Photosynthetica 2022, 60(1):70-78 | DOI: 10.32615/ps.2021.062

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

K. ZELIOU, A. KYZERIDOU, Y. PETROPOULOU
Laboratory of Plant Physiology, Department of Biology, University of Patras, Patras GR-26504, Greece

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.

Additional key words: fluorescence emission spectra; foliar anthocyanins; photosystem ratio; shade-acclimation syndrome.

Received: October 6, 2021; Revised: November 22, 2021; Accepted: December 1, 2021; Prepublished online: January 13, 2022; Published: March 18, 2022  Show citation

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ZELIOU, K., KYZERIDOU, A., & PETROPOULOU, Y. (2022). Exposed red leaves display adaptive adjustments in chlorophyll and photosystem ratios compatible with the shade imposed by anthocyanin accumulation. Photosynthetica, 60(SPECIAL ISSUE 2022), 70-78. doi: 10.32615/ps.2021.062
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    References

    1. Anderson J.M.: Photoregulation of the composition, function, and structure of thylakoid membranes. - Annu. Rev. Plant Phys. 37: 93-136, 1986. Go to original source...
    2. 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. Go to original source...
    3. 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. Go to original source...
    4. 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. Go to original source...
    5. 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. Go to original source...
    6. Chalker-Scott L.: Environmental significance of anthocyanins in plant stress responses. - Photochem. Photobiol. 70: 1-9, 1999. Go to original source...
    7. 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. Go to original source...
    8. Close D.C., Beadle C.L.: The ecophysiology of foliar anthocyanins. - Bot. Rev. 69: 149-161, 2003. Go to original source...
    9. 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. Go to original source...
    10. Gould K.S.: Nature's Swiss army knife: the diverse protective roles of anthocyanins in leaves. - J. Biomed. Biotechnol. 2004: 314-320, 2004. Go to original source...
    11. 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. Go to original source...
    12. Gould K.S., Neill S., Vogelmann T.C.: A unified explanation for anthocyanins in leaves? - Adv. Bot. Res. 37: 167-192, 2002a. Go to original source...
    13. 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. Go to original source...
    14. Harborne J.B.: The anthocyanin pigments. - In: Harborne J.B. (ed.): Comparative Biochemistry of the Flavonoids. Pp. 1-36. Academic Press, London 1976.
    15. Hoch W.A., Zeldin E.L., McCowan B.H.: Physiological significance of anthocyanins during autumnal leaf senescence. - Tree Physiol. 21: 1-8, 2001. Go to original source...
    16. Hogewoning S.W., Wientjes E., Douwstra P. et al.: Photosynthetic quantum yield dynamics: from photosystems to leaves. - Plant Cell 24: 1921-1935, 2012. Go to original source...
    17. Hrazdina G., Wagner G.J., Siegelman H.W.: Subcellular localization of enzymes of anthocyanin biosynthesis in protoplasts. - Phytochemistry 17: 53-56, 1978. Go to original source...
    18. Hughes N.M.: Winter leaf reddening in 'evergreen' species. - New Phytol. 190: 573-581, 2011. Go to original source...
    19. 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. Go to original source...
    20. 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. Go to original source...
    21. 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. Go to original source...
    22. Krause G.H., Weis E.: Chlorophyll fluorescence and photosynthesis: the basics. - Annu. Rev. Plant Phys.42: 313-49, 1991. Go to original source...
    23. 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. Go to original source...
    24. 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. Go to original source...
    25. 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. Go to original source...
    26. Lamb J.J., Røkke G., Hohmann-Marriott M.F.: Chlorophyll fluorescence emission spectroscopy of oxygenic organisms at 77 K. - Photosynthetica 56: 105-124, 2018. Go to original source...
    27. 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. Go to original source...
    28. 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. Go to original source...
    29. Lev-Yadun S., Dafni A., Flaishman M.A. et al.: Plant coloration undermines herbivorous insect camouflage. - BioEssays 26: 1126-1130, 2004. Go to original source...
    30. Lichtenthaler H.K., Aè 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. Go to original source...
    31. 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. Go to original source...
    32. 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. Go to original source...
    33. 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. Go to original source...
    34. 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. Go to original source...
    35. Manetas Y.: Why some leaves are anthocyanic and why most anthocyanic leaves are red? - Flora 201: 163-177, 2006. Go to original source...
    36. 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. Go to original source...
    37. Melis A.: Light regulation of photosynthetic membrane structure, organization and function. - J. Cell. Biochem. 24: 271-285, 1984. Go to original source...
    38. Melis A.: Dynamics of photosynthetic membrane composition and function. - BBA-Bioenergetics 1058: 87-106, 1991. Go to original source...
    39. 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. Go to original source...
    40. 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. Go to original source...
    41. 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. Go to original source...
    42. Neill S., Gould K.S.: Optical properties of leaves in relation to anthocyanin concentration and distribution. - Can. J. Bot. 77: 1777-1782, 2000. Go to original source...
    43. Papageorgiou G.C., Govindjee: Chlorophyll a Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and Respiration. Pp. 818. Springer, Dordrecht 2004. Go to original source...
    44. 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. Go to original source...
    45. 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. Go to original source...
    46. ©iffel P., Hunalová I., Roháèek K.: Light-induced quenching of chlorophyll fluorescence at 77 K in leaves, chloroplasts and Photosystem II particles. - Photosynth. Res. 65: 219-229, 2000. Go to original source...
    47. 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. Go to original source...
    48. 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. Go to original source...
    49. 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. Go to original source...
    50. Walters R.G.: Towards an understanding of photosynthetic acclimation. - J. Exp. Bot. 56: 435-447, 2005. Go to original source...
    51. 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. Go to original source...
    52. 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. Go to original source...
    53. 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. Go to original source...

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