Resistance of Primary Photosynthesis to Photoinhibition in Antarctic Lichen Xanthoria elegans: Photoprotective Mechanisms Activated during a Short Period of High Light Stress

. 2023 Jun 09 ; 12 (12) : . [epub] 20230609

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37375884

Grantová podpora
LM2010009 andLM2015078 Czech Ministry of Education, Youth and Sports
CZ.02.1.01/0.0/0.0/16_013/0001708 Czech Ministry of Education, Youth and Sports

The Antarctic lichen, Xanthoria elegans, in its hydrated state has several physiological mechanisms to cope with high light effects on the photosynthetic processes of its photobionts. We aim to investigate the changes in primary photochemical processes of photosystem II in response to a short-term photoinhibitory treatment. Several chlorophyll a fluorescence techniques: (1) slow Kautsky kinetics supplemented with quenching mechanism analysis; (2) light response curves of photosynthetic electron transport (ETR); and (3) response curves of non-photochemical quenching (NPQ) were used in order to evaluate the phenomenon of photoinhibition of photosynthesis and its consequent recovery. Our findings suggest that X. elegans copes well with short-term high light (HL) stress due to effective photoprotective mechanisms that are activated during the photoinhibitory treatment. The investigations of quenching mechanisms revealed that photoinhibitory quenching (qIt) was a major non-photochemical quenching in HL-treated X. elegans; qIt relaxed rapidly and returned to pre-photoinhibition levels after a 120 min recovery. We conclude that the Antarctic lichen species X. elegans exhibits a high degree of photoinhibition resistance and effective non-photochemical quenching mechanisms. This photoprotective mechanism may help it survive even repeated periods of high light during the early austral summer season, when lichens are moist and physiologically active.

Zobrazit více v PubMed

Tyystjärvi E. Photoinhibition of Photosystem II. Int. Rev. Cell Mol. Biol. 2013;300:243–303. doi: 10.1016/B978-0-12-405210-9.00007-2. PubMed DOI

Vítek P., Mishra K.B., Mishra A., Veselá B., Findurová H., Svobodová K., Oravec M., Sahu P.P., Klem K. Non-destructive insights into photosynthetic and photoprotective mechanisms in Arabidopsis thaliana grown under two light regimes. Spectrochim. Scta. Part A Mol. Biomol. Spectrosc. 2022;281:121531. doi: 10.1016/j.saa.2022.121531. PubMed DOI

Mafole T.C., Solhaug K.A., Minibayeva F.V., Beckett R.P. Tolerance to photoinhibition within lichen species is higher in melanised thalli. Photosynthetica. 2019;57:96–102. doi: 10.32615/ps.2019.008. DOI

Beckett R., Minibayeva F., Solhaug K., Roach T. Photoprotection in lichens: Adaptations of photobionts to high light. Lichenologist. 2021;53:21–33. doi: 10.1017/S0024282920000535. DOI

Mattila H., Mishra K.B., Kuusisto I., Mishra A., Novotná K., Šebela D., Tyystjärvi E. Effects of low temperature on photoinhibition and singlet oxygen production in four natural accessions of Arabidopsis. Planta. 2020;252:19. doi: 10.1007/s00425-020-03423-0. PubMed DOI PMC

Mattila H., Sotoudehnia P., Kuuslampi T., Stracke R., Mishra K.B., Tyystjärvi E. Singlet oxygen, flavonols and photoinhibition in green and senescing silver birch leaves. Trees. 2021;35:1267–1282. doi: 10.1007/s00468-021-02114-x. DOI

Puhovkin A., Bezsmertna O., Parnikoza I. Interspecific differences in desiccation tolerance of selected Antarctic lichens: Analysis of photosystem II effectivity and quenching mechanisms. Czech Polar Rep. 2022;12:31–43. doi: 10.5817/CPR2022-1-3. DOI

Hájek J., Puhovkin A., Giordano D., Sekerák J., Jr. What does critical temperature tell us about the resistance of polar lichens to freezing stress? Applicability of linear cooling method to ecophysiological studies. Czech Polar Rep. 2022;12:246–255. doi: 10.5817/CPR2022-2-18. DOI

Murchie E.H., Ruban A.V. Dynamic non-photochemical quenching in plants: From molecular mechanism to productivity. Plant J. 2019;101:885–896. doi: 10.1111/tpj.14601. PubMed DOI

Kalaji M.H., Goltsev V.N., Żuk-Golaszewska K., Zivcak M., Brestic M. Chlorophyll Fluorescence. Understanding Crop Performance—Basics and Applications. CRC Press; Boca Raton, FL, USA: 2017.

Cao S., Zhang X., Xu D., Fan X., Mou S., Wang Y., Ye N., Wang W. A transthylakoid proton gradient and inhibitors induce a non-photochemical fluorescence quenching in unicellular algae Nannochloropsis sp. FEBS Lett. 2013;587:1310–1315. doi: 10.1016/j.febslet.2012.12.031. PubMed DOI

Štepigová J., Vráblíková H., Lang J., Večeřová K., Barták M. Glutathione and zeaxanthin formation during high light stress in foliose lichens. Plant Soil Environ. 2007;53:340–344. doi: 10.17221/2187-PSE. DOI

Vráblíková H., Barták M., Wonisch A. Changes in glutathione and xanthophyll cycle pigments in the high light-stressed lichens Umbilicaria antarctica and Lasallia pustulata. J. Photochem. Photobiol. B-Biol. 2005;79:35–41. doi: 10.1016/j.jphotobiol.2004.11.017. PubMed DOI

Mishra K.B., Mishra A., Kubásek J., Urban O., Heyer A.G. Govindjee Low temperature induced modulation of photosynthetic induction in non-acclimated and cold-acclimated Arabidopsis thaliana: Chlorophyll a fluorescence and gas-exchange measurements. Photosynth. Res. 2019;139:123–143. doi: 10.1007/s11120-018-0588-7. PubMed DOI

Mishra A., Mishra K.B., Surá K., Veselá B., Klem K., Urban O. Non-photochemical quenching in natural accessions of Arabidopsis thaliana during cold acclimation. Environ. Exp. Bot. 2023;211:105372. doi: 10.1016/j.envexpbot.2023.105372. DOI

Ohnishi N., Allakhverdiev S.I., Takahashi S., Higashi S., Watanabe M., Nishiyama Y., Murata N. Two-step mechanism of photodamage to photosystem II: Step 1 occurs at the oxygen-evolving complex and step 2 occurs at the photochemical reaction center. Biochemistry. 2005;44:8494–8499. doi: 10.1021/bi047518q. PubMed DOI

Phinney N.H., Gauslaa Y., Solhaug K.A. Why chartreuse? The pigment vulpinic acid screens blue light in the lichen Letharia vulpina. Planta. 2019;249:709–718. doi: 10.1007/s00425-018-3034-3. PubMed DOI

Bianchi E., Paoli L., Colzi I., Coppi A., Gonnelli C., Lazzaro L., Loppi S., Papini A., Vannini A., Benesperi R. High-light stress in wet and dry thalli of the endangered Mediterranean lichen Seirophora villosa (Ach.) Frödén: Does size matter? Mycol. Progress. 2019;18:463–470. doi: 10.1007/s11557-018-1451-0. DOI

Gauslaa Y., Solhaug K.A. Fungal melanins as a sun screen for symbiotic green algae in the lichen Lobaria pulmonaria. Oecologia. 2001;126:462–471. doi: 10.1007/s004420000541. PubMed DOI

Singh R., Ranjan S., Nayaka S., Pathre U.V., Shirke P.A. Functional characteristics of a fruticose type of lichen, Stereocaulon foliolosum Nyl. in response to light and water stress. Acta Physiol. Plant. 2013;35:1605–1615. doi: 10.1007/s11738-012-1203-8. DOI

Solhaug K. Low-light recovery effects on assessment of photoinhibition with chlorophyll fluorescence in lichens. Lichenologist. 2018;50:139–145. doi: 10.1017/S0024282917000640. DOI

Barták M., Hájek J., Očenášová P. Photoinhibition of photosynthesis in Antarctic lichen Usnea antarctica. I. Light intensity- and light duration-dependent changes in functioning of photosystem II. Czech Polar Rep. 2012;2:42–51. doi: 10.5817/CPR2012-1-5. DOI

Očenášová P., Barták M., Hájek J. Photoinhibition of photosynthesis in Antarctic lichen Usnea antarctica. II. Analysis of non-photochemical quenching mechanisms activated by low to medium light doses. Czech Polar Rep. 2014;4:90–99. doi: 10.5817/CPR2014-1-10. DOI

Balarinová K., Barták M., Hazdrová J., Hájek J., Jílková J. Changes in photosynthesis, pigment composition and glutathione contents in two Antarctic lichens during a light stress and recovery. Photosynthetica. 2014;52:538–547. doi: 10.1007/s11099-014-0060-7. DOI

White A.J., Critchley C. Rapid light curves: A new fluorescence method to assess the state of the photosynthetic apparatus. Photosynth. Res. 1999;59:63–72. doi: 10.1023/A:1006188004189. DOI

Ralph P.J., Gademann R. Rapid light curves: A powerful tool to assess photosynthetic activity. Aquat. Bot. 2005;82:222–237. doi: 10.1016/j.aquabot.2005.02.006. DOI

Campbell S., Miller C., Steven A., Stephens A. Photosynthetic responses of two temperate seagrasses across a water quality gradient using chlorophyll fluorescence. J. Exp. Mar. Biol. Ecol. 2003;291:57–78. doi: 10.1016/S0022-0981(03)00090-X. DOI

Huang M.Y., Wong S.L., Weng J.H. Rapid light-response curve of chlorophyll fluorescence in terrestrial plants: Relationship to CO2 exchange among five woody and four fern species adapted to different light and water regimes. Plants. 2021;10:445. doi: 10.3390/plants10030445. PubMed DOI PMC

Serôdio J., Vieira S., Cruz S., Coelho H. Rapid light-response curves of chlorophyll fluorescence in microalgae: Relationship to steady-state light curves and non-photochemical quenching in benthic diatom-dominated assemblages. Photosynth. Res. 2006;90:29–43. doi: 10.1007/s11120-006-9105-5. PubMed DOI

Houliez E., Lefebvre S., Lizon F., Schmitt F.G. Rapid light curves (RLC) or non-sequential steady-state light curves (N-SSLC): Which fluorescence-based light response curve methodology robustly characterizes phytoplankton photosynthetic activity and acclimation status? Mar. Biol. 2017;164:175. doi: 10.1007/s00227-017-3208-8. DOI

Cho S.M., Lee H., Hong S.G., Lee J. Study of ecophysiological responses of the antarctic fruticose lichen Cladonia borealis using the PAM fluorescence system under natural and laboratory conditions. Plants. 2020;9:85. doi: 10.3390/plants9010085. PubMed DOI PMC

Li X.P., Muller-Moule P., Gilmore A.M., Niyogi K.K. PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc. Natl. Acad. Sci. USA. 2002;99:15222–15227. doi: 10.1073/pnas.232447699. PubMed DOI PMC

Dall’Osto L., Caffarri S., Bassi R. A mechanism of nonphotochemical energy dissipation, independent from PsbS, revealed by a conformational change in the antenna protein CP26. Plant Cell. 2005;17:1217–1232. doi: 10.1105/tpc.104.030601. PubMed DOI PMC

Brooks M.D., Sylak-Glassman E.J., Fleming G.R., Niyogi K.K. A thioredoxin-like/β-propeller protein maintains the efficiency of light harvesting in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2013;110:E2733–E2740. doi: 10.1073/pnas.1305443110. PubMed DOI PMC

Vráblíková H., McEvoy M., Solhaug K.A., Barták M., Gauslaa Y. Annual variation in photo acclimation and photoprotection of the photobiont in the foliose lichen Xanthoria parietina. J. Photochem. Photobiology. B Biol. 2006;83:151–162. doi: 10.1016/j.jphotobiol.2005.12.019. PubMed DOI

Mkhize K., Minibayeva F., Beckett R. Adaptions of photosynthesis in sun and shade in populations of some Afromontane lichens. Lichenologist. 2022;54:319–329. doi: 10.1017/S0024282922000214. DOI

Mkhize K.G.W., Minibayeva F., Beckett R.P. Lichen photobionts can be hardened to photoinhibition by pretreatment with light. Acta Physiol. Plant. 2022;44:122. doi: 10.1007/s11738-022-03458-8. DOI

Heber U., Bilger W., Bligny R., Lange O.L. Phototolerance of lichens, mosses and higher plants in an alpine environment: Analysis of photoreactions. Planta. 2000;211:770–780. doi: 10.1007/s004250000356. PubMed DOI

Heber U., Bukhov N.G., Shuvalov V.A., Kobayashi Y., Lange O.L. Protection of the photosynthetic apparatus against damage by excessive illumination in homoiohydric leaves and poikilohydric mosses and lichens. J. Exp. Bot. 2001;52:1999–2006. doi: 10.1093/jexbot/52.363.1999. PubMed DOI

Barták M., Hájek J., Vráblíková H., Dubová J. High-light stress and photoprotection in Umbilicaria antarctica monitored by chlorophyll fluorescence imaging and changes in zeaxanthin and glutathione. Plant Biol. 2004;6:333–341. doi: 10.1055/s-2004-820877. PubMed DOI

Barták M., Vrábliková H., Hájek J. Sensitivity of photosystem 2 of Antarctic lichens to high irradiance stress: Fluorometric study of fruticose (Usnea antarctica) and foliose (Umbilicaria decussata) species. Photosynthetica. 2003;41:497–504. doi: 10.1023/B:PHOT.0000027513.90599.ad. DOI

Hájek J., Barták M., Gloser J. Effects of thallus temperature and hydration on photosynthetic parameters of Cetraria islandica from contrasting habitats. Photosynthetica. 2001;39:427–435. doi: 10.1023/A:1015194713480. DOI

Barták M., Váczi P., Hájek J., Smykla J. Low-temperature limitation of primary photosynthetic processes in Antarctic lichens Umbilicaria antarctica and Xanthoria elegans. Polar Biol. 2007;31:47–51. doi: 10.1007/s00300-007-0331-x. DOI

Míguez F., Fernández-Marín B., Becerril J.M., García-Plazaola J.I. Diversity of winter photoinhibitory responses: A case study in co-occurring lichens, mosses, herbs and woody plants from subalpine environments. Physiol. Plant. 2017;160:282–296. doi: 10.1111/ppl.12551. PubMed DOI

Ndhlovu N.T., Solhaug K.A., Minibayeva F., Beckett R.P. Melanisation in boreal lichens is accompanied by variable changes in non-photochemical quenching. Plants. 2022;11:2726. doi: 10.3390/plants11202726. PubMed DOI PMC

Serôdio J., Lavaud J. A model for describing the light response of the nonphotochemical quenching of chlorophyll fluorescence. Photosynth Res. 2011;108:61–76. doi: 10.1007/s11120-011-9654-0. PubMed DOI

Xu J., Wu X., Yang Y., Xu S., Kang Y., Fu X., Yue H., Shi J., Wu Z. Changes in growth, photosynthesis and chlorophyll fluorescence in the freshwater dinoflagellate Peridinium umbonatum (Peridiniales, Pyrrophyta) in response to different temperatures. Phycologia. 2016;55:469–477. doi: 10.2216/PH15-148.1. DOI

Láska K., Barták M., Hájek J., Prošek P., Bohuslavová O. Climatic and ecological characteristics of deglaciated area of James Ross Island, Antarctica, with a special respect to vegetation cover. Czech Polar Rep. 2011;1:49–62. doi: 10.5817/CPR2011-1-5. DOI

Marečková M., Barták M. Effects of short-term low temperature stress on chlorophyll fluorescence transients in Antarctic lichen species. Czech Polar Rep. 2016;6:54–65. doi: 10.5817/CPR2016-1-6. DOI

Kitajima M., Butler W.L. Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim. Biophys. Acta (BBA)-Bioenerg. 1975;376:105–115. doi: 10.1016/0005-2728(75)90209-1. PubMed DOI

Genty B., Briantais J.-M., Baker N.E. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta (BBA)-Gen. Subj. 1989;990:87–92. doi: 10.1016/S0304-4165(89)80016-9. DOI

Bilger W., Schreiber U., Bock M. Determination of the quantum efficiency of photosystem II and of non-photochemical quenching of chlorophyll fluorescence in the field. Oecologia. 1995;102:425–432. doi: 10.1007/BF00341354. PubMed DOI

Tietz S., Hall C.C., Cruz J.A., Kramer D.M. NPQ(T): A chlorophyll fluorescence parameter for rapid estimation and imaging of non-photochemical quenching of excitons in photosystem-II-associated antenna complexes. Plant Cell Environ. 2017;40:1243–1255. doi: 10.1111/pce.12924. PubMed DOI

Oxborough K., Baker N.R. Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components—Calculation of qP and Fv′/Fm′; without measuring Fo′. Photosynth. Res. 1997;54:135–142. doi: 10.1023/A:1005936823310. DOI

Eilers P.H.C., Peeters J.C.H. A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecol. Model. 1988;42:199–215. doi: 10.1016/0304-3800(88)90057-9. DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...