature 2005, 437:1179-1182.
13. Bondarava N., Gross C.M., Mubarakshina M., Golecki J.R., Johnson G.N., Krieger-Liszkay A. Putative function of cytochrome b559 as a plastoquinol oxidase. Physiol. Plant 2010, 138:463-473.
14. + channel controls photosynthetic light utilization in plants. Science 2013, 342:114-118. 10.1126/science.1242113.
15. Chinchilla D., Bauer Z., Regenass M., Boller T., Felix G. The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 2006, 18:465-476. 10.1105/tpc.105.036574.
16. Chow W.S., Melis A., Anderson J.M. Adjustments of photosystem stoichiometry in chloroplasts improve the quantum efficiency of photosynthesis. Proc. Natl. Acad. Sci. U S A 1990, 87:7502-7506.
17. DalCorso G., Pesaresi P., Masiero S., Aseeva E., Schuenemann D., Finazzi G., Joliot P., Barbato R., Leister D. Acomplex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 2008, 132:273-285.
18. Dietzel L., Pfannschmidt T. Photosynthetic acclimation to light gradients in plant stands comes out of shade. Plant. Signal. Behav. 2008, 3:1116-1118.
19. 2 assimilation is restricted. Plant Cell Environ. 2011, 34:837-846. 10.1111/j.1365-3040.2011.02288.x.
20. Foyer C.H., Noctor G. Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid. Redox Signal. 2009, 11:861-905. 10.1089/ars.2008.2177.
21. García-Andrade J., Ramírez V., López A., Vera P. Mediated plastid RNA editing in plant immunity. PLoS Pathog. 2013, 9(10):e1003713. 10.1371/journal.ppat.1003713.
22. Gawroński P., Górecka M., Bederska M., Rusaczonek A., Ślesak I., Kruk J., Karpiński S. Isochorismate synthase 1 is required for thylakoid organization, optimal plastoquinone redox status, and state transitions in Arabidopsis thaliana. J.Exp. Bot. 2013, 64:3669-3679. 10.1093/jxb/ert203.
23. Göhre V., Jones A.M., Sklenář J., Robatzek S., Weber A.P. Molecular crosstalk between PAMP-triggered immunity and photosynthesis. Mol. Plant Microbe Interact. 2012, 25:1083-1092. 10.1094/MPMI-11-11-0301.
24. Grieco M., Tikkanen M., Paakkarinen V., Kangasjärvi S., Aro E.M. Steady-state phosphorylation of light-harvesting complex II proteins preserves photosystem I under fluctuating white light. Plant Physiol. 2012, 160:1896-1910. 10.1104/pp.112.206466.
25. Herbstova M., Tietz S., Kinzel C., Turkina M.V., Kirchhoff H. Architectural switch in plant photosynthetic membranes induced by light stress. Proc. Natl. Acad. Sci. U S A 2012, 109:20130-20135.
26. Hideg E., Kálai T., Hideg K., Vass I. Photoinhibition of photosynthesis invivo results in singlet oxygen production detection via nitroxide-induced fluorescence quenching in broad bean leaves. Biochemistry 1998, 37:11405-11411. 10.1021/bi972890+.
27. Hüner N.P., Bode R., Dahal K., Hollis L., Rosso D., Krol M., Ivanov A.G. Chloroplast redox imbalance governs phenotypic plasticity: the "grand design of photosynthesis" revisited. Front Plant Sci. 2012, 3:255. 10.3389/fpls.2012.00255.
28. Ifuku K., Endo T., Shikanai T., Aro E. Structure of the chloroplast NADH dehydrogenase-like complex: nomenclature for nuclear-encoded subunits. Plant Cell Physiol. 2011, 52:1560-1568.
29. Jahns P., Holzwarth A.R. The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim. Biophys. Acta 2012, 1817:182-193. 10.1016/j.bbabio.2011.04.012.
30. Jang C., Seo E.Y., Nam J., Bae H., Gim Y.G., Kim H.G., Cho I.S., Lee Z.W., Bauchan G.R., Hammond J., Lim H.S. Insights into Alternanthera mosaic virus TGB3 Functions: interactions with Nicotiana benthamiana PsbO correlate with chloroplast vesiculation and veinal necrosis caused by TGB3 over-expression. Front. Plant Sci. 2013, 31(4):5. 10.3389/fpls.2013.00005.
31. Jelenska J., Yao N., Vinatzer B.A., Wright C.M., Brodsky J.L., Greenberg J.T. AJ domain virulence effector of Pseudomonas syringae remodels host chloroplasts and suppresses defenses. Curr. Biol. 2007, 17:499-508. 10.1016/j.cub.2007.02.028.
32. Johansson Jänkänpää H., Frenkel M., Zulfugarov I., Reichelt M., Krieger-Liszkay A., Mishra Y., Gershenzon J., Moen J., Lee C.H., Jansson S. Non-photochemical quenching capacity in Arabidopsis thaliana affects herbivore behaviour. PLoS One 2013, 8(1):e53232. 10.1371/journal.pone.0053232.
33. Johnson G.N. Reprint of: physiology of PSI cyclic electron transport in higher plants. Biochim. Biophys. Acta 2011, 1807:906-911.
34. Jones A.M., Thomas V., Bennett M.H., Mansfield J., Grant M. Modifications to the Arabidopsis defense proteome occur prior to significant transcriptional change in response to inoculation with Pseudomonas syringae. Plant Physiol. 2006, 142:1603-1620. 10.1104/pp.106.086231.
35. Jones J.D., Dangl J.L. The plant immune system. Nature 2006, 444:323-329. 10.1038/nature05286.
36. Joo J.H., Wang S., Chen J.G., Jones A.M., Fedoroff N.V. Different signaling and cell death roles of heterotrimeric G protein alpha and beta subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell 2005, 17:957-970. http://dx.doi.org/10.1105/tpc.104.029603.
37. Kangasjärvi S., Neukermans J., Li S., Aro E.M., Noctor G. Photosynthesis, photorespiration, and light signalling in defense responses. J.Exp. Bot. 2012, 63:1619-1636. 10.1093/jxb/err402.
38. Karpinski S., Reynolds H., Karpinska B., Wingsle G., Creissen G., Mullineaux P. Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 1999, 284:654-657.
39. Karpiński S., Szechyńska-Hebda M., Wituszyńska W., Burdiak P. Light acclimation, retrograde signalling, cell death and immune defences in plants. Plant Cell Environ. 2013, 36:736-744. 10.1111/pce.12018.
40. Kim C., Meskauskiene R., Zhang S., Lee K.P., Lakshmanan Ashok M., Blajecka K., Herrfurth C., Feussner I., Apel K. Chloroplasts of Arabidopsis are the source and a primary target of a plant-specific programmed cell death signaling pathway. Plant Cell 2012, 24:3026-3039. 10.1105/tpc.112.100479.
41. Kramer D.M., Cruz J.A., Kanazawa A. Balancing the central roles of the thylakoid proton gradient. Trends Plant Sci. 2003, 8:27-32.
42. Külheim C., Agren J., Jansson S. Rapid regulation of light harvesting and plant fitness in the field. Science 2002, 297:91-93.
43. Lee K.P., Kim C., Landgraf F., Apel K. EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. Proc. Natl. Acad. Sci. U S A 2007, 104:10270-10275. 10.1073/pnas.0702061104.
44. Lehto K., Tikkanen M., Hiriart J.B., Paakkarinen V., Aro E.M. Depletion ofthe photosystem II core complex in mature tobacco leaves infected by the flavum strain of tobacco mosaic virus. Mol. Plant. Microbe. Interact. 2003, 16:1135-1144.
45. Li X.P., Gilmore A.M., Caffarri S., Bassi R., Golan T., Kramer D., Niyogi K.K. Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J.Biol. Chem. 2004, 279:22866-22874.
46. Macpherson A.N., Telfer A., Truscott T.G., Barber J. Direct detection of singlet oxygen from isolated photosystem II reaction centres. Biochim. Biophys. Acta 1993, 1143:301-309. 10.1016/0005-2728(93)90201-P.
47. Majeran W., Zybailov B., Ytterberg A.J., Dunsmore J., Sun Q., van Wijk K.J. Consequences of C-4 differentiation for chloroplast membrane proteomes in maize mesophyll and bundle sheath cells. Mol. Cell. Proteom. 2008, 7:1609-1638.
48. Melis A. Dynamics of photosynthetic membrane-composition and function. Biochim. Biophys. Acta 1991, 1058:87-106.
49. Miller G., Schlauch K., Tam R., Cortes D., Torres M.A., Shulaev V., Dangl J.L., Mittler R. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal 2009, 2(84):ra45. 10.1126/scisignal.2000448).
50. Mulo P., Sirpiö S., Suorsa M., Aro E.M. Auxiliary proteins involved in the assembly and sustenance of photosystem II. Photosynth. Res. 2008, 98:489-501.
51. Munekage Y., Hojo M., Meurer J., Endo T., Tasaka M., Shikanai T. PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 2002, 110:361-371.
52. Mühlenbock P., Szechynska-Hebda M., Plaszczyca M., Baudo M., Mateo A., Mullineaux P.M., Parker J.E., Karpinska B., Karpinski S. Chloroplast signaling and LESION SIMULATING DISEASE1 regulate crosstalk between light acclimation and immunity in Arabidopsis. Plant Cell 2008, 20:2339-2356. 10.1105/tpc.108.059618.
53. Müller P., Li X.P., Niyogi K.K. Non-photochemical quenching. A response to excess light energy. Plant Physiol. 2001, 125:1558-1566.
54. Nath K., Jajoo A., Poudyal R.S., Timilsina R., Park Y.S., Aro E.M., Nam H.G., Lee C.H. Towards a critical understanding of the photosystem II repair mechanism and its regulation during stress conditions. FEBS Lett. 2013, 587:3372-3381. 10.1016/j.febslet.2013.09.015.
55. Niyogi K.K., Grossman A.R., Björkman O. Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 1998, 10:1121-1134.
56. Niyogi K.K., Li X.P., Rosenberg V., Jung H.S. Is PsbS the site of non-photochemical quenching in photosynthesis?. J.Exp. Bot. 2005, 56:375-382.
57. Nomura H., Komori T., Uemura S., Kanda Y., Shimotani K., Nakai K., Furuichi T., Takebayashi K., Sugimoto T., Sano S., Suwastika I.N., Fukusaki E., Yoshioka H., Nakahira Y., Shiina T. Chloroplast-mediated activation of plant immune signalling in Arabidopsis. Nat. Commun. 2012, 3:926. 10.1038/ncomms1926.
58. Okegawa Y., Kobayashi Y., Shikanai T. Physiological links among alternative electron transport pathways that reduce and oxidize plastoquinone in Arabidopsis. Plant J. 2010, 63:458-468.
59. Peng L., Shikanai T. Supercomplex formation with photosystem I is required for the stabilization of the chloroplast NADH dehydrogenase-like complex in Arabidopsis. Plant Physiol. 2011, 155:1629-1639.
60. Pfannschmidt T. Plastidial retrograde signalling-a true "plastid factor" or just metabolite signatures?. Trends Plant Sci. 2010, 15:427-435. 10.1016/j.tplants.2010.05.009.
61. Ramel F., Birtic S., Cuiné S., Triantaphylidès C., Ravanat J.L., Havaux M. Chemical quenching of singlet oxygen by carotenoids in plants. Plant Physiol. 2012, 158:1267-1278. 10.1104/pp.111.182394.
62. Reiland S., Finazzi G., Endler A., Willig A., Baerenfaller K., Grossmann J., Gerrits B., Rutishauser D., Gruissem W., Rochaix J., Baginsky S. Comparative phosphoproteome profiling reveals a function of the STN8 kinase in fine-tuning of cyclic electron flow (CEF). Proc. Natl. Acad. Sci. U S A 2011, 108:12955-12960.
63. Rintamäki E., Martinsuo P., Pursiheimo S., Aro E.M. Cooperative regulation of light-harvesting complex II phosphorylation via the plastoquinol and ferredoxin-thioredoxin system in chloroplasts. Proc. Natl. Acad. Sci. U S A 2000, 97:11644-11649.
64. Rochaix J. Role of thylakoid protein kinases in photosynthetic acclimation. FEBS Lett. 2007, 581:2768-2775.
65. Rochaix J.D. Assembly of the photosynthetic apparatus. Plant Physiol. 2011, 155:1493-1500. 10.1104/pp.110.169839.
66. Rodríguez-Herva J.J., González-Melendi P., Cuartas-Lanza R., Antúnez-Lamas M., Río-Alvarez I., Li Z., López-Torrejón G., Díaz I., Del Pozo J.C., Chakravarthy S., Collmer A., Rodríguez-Palenzuela P., López-Solanilla E. Abacterial cysteine protease effector protein interferes with photosynthesis to suppress plant innate immune responses. Cell Microbiol. 2012, 14:669-681. 10.1111/j.1462-5822.2012.01749.x.
67. Rumberg B., Siggel U. pH changes in the inner phase of the thylakoids during photosynthesis. Naturwissenschaften 1969, 56:130-132.
68. Sabehi G., Shaulov L., Silver D.H., Yanai I., Harel A., Lindell D. Anovel lineage of myoviruses infecting cyanobacteria is widespread in the oceans. Proc. Natl. Acad. Sci. U S A 2012, 109:2037-2042. 10.1073/pnas.1115467109.
69. Sagi M., Fluhr R. Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol. 2006, 141:336-340. 10.1104/pp.106.078089.
70. Samol I., Shapiguzov A., Ingelsson B., Fucile G., Crevecoeur M., Vener A.V., Rochaix J., Goldschmidt-Clermont M. Identification of a photosystem II phosphatase involved in light acclimation in Arabidopsis. Plant Cell 2012, 24:2596-2609. 10.1105/tpc.112.095703.
71. Seo S., Okamoto M., Iwai T., Iwano M., Fukui K., Isogai A., Nakajima N., Ohashi Y. Reduced levels of chloroplast FtsH protein in tobacco mosaic virus-infected tobacco leaves accelerate the hypersensitive reaction. Plant Cell 2000, 12:917-932.
72. Shapiguzov A., Ingelsson B., Samol I., Andres C., Kessler F., Rochaix J., Vener A.V., Goldschmidt-Clermont M. The PPH1 phosphatase is specifically involved in LHCII dephosphorylation and state transitions in Arabidopsis. Proc. Natl. Acad. Sci. U S A 2010, 107:4782-4787.
73. Shinopoulos K.E., Brudvig G.W. Cytochrome b(559) and cyclic electron transfer within photosystem II. Biochim. Biophys. Acta 2012, 1817:66-75.
74. Shikanai T. Cyclic electron transport around photosystem I: genetic approaches. Annu. Rev. Plant Biol. 2007, 58:199-217.
75. Sierla M., Rahikainen M., Salojärvi J., Kangasjärvi J., Kangasjärvi S. Apoplastic and chloroplastic redox signaling networks in plant stress responses. Antioxid. Redox Signal. 2013, 18:2220-2239. 10.1089/ars.2012.5016.
76. Sonoike K. Photoinhibition of photosystem I. Physiol. Plant 2011, 142:56-64. 10.1111/j.1399-3054.2010.01437.x.
77. Strange R.N., Scott P.R. Plant disease: a threat to global food security. Annu. Rev. Phytopathol. 2005, 43:83-116.
78. Suorsa M., Sirpiö S., Aro E.M. Towards characterization of the chloroplast NAD(P)H dehydrogenase complex. Mol. Plant 2009, 2:1127-1140. 10.1093/mp/ssp052.
79. Suorsa M., Järvi S., Grieco M., Nurmi M., Pietrzykowska M., Rantala M., Kangasjärvi S., Paakkarinen V., Tikkanen M., Jansson S., Aro E.M. PROTON GRADIENT REGULATION5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions. Plant Cell 2012, 24:2934-2948. 10.1105/tpc.112.097162.
80. Szechyńska-Hebda M., Karpiński S. Light intensity-dependent retrograde signalling in higher plants. J.Plant Physiol. 2013, 170:1501-1516. 10.1016/j.jplph.2013.06.005.
81. Takizawa K., Cruz J.A., Kanazawa A., Kramer D.M. The thylakoid proton motive force invivo. Quantitative, non-invasive probes, energetics, and regulatory consequences of light-induced pmf. Biochim. Biophys. Acta 2007, 1767:1233-1244.
82. Tikkanen M., Aro E.M. Integrative regulatory network of plant thylakoid energy transduction. Trends Plant Sci. 2013, pii:S1360-1385(13)00190-8. 10.1016/j.tplants.2013.09.003.
83. Tikkanen M., Mekala N.R., Aro E.M. Photosystem II photoinhibition-repair cycle protects Photosystem I from irreversible damage. Biochim. Biophys. Acta 2014, 1837:210-215. (pii:S0005-2728(13)00171-0). 10.1016/j.bbabio.2013.10.001.
84. Tikkanen M., Gollan P.J., Suorsa M., Kangasjärvi S., Aro E.M. STN7 operates in retrograde signaling through controlling redox balance in the electron transfer chain. Front. Plant. Sci. 2012, 3:277. 10.3389/fpls.2012.00277.
85. Tikkanen M., Aro E.M. Thylakoid protein phosphorylation in dynamic regulation of photosystem II in higher plants. Biochim. Biophys. Acta 2012, 1817:232-238. 10.1016/j.bbabio.2011.05.005.
86. Tikkanen M., Grieco M., Kangasjärvi S., Aro E. Thylakoid protein phosphorylation in higher plant chloroplasts optimizes electron transfer under fluctuating light. Plant Physiol. 2010, 152:723-735.
87. Tikkanen M., Nurmi M., Kangasjärvi S., Aro E. Core protein phosphorylation facilitates the repair of photodamaged photosystem II at high light. Biochim. Biophys. Acta 2008, 1777:1432-1437. 10.1016/j.bbabio.2008.08.004.
88. Trotta A., Wrzaczek M., Scharte J., Tikkanen M., Konert G., Rahikainen M., Holmström M., Hiltunen H.M., Rips S., Sipari N., Mulo P., Weis E., von Schaewen A., Aro E.M., Kangasjärvi S. Regulatory subunit B'γ of protein phosphatase 2A prevents unnecessary defense reactions under low light in Arabidopsis. Plant Physiol. 2011, 156:1464-1480. 10.1104/pp.111.178442.
89. Tyystjärvi E. Photoinhibition of photosystem II. Int. Rev. Cell. Mol. Biol. 2013, 300:243-303. 10.1016/B978-0-12-405210-9.00007-2.
90. Umena Y., Kawakami K., Shen J.R., Kamiya N. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9Å. Nature 2011, 473:55-60. 10.1038/nature09913.
91. Wada M. Chloroplast movement. Plant Sci. 2013, 210:177-182. 10.1016/j.plantsci.2013.05.016.
92. Zurbriggen M.D., Carrillo N., Tognetti V.B., Melzer M., Peisker M., Hause B., Hajirezaei M.R. Chloroplast-generated reactive oxygen species play a major role in localized cell death during the non-host interaction between tobacco and Xanthomonas campestris pv. vesicatoria. Plant J. 2009, 60:962-973. 10.1111/j.1365-313X.2009.04010.x.