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The role of photosynthesis related pigments in light harvesting, photoprotection and enhancement of photosynthetic yield in planta

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Abstract

Photosynthetic pigments are an integral and vital part of all photosynthetic machinery and are present in different types and abundances throughout the photosynthetic apparatus. Chlorophyll, carotenoids and phycobilins are the prime photosynthetic pigments which facilitate efficient light absorption in plants, algae, and cyanobacteria. The chlorophyll family plays a vital role in light harvesting by absorbing light at different wavelengths and allowing photosynthetic organisms to adapt to different environments, either in the long-term or during transient changes in light. Carotenoids play diverse roles in photosynthesis, including light capture and as crucial antioxidants to reduce photodamage and photoinhibition. In the marine habitat, phycobilins capture a wide spectrum of light and have allowed cyanobacteria and red algae to colonise deep waters where other frequencies of light are attenuated by the water column. In this review, we discuss the potential strategies that photosynthetic pigments provide, coupled with development of molecular biological techniques, to improve crop yields through enhanced light harvesting, increased photoprotection and improved photosynthetic efficiency.

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References

  • Allakhverdiev S, Kreslavski V, Zharmukhamedov S, Voloshin R, Korol’kova D, Tomo T, Shen J-R (2016) Chlorophylls d and f and their role in primary photosynthetic processes of cyanobacteria. Biochem Mosc 81(3):201–212

    Article  CAS  Google Scholar 

  • Allen JF, Forsberg J (2001) Molecular recognition in thylakoid structure and function. Trends Plant Sci 6(7):317–326

    Article  CAS  PubMed  Google Scholar 

  • Alotaibi SS, Sparks CA, Parry MA, Simkin AJ, Raines CA (2018) Identification of leaf promoters for use in transgenic wheat. Plants 7(2):27

    Article  PubMed Central  CAS  Google Scholar 

  • Andreoni A, Lin S, Liu H, Blankenship RE, Yan H, Woodbury NW (2017) Orange carotenoid protein as a control element in an antenna system based on a DNA nanostructure. Nano Lett 17(2):1174–1180

    Article  CAS  PubMed  Google Scholar 

  • Ariizumi T, Kishimoto S, Kakami R, Maoka T, Hirakawa H, Suzuki Y, Ozeki Y, Shirasawa K, Bernillon S, Okabe Y, Moing A, Asamizu E, Rothan C, Ohmiya A, Ezura H (2014) Identification of the carotenoid modifying gene PALE YELLOW PETAL 1 as an essential factor in xanthophyll esterification and yellow flower pigmentation in tomato (Solanum lycopersicum). Plant J 79(3):453–465. https://doi.org/10.1111/tpj.12570

    Article  CAS  PubMed  Google Scholar 

  • Armbruster U, Galvis VC, Kunz H-H, Strand DD (2017) The regulation of the chloroplast proton motive force plays a key role for photosynthesis in fluctuating light. Curr Opin Plant Biol 37:56–62

    Article  CAS  PubMed  Google Scholar 

  • Auldridge ME, Block A, Vogel JT, Dabney-Smith C, Mila I, Bouzayen M, Magallanes-Lundback M, DellaPenna D, McCarty DR, Klee HJ (2006a) Characterization of three members of the Arabidopsis carotenoid cleavage dioxygenase family demonstrates the divergent roles of this multifunctional enzyme family. Plant J 45(6):982–993. https://doi.org/10.1111/j.1365-313X.2006.02666.x

    Article  CAS  PubMed  Google Scholar 

  • Auldridge ME, McCarty DR, Klee HJ (2006b) Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol 9(3):315–321

    Article  CAS  PubMed  Google Scholar 

  • Ayumi Tanaka A (1998) Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a. Proc Natl Acad Sci USA 95:12719–12723

    Article  PubMed Central  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113

    Article  CAS  PubMed  Google Scholar 

  • Ballottari M, Truong TB, De Re E, Erickson E, Stella GR, Fleming GR, Bassi R, Niyogi KK (2016) Identification of pH-sensing sites in the light harvesting complex stress-related 3 protein essential for triggering non-photochemical quenching in Chlamydomonas reinhardtii. J Biol Chem 291(14):7334–7346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bamsey M, Berinstain A, Graham T, Neron P, Giroux R, Braham S, Ferl R, Paul A-L, Dixon M (2009) Developing strategies for automated remote plant production systems: environmental control and monitoring of the Arthur Clarke Mars Greenhouse in the Canadian High Arctic. Adv Space Res 44(12):1367–1381

    Article  CAS  Google Scholar 

  • Bamsey MT, Zabel P, Zeidler C, Gyimesi D, Schubert D, Kohlberg E, Mengedoht D, Rae J, Graham T (2015) Review of Antarctic greenhouses and plant production facilities: A historical account of food plants on the ice. In: 45th international conference on environmental systems

  • Bassham JA, Calvin M (1960) The path of carbon in photosynthesis. In: Die CO2-assimilation/the assimilation of carbon dioxide. Springer, New York, pp 884–922

  • Beale S (1999) Enzymes of chlorophyll biosynthesis. Photosynth Res 60:43–73

    Article  CAS  Google Scholar 

  • Beckmann J, Lehr F, Finazzi G, Hankamer B, Posten C, Wobbe L, Kruse O (2009) Improvement of light to biomass conversion by de-regulation of light-harvesting protein translation in Chlamydomonas reinhardtii. J Biotechnol 142(1):70–77

    Article  CAS  PubMed  Google Scholar 

  • Biel K, Fomina I (2015) Benson-Bassham-Calvin cycle contribution to the organic life on our planet. Photosynthetica 53(2):161–167. https://doi.org/10.1007/s11099-015-0112-7

    Article  CAS  Google Scholar 

  • Blankenship R (2002) Molecular mechanisms of photosynthesis. Blackwell Science, Maiden

    Book  Google Scholar 

  • Blankenship RE (2010) Early evolution of photosynthesis. Plant Physiol 154(2):434–438. https://doi.org/10.1104/pp.110.161687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blankenship RE (2014) Molecular mechanisms of photosynthesis. Wiley, New York

    Google Scholar 

  • Bonente G, Ballottari M, Truong TB, Morosinotto T, Ahn TK, Fleming GR, Niyogi KK, Bassi R (2011) Analysis of LhcSR3, a protein essential for feedback de-excitation in the green alga Chlamydomonas reinhardtii. PLoS Biol 9(1):e1000577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Booker J, Auldridge M, Wills S, McCarty D, Klee H, Leyser O (2004) MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr Biol 14(14):1232–1238. https://doi.org/10.1016/j.cub.2004.06.061

    Article  CAS  PubMed  Google Scholar 

  • Bouvier F, Dogbo O, Camara B (2003a) Biosynthesis of the food and cosmetic plant pigment bixin (annatto). Science 300(5628):2089–2091

    Article  CAS  PubMed  Google Scholar 

  • Bouvier F, Suire C, Mutterer J, Camara B (2003b) Oxidative remodeling of chromoplast carotenoids: identification of the carotenoid dioxygenase CsCCD and CsZCD genes involved in Crocus secondary metabolite biogenesis. Plant Cell 15(1):47–62

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Budzikiewicz H, Taraz K (1971) Chlorophyll c. Tetrahedron 27(7):1447–1460. https://doi.org/10.1016/S0040-4020(01)98010-X

    Article  CAS  Google Scholar 

  • Bungard RA, Ruban AV, Hibberd JM, Press MC, Horton P, Scholes JD (1999) Unusual carotenoid composition and a new type of xanthophyll cycle in plants. Proc Natl Acad Sci 96(3):1135–1139. https://doi.org/10.1073/pnas.96.3.1135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calderini DF, Dreccer MF, Slafer GA (1995) Genetic improvement in wheat yield and associated traits. A re-examination of previous results and the latest trends. Plant Breeding 114:108–112

    Article  Google Scholar 

  • Calvin M, Benson AA (1948) The path of carbon in photosynthesis. Science 107(2784):476–480. https://doi.org/10.1126/science.107.2784.476

    Article  CAS  PubMed  Google Scholar 

  • Cazzaniga S, Bressan M, Carbonera D, Agostini A, Dall’Osto L (2016) Differential roles of carotenes and xanthophylls in photosystem I photoprotection. Biochemistry 55(26):3636–3649. https://doi.org/10.1021/acs.biochem.6b00425

    Article  CAS  PubMed  Google Scholar 

  • Chakdar H, Pabbi S (2016) Cyanobacterial phycobilins: production, purification, and regulation. Frontier discoveries and innovations in interdisciplinary microbiology. Springer, New York, pp 45–69

    Chapter  Google Scholar 

  • Chalker-Scott L (1999) Environmental significance of anthocyanins in plant stress responses. Photochem Photobiol 70(1):1–9

    Article  CAS  Google Scholar 

  • Chen M, Blankenship RE (2011) Expanding the solar spectrum used by photosynthesis. Trends Plant Sci 16(8):427–431

    Article  CAS  PubMed  Google Scholar 

  • Chen M, Schliep M, Willows RD, Cai ZL, Neilan BA, Scheer H (2010) A red-shifted chlorophyll. Science 329(5997):1318–1319. https://doi.org/10.1126/science.1191127

    Article  CAS  PubMed  Google Scholar 

  • Chida H, Nakazawa A, Akazaki H, Hirano T, Suruga K, Ogawa M, Satoh T, Kadokura K, Yamada S, Hakamata W, Isobe K, Ito T, Ishii R, Nishio T, Sonoike K, Oku T (2007) Expression of the algal cytochrome c6 gene in Arabidopsis enhances photosynthesis and growth. Plant Cell Physiol 48(7):948–957. https://doi.org/10.1093/pcp/pcm064

    Article  CAS  PubMed  Google Scholar 

  • Cho F (1970) Low-temperature (4–77 degrees K) spectroscopy of Chlorella: temperature dependence of energy transfer efficiency. Biochim Biophys Acta 216(1):139–150. https://doi.org/10.1016/0005-2728(70)90166-0

    Article  CAS  PubMed  Google Scholar 

  • Christie JM (2007) Phototropin blue-light receptors. Annu Rev Plant Biol 58:21–45

    Article  CAS  PubMed  Google Scholar 

  • Correa-Galvis V, Redekop P, Guan K, Griess A, Truong TB, Wakao S, Niyogi KK, Jahns P (2016) Photosystem II subunit PsbS is involved in the induction of LHCSR protein-dependent energy dissipation in Chlamydomonas reinhardtii. J Biol Chem 291(33):17478–17487. https://doi.org/10.1074/jbc.M116.737312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Croce R (2012) Chlorophyll-binding proteins of higher plants and cyanobacteria. In: Eaton-Rye JJ, Tripathy BC, Sharkey TD (eds) Photosynthesis: plastid biology, energy conversion and carbon assimilation. Springer, Dordrecht, pp 127–149

    Chapter  Google Scholar 

  • Croce R, Van Amerongen H (2014) Natural strategies for photosynthetic light harvesting. Nat Chem Biol 10(7):492

    Article  CAS  PubMed  Google Scholar 

  • Czarnecki O, Grimm B (2012) Post-translational control of tetrapyrrole biosynthesis in plants, algae, and cyanobacteria. J Exp Bot 63(4):1675–1687

    Article  CAS  PubMed  Google Scholar 

  • Dall’Osto L, Lico C, Alric J, Giuliano G, Havaux M, Bassi R (2006) Lutein is needed for efficient chlorophyll triplet quenching in the major LHCII antenna complex of higher plants and effective photoprotection in vivo under strong light. BMC Plant Biol 6(1):32

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dall’Osto L, Fiore A, Cazzaniga S, Giuliano G, Bassi R (2007) Different roles of alpha- and beta-branch xanthophylls in photosystem assembly and photoprotection. J Biol Chem 282(48):35056–35068. https://doi.org/10.1074/jbc.M704729200

    Article  CAS  PubMed  Google Scholar 

  • Dall’Osto L, Cazzaniga S, Havaux M, Bassi R (2010) Enhanced photoprotection by protein-bound vs free xanthophyll pools: a comparative analysis of chlorophyll b and xanthophyll biosynthesis mutants. Mol Plant 3(3):576–593

    Article  CAS  PubMed  Google Scholar 

  • de Bianchi S, Ballottari M, Dall’osto L, Bassi R (2010) Regulation of plant light harvesting by thermal dissipation of excess energy. Biochem Soc Trans 38(2):651–660. https://doi.org/10.1042/BST0380651

    Article  CAS  PubMed  Google Scholar 

  • Demmig-Adams B (1998) Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant Cell Physiol 39(5):474–482

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW III (1992) Carotenoid composition in sun and shade leaves of plants with different life forms. Plant Cell Environ 15(4):411–419. https://doi.org/10.1111/j.1365-3040.1992.tb00991.x

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW III (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1(1):21–26

    Article  Google Scholar 

  • Deruere J, Romer S, d’Harlingue A, Backhaus RA, Kuntz M, Camara B (1994) Fibril assembly and carotenoid overaccumulation in chromoplasts: a model for supramolecular lipoprotein structures. Plant Cell 6(1):119–133. https://doi.org/10.1105/tpc.6.1.119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Domonkos I, Kis M, Gombos Z, Ughy B (2013) Carotenoids, versatile components of oxygenic photosynthesis. Prog Lipid Res 52(4):539–561

    Article  CAS  PubMed  Google Scholar 

  • Dougherty RC, Strain HH, Svec WA, Uphaus RA, Katz JJ (1970) Structure, properties, and distribution of chlorophyll c. J Am Chem Soc 92(9):2826–2833. https://doi.org/10.1021/ja00712a037

    Article  CAS  PubMed  Google Scholar 

  • Driever SM, Simkin AJ, Alotaibi S, Fisk SJ, Madgwick PJ, Sparks CA, Jones HD, Lawson T, Parry MAJ, Raines CA (2017) Increased SBPase activity improves photosynthesis and grain yield in wheat grown in greenhouse conditions. Philos Trans R Soc B 372:1730

    Article  CAS  Google Scholar 

  • Engler C, Kandzia R, Marillonnet S (2008) A one pot, one step, precision cloning method with high throughput capability. PLoS ONE 3(11):e3647

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Esteban R, Becerril JM, García-Plazaola JI (2009a) Lutein epoxide cycle, more than just a forest tale. Plant Signal Behav 4(4):342–344. https://doi.org/10.4161/psb.4.4.8197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Esteban R, Olano JM, Castresana J, Fernández-Marín B, Hernández A, Becerril JM, García-Plazaola JI (2009b) Distribution and evolutionary trends of photoprotective isoprenoids (xanthophylls and tocopherols) within the plant kingdom. Physiol Plant 135(4):379–389. https://doi.org/10.1111/j.1399-3054.2008.01196.x

    Article  CAS  PubMed  Google Scholar 

  • Esteban R, Barrutia O, Artetxe U, Fernández-Marín B, Hernández A, García-Plazaola JI (2015) Internal and external factors affecting photosynthetic pigment composition in plants: a meta-analytical approach. New Phytol 206(1):268–280

    Article  CAS  PubMed  Google Scholar 

  • Evans TL, Fischer RA (1999) Yield potential: its definition, measurement, and significance. Crop Sci 39:1544–1551

    Article  Google Scholar 

  • Exposito-Rodriguez M, Laissue PP, López-Calcagno PE, Mullineaux PM, Raines CA, Simkin AJ (2017) Development of pGEMINI, a plant gateway destination vector allowing the simultaneous integration of two cDNA via a single LR-clonase reaction. Plants 6(4):55

    Article  PubMed Central  CAS  Google Scholar 

  • Fan Y, Chen J, Cheng Y, Raza MA, Wu X, Wang Z, Liu Q, Wang R, Wang X, Yong T (2018) Effect of shading and light recovery on the growth, leaf structure, and photosynthetic performance of soybean in a maize-soybean relay-strip intercropping system. PLoS ONE 13(5)

  • FAO (2017) The future of food and agriculture—trends and challenges. Rome

  • Farber A, Young AJ, Ruban AV, Horton P, Jahns P (1997) Dynamics of xanthophyll-cycle activity in different antenna subcomplexes in the photosynthetic membranes of higher plants (the relationship between zeaxanthin conversion and nonphotochemical fluorescence quenching). Plant Physiol 115(4):1609–1618. https://doi.org/10.1104/pp.115.4.1609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feild TS, Lee DW, Holbrook NM (2001) Why leaves turn red in autumn. The role of anthocyanins in senescing leaves of red-osier dogwood. Plant Physiol 127(2):566–574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng L, Raza MA, Li Z, Chen Y, Khalid MHB, Du J, Liu W, Wu X, Song C, Yu L, Zhang Z, Yuan S, Yang W, Yang F (2019) The influence of light intensity and leaf movement on photosynthesis characteristics and carbon balance of soybean. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01952

    Article  PubMed  PubMed Central  Google Scholar 

  • Frank HA, Cogdell RJ (1996) Carotenoids in photosynthesis. Photochem Photobiol 63(3):257–264. https://doi.org/10.1111/j.1751-1097.1996.tb03022.x

    Article  CAS  PubMed  Google Scholar 

  • Friedland N, Negi S, Vinogradova-Shah T, Wu G, Ma L, Flynn S, Kumssa T, Lee C-H, Sayre R (2019) Fine-tuning the photosynthetic light harvesting apparatus for improved photosynthetic efficiency and biomass yield. Sci Rep 9(1):1–12

    Article  CAS  Google Scholar 

  • Fryer MJ, Oxborough K, Mullineaux PM, Baker NR (2002) Imaging of photo-oxidative stress responses in leaves. J Exp Bot 53(372):1249–1254

    CAS  PubMed  Google Scholar 

  • Gale MD, Youssefian S (1985) Dwarfing genes in wheat. Progress in plant breeding. Butterworth and Co, London

    Google Scholar 

  • Gan F, Zhang S, Rockwell NC, Martin SS, Lagarias JC, Bryant DA (2014) Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345(6202):1312–1317. https://doi.org/10.1126/science.1256963

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Molina A, Leister D (2020) Accelerated relaxation of photoprotection impairs biomass accumulation in Arabidopsis. Nature Plants 6(1):9–12

    Article  PubMed  Google Scholar 

  • García-Plazaola JI, Hormaetxe K, Hernández A, Olano JM, Becerril JM (2004) The lutein epoxide cycle in vegetative buds of woody plants. Funct Plant Biol 31(8):815–823. https://doi.org/10.1071/FP04054

    Article  PubMed  Google Scholar 

  • García-Plazaola JI, Matsubara S, Osmond CB (2007) The lutein epoxide cycle in higher plants: its relationships to other xanthophyll cycles and possible functions. Funct Plant Biol 34(9):759–773

    Article  PubMed  Google Scholar 

  • Garrido JL, Zapata M, Muñiz S (1995) Spectral characterization of new chlorophyll c pigments isolated from emiliania huxleyi (prymnesiophyceae) by high-performance liquid chromatography. J Phycol 31(5):761–768. https://doi.org/10.1111/j.0022-3646.1995.00761.x

    Article  CAS  Google Scholar 

  • Giberti S, Giovannini D, Forlani G (2019) Carotenoid cleavage in chromoplasts of white and yellow-fleshed peach varieties. J Sci Food Agric 99(4):1795–1803

    Article  CAS  PubMed  Google Scholar 

  • Girolomoni L, Cazzaniga S, Pinnola A, Perozeni F, Ballottari M, Bassi R (2019) LHCSR3 is a nonphotochemical quencher of both photosystems in Chlamydomonas reinhardtii. Proc Natl Acad Sci 116(10):4212–4217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giroux R, Berinstain A, Braham S, Graham T, Bamsey M, Boyd K, Silver M, Lussier-Desbiens A, Lee P, Boucher M (2006) Greenhouses in extreme environments: the Arthur Clarke Mars Greenhouse design and operation overview. Adv Space Res 38(6):1248–1259

    Article  Google Scholar 

  • Glowacka K, Kromdijk J, Kucera K, Xie J, Cavanagh AP, Leonelli L, Leakey ADB, Ort DR, Niyogi KK, Long SP (2018) Photosystem II subunit S overexpression increases the efficiency of water use in a field-grown crop. Nat Commun 9(1):868. https://doi.org/10.1038/s41467-018-03231-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goss R (2003) Substrate specificity of the violaxanthin de-epoxidase of the primitive green alga Mantoniella squamata (Prasinophyceae). Planta 217(5):801–812

    Article  CAS  PubMed  Google Scholar 

  • Gotoh E, Suetsugu N, Yamori W, Ishishita K, Kiyabu R, Fukuda M, Higa T, Shirouchi B, Wada M (2018) Chloroplast accumulation response enhances leaf photosynthesis and plant biomass production. Plant Physiol 178(3):1358–1369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gould KS, Jay-Allemand C, Logan BA, Baissac Y, Bidel LP (2018) When are foliar anthocyanins useful to plants? Re-evaluation of the photoprotection hypothesis using Arabidopsis thaliana mutants that differ in anthocyanin accumulation. Environ Exp Bot 154:11–22

    Article  CAS  Google Scholar 

  • Granick S (1965) Evolution of heme and chlorophyll. In: Bryson G, Vogel H (eds) Evolving genes and proteins. Academic Press, New York, pp 67–88

    Chapter  Google Scholar 

  • Gruszecki WI, Strzałka K (2005) Carotenoids as modulators of lipid membrane physical properties. Biochim Biophys Acta 1740(2):108–115. https://doi.org/10.1016/j.bbadis.2004.11.015

    Article  CAS  PubMed  Google Scholar 

  • Gu J, Zhou Z, Li Z, Chen Y, Wang Z, Zhang H (2017) Rice (Oryza sativa L.) with reduced chlorophyll content exhibit higher photosynthetic rate and efficiency, improved canopy light distribution, and greater yields than normally pigmented plants. Field Crops Res. https://doi.org/10.1016/j.fcr.2016.10.008

    Article  Google Scholar 

  • Hashimoto H, Uragami C, Cogdell RJ (2016) Carotenoids and photosynthesis. Carotenoids in nature. Springer, Berlin, pp 111–139

    Chapter  Google Scholar 

  • Haupt W, Scheuerlein R (1990) Chloroplast movement. Plant Cell Environ 13(7):595–614. https://doi.org/10.1111/j.1365-3040.1990.tb01078.x

    Article  Google Scholar 

  • Havaux M (1998) Carotenoids as membrane stabilisers in chloroplasts. Trends Plant Sci 3:147–151

    Article  Google Scholar 

  • Havaux M, Dall’Osto L, Bassi R (2007) Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol 145(4):1506–1520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hieber AD, Bugos RC, Yamamoto HY (2000) Plant lipocalins: violaxanthin de-epoxidase and zeaxanthin epoxidase. Biochim Biophys Acta 1482(1–2):84–91

    Article  CAS  PubMed  Google Scholar 

  • Holt TK, Krogmann DW (1981) A carotenoid protein from cyanobacteria. Biochim Biophys Acta 637:408–414

    Article  CAS  Google Scholar 

  • Hughes NM, Lev-Yadun S (2015) Red/purple leaf margin coloration: potential ecological and physiological functions. Environ Exp Bot 119:27–39

    Article  Google Scholar 

  • Hughes NM, Smith WK (2007) Seasonal photosynthesis and anthocyanin production in 10 broadleaf evergreen species. Funct Plant Biol 34(12):1072–1079

    Article  CAS  Google Scholar 

  • Jahns P, Wehner A, Paulsen H, Hobe S (2001) De-epoxidation of violaxanthin after reconstitution into different carotenoid binding sites of light-harvesting complex II. J Biol Chem 276(25):22154–22159

    Article  CAS  PubMed  Google Scholar 

  • Jahns P, Latowski D, Strzalka K (2009) Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids. Biochim Biophys Acta 1787(1):3–14

    Article  CAS  PubMed  Google Scholar 

  • Jeffrey S (1989) Chlorophyll pigments and their distribution in the chromophyte algae. Chrompophyte Algae 13–36

  • Jia H, Förster B, Chow WS, Pogson BJ, Osmond CB (2013) Decreased photochemical efficiency of photosystem II following sunlight exposure of shade-grown leaves of avocado: because of, or in spite of, two kinetically distinct xanthophyll cycles? Plant Physiol 161(2):836–852

    Article  CAS  PubMed  Google Scholar 

  • Jiang Y, Hu H, Ma Y, Zhou J (2020) Genome-wide identification and characterization of the fibrillin gene family in Triticum aestivum. PeerJ 8:e9225

    Article  PubMed  PubMed Central  Google Scholar 

  • Jin H, Li M, Duan S, Fu M, Dong X, Liu B, Feng D, Wang J, Wang H-B (2016) Optimization of light-harvesting pigment improves photosynthetic efficiency. Plant Physiol 172(3):1720–1731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson MP, Ruban AV (2010) Arabidopsis plants lacking PsbS protein possess photoprotective energy dissipation. Plant J 61(2):283–289

    Article  CAS  PubMed  Google Scholar 

  • Johnson MP, Havaux M, Triantaphylides C, Ksas B, Pascal AA, Robert B, Davison PA, Ruban AV, Horton P (2007) Elevated zeaxanthin bound to oligomeric LHCII enhances the resistance of Arabidopsis to photooxidative stress by a lipid-protective, antioxidant mechanism. J Biol Chem 282(31):22605–22618. https://doi.org/10.1074/jbc.M702831200

    Article  CAS  PubMed  Google Scholar 

  • Johnson MP, Davison PA, Ruban AV, Horton P (2008) The xanthophyll cycle pool size controls the kinetics of non-photochemical quenching in Arabidopsis thaliana. FEBS Lett 582(2):262–266

    Article  CAS  PubMed  Google Scholar 

  • Jordheim M, Calcott K, Gould KS, Davies KM, Schwinn KE, Andersen ØM (2016) High concentrations of aromatic acylated anthocyanins found in cauline hairs in Plectranthus ciliatus. Phytochemistry 128:27–34

    Article  CAS  PubMed  Google Scholar 

  • Josse EM, Simkin AJ, Gaffe J, Laboure AM, Kuntz M, Carol P (2000) A plastid terminal oxidase associated with carotenoid desaturation during chromoplast differentiation. Plant Physiol 123(4):1427–1436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalve S, Fotschki J, Beeckman T, Vissenberg K, Beemster GT (2014) Three-dimensional patterns of cell division and expansion throughout the development of Arabidopsis thaliana leaves. J Exp Bot 65(22):6385–6397

    Article  CAS  PubMed  Google Scholar 

  • Kanazawa A, Kramer DM (2002) In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase. Proc Natl Acad Sci 99(20):12789–12794. https://doi.org/10.1073/pnas.182427499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420(6917):829

    Article  CAS  PubMed  Google Scholar 

  • Kashiyama Y, Miyashita H, Ohkubo S, Ogawa NO, Chikaraishi Y, Takano Y, Suga H, Toyofuku T, Nomaki H, Kitazato H, Nagata T, Ohkouchi N (2008) Evidence of global chlorophyll d. Science 321(5889):658. https://doi.org/10.1126/science.1158761

    Article  CAS  PubMed  Google Scholar 

  • Kerfeld CA (2004a) Structure and function of the water-soluble carotenoid-binding proteins of cyanobacteria. Photosynth Res 81(3):215–225. https://doi.org/10.1023/B:PRES.0000036886.60187.c8

    Article  CAS  PubMed  Google Scholar 

  • Kerfeld CA (2004b) Water-soluble carotenoid proteins of cyanobacteria. Arch Biochem Biophys 430(1):2–9. https://doi.org/10.1016/j.abb.2004.03.018

    Article  CAS  PubMed  Google Scholar 

  • Kim E-H, Lee Y, Kim HU (2015) Fibrillin 5 is essential for plastoquinone-9 biosynthesis by binding to solanesyl diphosphate synthases in Arabidopsis. Plant Cell 27(10):2956–2971. https://doi.org/10.1105/tpc.15.00707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirilovsky D (2007) Photoprotection in cyanobacteria: the orange carotenoid protein (OCP)-related non-photochemical-quenching mechanism. Photosynth Res 93(1–3):7–16. https://doi.org/10.1007/s11120-007-9168-y

    Article  CAS  PubMed  Google Scholar 

  • Kirilovsky D, Kerfeld CA (2012) The orange carotenoid protein in photoprotection of photosystem II in cyanobacteria. Biochim Biophys Acta 1:158–166

    Google Scholar 

  • Kirk JTO (2011) Light and photosynthesis in aquatic ecosystems. Cambridge University Press, Cambridge

    Google Scholar 

  • Koch TC, Goldman IL (2005) Relationship of carotenoids and tocopherols in a sample of carrot root-color accessions and carrot germplasm carrying Rp and rp alleles. J Agric Food Chem 53(2):325–331. https://doi.org/10.1021/jf048272z

    Article  CAS  PubMed  Google Scholar 

  • Kodama Y, Tsuboi H, Kagawa T, Wada M (2008) Low temperature-induced chloroplast relocation mediated by a blue light receptor, phototropin 2, in fern gametophytes. J Plant Res 121(4):441–448. https://doi.org/10.1007/s10265-008-0165-9

    Article  CAS  PubMed  Google Scholar 

  • Komatsu A, Terai M, Ishizaki K, Suetsugu N, Tsuboi H, Nishihama R, Yamato KT, Wada M, Kohchi T (2014) Phototropin encoded by a single-copy gene mediates chloroplast photorelocation movements in the liverwort Marchantia polymorpha. Plant Physiol 166(1):411–427. https://doi.org/10.1104/pp.114.245100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krieger-Liszkay A, Fufezan C, Trebst A (2008) Singlet oxygen production in photosystem II and related protection mechanism. Photosynth Res 98(1–3):551–564. https://doi.org/10.1007/s11120-008-9349-3

    Article  CAS  PubMed  Google Scholar 

  • Kromdijk J, Glowacka K, Leonelli L, Gabilly ST, Iwai M, Niyogi KK, Long SP (2016) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354(6314):857–861. https://doi.org/10.1126/science.aai8878

    Article  CAS  PubMed  Google Scholar 

  • Kume A, Akitsu T, Nasahara KN (2018) Why is chlorophyll b only used in light-harvesting systems? J Plant Res 131(6):961–972. https://doi.org/10.1007/s10265-018-1052-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Langenkämper G, Manac’h N, Broin M, Cuiné S, Becuwe N, Kuntz M, Rey P (2001) Accumulation of plastid lipid-associated proteins (fibrillin/CDSP34) upon oxidative stress, ageing and biotic stress in Solanaceae and in response to drought in other species. J Exp Bot 52(360):1545–1554. https://doi.org/10.1093/jexbot/52.360.1545

    Article  PubMed  Google Scholar 

  • Latowski D, Burda K, Strzalka K (2000) A mathematical model describing kinetics of conversion of violaxanthin to zeaxanthin via intermediate antheraxanthin by the xanthophyll cycle enzyme violaxanthin de-epoxidase. J Theor Biol 206(4):507–514. https://doi.org/10.1006/jtbi.2000.2141

    Article  CAS  PubMed  Google Scholar 

  • Latowski D, Kuczynska P, Strzalka K (2011) Xanthophyll cycle—a mechanism protecting plants against oxidative stress. Redox Rep 16(2):78–90. https://doi.org/10.1179/174329211X13020951739938

    Article  CAS  PubMed  Google Scholar 

  • Ledford HK, Niyogi KK (2005) Singlet oxygen and photo-oxidative stress management in plants and algae. Plant Cell Environ 28:1037–1045

    Article  CAS  Google Scholar 

  • Lefebvre S, Lawson T, Fryer M, Zakhleniuk OV, Lloyd JC, Raines CA (2005) Increased sedoheptulose-1,7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development. Plant Physiol 138(1):451–460. https://doi.org/10.1104/pp.104.055046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Z, Ahn TK, Avenson TJ, Ballottari M, Cruz JA, Kramer DM, Bassi R, Fleming GR, Keasling JD, Niyogi KK (2009) Lutein accumulation in the absence of zeaxanthin restores nonphotochemical quenching in the Arabidopsis thaliana npq1 mutant. Plant Cell 21(6):1798–1812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin J, Rouseff RL, Barros S, Naim M (2002) Aroma composition changes in early season grapefruit juice produced from thermal concentration. J Agric Food Chem 50(4):813–819

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Zhang H, Niedzwiedzki DM, Prado M, He G, Gross ML, Blankenship RE (2013) Phycobilisomes supply excitations to both photosystems in a megacomplex in cyanobacteria. Science 342(6162):1104–1107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • López-Calcagno PE, Fisk SJ, Brown K, Bull SE, P.F. S, Raines CA, (2018) Overexpressing the H-protein of the glycine cleavage system increases biomass yield in glasshouse and field-grown transgenic tobacco plants. Plant Biotechnol J 17(1):141–151. https://doi.org/10.1111/pbi.12953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lopez-Calcagno PE, Brown KL, Simkin AJ, Fisk SJ, Lawson T, Raines CA (2020) Simultaneous stimulation of RuBP regeneration and electron transport increases productivity and water use efficiency under field conditions. bioRxiv

  • Lopez-Obando M, Ligerot Y, Bonhomme S, Boyer F-D, Rameau C (2015) Strigolactone biosynthesis and signaling in plant development. Development 142(21):3615–3619. https://doi.org/10.1242/dev.120006

    Article  CAS  PubMed  Google Scholar 

  • Lovelock CE, Clough BF, Woodrow IE (1992) Distribution and accumulation of ultraviolet-radiation-absorbing compounds in leaves of tropical mangroves. Planta 188(2):143–154

    Article  CAS  PubMed  Google Scholar 

  • Mahattanatawee K, Rouseff R, Valim MF, Naim M (2005) Identification and aroma impact of norisoprenoids in orange juice. J Agric Food Chem 53(2):393–397

    Article  CAS  PubMed  Google Scholar 

  • Matsubara S, Naumann M, Martin R, Nichol C, Rascher U, Morosinotto T, Bassi R, Osmond B (2005) Slowly reversible de-epoxidation of lutein-epoxide in deep shade leaves of a tropical tree legume may ‘lock-in’ lutein-based photoprotection during acclimation to strong light. J Exp Bot 56(411):461–468. https://doi.org/10.1093/jxb/eri012

    Article  CAS  PubMed  Google Scholar 

  • Matsubara S, Morosinotto T, Osmond CB, Bassi R (2007) Short-and long-term operation of the lutein-epoxide cycle in light-harvesting antenna complexes. Plant Physiol 144(2):926–941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsubara S, Krause GH, Aranda J, Virgo A, Beisel KG, Jahns P, Winter K (2009) Sun-shade patterns of leaf carotenoid composition in 86 species of neotropical forest plants. Funct Plant Biol 36(1):20–36

    Article  CAS  PubMed  Google Scholar 

  • Matsubara S, Förster B, Waterman M, Robinson SA, Pogson BJ, Gunning B, Osmond B (2012) From ecophysiology to phenomics: some implications of photoprotection and shade–sun acclimation in situ for dynamics of thylakoids in vitro. Philos Trans R Soc B 367(1608):3503–3514

    Article  CAS  Google Scholar 

  • Merzlyak MN, Chivkunova OB, Solovchenko AE, Naqvi KR (2008) Light absorption by anthocyanins in juvenile, stressed, and senescing leaves. J Exp Bot 59(14):3903–3911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mielke SP, Kiang NY, Blankenship RE, Gunner MR, Mauzerall D (2011) Efficiency of photosynthesis in a Chl d-utilizing cyanobacterium is comparable to or higher than that in Chl a-utilizing oxygenic species. Biochim Biophys Acta 9:1231–1236. https://doi.org/10.1016/j.bbabio.2011.06.007

    Article  CAS  Google Scholar 

  • Millenaar FF, Van Zanten M, Cox MC, Pierik R, Voesenek LA, Peeters AJ (2009) Differential petiole growth in Arabidopsis thaliana: photocontrol and hormonal regulation. New Phytol 184(1):141–152

    Article  CAS  PubMed  Google Scholar 

  • Mimuro M, Akimoto S, Gotoh T, Yokono M, Akiyama M, Tsuchiya T, Miyashita H, Kobayashi M, Yamazaki I (2004) Identification of the primary electron donor in PS II of the Chl d-dominated cyanobacterium Acaryochloris marina. FEBS Lett 556(1–3):95–98. https://doi.org/10.1016/s0014-5793(03)01383-8

    Article  CAS  PubMed  Google Scholar 

  • Mirkovic T, Ostroumov EE, Anna JM, van Grondelle R, Govindjee SGD (2017) Light absorption and energy transfer in the antenna complexes of photosynthetic organisms. Chem Rev 117(2):249–293. https://doi.org/10.1021/acs.chemrev.6b00002

    Article  CAS  PubMed  Google Scholar 

  • Miyashita H, Ikemoto H, Kurano N, Adachi K, Chihara M, Miyachi S (1996) Chlorophyll d as a major pigment. Nature 383(6599):402

    Article  CAS  Google Scholar 

  • Miyashita H, Ohkubo S, Komatsu H, Sorimachi Y, Fukayama D, Fujinuma D, Akutsu S, Kobayashi M (2014) Discovery of Chlorophyll d in Acaryochloris marina and Chlorophyll f in a unicellular Cyanobacterium, strain KC1, isolated from Lake Biwa. J Phys Chem Biophys 4(4):149

    Article  CAS  Google Scholar 

  • Mukherjee S, Stasolla C, Brûlé-Babel A, Ayele BT (2015) Isolation and characterization of rubisco small subunit gene promoter from common wheat (Triticum aestivum L.). Plant Signal Behav 10(2):e989033

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125(4):1558–1566

    Article  PubMed  PubMed Central  Google Scholar 

  • Mullineaux CW, Emlyn-Jones D (2005) State transitions: an example of acclimation to low-light stress. J Exp Bot 56(411):389–393

    Article  CAS  PubMed  Google Scholar 

  • Niyogi KK, Li X-P, Rosenberg V, Jung H-S (2004) Is PsbS the site of non-photochemical quenching in photosynthesis? J Exp Bot 56(411):375–382. https://doi.org/10.1093/jxb/eri056

    Article  CAS  PubMed  Google Scholar 

  • Nobel PS (2009) Chapter 5—photochemistry of photosynthesis. In: Nobel PS (ed) Physicochemical and environmental plant physiology, 4th edn. Academic Press, San Diego, pp 228–275

    Chapter  Google Scholar 

  • Nürnberg DJ, Morton J, Santabarbara S, Telfer A, Joliot P, Antonaru LA, Ruban AV, Cardona T, Krausz E, Boussac A (2018) Photochemistry beyond the red limit in chlorophyll f–containing photosystems. Science 360(6394):1210–1213

    Article  PubMed  CAS  Google Scholar 

  • Ort DR, Melis A (2011) Optimizing antenna size to maximize photosynthetic efficiency. Plant Physiol 155(1):79–85. https://doi.org/10.1104/pp.110.165886

    Article  CAS  PubMed  Google Scholar 

  • Ort DR, Merchant SS, Alric J, Barkan A, Blankenship RE, Bock R, Croce R, Hanson MR, Hibberd JM, Long SP (2015a) Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc Natl Acad Sci 112(28):8529–8536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ort DR, Merchant SS, Alric J, Barkan A, Blankenship RE, Bock R, Croce R, Hanson MR, Hibberd JM, Long SP, Moore TA, Moroney J, Niyogi KK, Parry MAJ, Peralta-Yahya PP, Prince RC, Redding KE, Spalding MH, van Wijk KJ, Vermaas WFJ, von Caemmerer S, Weber APM, Yeates TO, Yuan JS, Zhu XG (2015b) Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc Natl Acad Sci 112(28):8529–8536. https://doi.org/10.1073/pnas.1424031112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parry AD, Babiano MJ, Horgan R (1990) The role of cis-carotenoids in abscisic acid biosynthesis. Planta 182:118–128

    Article  CAS  PubMed  Google Scholar 

  • Parry MA, Reynolds M, Salvucci ME, Raines C, Andralojc PJ, Zhu XG, Price GD, Condon AG, Furbank RT (2011) Raising yield potential of wheat. II. Increasing photosynthetic capacity and efficiency. J Exp Bot 62(2):453–467. https://doi.org/10.1093/jxb/erq304

    Article  CAS  PubMed  Google Scholar 

  • Parson WW, Green BR, Van Amerongen H, Dekker J (2003) Light-harvesting antennas in photosynthesis. Kluwer Academic

    Google Scholar 

  • Pastenes C, Pimentel P, Lillo J (2005) Leaf movements and photoinhibition in relation to water stress in field-grown beans. J Exp Bot 56(411):425–433. https://doi.org/10.1093/jxb/eri061

    Article  CAS  PubMed  Google Scholar 

  • Perrine Z, Negi S, Sayre RT (2012) Optimization of photosynthetic light energy utilization by microalgae. Algal Res 1(2):134–142

    Article  Google Scholar 

  • Pettigrew WT, Hesketh JD, Peters DB, Woolley JT (1989) Characterization of canopy photosynthesis of chlorophyll-deficient soybean isolines. Crop Sci. https://doi.org/10.2135/cropsci1989.0011183X002900040040x

    Article  Google Scholar 

  • Pharis RP, King RW (1985) Gibberellins and reproductive development in seed plants. Annu Rev Plant Physiol 36(1):517–568

    Article  CAS  Google Scholar 

  • Piccolo EL, Landi M, Massai R, Remorini D, Guidi L (2020) Girled-induced anthocyanin accumulation in red-leafed Prunus cerasifera: effect on photosynthesis, photoprotection and sugar metabolism. Plant Sci 294:110456

    Article  PubMed  CAS  Google Scholar 

  • Pieters AJ, El Souki S (2005) Effects of drought during grain filling on PS II activity in rice. J Plant Physiol 162(8):903–911. https://doi.org/10.1016/j.jplph.2004.11.001

    Article  CAS  PubMed  Google Scholar 

  • Pieters AJ, Tezara W, Herrera A (2003) Operation of the xanthophyll cycle and degradation of D1 protein in the inducible CAM plant, Talinum triangulare, under water deficit. Ann Bot 92(3):393–399. https://doi.org/10.1093/aob/mcg153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pietrini F, Iannelli M, Massacci A (2002) Anthocyanin accumulation in the illuminated surface of maize leaves enhances protection from photo-inhibitory risks at low temperature, without further limitation to photosynthesis. Plant Cell Environ 25(10):1251–1259

    Article  CAS  Google Scholar 

  • Poisson L, Schieberle P (2008) Characterization of the most odor-active compounds in an American Bourbon whisky by application of the aroma extract dilution analysis. J Agric Food Chem 56(14):5813–5819

    Article  CAS  PubMed  Google Scholar 

  • Poulet L, Massa G, Morrow R, Bourget C, Wheeler R, Mitchell C (2014) Significant reduction in energy for plant-growth lighting in space using targeted LED lighting and spectral manipulation. Life Sci Space Res 2:43–53

    Article  Google Scholar 

  • Qin X, Zeevaart JAD (1999) The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc Natl Acad Sci 96(26):15354–15361. https://doi.org/10.1073/pnas.96.26.15354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rabinowitch HD, Budowski P, Kedar N (1975) Carotenoids and epoxide cycles in mature-green tomatoes. Planta 122(1):91–97. https://doi.org/10.1007/BF00385408

    Article  CAS  PubMed  Google Scholar 

  • Raines CA (2003) The Calvin cycle revisited. Photosynth Res 75(1):1–10. https://doi.org/10.1023/A:1022421515027

    Article  CAS  PubMed  Google Scholar 

  • Raines CA, Cavanagh AP, Simkin AJ (2022) Chapter 9. Improving carbon fixation. In: Ruban A, Murchie E, Foyer C (eds) Photosynthesis in action, 1st edn. Academic Press, New York

    Google Scholar 

  • Ramel F, Birtic S, Ginies C, Soubigou-Taconnat L, Triantaphylidès C, Havaux M (2012) Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. Proc Natl Acad Sci 109(14):5535–5540. https://doi.org/10.1073/pnas.1115982109

    Article  PubMed  PubMed Central  Google Scholar 

  • Ray DK, Ramankutty N, Mueller ND, West PC, Foley JA (2012) Recent patterns of crop yield growth and stagnation. Nat Commun 3(1):1–7

    Article  CAS  Google Scholar 

  • Ray DK, Mueller ND, West PC, Foley JA (2013) Yield trends are insufficient to double global crop production by 2050. PLoS ONE 8(6):e66428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raymond J, Blankenship RE (2004) Biosynthetic pathways, gene replacement and the antiquity of life. Geobiology 2:199–203

    Article  CAS  Google Scholar 

  • Renger T, Schlodder E (2008) The primary electron donor of Photosystem II of the Cyanobacterium Acaryochloris marina is a Chlorophyll d and the water oxidation is driven by a Chlorophyll a/Chlorophyll d heterodimer. J Phys Chem B 112(25):7351–7354. https://doi.org/10.1021/jp801900e

    Article  CAS  PubMed  Google Scholar 

  • Rey P, Gillet B, Romer S, Eymery F, Massimino J, Peltier G, Kuntz M (2000) Over-expression of a pepper plastid lipid-associated protein in tobacco leads to changes in plastid ultrastructure and plant development upon stress. Plant J 21(5):483–494

    Article  CAS  PubMed  Google Scholar 

  • Reynolds M, Foulkes MJ, Slafer GA, Berry P, Parry MAJ, Snape JW, Angus WJ (2009) Raising yield potential in wheat. J Exp Bot 60(7):1899–1918. https://doi.org/10.1093/jxb/erp016

    Article  CAS  PubMed  Google Scholar 

  • RSOL (2009) Royal Society of London. Science and the Sustainable Intensification of Global Agriculture (Royal Society, London, Reaping the Benefits, p 2009

    Google Scholar 

  • Ruban AV, Young AJ, Pascal AA, Horton P (1994) The effects of illumination on the xanthophyll composition of the Photosystem II light-harvesting complexes of spinach thylakoid membranes. Plant Physiol 104(1):227–234. https://doi.org/10.1104/pp.104.1.227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rubio A, Rambla JL, Santaella M, Gomez MD, Orzaez D, Granell A, Gomez-Gomez L (2008) Cytosolic and plastoglobule-targeted carotenoid dioxygenases from Crocus sativus are both involved in beta-ionone release. J Biol Chem 283(36):24816–24825. https://doi.org/10.1074/jbc.M804000200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sacharz J, Giovagnetti V, Ungerer P, Mastroianni G, Ruban AV (2017) The xanthophyll cycle affects reversible interactions between PsbS and light-harvesting complex II to control non-photochemical quenching. Nat Plants 3(2):1–9

    Article  CAS  Google Scholar 

  • Sakowska K, Alberti G, Genesio L, Peressotti A, Delle Vedove G, Gianelle D, Colombo R, Rodeghiero M, Panigada C, Juszczak R (2018) Leaf and canopy photosynthesis of a chlorophyll deficient soybean mutant. Plant Cell Environ 41(6):1427–1437

    Article  CAS  PubMed  Google Scholar 

  • Sandmann G (1989) Inhibition of carotenoid biosynthesis by herbicides. Target sites of herbicides action

  • Sankari M, Rao PR, Hemachandran H, Pullela PK, Tayubi IA, Subramanian B, Gothandam K, Singh P, Ramamoorthy S (2018) Prospects and progress in the production of valuable carotenoids: insights from metabolic engineering, synthetic biology, and computational approaches. J Biotechnol 266:89–101

    Article  CAS  PubMed  Google Scholar 

  • Scheer H (1991) Chemistry of chlorophylls. Chlorophylls 3–30

  • Schwartz SH, Qin X, Zeevaart JA (2001) Characterization of a novel carotenoid cleavage dioxygenase from plants. J Biol Chem 276(27):25208–25211. https://doi.org/10.1074/jbc.M102146200

    Article  CAS  PubMed  Google Scholar 

  • Schwartz SH, Qin X, Loewen MC (2004) The biochemical characterization of two carotenoid cleavage enzymes from Arabidopsis indicates that a carotenoid-derived compound inhibits lateral branching. J Biol Chem 279(45):46940–46945

    Article  CAS  PubMed  Google Scholar 

  • Senge M, Ryan A, Letchford K, MacGowan S, Mielke T (2014) Chlorophylls, symmetry, chirality, and photosynthesis. Symmetry 6(3):781–843

    Article  Google Scholar 

  • Siefermann-Harms D (1994) Light and temperature control of season-dependent changes in the α- and β-carotene content of spruce needles. J Plant Physiol 143(4):488–494. https://doi.org/10.1016/S0176-1617(11)81811-0

    Article  CAS  Google Scholar 

  • Simkin AJ (2019) Genetic engineering for global food security: photosynthesis and biofortification. Plants 8(12):586

    Article  CAS  PubMed Central  Google Scholar 

  • Simkin AJ (2021) Carotenoids and apocarotenoids in planta: their role in plant development, contribution to the flavour and aroma of fruits and flowers, and their nutraceutical benefits. Plants 10(11):2321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simkin AJ, Breitenbach J, Kuntz M, Sandmann G (2000) In vitro and in situ inhibition of carotenoid biosynthesis in Capsicum annuum by bleaching herbicides. J Agric Food Chem 48(10):4676–4680

    Article  CAS  PubMed  Google Scholar 

  • Simkin AJ, Laizet Y, Kuntz M (2004a) Plastid lipid associated proteins of the fibrillin family: structure, localisation, functions and gene expression. In: Pandalai SG (ed) Recent research developmetns in biochemistry, vol 5. Research Signpost, India, pp 307–316

    Google Scholar 

  • Simkin AJ, Schwartz SH, Auldridge M, Taylor MG, Klee HJ (2004b) The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles β-ionone, pseudoionone, and geranylacetone. Plant J 40(6):882–892

    Article  CAS  PubMed  Google Scholar 

  • Simkin AJ, Underwood BA, Auldridge M, Loucas HM, Shibuya K, Schmelz E, Clark DG, Klee HJ (2004c) Circadian regulation of the PhCCD1 carotenoid cleavage dioxygenase controls emission of β-ionone, a fragrance volatile of petunia flowers. Plant Physiol 136(3):3504–3514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simkin AJ, Gaffé J, Alcaraz J-P, Carde J-P, Bramley PM, Fraser PD, Kuntz M (2007a) Fibrillin influence on plastid ultrastructure and pigment content in tomato fruit. Phytochemistry 68(11):1545–1556

    Article  CAS  PubMed  Google Scholar 

  • Simkin AJ, Gaffe J, Alcaraz JP, Carde JP, Bramley PM, Fraser PD, Kuntz M (2007b) Fibrillin influence on plastid ultrastructure and pigment content in tomato fruit. Phytochemistry 68(11):1545–1556. https://doi.org/10.1016/j.phytochem.2007.03.014

    Article  CAS  PubMed  Google Scholar 

  • Simkin AJ, Moreau H, Kuntz M, Pagny G, Lin C, Tanksley S, McCarthy J (2008) An investigation of carotenoid biosynthesis in Coffea canephora and Coffea arabica. J Plant Physiol 165(10):1087–1106. https://doi.org/10.1016/j.jplph.2007.06.016

    Article  CAS  PubMed  Google Scholar 

  • Simkin AJ, Kuntz M, Moreau H, McCarthy J (2010) Carotenoid profiling and the expression of carotenoid biosynthetic genes in developing coffee grain. Plant Physiol Biochem 48(6):434–442. https://doi.org/10.1016/j.plaphy.2010.02.007

    Article  CAS  PubMed  Google Scholar 

  • Simkin AJ, McAusland L, Headland LR, Lawson T, Raines CA (2015) Multigene manipulation of photosynthetic carbon assimilation increases CO2 fixation and biomass yield in tobacco. J Exp Bot 66(13):4075–4090. https://doi.org/10.1093/jxb/erv204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simkin AJ, Lopez-Calcagno PE, Davey PA, Headland LR, Lawson T, Timm S, Bauwe H, Raines CA (2017a) Simultaneous stimulation of sedoheptulose 1, 7-bisphosphatase, fructose 1, 6-bisphophate aldolase and the photorespiratory glycine decarboxylase-H protein increases CO 2 assimilation, vegetative biomass and seed yield in Arabidopsis. Plant Biotechnol J 15(7):805–816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simkin AJ, McAusland L, Lawson T, Raines CA (2017b) Over-expression of the RieskeFeS protein increases electron transport rates and biomass yield. Plant Physiol 175:134–145. https://doi.org/10.1101/133702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simkin AJ, Lopez-Calcagno PE, Raines CA (2019) Feeding the world: improving photosynthetic efficiency for sustainable crop production. J Exp Bot 70(4):1119–1140. https://doi.org/10.1093/jxb/ery445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simkin AJ, Faralli M, Ramamoorthy S, Lawson T (2020) Photosynthesis in non-foliar tissues: implications for yield. Plant J 101(4):1001–1015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh DK, McNellis TW (2011) Fibrillin protein function: the tip of the iceberg? Trends Plant Sci 16(8):432–441. https://doi.org/10.1016/j.tplants.2011.03.014

    Article  CAS  PubMed  Google Scholar 

  • Singh DK, Maximova SN, Jensen PJ, Lehman BL, Ngugi HK, McNellis TW (2010) FIBRILLIN4 is required for plastoglobule development and stress resistance in apple and Arabidopsis. Plant Physiol 154(3):1281–1293. https://doi.org/10.1104/pp.110.164095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siva R (2007) Status of natural dyes and dye-yielding plants in India. Curr Sci 92(7):00113891

    Google Scholar 

  • Slattery RA, VanLoocke A, Bernacchi CJ, Zhu X-G, Ort DR (2017) Photosynthesis, light use efficiency, and yield of reduced-chlorophyll soybean mutants in field conditions. Front Plant Sci 8:549

    Article  PubMed  PubMed Central  Google Scholar 

  • Snowden KC, Simkin AJ, Janssen BJ, Templeton KR, Loucas HM, Simons JL, Karunairetnam S, Gleave AP, Clark DG, Klee HJ (2005) The decreased apical dominance1/Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. Plant Cell 17(3):746–759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sobiechowska-Sasim M, Ston-Egiert J, Kosakowska A (2014) Quantitative analysis of extracted phycobilin pigments in cyanobacteria-an assessment of spectrophotometric and spectrofluorometric methods. J Appl Phycol 26(5):2065–2074. https://doi.org/10.1007/s10811-014-0244-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Solovchenko A, Merzlyak M (2008) Screening of visible and UV radiation as a photoprotective mechanism in plants. Russ J Plant Physiol 55(6):719

    Article  CAS  Google Scholar 

  • Songaila E, Augulis RN, Gelzinis A, Butkus V, Gall A, Büchel C, Robert B, Zigmantas D, Abramavicius D, Valkunas L (2013) Ultrafast energy transfer from chlorophyll c2 to chlorophyll a in fucoxanthin–chlorophyll protein complex. J Phys Chem Lett 4:3590–3595

    Article  CAS  Google Scholar 

  • Standfuss J, Terwisscha van Scheltinga AC, Lamborghini M, Kuhlbrandt W (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 A resolution. EMBO J 24 (5):919–928. doi:https://doi.org/10.1038/sj.emboj.7600585

  • Steyn WJ, Wand S, Holcroft D, Jacobs G (2002) Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. New Phytol 155(3):349–361

    Article  CAS  PubMed  Google Scholar 

  • Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16(1):53–60

    Article  CAS  PubMed  Google Scholar 

  • Takizawa K, Kanazawa A, Kramer DM (2008) Depletion of stromal Pi induces high “energy-dependent” antenna exciton quenching qE by decreasing proton conductivity at CFO-CF1 ATP synthase. Plant Cell Environ 31(2):235–243. https://doi.org/10.1111/j.1365-3040.2007.01753.x

    Article  CAS  PubMed  Google Scholar 

  • Tan B-C, Joseph LM, Deng W-T, Liu L, Li Q-B, Cline K, McCarty DR (2003) Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. Plant J 35(1):44–56. https://doi.org/10.1046/j.1365-313X.2003.01786.x

    Article  CAS  PubMed  Google Scholar 

  • Tanaka R, Kobayashi K, Masuda T (2011) Tetrapyrrole metabolism in Arabidopsis thaliana. Arabidopsis Book 9:e0145. https://doi.org/10.1199/tab.0145

    Article  PubMed  PubMed Central  Google Scholar 

  • Tattini M, Landi M, Brunetti C, Giordano C, Remorini D, Gould KS, Guidi L (2014) Epidermal coumaroyl anthocyanins protect sweet basil against excess light stress: multiple consequences of light attenuation. Physiol Plant 152(3):585–598

    Article  CAS  PubMed  Google Scholar 

  • Thayer SS, Björkman O (1990) Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynth Res 23(3):331–343

    Article  CAS  PubMed  Google Scholar 

  • Tilman D, Clark M (2015) Food, agriculture and the environment: can we feed the world and save the Earth? Daedalus 144:8–23

    Article  Google Scholar 

  • Timm S, Florian A, Arrivault S, Stitt M, Fernie AR, Bauwe H (2012) Glycine decarboxylase controls photosynthesis and plant growth. FEBS Lett 586(20):3692–3697. https://doi.org/10.1016/j.febslet.2012.08.027

    Article  CAS  PubMed  Google Scholar 

  • Tlałka M, Runquist M, Fricker M (1999) Light perception and the role of the xanthophyll cycle in blue-light-dependent chloroplast movements in Lemna trisulca L. Plant J 20(4):447–459

    Article  PubMed  Google Scholar 

  • Verhoeven A (2014) Sustained energy dissipation in winter evergreens. New Phytol 201(1):57–65

    Article  Google Scholar 

  • Vialet-Chabrand S, Matthews JS, Simkin AJ, Raines CA, Lawson T (2017) Importance of fluctuations in light on plant photosynthetic acclimation. Plant Physiol 173(4):2163–2179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vishnevetsky M, Ovadis M, Vainstein A (1999) Carotenoid sequestration in plants: the role of carotenoid-associated proteins. Trends Plant Sci 4(6):232–235

    Article  CAS  PubMed  Google Scholar 

  • Vogel JT, Walter MH, Giavalisco P, Lytovchenko A, Kohlen W, Charnikhova T, Simkin AJ, Goulet C, Strack D, Bouwmeester HJ (2010) SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato. Plant J 61(2):300–311

    Article  CAS  PubMed  Google Scholar 

  • Voitsekhovskaja O, Tyutereva E (2015) Chlorophyll b in angiosperms: functions in photosynthesis, signaling and ontogenetic regulation. J Plant Physiol 189:51–64

    Article  CAS  PubMed  Google Scholar 

  • Wada M, Kong SG (2011) Analysis of chloroplast movement and relocation in Arabidopsis. Methods Mol Biol 774:87–102. https://doi.org/10.1007/978-1-61779-234-2_6

    Article  CAS  PubMed  Google Scholar 

  • Walters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56(411):435–447. https://doi.org/10.1093/jxb/eri060

    Article  CAS  PubMed  Google Scholar 

  • Wilson A, Ajlani G, Verbavatz JM, Vass I, Kerfeld CA, Kirilovsky D (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18(4):992–1007. https://doi.org/10.1105/tpc.105.040121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Winterhalter P, Gök R (2013) TDN and β-Damascenone: two important carotenoid metabolites in wine. Carotenoid cleavage products. ACS Publications, Washington, pp 125–137

    Chapter  Google Scholar 

  • Woitsch S, Romer S (2003) Expression of xanthophyll biosynthetic genes during light-dependent chloroplast differentiation. Plant Physiol 132(3):1508–1517. https://doi.org/10.1104/pp.102.019364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • WorldBank (2008) World development report 2008: agriculture for development. World Bank, Washington

    Google Scholar 

  • Wu YP, Krogmann DW (1997) The orange carotenoid protein of Synechocystis PCC 6803. Biochim Biophys Acta 1322(1):1–7. https://doi.org/10.1016/s0005-2728(97)00067-4

    Article  CAS  PubMed  Google Scholar 

  • Yadav SK, Khatri K, Rathore MS, Jha B (2018) Introgression of UfCyt c6, a thylakoid lumen protein from a green seaweed Ulva fasciata Delile enhanced photosynthesis and growth in tobacco. Mol Biol Rep 45(6):1745–1758. https://doi.org/10.1007/s11033-018-4318-1

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto HY, Higashi RM (1978) Violaxanthin de-epoxidase: lipid composition and substrate specificity. Arch Biochem Biophys 190(2):514–522

    Article  CAS  PubMed  Google Scholar 

  • Yamori W (2016) Photosynthetic response to fluctuating environments and photoprotective strategies under abiotic stress. J Plant Res 129(3):379–395

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Sulpice R, Himmelbach A, Meinhard M, Christmann A, Grill E (2006) Fibrillin expression is regulated by abscisic acid response regulators and is involved in abscisic acid-mediated photoprotection. Proc Natl Acad Sci 103(15):6061–6066. https://doi.org/10.1073/pnas.0501720103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Youssef A, Laizet Y, Block MA, Marechal E, Alcaraz JP, Larson TR, Pontier D, Gaffe J, Kuntz M (2010) Plant lipid-associated fibrillin proteins condition jasmonate production under photosynthetic stress. Plant J 61(3):436–445. https://doi.org/10.1111/j.1365-313X.2009.04067.x

    Article  CAS  PubMed  Google Scholar 

  • Zapata M, Garrido JL, Jeffrey SW (2006) Chlorophyll c pigments: current status. In: Grimm B, Porra RJ, Rüdiger W, Scheer H (eds) Chlorophylls and bacteriochlorophylls: biochemistry, biophysics, functions and applications. Springer, Dordrecht, pp 39–53

    Chapter  Google Scholar 

  • Zeidler C, Vrakking V, Bamsey M, Poulet L, Zabel P, Schubert D, Paille C, Mazzoleni E, Domurath N (2017) Greenhouse module for space system: a lunar greenhouse design. Open Agric 2(1):116–132

    Article  Google Scholar 

  • Zhen S, Bugbee B (2020) Far-red photons have equivalent efficiency to traditional photosynthetic photons: implications for redefining photosynthetically active radiation. Plant Cell Environ. https://doi.org/10.1111/pce.13730

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors take this opportunity to thank the management of VIT for providing facilities to carry out this research work.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. AJS is supported by the Growing Kent and Medway Programme, UK; Ref 107139.

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  1. Andrew J. Simkin and Leepica Kapoor have contributed equally to this work.

Authors and Affiliations

  1. School of Biosciences, University of Kent, Canterbury, CT2 7NJ, United Kingdom

    Andrew J. Simkin

  2. School of Bio Sciences and Technology, Vellore Institute of Technology, Vellore, 632014, Tamil Nadu, India

    Leepica Kapoor, C. George Priya Doss & Siva Ramamoorthy

  3. School of Life Sciences, University of Essex, Wivenhoe Park, Colchester, CO4 3SQ, United Kingdom

    Tracy Lawson

  4. OSFC, Scrivener Drive, Pinewood, Ipswich, IP8 3SU, United Kingdom

    Tanja A. Hofmann

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AJS, TL and SR conceived the project and supervised the co-authors in writing the draft. AJS and LK wrote the article. TL, TAH and GPDC had an equal contribution in collecting information. AS, TL and SR supervised the co- authors in writing the draft, SR agrees to serve as the author responsible for contact and ensures communication.

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Correspondence to Siva Ramamoorthy.

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Simkin, A.J., Kapoor, L., Doss, C.G.P. et al. The role of photosynthesis related pigments in light harvesting, photoprotection and enhancement of photosynthetic yield in planta. Photosynth Res 152, 23–42 (2022). https://doi.org/10.1007/s11120-021-00892-6

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