UV-A screening in Cladophora sp. lowers internal UV-A availability and photoreactivation as compared to non-UV screening in Ulva intestinalis

In the Baltic Sea, two co-occurring green macroalgae Cladophora sp. and Ulva intestinalis grow in the upper eulittoral. Due to regular and high sunlight exposure in their habitat, both species need resistance mechanisms to protect themselves against ultraviolet-B (UV-B)-induced DNA damage. While Cladophora sp. possesses efficient screening of UV-B and ultraviolet-A (UV-A) radiation, U. intestinalis was recently shown to have higher DNA repair by UVA-driven photoreactivation than Cladophora sp. [F. Pescheck and W. Bilger, Mar. Biol., 2018, 165, 132]. In the present study, the hypothesis that the screening of UV-A radiation limits internal UV-A availability for photoreactivation in Cladophora sp. was tested. Both species had identical and much lower fractions of damaged DNA when sampled in situ under direct sunlight as expected based on a photophysical prediction. To quantify the effect of UV-A screening spectrally and physiologically, in vivo UV screening spectra were determined and the UV-A photon flux dependency of photoreactivation was investigated for both species. Identical intrinsic photoreactivation rates were revealed by the applied correction for internal UV-A photon flux density and under irradiation with visible radiation which is not screened by the UV absorbing compounds in Cladophora sp. Natural sunlight was weighted with in vivo action spectra for DNA damage induction and light-dependent repair. The resulting spectrum was further corrected for the apparent UV screening spectra of both species to calculate the species-specific internal ratios of DNA damaging and photoreactivating photons. This photophysical modelling improves the understanding of UV damage and tolerance mechanisms in the two co-occurring green macroalgae under solar irradiation.

[1]  W. Bilger,et al.  High impact of seasonal temperature changes on acclimation of photoprotection and radiation-induced damage in field grown Arabidopsis thaliana. , 2019, Plant physiology and biochemistry : PPB.

[2]  G. Jenkins,et al.  Difference in the action spectra for UVR8 monomerisation and HY5 transcript accumulation in Arabidopsis , 2018, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[3]  W. Bilger,et al.  Compensation of lack of UV screening by cellular tolerance in green macroalgae (Ulvophyceae) from the upper eulittoral , 2018, Marine Biology.

[4]  W. Bilger,et al.  Quantification of light screening by anthocyanins in leaves of Berberis thunbergii , 2017, Planta.

[5]  S. Neugart,et al.  UV-A radiation effects on higher plants: Exploring the known unknown. , 2017, Plant science : an international journal of experimental plant biology.

[6]  W. Bilger,et al.  Relative sensitivity of DNA and photosystem II in Ulva intestinalis (Chlorophyta) under natural solar irradiation , 2016 .

[7]  G. Agati,et al.  UV radiation promotes flavonoid biosynthesis, while negatively affecting the biosynthesis and the de-epoxidation of xanthophylls: Consequence for photoprotection? , 2016 .

[8]  S. Takagi,et al.  Plant Nuclei Move to Escape Ultraviolet-Induced DNA Damage and Cell Death1[OPEN] , 2015, Plant Physiology.

[9]  L. Essen,et al.  Structural and Evolutionary Aspects of Antenna Chromophore Usage by Class II Photolyases* , 2014, The Journal of Biological Chemistry.

[10]  W. Bilger,et al.  UVB-induced DNA and photosystem II damage in two intertidal green macroalgae: distinct survival strategies in UV-screening and non-screening Chlorophyta. , 2014, Journal of photochemistry and photobiology. B, Biology.

[11]  J. Cadet,et al.  Photoinduced Damage to Cellular DNA: Direct and Photosensitized Reactions † , 2012, Photochemistry and photobiology.

[12]  Giovanni Agati,et al.  Light-induced accumulation of ortho-dihydroxylated flavonoids as non-destructively monitored by chlorophyll fluorescence excitation techniques , 2011 .

[13]  F. Leliaert,et al.  Evolution and cytological diversification of the green seaweeds (Ulvophyceae). , 2010, Molecular biology and evolution.

[14]  W. Bilger,et al.  SCREENING OF ULTRAVIOLET‐A AND ULTRAVIOLET‐B RADIATION IN MARINE GREEN MACROALGAE (CHLOROPHYTA) 1 , 2010 .

[15]  G. Agati,et al.  Mesophyll distribution of 'antioxidant' flavonoid glycosides in Ligustrum vulgare leaves under contrasting sunlight irradiance. , 2009, Annals of botany.

[16]  Sung-Ho Kang,et al.  Photosynthesis and photoinhibition of two green macroalgae with contrasting habitats , 2007, Journal of Plant Biology.

[17]  M. Teranishi,et al.  Increase in CPD photolyase activity functions effectively to prevent growth inhibition caused by UVB radiation. , 2007, The Plant journal : for cell and molecular biology.

[18]  D. Hanelt,et al.  Ultraviolet radiation shapes seaweed communities , 2006 .

[19]  A. Britt Repair of DNA Damage Induced by Solar UV , 2004, Photosynthesis Research.

[20]  M. Maekawa,et al.  Higher amounts of anthocyanins and UV-absorbing compounds effectively lowered CPD photorepair in purple rice (Oryza sativa L.) , 2003 .

[21]  G. Weissenböck,et al.  Contribution of phenolic compounds to the UV-B screening capacity of developing barley primary leaves in relation to DNA damage and repair under elevated UV-B levels. , 2003, Phytochemistry.

[22]  J. Cadet,et al.  Bipyrimidine photoproducts rather than oxidative lesions are the main type of DNA damage involved in the genotoxic effect of solar UVA radiation. , 2003, Biochemistry.

[23]  A. Britt,et al.  Growth responses of Arabidopsis DNA repair mutants to solar irradiation , 2003 .

[24]  Aziz Sancar,et al.  Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. , 2003, Chemical reviews.

[25]  F. Figueroa,et al.  Tissular localization of coumarins in the green alga Dasycladus vermicularis (Scopoli) Krasser: a photoprotective role? , 2003, Journal of experimental botany.

[26]  J. L. Pérez-Lloréns,et al.  Effects of solar UV-B radiation on canopy structure of Ulva communities from southern Spain. , 2002, Journal of experimental botany.

[27]  D. Hanelt,et al.  Ultraviolet-B–Induced Cyclobutane-pyrimidine Dimer Formation and Repair in Arctic Marine Macrophytes¶ , 2002 .

[28]  W. Waterworth,et al.  Characterization of Arabidopsis photolyase enzymes and analysis of their role in protection from ultraviolet-B radiation. , 2002, Journal of experimental botany.

[29]  J. Cadet,et al.  Repair of the main UV-induced thymine dimeric lesions within Arabidopsis thaliana DNA: evidence for the major involvement of photoreactivation pathways. , 2001, Journal of photochemistry and photobiology. B, Biology.

[30]  A. Eggert,et al.  EFFECTS OF UV‐B‐INDUCED DNA DAMAGE AND PHOTOINHIBITION ON GROWTH OF TEMPERATE MARINE RED MACROPHYTES: HABITAT‐RELATED DIFFERENCES IN UV‐B TOLERANCE  , 2001 .

[31]  A. Britt,et al.  Growth of Arabidopsis flavonoid mutants under solar radiation and UV filters , 1999 .

[32]  Ismael Moya,et al.  Ultraviolet-induced fluorescence for plant monitoring: present state and prospects , 1999 .

[33]  J. Hidema,et al.  Effects of Light Environment During Culture on UV‐lnduced Cyclobutyl Pyrimidine Dimers and Their Photorepair in Rice (Oryza sativa L.) , 1998 .

[34]  O. Nikaido,et al.  The Photorepair and Photoisomerization of DNA Lesions in Etiolated Cucumber Cotyledons after Irradiation by UV-B Depends on Wavelength , 1998 .

[35]  Ulrich Schreiber,et al.  Measurement of leaf epidermal transmittance of UV radiation by chlorophyll fluorescence , 1997 .

[36]  O. Nikaido,et al.  Induction and Repair of Damage to DNA in Cucumber Cotyledons Irradiated with UV-B , 1996 .

[37]  W. Bilger,et al.  Diurnal changes in flavonoids , 1996 .

[38]  C. F. Musil Differential effects of elevated ultraviolet‐B radiation on the photochemical and reproductive performances of dicotyledonous and monocotyledonous arid‐environment ephemerals , 1995 .

[39]  R. F. Hartman,et al.  Photoenzymic repair of UV-damaged DNA: a chemist's perspective , 1995 .

[40]  A. Sancar,et al.  Characterization of a medium wavelength type DNA photolyase: purification and properties of photolyase from Bacillus firmus. , 1994, Biochemistry.

[41]  R. Castenholz,et al.  Occurrence of UV-Absorbing, Mycosporine-Like Compounds among Cyanobacterial Isolates and an Estimate of Their Screening Capacity , 1993, Applied and environmental microbiology.

[42]  J. C. Sutherland,et al.  Action spectrum for DMA damage in alfalfa lowers predicted impact of ozone depletion , 1992, Nature.

[43]  A. Sancar,et al.  Effect of base, pentose, and phosphodiester backbone structures on binding and repair of pyrimidine dimers by Escherichia coli DNA photolyase. , 1991, Biochemistry.

[44]  D. Karentz,et al.  CELL SURVIVAL CHARACTERISTICS AND MOLECULAR RESPONSES OF ANTARCTIC PHYTOPLANKTON TO ULTRAVIOLET‐B RADIATION 1 , 1991 .

[45]  J. Hays,et al.  UV-B-Inducible and Temperature-Sensitive Photoreactivation of Cyclobutane Pyrimidine Dimers in Arabidopsis thaliana. , 1991, Plant physiology.

[46]  C. Walsh,et al.  Reconstitution of Escherichia coli photolyase with flavins and flavin analogues. , 1990, Biochemistry.

[47]  S. Britz,et al.  Circadian rhythms of chloroplast orientation and photosynthetic capacity in ulva. , 1976, Plant physiology.

[48]  L. Provasoli Cultures and collections of algae , 1968 .