• This record comes from PubMed

Exposed red leaves display adaptive adjustments in chlorophyll and photosystem ratios compatible with the shade imposed by anthocyanin accumulation

. 2022 ; 60 (1) : 70-78. [epub] 20220113

Status PubMed-not-MEDLINE Language English Country Czech Republic Media electronic-ecollection

Document type Journal Article

Foliar anthocyanins shape a peculiar shade in a red leaf's interior leading to uneven energy distribution between the two photosystems. Accordingly, a readjustment of PSII/PSI stoichiometry could restore excitation balance. To test this hypothesis, 77 K fluorescence emission spectra of thylakoids from green and red leaves of seven species with different pigment profiles were compared. The ratio of F686/F736 served as an indication of the PSII/PSI functional ratio. To avoid possible species-dependent differences in the measured parameters, plants showing intra-individual, intra-species, or intra-leaf variation in the expression of the anthocyanic character were used. Red leaves or red leaf areas displayed higher PSII/PSI ratio, irrespectively of species and anthocyanin accumulation pattern. PSII/PSI ratio declined in parallel with anthocyanin decrease. In five species, red leaves displayed also a lower Chl a/b ratio. We conclude that red leaves growing in full sunlight develop adaptive adjustments in their chlorophyll and photosystem ratios, compatible with the shade-acclimation syndrome.

See more in PubMed

Anderson J.M.: Photoregulation of the composition, function, and structure of thylakoid membranes. – Annu. Rev. Plant Phys. 37: 93-136, 1986. https://www.annualreviews.org/doi/10.1146/annurev.pp.37.060186.000521 DOI

Anderson J.M., Chow W.S., Park Y.-I.: The grand design of photosynthesis: Acclimation of the photosynthetic apparatus to environmental cues. – Photosynth. Res. 46: 129-139, 1995. https://link.springer.com/article/10.1007/BF00020423 PubMed DOI

Andrizhiyevskaya E.G., Chojnicka A., Bautista J.A. et al.: Origin of the F685 and F695 fluorescence in Photosystem II. – Photosynth. Res. 84: 173-180, 2005. https://link.springer.com/article/10.1007%2Fs11120-005-0478-7 PubMed

Archetti M., Döring T.F., Hagen S.B. et al.: Unravelling the evolution of autumn colours: an interdisciplinary approach. – Trends Ecol. Evol. 24: 166-173, 2009. https://www.sciencedirect.com/science/article/pii/S0169534709000214?via%3Dihub PubMed

Burger J., Edwards G.E.: Photosynthetic efficiency and photodamage by UV and visible radiation in red versus green leaf coleus varieties. – Plant Cell Physiol. 37: 395-399, 1996. https://academic.oup.com/pcp/article/37/3/395/1931190

Chalker-Scott L.: Environmental significance of anthocyanins in plant stress responses. – Photochem. Photobiol. 70: 1-9, 1999. https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1751-1097.1999.tb01944.x DOI

Chow W.S., Melis A., Anderson J.M.: Adjustments of photosystem stoichiometry in chloroplasts improve the quantum efficiency of photosynthesis. – P. Natl. Acad. Sci. USA 87: 7502-7506, 1990. https://www.pnas.org/content/87/19/7502 PubMed PMC

Close D.C., Beadle C.L.: The ecophysiology of foliar anthocyanins. – Bot. Rev. 69: 149-161, 2003. https://link.springer.com/article/10.1663/0006-8101(2003)069%5b0149:TEOFA%5d2.0.CO;2 DOI

Glick R.E., McCauley S.W., Melis A.: Effect of light quality on chloroplast-membrane organization and function in pea. – Planta 164: 487-494, 1985. https://link.springer.com/article/10.1007/BF00395964 PubMed DOI

Gould K.S.: Nature’s Swiss army knife: the diverse protective roles of anthocyanins in leaves. – J. Biomed. Biotechnol. 2004: 314-320, 2004. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1082902/pdf/S1110724304406147.pdf PubMed PMC

Gould K.S., Jay-Allemand C., Logan B.A. et al.: 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, 2018. https://www.sciencedirect.com/science/article/pii/S009884721830248X?via%3Dihub

Gould K.S., Neill S., Vogelmann T.C.: A unified explanation for anthocyanins in leaves? – Adv. Bot. Res. 37: 167-192, 2002a. https://www.sciencedirect.com/science/article/pii/S0065229602370496?via%3Dihub

Gould K.S., Vogelmann T.C., Han T., Clearwater M.J.: Profiles of photosynthesis within red and green leaves of Quintinia serrata A. Cunn. – Physiol. Plantarum 116: 127-133, 2002b. https://onlinelibrary.wiley.com/doi/full/10.1034/j.1399-3054.2002.1160116.x PubMed DOI

Harborne J.B.: The anthocyanin pigments. – In: Harborne J.B. (ed.): Comparative Biochemistry of the Flavonoids. Pp. 1-36. Academic Press, London: 1976.

Hoch W.A., Zeldin E.L., McCowan B.H.: Physiological significance of anthocyanins during autumnal leaf senescence. – Tree Physiol. 21: 1-8, 2001. https://academic.oup.com/treephys/article/21/1/1/1643162 PubMed

Hogewoning S.W., Wientjes E., Douwstra P. et al.: Photosynthetic quantum yield dynamics: from photosystems to leaves. – Plant Cell 24: 1921-1935, 2012. https://academic.oup.com/plcell/article/24/5/1921/6097455 PubMed PMC

Hrazdina G., Wagner G.J., Siegelman H.W.: Subcellular localization of enzymes of anthocyanin biosynthesis in protoplasts. – Phytochemistry 17: 53-56, 1978. https://www.sciencedirect.com/science/article/pii/S003194220089679X

Hughes N.M.: Winter leaf reddening in ‘evergreen’ species. – New Phytol. 190: 573-581, 2011. https://nph.onlinelibrary.wiley.com/doi/10.1111/j.1469-8137.2011.03662.x PubMed DOI

Hughes N.M., Morley C.B., Smith W.K.: Coordination of anthocyanin decline and photosynthetic maturation in juvenile leaves of three deciduous tree species. – New Phytol. 175: 675-685, 2007. https://nph.onlinelibrary.wiley.com/doi/10.1111/j.1469-8137.2007.02133.x PubMed DOI

Hughes N.M., Smith W.K.: Attenuation of incident light in Galax urceolata (Diapensiaceae): concerted influence of adaxial and abaxial anthocyanic layers on photoprotection. – Am. J. Bot. 94: 784-790, 2007. https://bsapubs.onlinelibrary.wiley.com/doi/abs/10.3732/ajb.94.5.784 PubMed DOI

Karabourniotis G., Bornman J.F., Liakoura V.: Different leaf surface characteristics of three grape cultivars affect leaf optical properties as measured with fibre optics: possible implication in stress tolerance. – Aust. J. Plant Physiol. 26: 47-53, 1999. https://www.publish.csiro.au/fp/PP98052

Krause G.H., Weis E.: Chlorophyll fluorescence and photosynthesis: the basics. – Annu. Rev. Plant Phys. 42: 313-49, 1991. https://www.annualreviews.org/doi/abs/10.1146/annurev.pp.42.060191.001525 DOI

Kyparissis A., Grammatikopoulos G., Manetas Y.: Leaf morphological and physiological adjustments to the spectrally selective shade imposed by anthocyanins in Prunus cerasifera. – Tree Physiol. 27: 849-857, 2007. https://academic.oup.com/treephys/article/27/6/849/1664682 PubMed

Kytridis V.-P., Karageorgou P., Levizou E., Manetas Y.: Intraspecies variation in transient accumulation of leaf anthocyanins in Cistus creticus during winter: evidence that anthocyanins may compensate for an inherent photosynthetic and photoprotective inferiority of the red-leaf phenotype. – J. Plant Physiol. 165: 952-959, 2008. https://www.sciencedirect.com/science/article/pii/S0176161707002210?via%3Dihub PubMed

Kytridis V.-P., Manetas Y.: Mesophyll versus epidermal anthocyanins as potential in vivo antioxidants: evidence linking the putative antioxidant role to the proximity of oxy-radical source. – J. Exp. Bot. 57: 2203-2210, 2006. https://academic.oup.com/jxb/article/57/10/2203/470351 PubMed

Lamb J.J., Røkke G., Hohmann-Marriott M.F.: Chlorophyll fluorescence emission spectroscopy of oxygenic organisms at 77 K. – Photosynthetica 56: 105-124, 2018. https://link.springer.com/article/10.1007/s11099-018-0791-y DOI

Landi M., Agati G., Fini A. et al.: Unveiling the shade nature of cyanic leaves: A view from the “blue absorbing side” of anthocyanins. – Plant Cell Environ. 44: 1119-1129, 2021. https://onlinelibrary.wiley.com/doi/10.1111/pce.13818 PubMed DOI

Lee D.W., Collins T.M.: Phylogenetic and ontogenetic influences on the distribution of anthocyanins and betacyanins in leaves of tropical plants. – Int. J. Plant Sci. 162: 1141-1153, 2001.

Lev-Yadun S., Dafni A., Flaishman M.A. et al.: Plant coloration undermines herbivorous insect camouflage. – BioEssays 26: 1126-1130, 2004. PubMed

Lichtenthaler H.K., Ač A., Marek M.V. et al.: Differences in pigment composition, photosynthetic rates and chlorophyll fluorescence images of sun and shade leaves of four tree species. – Plant Physiol. Bioch. 45: 577-588, 2007. https://www.sciencedirect.com/science/article/pii/S0981942807000939?via%3Dihub PubMed

Lichtenthaler H.K., Babani F., Navrátil M., Buschmann C.: Chlorophyll fluorescence kinetics, photosynthetic activity, and pigment composition of blue-shade and half-shade leaves as compared to sun and shade leaves of different trees. – Photosynth. Res. 117: 355-366, 2013. https://link.springer.com/article/10.1007%2Fs11120-013-9834-1 PubMed

Lichtenthaler H.K., Babani F.: Light adaptation and senescence of the photosynthetic apparatus: changes in pigment composition, chlorophyll fluorescence parameters and photosynthetic activity during light adaptation and senescence of leaves. – In: Papageorgiou G.C., Govindjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and Respiration. Pp. 713-736. Springer, Dordrecht: 2004. https://link.springer.com/chapter/10.1007/978-1-4020-3218-9_28 DOI

Lichtenthaler H.K., Wellburn A.R.: Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. – Biochem. Soc. T. 11: 591-592, 1983. https://portlandpress.com/biochemsoctrans/article-abstract/11/5/591/57549/Determinations-of-total-carotenoids-and?redirectedFrom=fulltext

Lindoo S.J., Caldwell M.M.: Ultraviolet-B radiation-induced inhibition of leaf expansion and promotion of anthocyanin production – lack of involvement of low irradiance phytochrome system. – Plant Physiol. 61: 278-282, 1978. https://academic.oup.com/plphys/article/61/2/278/6076250 PubMed PMC

Manetas Y.: Why some leaves are anthocyanic and why most anthocyanic leaves are red? – Flora 201: 163-177, 2006. https://www.sciencedirect.com/science/article/pii/S0367253005001258?via%3Dihub

Manetas Y., Petropoulou Y., Psaras G.K., Drinia A.: Exposed red (anthocyanic) leaves of Quercus coccifera display shade characteristics. – Funct. Plant Biol. 30: 265-270, 2003. https://www.publish.csiro.au/fp/FP02226 PubMed

Melis A.: Light regulation of photosynthetic membrane structure, organization and function. – J. Cell. Biochem. 24: 271-285, 1984. https://onlinelibrary.wiley.com/doi/10.1002/jcb.240240308 PubMed DOI

Melis A.: Dynamics of photosynthetic membrane composition and function. – BBA-Bioenergetics 1058: 87-106, 1991. https://www.sciencedirect.com/science/article/pii/S0005272805802257?via%3Dihub

Merzlyak M.N., Chivkunova O.B., Solovchenko A.E., Naqvi K.R.: Light absorption by anthocyanins in juvenile, stressed, and senescing leaves. – J. Exp. Bot. 59: 3903-3911, 2008. https://academic.oup.com/jxb/article/59/14/3903/548787 PubMed PMC

Murchie E.H., Horton P.: Contrasting patterns of photosynthetic acclimation to the light environment are dependent on the differential expression of the responses to altered irradiance and spectral quality. – Plant Cell Environ. 21: 139-148, 1998. https://onlinelibrary.wiley.com/doi/full/10.1046/j.1365-3040.1998.00262.x DOI

Murray J.R., Hackett W.P.: Dihydroflavonol reductase activity in relation to differential anthocyanin accumulation in juvenile and mature phase Hedera helix L. – Plant Physiol. 97: 343-351, 1991. https://academic.oup.com/plphys/article/97/1/343/6087228 PubMed PMC

Neill S., Gould K.S.: Optical properties of leaves in relation to anthocyanin concentration and distribution. – Can. J. Bot. 77: 1777-1782, 2000. https://cdnsciencepub.com/doi/10.1139/b99-153 DOI

Papageorgiou G.C., Govindjee: Chlorophyll a Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and Respiration. Pp. 818. Springer, Dordrecht: 2004. https://link.springer.com/book/10.1007%2F978-1-4020-3218-9

Pfannschmidt T.: Acclimation to varying light qualities: toward the functional relationship of state transitions and adjustment of photosystem stoichiometry. – J. Phycol. 41: 723-725, 2005. https://onlinelibrary.wiley.com/doi/10.1111/j.1529-8817.2005.00116.x DOI

Pietrini F., Massacci A.: Leaf anthocyanin content changes in Zea mays L. grown at low temperature: significance for the relationship between the quantum yield of PSII and the apparent quantum yield of CO2 assimilation. – Photosynth. Res. 58: 213-219, 1998. https://link.springer.com/article/10.1023%2FA%3A1006152610137

Šiffel P., Hunalová I., Roháček K.: Light-induced quenching of chlorophyll fluorescence at 77 K in leaves, chloroplasts and Photosystem II particles. – Photosynth. Res. 65: 219-229, 2000. https://link.springer.com/article/10.1023/A:1010730103382 PubMed DOI

Steyn W.J., Wand S.J.E., Holcroft D.M., Jacobs G.: Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. – New Phytol. 155: 349-361, 2002. PubMed

Tang Y., Wen X., Lu C.: Differential changes in degradation of chlorophyll–protein complexes of photosystem I and photosystem II during flag leaf senescence of rice. – Plant Physiol. Bioch. 43: 193-201, 2005. PubMed

Velitchkova M., Popova A.: High light-induced changes of 77 K fluorescence emission of pea thylakoid membranes with altered membrane fluidity. – Bioelectrochemistry 67: 81-90, 2005. https://www.sciencedirect.com/science/article/pii/S1567539404002737?via%3Dihub PubMed

Walters R.G.: Towards an understanding of photosynthetic acclimation. – J. Exp. Bot. 56: 435-447, 2005. https://academic.oup.com/jxb/article/56/411/435/429894 PubMed

Weis E.: Chlorophyll fluorescence at 77 K in intact leaves: characterization of a technique to eliminate artifacts related to self-absorption. – Photosynth. Res. 6: 73-86, 1985. https://link.springer.com/article/10.1007%2FBF00029047 PubMed

Yiotis C., Petropoulou Y., Manetas Y.: Evidence for light-independent and steeply decreasing PSII efficiency along twig depth in four tree species. – Photosynthetica 47: 223-231, 2009.

Zeliou K., Manetas Y., Petropoulou Y.: Transient winter leaf reddening in Cistus creticus characterizes weak (stress-sensitive) individuals, yet anthocyanins cannot alleviate the adverse effects on photosynthesis. – J. Exp. Bot. 60: 3031-3042, 2009. https://academic.oup.com/jxb/article/60/11/3031/529955 PubMed PMC

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...