Advertisement

Photosynthesis Research

, Volume 140, Issue 1, pp 93–102 | Cite as

Distinct UV-A or UV-B irradiation induces protochlorophyllide photoreduction and bleaching in dark-grown pea (Pisum sativum L.) epicotyls

  • Anna Laura Erdei
  • Annamária Kósa
  • Béla BöddiEmail author
Original Article
  • 144 Downloads

Abstract

The effects of distinct UV-A and UV-B radiations were studied on etiolated pea (Pisum sativum L.) epicotyls. Emission spectra of the native protochlorophyll and protochlorophyllide forms were measured when epicotyls were excited with 360 or 300 nm light. The UV-A (360 nm) excited mainly the non-enzyme-bound monomers of protochlorophyll and protochlorophyllide and the UV-B (300 nm) excited preferentially the flash-photoactive protochlorophyllide complexes. These latter complexes converted into short- and long-wavelength chlorophyllide forms at 10-s illumination with both wavelength irradiations. As the spectral changes were very small, the effects of longer illumination periods were studied. Room temperature fluorescence emission spectra were measured from the same epicotyl spots before and after irradiation with various wavelengths between 280 and 360 nm for 15 min and the “illuminated” minus “dark” difference spectra were calculated. Both the UV-A and the UV-B irradiations caused photoreduction of protochlorophyllide into chlorophyllide. At 10 µmol photons m−2 s−1, the photoreduction rates were similar, however, at 60 µmol photons m−2 s−1, the UV-B irradiation was more effective in inducing chlorophyllide formation than the UV-A. The action spectra of protochlorophyllide plus protochlorophyll loss and chlorophyllide production showed that the radiation around 290 nm was the most effective in provoking protochlorophyllide photoreduction and the UV light above 320 nm caused strong bleaching. These results show that the effect of the UV radiation should be considered when discussing the protochlorophyllide–chlorophyllide photoreduction during germination and as a part of the regeneration of the photosynthetic apparatus proceeding in the daily run of photosynthesis.

Keywords

Action spectrum Bleaching Fluorescence spectroscopy Protochlorophyllide Phototransformation Ultraviolet light 

Abbreviations

Chlide

Chlorophyllide

Chl

Chlorophyll

Chl(ide)

Chlorophyll and chlorophyllide not distinguished

L-POR

Light-dependent NADPH:protochlorophyllide-oxidoreductase enzyme

Pchlide

Protochlorophyllide

Pchl

Protochlorophyll

Pchl(ide)

Protochlorophyll and protochlorophyllide not distinguished

PAR

Photosynthetically active radiation

PFD

Photon flux density

Notes

Acknowledgements

We are grateful to Éva Hideg and Gyula Czégény (University of Pécs, Hungary) for their contribution to the UV photon flux density measurements.

Supplementary material

11120_2018_584_MOESM1_ESM.docx (271 kb)
Supplementary material 1 (DOCX 272 KB)

References

  1. Antosiewicz JM, Shugar D (2016) UV–Vis spectroscopy of tyrosine side-groups in studies of protein structure. Part 2: selected applications. Biophys Rev 8:163–177CrossRefGoogle Scholar
  2. Archipowa N, Kutta R, Heyes D, Scrutton N (2018) Stepwise hydride transfer in a biological system: insights into the reaction mechanism of the light-dependent protochlorophyllide oxidoreductase. Angew Chem 130:2712–2716CrossRefGoogle Scholar
  3. Belyaeva OB, Litvin FF (2014) Mechanisms of phototransformation of protochlorophyllide into chlorophyllide. Biochemistry 79:337–348Google Scholar
  4. Björn LO (2018) Photoenzymes and related topics: an update. Photochem Photobiol 94:459–465CrossRefGoogle Scholar
  5. Böddi B, Ryberg M, Sundqvist C (1992) Identification of four universal protochlorophyllide forms in dark-grown leaves by analyses of the 77K fluorescence emission spectra. J Photochem Photobiol B 12:389–401CrossRefGoogle Scholar
  6. Böddi B, Mc Ewen B, Ryberg M, Sundqvist C (1994) Protochlorophyllide forms in non-greening epicotyls of dark-grown pea (Pisum sativum). Physiol Plant 92:160–170CrossRefGoogle Scholar
  7. Böddi B, Evertsson I, Ryberg M, Sundqvist C (1996) Protochlorophyllide transformations and chlorophyll accumulation in epicotyls of pea (Pisum sativum). Physiol Plant 96:706–713CrossRefGoogle Scholar
  8. Böddi B, Kis-Petik K, Kaposi AD, Fidy J, Sundqvist C (1998) The two spectroscopically different short wavelength protochlorophyllide forms in pea epicotyls are both monomeric. BBA 1365:531–540Google Scholar
  9. Böddi B, Loudèche R, Franck F (2005) Delayed chlorophyll accumulation and pigment photodestruction in the epicotyls of dark-grown pea (Pisum sativum). Physiol Plantarum 125:365–372CrossRefGoogle Scholar
  10. Dodd AN, Salathia N, Hall A, Kevei E, Toth R (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–633CrossRefGoogle Scholar
  11. Eckhardt U, Grimm B, Hörtensteiner S (2004) Recent advances in chlorophyll biosynthesis and breakdown in higher plants. Plant Mol Biol 56:1–14CrossRefGoogle Scholar
  12. El Hamouri B, Brouers M, Sironval C (1981) Pathway from photoinactive p 633–628 protochlorophyllide to the p 696–682 chlorophyllide in cucumber etioplast suspension. Plant Sci Lett 21:375–379CrossRefGoogle Scholar
  13. Erdei N, Barta CS, Hideg E, Böddi B (2005) Light-induced wilting and its molecular mechanism in epicotyls of dark-germinated pea (Pisum sativum L.) seedlings. Plant Cell Physiol 46:185–191CrossRefGoogle Scholar
  14. Erdei AL, Kósa A, Kovács-Smirová L, Böddi B (2016) Wavelength-dependent photooxidation and photoreduction of protochlorophyllide and protochlorophyll in the innermost leaves of cabbage (Brassica oleracea var. capitata L.). Photosynth Res 128:73–83CrossRefGoogle Scholar
  15. Franck F, Inoue Y (1984) Light-driven reversible transformation of chlorophyllide P696, 682 into chlorophyllide P688, 678 in illuminated etiolated bean leaves. Photobioch Photobiop 8:85–96Google Scholar
  16. Franck F, Bereza B, Böddi B (1999) Protochlorophyllide-NADP+ and protochlorophyllide-NADPH complexes and their regeneration after flash illumination in leaves and etioplast membranes of dark-grown wheat. Photosynth Res 59:53–61CrossRefGoogle Scholar
  17. Franck F, Sperling U, Frick G, Pochert B, van Cleve B, Apel K, Armstrong GA (2000) Regulation of etioplast pigment-protein complexes, inner membrane architecture, and protochlorophyllide alpha chemical heterogeneity by light-dependent NADPH:protochlorophyllide oxidoreductases A and B. Plant Physiol 124:1678–1696CrossRefGoogle Scholar
  18. Gabruk M, Mysliwa-Kurdziel B (2015) Light-dependent protochlorophyllide oxidoreductase: phylogeny, regulation, and catalytic properties. Biochemistry 54:5255–5262CrossRefGoogle Scholar
  19. Griffiths WT, Kay AS, Oliver RP (1985) The presence of photoregulation of protochlorophyllide reductase in green tissue. Plant Mol Biol 4:13–22CrossRefGoogle Scholar
  20. Hectors K, Prinsen E, de Coen W, Jansen MAK (2007) Arabidopsis thaliana plants acclimated to low dose rates of ultraviolet B radiation show specific changes in morphology and gene expression in the absence of stress symptoms. New Phytol 175:255–270CrossRefGoogle Scholar
  21. Herndon JM, Hoisington D, Whiteside M (2018) Deadly ultraviolet UV-C and UV-B penetration to Earth’s surface: human and environmental health implications. J Geog Environ Earth Sci Int 14:1–11CrossRefGoogle Scholar
  22. Heyes DJ, Hunter CN (2005) Making light work of enzyme catalysis: protochlorophyllide oxidoreductase. Trends Biochem Sci 30:642–649CrossRefGoogle Scholar
  23. Hideg É, Vitányi B, Kósa A, Solymosi K, Bóka K, Won S, Inoue Y, Ridge R, Böddi B (2010) Reactive oxygen species from type-I photosensitized reactions contribute to the light-induced wilting of dark-grown pea (Pisum sativum) epicotyls. Physiol Plant 138:485–492CrossRefGoogle Scholar
  24. Hideg É, Jansen MAK, Strid Å (2013) UV-B exposure, ROS, and stress: inseparable companions or loosely linked associates? Trends Plant Sci 18:107–115CrossRefGoogle Scholar
  25. Houssier C, Sauer K (1969) Optical properties of the protochlorophyll pigments II. Electronic absorption, fluorescence, and circular dichroism spectra. BBA 172:492–502Google Scholar
  26. Jordan BR, James PE, Strid Å, Anthony RG (1994) The effect of ultraviolet-B radiation on gene expression and pigment composition in etiolated and green pea leaf tissue: UV-B induced changes are gene-specific and dependent upon the development stage. Plant Cell Environ 17:45–54CrossRefGoogle Scholar
  27. Juneau P, Eullaffroy P, Popovic R (1997) Evidence of UV-B effect on the photoconversion of active protochlorophyllides into chlorophyllides in etiolated barley leaves. Photochem Photobiol 65:564–569CrossRefGoogle Scholar
  28. Kerr JB, Fioletov VE (2008) Surface ultraviolet radiation. Atmos-Ocean 46:159–184CrossRefGoogle Scholar
  29. Kim C, Meskauskiene R, Apel K, Laloi C (2008) No single way to understand singlet oxygen signalling in plants. EMBO Rep 9(5):435–439CrossRefGoogle Scholar
  30. Kósa A, Böddi B (2012) Dominance of a 675 nm chlorophyll(ide) form upon selective 632.8 or 654 nm laser illumination after partial protochlorophyllide phototransformation. Photosynth Res 114:111–120CrossRefGoogle Scholar
  31. Kósa A, Márton Z, Böddi B (2005) Fast phototransformation of the 636 nm-emitting protochlorophyllide form in epicotyls of dark-grown pea (Pisum sativum). Physiol Plant 124:132–142CrossRefGoogle Scholar
  32. Kósa A, Márton ZS, Solymosi K, Bóka K, Böddi B (2006) Aggregation of the 636 nm emitting monomeric protochlorophyllide form into flash-photoactive, oligomeric 644 and 655 nm emitting forms in vitro. BBA 1757:811–820Google Scholar
  33. Lebedev NN, Dujardin E (1993) Energy transfer from NADPH to protochlorophyllide in isolated protochlorophyllide holochrome as determined by fluorescence excitation spectropy. Z Naturforsch C 48:402–405CrossRefGoogle Scholar
  34. Lebedev N, Karginova O, McIvor W, Timko MP (2001) Tyr275 and Lys279 stabilize NADPH within the catalytic site of NADPH:protochlorophyllide oxidoreductase and are involved in the formation of the enzyme photoactive state. Biochemistry 40:12562–12574CrossRefGoogle Scholar
  35. Mackerness SA-H, Jordan BR, Thomas B (1999) Reactive oxygen species in the regulation of photosynthetic genes by ultraviolet-B radiation (UV-B: 280–320 nm) in green and etiolated buds of pea (Pisum sativum) L. J Photochem Photobiol B 48:180–188CrossRefGoogle Scholar
  36. Marchand M, Dewez D, Franck F, Popovic R (2004) Protochlorophyllide phototransformation in the bundle sheath cells of Zea mays. J Photochem Photobiol B 75:73–80CrossRefGoogle Scholar
  37. Marwood CA, Greenberg BM (1996) Effect of supplementary UVB radiation on chlorophyll synthesis and accumulation of photosystems during chloroplast development in Spirodela oligorrhiza. Photochem Photobiol 64:664–670CrossRefGoogle Scholar
  38. Menon BR, Hardman SJ, Scrutton NS, Heyes DJ (2016) Multiple active site residues are important for photochemical efficiency in the light-activated enzyme protochlorophyllide oxidoreductase (POR). J Photochem Photobiol B 161:236–243CrossRefGoogle Scholar
  39. Rao MV, Paliyath G, Ormrod DP (1996) Ultraviolet-B- and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. Plant Physiol 110:125–136CrossRefGoogle Scholar
  40. Rassadina V, Domanskii V, Averina NG, Schoch S, Rüdiger W (2004) Correlation between chlorophyllide esterification, Shibata shift and regeneration of protochlorophyllide650 in flash-irradiated etiolated barley leaves. Physiol Plant 121:556–567CrossRefGoogle Scholar
  41. Schoefs B (2005) Protochlorophyllide reduction—what is new in 2005? Photosynthetica 43:329–343CrossRefGoogle Scholar
  42. Schoefs B, Franck F (2008) The photoenzymatic cycle of NADPH:protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) during the first days of photoperiodic growth. Photosynth Res 96:15–26CrossRefGoogle Scholar
  43. Shibata K (1957) Spectroscopic studies on chlorophyll formation in intact leaves. J Biochem 44:147–173CrossRefGoogle Scholar
  44. Skribanek A, Apatini D, Inaoka M, Böddi B (2000) Protochlorophyllide and chlorophyll forms in dark-grown stems and stem-related organs. J Photochem Photobiol B 55:172–177CrossRefGoogle Scholar
  45. Solymosi K, Martinez K, Kristóf Z, Sundqvist C, Böddi B (2004) Plastid differentiation and chlorophyll biosynthesis in different leaf layers of white cabbage (Brassica oleracea cv. capitata). Physiol Plant 121:520–529CrossRefGoogle Scholar
  46. Spano AJ, He Z, Michel H, Hunt DF, Timko MP (1992) Molecular cloning, nuclear gene structure, and developmental expression of NADPH:protochlorophyllide oxidoreductase in pea (Pisum sativum L.). Plant Mol Biol 18:967–972CrossRefGoogle Scholar
  47. Strid Å, Porra RJ (1992) Alterations in pigment content in leaves of Pisum sativum after exposure to supplementary UV-B. Plant Cell Physiol 33:1015–1023Google Scholar
  48. Surabhi GK, Reddy KR, Singh SK (2009) Photosynthesis, fluorescence, shoot biomass and seed weight responses of three cowpea (Vigna unguiculata (L.) Walp.) cultivars with contrasting sensitivity to UV-B radiation. Environ Exp Bot 66:160–171CrossRefGoogle Scholar
  49. Szenzenstein A, Kósa A, Solymosi K, Sárvári É, Böddi B (2010) Preferential regeneration of the NADPH:protochlorophyllide oxidoreductase oligomer complexes in pea epicotyls after bleaching. Physiol Plant 138:102–112CrossRefGoogle Scholar
  50. Vitányi B, Kósa A, Solymosi K, Böddi B (2013) Etioplasts with protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of pea (Pisum sativum) seedlings grown under natural light conditions. Physiol Plant 148:307–315CrossRefGoogle Scholar
  51. Wang Y, Frei M (2011) Stressed food—the impact of abiotic environmental stresses on crop quality. Agric Ecosyst Environ 141:271–286CrossRefGoogle Scholar
  52. Wilks HM, Timko MP (1995) A light-dependent complementation system for analysis of NADPH:protochlorophyllide oxidoreductase: identification and mutagenesis of two conserved residues that are essential for enzyme activity. Proc Natl Acad Sci USA 92:724–728CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Department of Plant Anatomy, Faculty of Science, Institute of BiologyELTE Eötvös Loránd UniversityBudapestHungary
  2. 2.Department of Zoology, Plant Protection Institute, Centre for Agricultural ResearchHungarian Academy of SciencesBudapestHungary

Personalised recommendations