Abstract
Key message
The results of this study indicate the roles of polyamines and phenylpropanoids in the prevention of oxidative damage provoked by UV-B treatment.
Abstract
Plants respond to UV-B exposure by synthesizing a broad range of secondary metabolites, including ROS-scavenging antioxidants and UV-B screening phenylpropanoids. Our recent results indicated that the accumulation of higher levels of polyamines in fully developed somatic embryos of Norway spruce may be causally linked to better tolerance of UV-B irradiation. In the present work, we concentrated primarily on changes in phenolics and their localization in irradiated embryos. Somatic embryos, after 14 days of desiccation, were exposed to 6 W m−2 h−1 of 312 nm UV-B radiation. The accumulation of higher levels of spermidine and spermine (by about 20%) and total phenolics (about 25%) in these embryos indicates their participation in stress response. Histological localization of polyphenolic compounds was performed under a transmission light microscope. UV-B radiation elicited the accumulation of polyphenolics in the junction zone between root cap and hypocotyl and in the epidermal and subepidermal cells of hypocotyl and cotyledons. The deposition of polyphenolics in intact epidermal cells which were located in the neighbourhood of damaged cells may demonstrate that there is potential for transmission of a signal from injured cells to tissues protected against the direct effects of UV-B irradiation. UV-B irradiation evoked striking polyphenolic accumulation in specialized idioblastic cells localized beneath the epidermis of the somatic embryo hypocotyl and cotyledons. The fluorescence due to flavonoids, detected under confocal laser scanning microscope, increased dramatically after UV-B irradiation in the epidermis of the hypocotyl and cotyledons and in the surface of the root cap of spruce somatic embryos.
Similar content being viewed by others
Abbreviations
- MDA:
-
Malondialdehyde
- PAs:
-
Polyamines
- Put:
-
Putrescine
- ROS:
-
Reactive oxygen species
- Spd:
-
Spermidine
- Spm:
-
Spermine
- UV-B:
-
Ultraviolet-B radiation
References
Agati G, Tattini M (2010) Multiple functional roles of flavonoids in photoprotection. New Phytol 186:786–793
Agati G, Azzarello E, Pollastri S, Tattini M (2012) Flavonoids as antioxidants in plants: location and functional significance. Plant Sci 196:67–76
Agati G, Brunetti C, Di Ferdinando M, Ferrini F, Pollastri S, Tattini M (2013) Functional roles of flavonoids in photoprotection: new evidence, lessons from the past. Plant Physiol Biochem 72:35–45
Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio A (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249
Bandurska H, Niedziela J, Chadzinikolau T (2013) Separate and combined responses to water deficit and UV-B radiation. Plant Sci 213:98–105
Besson-Bard A, Courtois C, Gauthier A, Dahan J, Dobrowolska G, Jeandroz S, Pugin A, Wendehenne D (2008) Nitric oxide in plants: production and cross-talk with Ca2+ signaling. Mol Plant 1:218–228
Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179–194
Brown DE, Rashotte AM, Murphy AS, Normanly J, Tague BW, Peer WA, Taiz L, Muday GK (2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol 126:524–535
Burchard P, Bilger W, Weissenböck G (2000) Contribution of hydroxycinnamates and flavonoids to, epidermal shielding of UV-A and UV-B radiation in developing rye primary leaves as assessed by ultraviolet-induced chlorophyll fluorescence measurements. Plant Cell Environ 23:1373–1380
Cvikrová M, Meravý L, Macháčková I, Eder J (1991) Phenylalanine ammonia-lyase, phenolic acids and ethylene in alfalfa (Medicago sativa L.) cell cultures in relation to their embryogenic ability. Plant Cell Rep 10:251–255
Cvikrová M, Malá J, Hrubcová M, Martincová O, Cvrčková H, Lipavská H (2010) Defence responses induced in embryogenic cultures of Norway spruce by two fractions of Gremmeniella abietina mycelia. For Pathol 40:467–484
Cvikrová M, Gemperlová L, Martincová O, Vanková R (2013) Effect of drought and combined drought and heat stress on polyamine metabolism in proline-over-producing tobacco plants. Plant Physiol Biochem 73:7–15
Cvikrová M, Vondráková Z, Eliášová K, Pešek B, Trávníčková A, Vágner M (2016) The impact of UV-B irradiation applied at different phases of somatic embryo development in Norway spruce on polyamine metabolism. Trees 30:113–124
Day TA, Howells BW, Rice WJ (1994) Ultraviolet absorption and epidermal-transmittance spectra in foliage. Physiol Plant 92:207–218
DeLucia EH, Day TA, Vogelman TC (1992) Ultraviolet-b and visible-light penetration into needles of 2 species of sub-alpine conifers during foliar development. Plant Cell Environ 15:921–929
Farooq M, Aziz T, Cheema ZA, Hussain M, Khaliq A (2008) Activation of antioxidant system by KCl improves the chilling tolerance in hybrid maize. J Agron Crop Sci 194:438–448
Franceschi VR, Krokene P, Krekling T, Christiansen E (2000) Phloem parenchyma cells are involved in local and distant defense responses to fungal inoculation or bark-beetle attack in Norway spruce (Pinaceae). Am J Bot 87:314–326
Gardner RO (1975) Vanillin hydrochloric acid as a histochemical test for tannin. Stain Technol 50:315–317
Gemperlová L, Fischerová L, Cvikrová M, Malá J, Vondráková Z, Martincová O, Vágner M (2009) Polyamine profiles and biosynthesis in somatic embryo development and comparison of germinating somatic and zygotic embryos of Norway spruce. Tree Physiol 29:1287–1298
Gill SS, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant Signal Behav 5:26–33
Gutmann M, Feucht W (1991) A new method for selective localization of flavan-3-ols in plant tissues involving glycolmethacrylate embedding and microwave irradiation. Histochemistry 96:83–86
Hasegawa T, Yamada K, Kosemura S, Yamamura S, Hasegawa K (2000) Phototropic stimulation induces the conversion of glucosinolate to phototropism-regulating substances of radish hypocotyls. Phytochemistry 54:275–279
Hectors K, Van Oevelen S, Guisez Y, Prinsen E, Jansen MAK (2012) The phytohormone auxin is a component of the regulatory system that controls UV-mediated accumulation of flavonoids and UV-induced morphogenesis. Physiol Plant 145:594–603
Hideg É, Jansen MAK, Strid Å (2013) UV-B exposure, ROS, and stress: inseparable companions or loosely linked associates? Trends Plant Sci 18:107–115
Hussain SS, Ali M, Ahmad M, Siddique KHM (2011) Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol Adv 29:300–311
Hutzler P, Fischbach R, Heller W, Jungblut TP, Reuber S, Schmitz R, Veit M, Weissenböck G, Schnitzler J-P (1998) Tissue localization of phenolic compounds in plants by confocal laser scanning microscopy. J Exp Bot 49:953–965
Ibañez S, Rosa M, Hilal M, González JA, Prado FE (2008) Leaves of Citrus aurantifolia exhibit a different sensibility to solar UV-B radiation according to development stage in relation to photosynthetic pigments and UV-B absorbing compounds production. J Photochem Photobiol B Biol 90:163–169
Jansen MAK (2002) Ultraviolet-B radiation effects on plants: induction of morphogenic responses. Physiol Plant 116:423–429
Jansen MAK, Gaba V, Greenberg BM (1998) Higher plants and UV-B radiation: balancing damage, repair and acclimation. Trends Plant Sci 3:131–135
Jansen MAK, Van den Noort RE, Adillah Tan MY, Prinsen E, Lagrimini LM, Thorneley RNF (2001) Phenol-oxidizing peroxidases contribute to the protection of plants from ultraviolet radiation stress. Plant Physiol 126:1012–1023
Jenkins GI (2009) Signal transduction in responses to UV-B radiation. Annu Rev Plant Biol 60:407–431
Kotilainen T, Tegelberg R, Julkunen-Tiitto R, Lindfors A, Aphalo PJ (2008) Metabolite specific effects of solar UV-A and UV-B on alder and birch leaf phenolics. Glob Change Biol 14:1294–1304
Krokene P, Solheim H, Krekling T, Christiansen E (2003) Inducible anatomical defense responses in Norway spruce stems and their possible role in induced resistance. Tree Physiol 23:191–197
Kuthanová A, Gemperlová L, Zelenková S, Eder J, Macháčková I, Opatrný Z, Cvikrová M (2004) Cytological changes and alterations in polyamine contents induced by cadmium in tobacco BY-2 cells. Plant Physiol Biochem 42:149–156
Laakso K, Sullivan JH, Huttunen S (2000) The effects of UV-B radiation on epidermal anatomy in loblolly pine (Pinus taeda L.) and Scots pine (Pinus sylvestris L.). Plant Cell Environ 23:461–472
Leshem Y, Seri L, Levine A (2007) Induction of phosphatidylinositol 3-kinase-mediated endocytosis by salt stress leads to intracellular production of reactive oxygen species and salt tolerance. Plant J 51:185–197
Liu JH, Wang W, Wu H, Gong X, Moriguchi T (2015) Polyamines function in stress tolerance: from synthesis to regulation. Front Plant Sci 6:827. doi:10.3389/fpls.2015.00827
Lütz C, Navakoudis E, Seidlitz HK, Kotzabasis K (2005) Simulated solar irradiation with enhanced UV-B adjust plastid- and thylakoid-associated polyamine changes for UV-B protection. Biochimi Biophysic Acta Bioenerg 1710:24–33
Morales LO, Tegelberg R, Brosché M, Keinänen M, Lindfors A, Aphalo PJ (2010) Effects of solar UV-A and UV-B radiation on gene expression and phenolic accumulation in Betula pendula leaves. Tree Physiol 30:923–934
Morales LO, Brosché M, Vainonen J, Jenkins GI, Wargent JJ, Sipari N, Strid Å, Lindfors AV, Tegelberg R, Aphalo PJ (2013) Multiple roles for UV RESISTANCE LOCUS8 in regulating gene expression and metabolite accumulation in Arabidopsis under solar ultraviolet radiation. Plant Physiol 161:744–759
O’Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59:368–373
Peer WA, Brown DE, Tague BW, Muday GK, Taiz L, Murphy AS (2001) Flavonoid accumulation patterns of transparent testa mutants of arabidopsis. Plant Physiol 126:536–548
Peng D, Wang X, Li Z, Zhang Y, Peng Y, Li Y, He X, Zhang X, Ma X, Huang L, Yan Y (2016) NO is involved in spermidine-induced drought tolerance in white clover via activation of antioxidant enzymes and genes. Protoplasma 253:1243–1254
Potters G, Pasternak TP, Guisez Y, Jansen MAK (2009) Different stresses, similar morphogenic responses: integrating a plethora of pathways. Plant Cell Environ 32:158–169
Pottosin I, Velarde-Buendía AM, Bose J, Zepeda-Jazo I, Shabala S, Dobrovinskaya O (2014) Cross-talk between reactive oxygen species and polyamines in regulation of ion transport across the plasma membrane: implications for plant adaptive responses. J Exp Bot 65:1271–1283
Ruzin SE (1999) Plant microtechnique and microscopy. Oxford University Press Inc, New York
Saleem A, Kivela H, Pihlaja K (2003) Antioxidant activity of pine bark constituents. Z Naturforsch (C) 58:351–354
Schmitz-Hoerner R, Weissenböck G (2003) 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. Phytochemistry 64:243–255
Schweikert K, Sutherland JES, Hurd CL, Burritt DJ (2011) UV-B radiation induces changes in polyamine metabolism in the red seaweed Porphyra cinnamomea. Plant Growth Regul 65:389–399
Sfichi-Duke L, Ioannidis NE, Kotzabasis K (2008) Fast and reversible response of thylakoid-associated polyamines during and after UV-B stress: a comparative study of the wild type and a mutant lacking chlorophyll b of unicellular green alga Scenedesmus obliquus. Planta 228:341–353
Shaukat SS, Farooq MA, Siddiqui MF, Zaidi S (2013) Effect of enhanced UV-B radiation on germination, seedling growth and biochemical responses of Vigna mungo (L.) Hepper. Pak J Bot 45:779–785
Shein IV, Andreeva ON, Polyakova GG, Zrazhevskaya GK (2003) Effect of pine callus elicitation by the Fusarium strains of various pathogenicity on the content of phenolic compounds. Rus J Plant Physiol 50:634–639
Slocum RD, Flores HE, Galston AW, Weinstein LH (1989) Improved method for HPLC analysis of polyamines, agmatine and aromatic monoamines in plant tissue. Plant Physiol 89:512–517
Tattini M, Guidi L, Morassi-Bonzi L, Pinelli P, Remorini D, Degl’Innocenti E, Giordano C, Massai R, Agati G (2005) On the role of flavonoids in the integrated mechanisms of response of Ligustrum vulgare and Phillyrea latifolia to high solar radiation. New Phytol 167:457–470
Treutter D (2005) Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biol 7:581–591
Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EIS, Scherer GFE (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47:346–354
Von Aderkas P, Rohr R, Sundberg B, Gutmann M, Dumont-BéBoux N, Lelu MA (2002) Abscisic acid and its influence on development of the embryonal root cap, storage product and secondary metabolite accumulation in hybrid larch somatic embryos. Plant Cell Tissue Organ Cult 69:111–120
von Aderkas P, Teyssier C, Charpentier J-P, Gutmann M, Pâques L, Le Metté C, Ader K, Label P, Kong L, Lelu-Walter M-A (2015) Effect of light conditions on anatomical and biochemical aspects of somatic and zygotic embryos of hybrid larch (Larix × marschlinsii). Ann Bot 115:605–615
Wargent JJ, Nelson BCW, McGhie TK, Barnes PW (2015) Acclimation to UV-B radiation and visible light in Lactuca sativa involves up-regulation of photosynthetic performance and orchestration of metabolome-wide responses. Plant Cell Environ 38:929–940
Woodenberg W, Berjak P, Pammenter NW, Farrant J (2014) Development of cycad ovules and seeds. 2. Histological and ultrastructural aspects of ontogeny of the embryo in Encephalartos natalensis (Zamiaceae). Protoplasma 251:797–816
Yin R, Han K, Heller W, Albert A, Dobrev PI, Zažímalová E, Schäffner AR (2014) Kaempferol 3-O-rhamnoside-7-O-rhamnoside is an endogenous flavonol inhibitor of polar auxin transport in Arabidopsis shoots. New Phytol 201:466–475
Zhao H, Yang H (2008) Exogenous polyamines alleviate the lipid peroxidation induced by cadmium chloride stress in Malus hupehensis Rehd. Scientia Hort 116:442–447
Acknowledgements
We thank Sees-editing Ltd. for linguistic editing. This work was supported by the Ministry of Education, Youth and Sports of the Czech Republic (Projects COST No. LD13050 and COST No. LD13051).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by I. Porth.
Electronic supplementary material
Below is the link to the electronic supplementary material.
468_2017_1547_MOESM1_ESM.pdf
Online resource S1: LC/MS analysis of glycoside-bound methanol-soluble phenolic acids (F4) extracted from untreated somatic embryos and embryos on the 7th day after UV-B irradiation (PDF 276 kb)
468_2017_1547_MOESM2_ESM.pdf
Online resource S2: Detail of polyphenolic deposits in cells of root cap of UV-B irradiated spruce somatic embryo (PDF 562 kb)
468_2017_1547_MOESM3_ESM.pdf
Online resource S3: Detail of polyphenolic deposits in epidermal cells of the hypocotyl of UV-B irradiated spruce somatic embryo (PDF 464 kb)
468_2017_1547_MOESM4_ESM.pdf
Online resource S4: Detail of polyphenolic deposits in epidermal cells of the junction zone between the hypocotyl and root cap of UV-B irradiated spruce somatic embryo (PDF 391 kb)
468_2017_1547_MOESM5_ESM.pdf
Online resource S5: Polyphenolic deposits in epidermal cells of UV-B irradiated spruce somatic embryo (an overview) (PDF 379 kb)
Rights and permissions
About this article
Cite this article
Eliášová, K., Vondráková, Z., Malbeck, J. et al. Histological and biochemical response of Norway spruce somatic embryos to UV-B irradiation. Trees 31, 1279–1293 (2017). https://doi.org/10.1007/s00468-017-1547-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-017-1547-1