Light signaling-dependent regulation of photoinhibition and photoprotection in Tomato

Plant Physiology

Volumn 176, Issue 2, 2018, Pages 1311-1326

  Wang, Feng ^a   Wu, Nan ^a   Zhang, Luyue ^a   Ahammed, Golam Jalal ^a   Chen, Xiaoxiao ^a   Xiang, Xun ^a   Zhou, Jie ^a   Xia, Xiaojian ^a   Shi, Kai ^a   Yu, Jingquan ^a,b   Foyer, Christine H ^c   Zhou, Yanhong ^a,b  

^a ZHEJIANG UNIVERSITY   (China)

^b Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology   (China)

^c UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISIC ACID; HYDROGEN PEROXIDE; PHYTOCHROME A; PLANT PROTEIN; REACTIVE OXYGEN METABOLITE;

GENE EXPRESSION REGULATION; GENETICS; LIGHT; METABOLISM; PHOTOSYSTEM I; PHOTOTRANSDUCTION; PHYSIOLOGY; PLANT LEAF; TOMATO; TRANSGENIC PLANT;

ABSCISIC ACID; GENE EXPRESSION REGULATION, PLANT; HYDROGEN PEROXIDE; LIGHT; LIGHT SIGNAL TRANSDUCTION; LYCOPERSICON ESCULENTUM; PHOTOSYSTEM I PROTEIN COMPLEX; PHYTOCHROME A; PLANT LEAVES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; REACTIVE OXYGEN SPECIES;

EID: 85041723214     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.17.01143     Document Type: Article

References (77)

1. Ahn TK, Avenson TJ, Ballottari M, Cheng Y-C, Niyogi KK, Bassi R, Fleming GR (2008) Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320: 794-797
2. Allorent G, Lefebvre-Legendre L, Chappuis R, Kuntz M, Truong TB, Niyogi KK, Ulm R, Goldschmidt-Clermont M (2016) UV-B photoreceptor-mediated protection of the photosynthetic machinery in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 113: 14864-14869
3. Allorent G, Petroutsos D (2017) Photoreceptor-dependent regulation of photoprotection. Curr Opin Plant Biol 37: 102-108
4. Ballaré CL (2014) Light regulation of plant defense. Annu Rev Plant Biol 65: 335-363
5. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254
6. Cao WH, Liu J, He XJ, Mu RL, Zhou HL, Chen SY, Zhang JS (2007) Modulation of ethylene responses affects plant salt-stress responses. Plant Physiol 143: 707-719
7. Catalá R, Medina J, Salinas J (2011) Integration of low temperature and light signaling during cold acclimation response in Arabidopsis. Proc Natl Acad Sci USA 108: 16475-16480
8. Cerrudo I, Keller MM, Cargnel MD, Demkura PV, de Wit M, Patitucci MS, Pierik R, Pieterse CMJ, Ballaré CL (2012) Low red/far-red ratios reduce Arabidopsis resistance to Botrytis cinerea and jasmonate responses via a COI1-JAZ10-dependent, salicylic acid-independent mechanism. Plant Physiol 158: 2042-2052
9. Chen H, Zhang J, Neff MM, Hong SW, Zhang H, Deng XW, Xiong L (2008) Integration of light and abscisic acid signaling during seed germination and early seedling development. Proc Natl Acad Sci USA 105: 4495-4500
10. Chen M, Chory J, Fankhauser C (2004) Light signal transduction in higher plants. Annu Rev Genet 38: 87-117
11. Chen Z, Gallie DR (2012) Violaxanthin de-epoxidase is rate-limiting for non-photochemical quenching under subsaturating light or during chilling in Arabidopsis. Plant Physiol Biochem 58: 66-82
12. Cluis CP, Mouchel CF, Hardtke CS (2004) The Arabidopsis transcription factor HY5 integrates light and hormone signaling pathways. Plant J 38: 332-347
13. de Wit M, Spoel SH, Sanchez-Perez GF, Gommers CMM, Pieterse CMJ, Voesenek LACJ, Pierik R (2013) Perception of low red:far-red ratio compromises both salicylic acid- and jasmonic acid-dependent pathogen defences in Arabidopsis. Plant J 75: 90-103
14. Duan M, Ma NN, Li D, Deng YS, Kong FY, Lv W, Meng QW (2012) Antisense-mediated suppression of tomato thylakoidal ascorbate peroxidase influences anti-oxidant network during chilling stress. Plant Physiol Biochem 58: 37-45
15. Fillatti JJ, Kiser J, Rose R, Comai L (1987) Efficient transfer of a glyphosate tolerance gene into tomato using a binary Agrobacterium tumefaciens vector. Biotechnology (N Y) 5: 726-730
16. Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J (2012) Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot 63: 1637-1661
17. Foyer CH, Ruban AV, Noctor G (2017) Viewing oxidative stress through the lens of oxidative signalling rather than damage. Biochem J 474: 877-883
18. Foyer CH, Souriau N, Perret S, Lelandais M, Kunert KJ, Pruvost C, Jouanin L (1995) Overexpression of glutathione reductase but not glutathione synthetase leads to increases in antioxidant capacity and resistance to photoinhibition in poplar trees. Plant Physiol 109: 1047-1057
19. Franklin KA, Quail PH (2010) Phytochrome functions in Arabidopsis development. J Exp Bot 61: 11-24
20. Gangappa SN, Botto JF (2016) The multifaceted roles of HY5 in plant growth and development. Mol Plant 9: 1353-1365
21. Guo Z, Wang F, Xiang X, Ahammed GJ, Wang M, Onac E, Zhou J, Xia X, Shi K, Yin X, et al (2016) Systemic induction of photosynthesis via illumination of the shoot apex is mediated sequentially by phytochrome B, auxin and hydrogen peroxide in tomato. Plant Physiol 172: 1259-1272
22. Han H, Gao S, Li B, Dong XC, Feng HL, Meng QW (2010) Overexpression of violaxanthin de-epoxidase gene alleviates photoinhibition of PSII and PSI in tomato during high light and chilling stress. J Plant Physiol 167: 176-183
23. Hertle AP, Blunder T, Wunder T, Pesaresi P, Pribil M, Armbruster U, Leister D (2013) PGRL1 is the elusive ferredoxin-plastoquinone reductase in photosynthetic cyclic electron flow. Mol Cell 49: 511-523
24. Jiao Y, Lau OS, Deng XW (2007) Light-regulated transcriptional networks in higher plants. Nat Rev Genet 8: 217-230
25. Jin H, Liu B, Luo L, Feng D, Wang P, Liu J, Da Q, He Y, Qi K, Wang J, Wang HB (2014) HYPERSENSITIVE TO HIGH LIGHT1 interacts with LOW QUANTUM YIELD OF PHOTOSYSTEM II1 and functions in protection of photosystem II from photodamage in Arabidopsis. Plant Cell 26: 1213-1229
26. Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420: 829-832
27. Kim HE, Tokura H (1995) Influence of different light intensities during the daytime on evening dressing behavior in the cold. Physiol Behav 58: 779-783
28. Kingston-Smith AH, Foyer CH (2000) Bundle sheath proteins are more sensitive to oxidative damage than those of the mesophyll in maize leaves exposed to paraquat or low temperatures. J Exp Bot 51: 123-130
29. Kingston-Smith AH, Harbinson J, Williams J, Foyer CH (1997) Effect of chilling on carbon assimilation, enzyme activation, and photosynthetic electron transport in the absence of photoinhibition in maize leaves. Plant Physiol 114: 1039-1046
30. Klughammer C, Schreiber U (2008) Saturation pulse method for assessment of energy conversion in PSI. PAM Appl Notes 1: 11-14
31. Kromdijk J, Głowacka K, Leonelli L, Gabilly ST, Iwai M, Niyogi KK, Long SP (2016) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354: 857-861
32. Lau OS, Deng XW (2010) Plant hormone signaling lightens up: integrators of light and hormones. Curr Opin Plant Biol 13: 571-577
33. Lei Y, Lu L, Liu HY, Li S, Xing F, Chen LL (2014) CRISPR-P: a web tool for synthetic single-guide RNA design of CRISPR-system in plants. Mol Plant 7: 1494-1496
34. Li XP, Muller-Moule P, Gilmore AM, Niyogi KK (2002) PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc Natl Acad Sci USA 99: 15222-15227
35. Li Z, Zhang L, Yu Y, Quan R, Zhang Z, Zhang H, Huang R (2011) The ethylene response factor AtERF11 that is transcriptionally modulated by the bZIP transcription factor HY5 is a crucial repressor for ethylene biosynthesis in Arabidopsis. Plant J 68: 88-99
36. Liu J, Last RL (2015) A land plant-specific thylakoid membrane protein contributes to photosystem II maintenance in Arabidopsis thaliana. Plant J 82: 731-743
37. Liu Y, Roof S, Ye Z, Barry C, van Tuinen A, Vrebalov J, Bowler C, Giovannoni J (2004) Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proc Natl Acad Sci USA 101: 9897-9902
38. Liu Y, Schiff M, Dinesh-Kumar SP (2002) Virus-induced gene silencing in tomato. Plant J 31: 777-786
39. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 22DDDCTmethod. Methods 25: 402-408
40. Maruta T, Tanouchi A, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S (2010) Arabidopsis chloroplastic ascorbate peroxidase isoenzymes play a dual role in photoprotection and gene regulation under photooxidative stress. Plant Cell Physiol 51: 190-200
41. Mittal A, Gampala SSL, Ritchie GL, Payton P, Burke JJ, Rock CD (2014) Related to ABA-Insensitive3(ABI3)/Viviparous1 and AtABI5 transcription factor coexpression in cotton enhances drought stress adaptation. Plant Biotechnol J 12: 578-589
42. Möglich A, Yang X, Ayers RA, Moffat K (2010) Structure and function of plant photoreceptors. Annu Rev Plant Biol 61: 21-47
43. Munekage Y, Hashimoto M, Miyake C, Tomizawa K, Endo T, Tasaka M, Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429: 579-582
44. Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110: 361-371
45. Murata Y, Pei ZM, Mori IC, Schroeder J (2001) Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell 13: 2513-2523
46. Nagata M, Yamamoto N, Shigeyama T, Terasawa Y, Anai T, Sakai T, Inada S, Arima S, Hashiguchi M, Akashi R, Nakayama H, Ueno D, et al (2015) Red/far red light controls arbuscular mycorrhizal colonization via jasmonic acid and strigolactone signaling. Plant Cell Physiol 56: 2100-2109
47. Nashilevitz S, Melamed-Bessudo C, Izkovich Y, Rogachev I, Osorio S, Itkin M, Adato A, Pankratov I, Hirschberg J, Fernie AR, Wolf S, Usadel B, et al (2010) An orange ripening mutant links plastid NAD(P) H dehydrogenase complex activity to central and specialized metabolism during tomato fruit maturation. Plant Cell 22: 1977-1997
48. Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757: 742-749
49. Niyogi KK, Björkman O, Grossman AR (1997) The roles of specific xanthophylls in photoprotection. Proc Natl Acad Sci USA 94: 14162-14167
50. Niyogi KK, Grossman AR, 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
51. Okegawa Y, Kagawa Y, Kobayashi Y, Shikanai T (2008) Characterization of factors affecting the activity of photosystem I cyclic electron transport in chloroplasts. Plant Cell Physiol 49: 825-834
52. Osterlund MT, Hardtke CS, Wei N, Deng XW (2000) Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405: 462-466
53. Pan C, Ye L, Qin L, Liu X, He Y, Wang J, Chen L, Lu G (2016) CRISPR/ Cas9-mediated efficient and heritable targeted mutagenesis in tomato plants in the first and later generations. Sci Rep 6: 24765 10.1038/srep24765
54. Petroutsos D, Tokutsu R, Maruyama S, Flori S, Greiner A, Magneschi L, Cusant L, Kottke T, Mittag M, Hegemann P, Finazzi G, Minagawa J (2016) A blue-light photoreceptor mediates the feedback regulation of photosynthesis. Nature 537: 563-566
55. Porra RJ, Thompson WA, Kriedemann PE (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
56. Quail PH (2002a) Photosensory perception and signalling in plant cells: new paradigms? Curr Opin Cell Biol 14: 180-188
57. Quail PH (2002b) Phytochrome photosensory signalling networks. Nat Rev Mol Cell Biol 3: 85-93
58. Ruban AV, Berera R, Ilioaia C, van Stokkum IHM, Kennis JTM, Pascal AA, van Amerongen H, Robert B, Horton P, van Grondelle R (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450: 575-578
59. Sasidharan R, Chinnappa CC, Voesenek LACJ, Pierik R (2009) A molecular basis for the physiological variation in shade avoidance responses: a tale of two ecotypes. Plant Signal Behav 4: 528-529
60. Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol 58: 199-217
61. Strand DD, Livingston AK, Satoh-Cruz M, Froehlich JE, Maurino VG, Kramer DM (2015) Activation of cyclic electron flow by hydrogen peroxide in vivo. Proc Natl Acad Sci USA 112: 5539-5544
62. Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16: 53-60
63. Takahashi S, Milward SE, Fan DY, Chow WS, Badger MR (2009) How does cyclic electron flow alleviate photoinhibition in Arabidopsis? Plant Physiol 149: 1560-1567
64. Wang F, Guo Z, Li H, Wang M, Onac E, Zhou J, Xia X, Shi K, Yu J, Zhou Y (2016) Phytochrome A and B function antagonistically to regulate cold tolerance via abscisic acid-dependent jasmonate signaling. Plant Physiol 170: 459-471
65. Xia XJ, Gao CJ, Song LX, Zhou YH, Shi K, Yu JQ (2014) Role of H2O2 dynamics in brassinosteroid-induced stomatal closure and opening in Solanum lycopersicum. Plant Cell Environ 37: 2036-2050
66. Xia XJ, Wang YJ, Zhou YH, Tao Y, Mao WH, Shi K, Asami T, Chen Z, Yu JQ (2009) Reactive oxygen species are involved in brassinosteroidinduced stress tolerance in cucumber. Plant Physiol 150: 801-814
67. Xie XZ, Xue YJ, Zhou JJ, Zhang B, Chang H, Takano M (2011) Phytochromes regulate SA and JA signaling pathways in rice and are required for developmentally controlled resistance to Magnaporthe grisea. Mol Plant 4: 688-696
68. Xing Y, Jia W, Zhang J (2008) AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. Plant J 54: 440-451
69. Xu CJ, Fraser PD, Wang WJ, Bramley PM (2006) Differences in the carotenoid content of ordinary citrus and lycopene-accumulating mutants. J Agric Food Chem 54: 5474-5481
70. Xu D, Li J, Gangappa SN, Hettiarachchi C, Lin F, Andersson MX, Jiang Y, Deng XW, Holm M (2014) Convergence of Light and ABA signaling on the ABI5 promoter. PLoS Genet 10: e1004197
71. Yamori W, Makino A, Shikanai T (2016) A physiological role of cyclic electron transport around photosystem I in sustaining photosynthesis under fluctuating light in rice. Sci Rep 6: 20147 10.1038/srep20147
72. Yi C, Deng XW (2005) COP1—from plant photomorphogenesis to mammalian tumorigenesis. Trends Cell Biol 15: 618-625
73. Zhang A, Jiang M, Zhang J, Ding H, Xu S, Hu X, Tan M (2007) Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen-activated protein kinase cascade involved in antioxidant defense in maize leaves. New Phytol 175: 36-50
74. Zhao Y, Chan Z, Xing L, Liu X, Hou YJ, Chinnusamy V, Wang P, Duan C, Zhu JK (2013) The unique mode of action of a divergent member of the ABA-receptor protein family in ABA and stress signaling. Cell Res 23: 1380-1395
75. Zhou J, Wang J, Li X, Xia XJ, Zhou YH, Shi K, Chen Z, Yu JQ (2014) H2O2 mediates the crosstalk of brassinosteroid and abscisic acid in tomato responses to heat and oxidative stresses. J Exp Bot 65: 4371-4383
76. Zhou J, Wang J, Shi K, Xia XJ, Zhou YH, Yu JQ (2012) Hydrogen peroxide is involved in the cold acclimation-induced chilling tolerance of tomato plants. Plant Physiol Biochem 60: 141-149
77. Zhu J, Dong CH, Zhu JK (2007) Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr Opin Plant Biol 10: 290-295