Abstract
Plants grown in the field experience sharp changes in irradiation due to shading effects caused by clouds, other leaves, etc. The excess of absorbed light energy is dissipated by a number of mechanisms including cyclic electron transport, photorespiration, and Mehler-type reactions. This protection is essential for survival but decreases photosynthetic efficiency. All phototrophs except angiosperms harbor flavodiiron proteins (Flvs) which relieve the excess of excitation energy on the photosynthetic electron transport chain by reducing oxygen directly to water. Introduction of cyanobacterial Flv1/Flv3 in tobacco chloroplasts resulted in transgenic plants that showed similar photosynthetic performance under steady-state illumination, but displayed faster recovery of various photosynthetic parameters, including electron transport and non-photochemical quenching during dark–light transitions. They also kept the electron transport chain in a more oxidized state and enhanced the proton motive force of dark-adapted leaves. The results indicate that, by acting as electron sinks during light transitions, Flvs contribute to increase photosynthesis protection and efficiency under changing environmental conditions as those found by plants in the field.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahn TK, Avenson TJ, Peers G, Li Z, Dall’Osto L, Bassi R, Niyogi KK, Fleming GR (2009) Investigating energy partitioning during photosynthesis using an expanded quantum yield convention. Chem Phys 357:151–158
Allahverdiyeva Y, Isojärvi J, Zhang P, Aro EM (2015) Cyanobacterial oxygenic photosynthesis is protected by flavodiiron proteins. Life 5:716–743
Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Biol 50:601–639
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113
Duffy CD, Ruban AV (2015) Dissipative pathways in the photosystem-II antenna in plants. J Photochem Photobiol B 152:215–226
Ermakova M, Battchikova N, Allahverdiyeva Y, Aro EM (2013) Novel heterocyst-specific flavodiiron proteins in Anabaena sp. PCC 7120. FEBS Lett 587:82–87
Gallois P, Marinho P (1995) Leaf disk transformation using Agrobacterium tumefaciens-expression of heterologous genes in tobacco. In: Jones H (ed) Methods in molecular biology. Plant gene transfer and expression protocols, vol 49. Humana Press Inc, Totowa, NJ, pp 39–48
Gerotto C, Alboresi A, Meneghesso A, Jokel M, Suorsa M, Aro EM, Morosinotto T (2016) Flavodiiron proteins act as safety valve for electrons in Physcomitrella patens. Proc Natl Acad Sci USA 113:12322–12327
Giró M, Ceccoli RD, Poli HO, Carrillo N, Lodeyro AF (2011) An in vivo system involving co-expression of cyanobacterial flavodoxin and ferredoxin–NADP+ reductase confers increased tolerance to oxidative stress in plants. FEBS Open Biol 1:7–13
Hagemann M, Fernie A, Espie G, Kern R, Eisenhut M, Reumann S, Bauwe H, Weber A (2013) Evolution of the biochemistry of the photorespiratory C2 cycle. Plant Biol 15:639–647
Hope AB, Valente P, Matthews DB (1994) Effects of pH on the kinetics of redox reactions in and around the cytochromebf complex in an isolated system. Photosynth Res 42:111–120
Ilík P, Pavlovič A, Kouřil R, Alboresi A, Morosinotto T, Allahverdiyeva Y, Aro EM, Yamamoto H, Shikanai T (2017) Alternative electron transport mediated by flavodiiron proteins is operational in organisms from cyanobacteria up to gymnosperms. New Phytol 214:967–972
Jagannathan B, Shen G, Golbeck JH (2012) The evolution of Type I reaction centers: the response to oxygenic photosynthesis. In: Burnap RL, Vermaas WFJ (eds) Functional genomics and evolution of photosynthetic systems. Springer, pp 285–316
Jarvis P, Chen L-J, Li H-M, Peto CA, Fankhauser C, Chory J (1998) An Arabidopsis mutant defective in the plastid general protein import apparatus. Science 282:100–103
Joët T, Cournac L, Horvath EM, Medgyesy P, 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
Kanazawa A, Ostendorf E, Kohzuma K, Hoh D, Strand D, Sato-Cruz M, Savage L, Cruz J, Fisher N, Froechlich J, Kramer D (2017) Chloroplast ATP synthase modulation of the thylakoid proton motive force: implications for Photosystem I and Photosystem II photoprotection. Front Plant Sci. doi:10.3389/fpls.2017.00719
Kramer DM, Evans JR (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiol 155:70–78
Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of Q A redox state and excitation energy fluxes. Photosynth Res 79:209–218
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
Kuhlgert S, Austic G, Zegarac R, Osei-Bonsu I, Hoh D, Chilvers MI, Roth MG, Bi K, TerAvest D, Weebadde P (2016) MultispeQ Beta: a tool for large-scale plant phenotyping connected to the open PhotosynQ network. Royal Soc Open Sci 3:160592
Külheim C, Ågren J, Jansson S (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297:91–93
Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566
Nishio JN, Whitmarsh J (1993) Dissipation of the proton electrochemical potential in intact chloroplasts (II. The pH gradient monitored by cytochrome f reduction kinetics). Plant Physiol 101:89–96
Pierella Karlusich JJ, Lodeyro AF, Carrillo N (2014) The long goodbye: the rise and fall of flavodoxin during plant evolution. J Exp Bot 65:5161–5178
Schmittgen T, Livak K (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108
Shimakawa G, Ishizaki K, Tsukamoto S, Tanaka M, Sejima T, Miyake C (2017) The liverwort, Marchantia, drives alternative electron flow using a flavodiiron protein to protect PSI. Plant Physiol 173:1636–1647
Shirao M, Kuroki S, Kaneko K, Kinjo Y, Tsuyama M, Förster B, Takahashi S, Badger MR (2013) Gymnosperms have increased capacity for electron leakage to oxygen (Mehler and PTOX reactions) in photosynthesis compared with angiosperms. Plant Cell Physiol 54:1152–1163
Sugimoto K, Okegawa Y, Tohri A, Long TA, Covert SF, Hisabori T, Shikanai T (2013) A single amino acid alteration in PGR5 confers resistance to antimycin A in cyclic electron transport around PSI. Plant Cell Physiol 54:1525–1534
Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16:53–60
Vicente JB, Gomes CM, Wasserfallen A, Teixeira M (2002) Module fusion in an A-type flavoprotein from the cyanobacterium Synechocystis condenses a multiple-component pathway in a single polypeptide chain. Biochem Biophys Res Comm 294:82–87
Vicente JB, Justino MC, Gonçalves VL, Saraiva LM, Teixeira M (2008) Biochemical, spectroscopic, and thermodynamic properties of flavodiiron proteins. Methods Enzymol 437:21–45
Yamamoto H, Takahashi S, Badger MR, Shikanai T (2016) Artificial remodelling of alternative electron flow by flavodiiron proteins in Arabidopsis. Nat Plants. doi:10.1038/nplants.2016.12
Yamori W, Shikanai T (2016) Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth. Ann Rev Plant Biol 67:81–106
Zhu XG, Ort DR, Whitmarsh J, Long SP (2004) The slow reversibility of photosystem II thermal energy dissipation on transfer from high to low light may cause large losses in carbon gain by crop canopies: a theoretical analysis. J Exp Bot 55:1167–1175
Acknowledgements
We thank Álvaro Quijano (Universidad Nacional de Rosario, FCAgR, Argentina) for providing the MultispeQ-Beta device. This work was supported by Grants PICT 2014-2496 and PICT 2015-3828 from the National Agency for the Promotion of Science and Technology (ANPCyT, Argentina), by PIP 1075 from the National Research Council of Argentina (CONICET), by the Federal Ministry of Education and Research (BMBF, Germany), and by the Project Management Juelich (PTJ, Germany). RG is a Fellow of the Bunge & Born Foundation. NC and AFL are faculty members of the School of Biochemical and Pharmaceutical Sciences, University of Rosario (Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Argentina) and staff members of the National Research Council (CONICET, Argentina).
Funding
The funding were provided by National Agency for the Promotion of Science and Technology (PICT 2014-2496 and PICT 2015-3828), National Research Council of Argentina (PIP 1075), Federal Ministry of Education and Research and Bundesministerium für Bildung und Forschung.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Gómez, R., Carrillo, N., Morelli, M.P. et al. Faster photosynthetic induction in tobacco by expressing cyanobacterial flavodiiron proteins in chloroplasts. Photosynth Res 136, 129–138 (2018). https://doi.org/10.1007/s11120-017-0449-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-017-0449-9