Thioredoxins m are major players in the multifaceted light-adaptive response in Arabidopsis thaliana.
Arabidopsis thaliana
anthocyanins
chlorophyll fluorescence
chloroplast
light acclimation
redox regulation
thioredoxins
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
10 2021
10 2021
Historique:
received:
27
08
2020
accepted:
15
07
2021
pubmed:
22
7
2021
medline:
28
12
2021
entrez:
21
7
2021
Statut:
ppublish
Résumé
Thioredoxins (TRXs) are well-known redox signalling players, which carry out post-translational modifications in target proteins. Chloroplast TRXs are divided into different types and have central roles in light energy uptake and the regulation of primary metabolism. The isoforms TRX m1, m2, and m4 from Arabidopsis thaliana are considered functionally related. Knowing their key position in the hub of plant metabolism, we hypothesized that the impairment of the TRX m signalling would not only have harmful consequences on chloroplast metabolism but also at different levels of plant development. To uncover the physiological and developmental processes that depend on TRX m signalling, we carried out a comprehensive study of Arabidopsis single, double, and triple mutants defective in the TRX m1, m2, and m4 proteins. As light and redox signalling are closely linked, we investigated the response to high light (HL) of the plants that are gradually compromised in TRX m signalling. We provide experimental evidence relating the lack of TRX m and the appearance of novel phenotypic features concerning mesophyll structure, stomata biogenesis, and stomatal conductance. We also report new data indicating that the isoforms of TRX m fine-tune the response to HL, including the accumulation of the protective pigment anthocyanin. These results reveal novel signalling functions for the TRX m and underline their importance for plant growth and fulfilment of the acclimation/response to HL conditions.
Substances chimiques
Anthocyanins
0
Chloroplast Thioredoxins
0
Protein Isoforms
0
Chlorophyll
1406-65-1
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
120-133Informations de copyright
© 2021 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Balfagón, D., Sengupta, S., Gómez-Cadenas, A., Fritschi, F.B., Azad, R.K., Mittler, R. et al. (2019) Jasmonic acid is required for plant acclimation to a combination of high light and heat stress. Plant Physiology, 181, 1668-1682.
Barajas-López, J.D., Serrato, A.J., Olmedilla, A., Chueca, A. & Sahrawy, M. (2007) Localization in roots and flowers of pea chloroplastic thioredoxin f and thioredoxin m proteins reveals new roles in non photosynthetic organs. Plant Physiology, 145, 946-960.
Benitez-Alfonso, Y., Cilia, M., San Roman, A., Thomas, C., Maule, A., Hearn, S. et al. (2009) Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport. Proceedings of the National Academy of Sciences of the United States of America, 106, 3615-3620.
Brooks, M.D., Sylak-Glassman, E.J., Fleming, G.R. & Niyogi, K.K. (2013) A thioredoxin-like/β-propeller protein maintains the efficiency of light harvesting in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 110, 2733-2740.
Chi, Y.H., Moon, J.C., Park, J.H., Kim, H.-S., Zulfugarov, I.S., Fanata, W.I. et al. (2008) Abnormal chloroplast development and growth inhibition in rice thioredoxin m knock-down plants. Plant Physiology, 148, 808-817.
Collin, V., Issakidis-Bourguet, E., Marchand, C., Hirasawa, M., Lancelin, J.-M., Knaff, D.B. et al. (2003) The Arabidopsis plastidial thioredoxins: new functions and new insights into specificity. Journal of Biological Chemistry, 278, 23747-23752.
Courteille, A., Vesa, S., Sanz-Barrio, R., Cazalé, A.-C., Becuwe-Linka, N., Farran, I. et al. (2013) Thioredoxin m4 controls photosynthetic alternative electron pathways in Arabidopsis. Plant Physiology, 161, 508-520.
Da, Q., Sun, T., Wang, M., Jin, H., Li, M., Feng, D. et al. (2018) M-type thioredoxins are involved in the xanthophyll cycle and proton motive force to alter NPQ under low-light conditions in Arabidopsis. Plant Cell Reports, 37, 279-291.
Das, P.K., Geul, B., Choi, S.-B., Yoo, S.-D. & Park, Y.-I. (2011) Photosynthesis-dependent anthocyanin pigmentation in Arabidopsis. Plant Signaling & Behavior, 6, 23-25.
Fernández-Trijueque, J., Serrato, A.J. & Sahrawy, M. (2019) Proteomic analyses of thioredoxins f and m Arabidopsis thaliana mutants indicate specific functions for these proteins in plants. Antioxidants, 8, 54.
Gollan, P.J., Tikkanen, M. & Aro, E.M. (2015) Photosynthetic light reactions: integral to chloroplast retrograde signalling. Current Opinion in Plant Biology, 27, 180-191.
Gütle, D.D., Roret, T., Hecker, A., Reski, R. & Jacquot, J.P. (2017) Dithiol disulphide exchange in redox regulation of chloroplast enzymes in response to evolutionary and structural constraints. Plant Science, 255, 1-11.
Hallin, E.I., Guo, K. & Åkerlund, H.E. (2015) Violaxanthin de-epoxidase disulphides and their role in activity and thermal stability. Photosynthesis Research, 124, 191-198.
Hoshino, R., Yoshida, Y. & Tsukaya, H. (2019) Multiple steps of leaf thickening during sun-leaf formation in Arabidopsis. The Plant Journal, 100, 738-753.
Kang, Z., Qin, T. & Zhao, Z. (2019) Thioredoxins and thioredoxin reductase in chloroplasts: a review. Gene, 706, 32-42.
Kang, Z.H. & Wang, G.X. (2016) Redox regulation in the thylakoid lumen. Journal of Plant Physiology, 192, 28-37.
Karamoko, M., Cline, S., Redding, K., Ruiz, N. & Hamel, P.P. (2011) Lumen thiol oxidoreductase1, a disulfide bond-forming catalyst, is required for the assembly of photosystem II in Arabidopsis. The Plant Cell, 23, 4462-4475.
Laughlin, T.G., Bayne, A.N., Trempe, J.F., Savage, D.F. & Davies, K.M. (2019) Structure of the complex I-like molecule NDH of oxygenic photosynthesis. Nature, 566, 411-414.
Lemaire, S.D., Michelet, L., Zaffagnini, M., Massot, V. & Issakidis-Bourguet, E. (2007) Thioredoxins in chloroplasts. Current Genetics, 51, 343-365.
Li, G., Zhao, J., Qin, B., Yin, Y., An, W., Mu, Z. et al. (2019) ABA mediates development-dependent anthocyanin biosynthesis and fruit coloration in Lycium plants. BMC Plant Biology, 19, 317.
Li, X.P., Muller-Moule, P., Gilmore, A.M. & Niyogi, K.K. (2002) PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proceedings of the National Academy of Sciences of the United States of America, 99, 15222-15227.
Livak, K.J. & Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods, 25, 402-408.
Loreti, E., Povero, G., Novi, G., Solfanelli, C., Alpi, A. & Perata, P. (2008) Gibberellins, jasmonate and abscisic acid modulate the sucrose-induced expression of anthocyanin biosynthetic genes in Arabidopsis. New Phytologist, 179, 1004-1016.
Mahmood, K., Xu, Z., El-Kereamy, A., Casaretto, J.A. & Rothstein, S.J. (2016) The Arabidopsis transcription factor ANAC032 represses anthocyanin biosynthesis in response to high sucrose and oxidative and abiotic stresses. Frontiers in Plant Science, 7, 1548.
Massonnet, C., Vile, D., Fabre, J., Hannah, M.A., Caldana, C., Lisec, J. et al. (2010) Probing the reproducibility of leaf growth and molecular phenotypes: a comparison of three Arabidopsis accessions cultivated in ten laboratories. Plant Physiology, 152, 2142-2157.
Meyer, Y., Buchanan, B.B., Vignols, F. & Reichheld, J.P. (2009) Thioredoxins and glutaredoxins: unifying elements in redox biology. Annual Review of Genetics, 43, 335-367.
Motohashi, K. & Hisabori, T. (2006) HCF164 receives reducing equivalents from stromal thioredoxin across the thylakoid membrane and mediates reduction of target proteins in the thylakoid lumen. Journal of Biological Chemistry, 281, 35039-35047.
Motohashi, K. & Hisabori, T. (2010) CcdA is a thylakoid membrane protein required for the transfer of reducing equivalents from stroma to thylakoid lumen in the higher plant chloroplast. Antioxidants & Redox Signaling, 13, 1169-1176.
Müller, P., Li, X.P. & Niyogi, K.K. (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiology, 125, 1558-1566.
Munekage, Y., Hashimoto, M., Miyake, C., Tomizawa, K.I., Endo, T., Tasaka, M. et al. (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature, 429, 579-582.
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.
Naranjo, B., Mignée, C., Krieger-Liszkay, A., Hornero-Méndez, D., Gallardo-Guerrero, L., Cejudo, F.J. et al. (2016) The chloroplast NADPH thioredoxin reductase C, NTRC, controls non-photochemical quenching of light energy and photosynthetic electron transport in Arabidopsis. Plant, Cell and Environment, 39, 804-822.
Nikkanen, L. & Rintamäki, E. (2019) Chloroplast thioredoxin systems dynamically regulate photosynthesis in plants. The Biochemical Journal, 476, 1159-1172.
Nikkanen, L., Toivola, J. & Rintamäki, E. (2016) Crosstalk between chloroplast thioredoxin systems in regulation of photosynthesis. Plant, Cell and Environment, 39, 1691-1705.
Ojeda, V., Pérez-Ruiz, J.M., González, M., Nájera, V.A., Sahrawy, M., Serrato, A.J. et al. (2017) NADPH thioredoxin reductase C and thioredoxins act concertedly in seedling development. Plant Physiology, 174, 1436-1448.
Okegawa, Y. & Motohashi, K. (2015) Chloroplastic thioredoxin m functions as a major regulator of Calvin cycle enzymes during photosynthesis in vivo. The Plant Journal, 84, 900-913.
Peng, L., Fukao, Y., Fujiwara, M., Takami, T. & Shikanai, T. (2009) Efficient operation of NAD(P)H dehydrogenase requires supercomplex formation with photosystem I via minor LHCI in Arabidopsis. The Plant Cell, 21, 3623-3640.
Pfannschmidt, T., Bräutigam, K., Wagner, R., Dietzel, L., Schröter, Y., Steiner, S. et al. (2009) Potential regulation of gene expression in photosynthetic cells by redox and energy state: approaches towards better understanding. Annals of Botany, 103, 599-607.
Rabino, I. & Mancinelli, A.L. (1986) Light, temperature, and anthocyanin production. Plant Physiology, 81, 922-924.
Ren, T., Weraduwage, S.M. & Sharkey, T.D. (2019) Prospects for enhancing leaf photosynthetic capacity by manipulating mesophyll cell morphology. Journal of Experimental Botany, 70, 1153-1165.
Schürmann, P. & Buchanan, B.B. (2008) The ferredoxin/thioredoxin system of oxygenic photosynthesis. Antioxidants & Redox Signaling, 10, 1235-1274.
Serrato, A.J., Fernández-Trijueque, J., Barajas-López, J.D., Chueca, A., Sahrawy, M. & Reichheld, J.P. (2013) Plastid thioredoxins: a “one-for-all” redox-signaling system in plants. Frontiers in Plant Science, 4, 463.
Shan, X., Zhang, Y., Peng, W., Wang, Z. & Xie, D. (2009) Molecular mechanism for jasmonate-induction of anthocyanin accumulation in Arabidopsis. Journal of Experimental Botany, 60, 3849-3860.
Simionato, D., Basso, S., Zaffagnini, M., Lana, T., Marzotto, F., Trost, P. et al. (2015) Protein redox regulation in the thylakoid lumen: the importance of disulfide bonds for violaxanthin de-epoxidase. FEBS Letters, 589, 919-923.
Thormählen, I., Zupok, A., Rescher, J., Leger, J., Weissenberger, S., Groysman, J. et al. (2017) Thioredoxins play a crucial role in dynamic acclimation of photosynthesis in fluctuating light. Molecular Plant, 10, 168-182.
Wang, P., Liu, J., Liu, B., Feng, D., Da, Q., Shu, S. et al. (2013) Evidence for a role of chloroplastic m-type thioredoxins in the biogenesis of photosystem II in Arabidopsis. Plant Physiology, 163, 1710-1728.
Yamori, W. & Shikanai, T. (2016) Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth. Annual Review of Plant Biology, 67, 81-106.
Zhang, M., Takano, T., Liu, S. & Zhang, X. (2015) Arabidopsis mitochondrial voltage-dependent anion channel 3 (AtVDAC3) protein interacts with thioredoxin m2. FEBS Letters, 589, 1207-1213.