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Performing Photosynthesis Without B-Carotene

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Performing Photosynthesis Without B-Carotene INSIGHT PHOTOSYSTEMS Performing photosynthesis without b-carotene Research on mutant tobacco plants shows that a pigment called b- carotene is not necessary for photosynthesis. ALISON TELFER Photosynthesis typically happens in pigment Related research article Xu P, Chukhutsina protein complexes called photosystems. At the VU, Nawrocki WJ, Schansker G, Bielczynski heart of the photosystem is the reaction centre, LW, Lu Y, Karcher D, Bock R, Croce R. an enzyme that uses light to reduce molecules. 2020. b-carotene is not essential for photo- This reaction centre is surrounded by light-har- synthesis in higher plants. eLife 9:e58984. vesting complexes, protein assemblies that doi: 10.7554/eLife.58984 enhance the absorption of light. These assem- blies contain two types of carotenoids: b-caro- tene, which binds to the reaction centres, and several kinds of xanthophyll, which bind to the light harvesting complexes (Siefermann- arotenoids are organic pigments that Harms, 1985; Telfer, 2002). C have an important role in photosynthe- Previous research has shown that mutant sis, but they remain hidden for most of plants that lack xanthophyll but not b-carotene the year, only revealing their wonderful yellow can still conduct photosynthesis (To´th et al., and orange colours during the autumn, when 2015). And since b-carotene can be found in chlorophyll – the pigment that makes plants every photosynthetic organism, it has long been green – is degraded. The most common carote- assumed that this pigment must be essential for noids involved in photosynthesis are carotenes photosynthesis. Now, in eLife, Roberta Croce (which contain 40 carbon atoms and a variable and colleagues at the VU University Amsterdam number of hydrogen atoms) and xanthophylls and the Max Planck Institute of Molecular Plant (which are oxidised carotenes). Physiology – including Pengqui Xu as first author The carotenoids involved in photosynthesis – report that this may not be the case after all have two major roles – to harvest light and to (Xu et al., 2020). prevent damage when the plant is overexposed The researchers engineered a mutant to sunlight (Frank and Cogdell, 1996). The first tobacco plants that lacked b-carotene and con- role involves absorbing visible light and transfer- tained a xanthophyll called astaxanthin (a pig- ring the energy to chlorophyll. The second ment that is found in salmon, shrimps and some involves inactivating or ’quenching’ an excited algae but not plants). Xu et al. discovered that state of chlorophyll called a triplet state: if this these plants were still able to perform photosyn- Copyright Telfer. This article is state is not quenched it reacts with oxygen mol- thesis and concluded that b-carotene is not distributed under the terms of the ecules to form singlet oxygen – an excited state essential for this process. Instead, astaxanthin Creative Commons Attribution of oxygen that can destroy chlorophyll and acted as a substitute for b-carotene and was License, which permits unrestricted cause damage to proteins and lipid membranes able to bind to both the reaction centre and the use and redistribution provided that the original author and source are in the photosynthetic machinery of the plant light harvesting complex. Moreover, the photo- credited. (Krieger-Liszkay, 2005). systems were stable, and the plants were still Telfer. eLife 2020;9:e63584. DOI: https://doi.org/10.7554/eLife.63584 1 of 2 Insight Photosystems Performing photosynthesis without b-carotene able to conduct photosynthesis, even though [email protected] some of the b-carotene binding sites remained https://orcid.org/0000-0002-3654-4558 empty. Mutant plants were more sensitive to light, which is likely due to the reduced level of Competing interests: The author declares that no b-carotene (and hence a reduced ability to competing interests exist. quench the triplet state of chlorophyll). Published 03 November 2020 However, previous research has shown that xanthophylls can also quench chlorophyll in a References triplet state if they are close enough. This reac- Edge R, McGarvey DJ, Truscott TG. 1997. The tion also leaves the xanthophyll in a triplet state carotenoids as anti-oxidants — a review. Journal of (which decays harmlessly producing Photochemistry and Photobiology B: Biology 41:189– 200. DOI: https://doi.org/10.1016/S1011-1344(97) heat) and quenching by xanthophylls is faster 00092-4 than the reaction producing singlet oxygen. Xan- Frank HA, Cogdell RJ. 1996. Carotenoids in thophylls located in the light harvesting com- photosynthesis. Photochemistry and Photobiology 63: plexes help to prevent bleaching of chlorophyll 257–264. DOI: https://doi.org/10.1111/j.1751-1097. 1996.tb03022.x, PMID: 8881328 at high light intensities (Mozzo et al., 2008; Krieger-Liszkay A. 2005. Singlet oxygen production in Edge et al., 1997), which is not the case for b- photosynthesis. Journal of Experimental Botany 56: carotene in the reaction centres (Telfer, 2002). 337–346. DOI: https://doi.org/10.1093/jxb/erh237, The discovery that a xanthophyll (astaxanthin) PMID: 15310815 can take over from b-carotene in the reaction Mozzo M, Dall’Osto L, Hienerwadel R, Bassi R, Croce centres of both photosystems in R. 2008. Photoprotection in the antenna complexes of photosystem II: role of individual xanthophylls in tobacco mutants raises the question of why, in chlorophyll triplet quenching. The Journal of Biological wild type plants, the reaction centres only bind Chemistry 283:6184–6192. DOI: https://doi.org/10. b-carotene and not a xanthophyll. Is b-carotene 1074/jbc.M708961200, PMID: 18079125 simply better at quenching singlet oxygen Siefermann-Harms D. 1985. Carotenoids in (Telfer et al., 1994)? This idea seems to be sup- photosynthesis. I. Location in photosynthetic membranes and light-harvesting function. Biochimica ported by the fact that the rate of irreversible Et Biophysica Acta (BBA) - Reviews on Bioenergetics bleaching of chlorophyll was greater the less b- 811:325–355. DOI: https://doi.org/10.1016/0304-4173 carotene was present in reaction centres, due to (85)90006-0 a higher number of singlet oxygen molecules Telfer A, Dhami S, Bishop SM, Phillips D, Barber J. 1994. b-carotene quenches singlet oxygen formed by being formed there. isolated photosystem II reaction centers. Biochemistry The mutant plants of Xu et al. did not grow 33:14469–14474. DOI: https://doi.org/10.1021/ as fast as wild type plants, nor do they contain bi00252a013, PMID: 7981207 as much chlorophyll per unit area of the leaves. Telfer A. 2002. What is b–carotene doing in the Further work is needed to assess the viability photosystem II reaction centre? Philosophical and competitiveness of the mutant plant com- Transactions of the Royal Society of London. Series B: Biological Sciences 357:1431–1440. DOI: https://doi. pared to the wild type, which may reveal why org/10.1098/rstb.2002.1139, PMID: 12437882 native plants use b-carotene and not xantho- To´ th TN, Chukhutsina V, Domonkos I, Knoppova´J, phylls in their reaction centres. Nevertheless, Xu Komenda J, Kis M, Le´na´rt Z, Garab G, Kova´cs L, et al. show that the photosynthetic system can Gombos Z, van Amerongen H. 2015. Carotenoids are essential for the assembly of cyanobacterial adapt to changes, even if they are unnatural. photosynthetic complexes. Biochimica Et Biophysica This could play an important role for redesigning Acta (BBA) - Bioenergetics 1847:1153–1165. photosynthetic complexes to, for example, DOI: https://doi.org/10.1016/j.bbabio.2015.05.020 improve the productivity of crops. Xu P, Chukhutsina VU, Nawrocki WJ, Schansker G, Bielczynski LW, Lu Y, Karcher D, Bock R, Croce R. 2020. b-carotene is not essential for photosynthesis in Alison Telfer is in the Department of Life Sciences, higher plants. eLife 9:e58984. DOI: https://doi.org/10. Imperial College London, London, United Kingdom 7554/eLife.58984 Telfer. eLife 2020;9:e63584. DOI: https://doi.org/10.7554/eLife.63584 2 of 2.
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