The Response of Picea abies Somatic Embryos to UV-B Radiation Depends on the Phase of Maturation

. 2018 ; 9 () : 1736. [epub] 20181127

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

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid30538715

Ultraviolet-B (UV-B) radiation is a key environmental signal which initiates diverse responses that affect the metabolism, development, and viability of plants. In keeping with our previous studies, we concentrated primarily on how UV-B radiation affects Norway spruce [Picea abies (L.) Karst.] somatic embryo maturation and how phenolics and polyamines (PAs) are linked to the defense response invoked by UV-B irradiation. We treated clusters of Norway spruce embryogenic culture (EC) with UV-B during the five stages of embryo maturation (early, cylindrical, precotyledonary, cotyledonary, and mature embryos). For the first time, we take an advantage of the unique environmental scanning electron microscope AQUASEM II to characterize somatic embryos in their native state. The severity of the irradiation effect on embryonal cell viability was shown to be dependent on the intensity of radiation as well as the stage of embryo development, and might be related to the formation of protoderm. The response of early embryos was characterized by an increase in malondialdehyde (MDA), a marked decrease in PA contents and a decline in phenolics. The reduced ability to activate the defense system seems to be responsible not only for the severe cell damage and decrease in viability but also for the inhibition of embryo development. The significant reduction in spermidine (Spd), which has been reported to be crucial for the somatic embryo development of several coniferous species, may be causally linked to the limited development of embryos. The pronounced decrease in cell wall-bound ferulic acid might correspond to failure of somatic embryos to reach more advanced stages of development. Embryos at later stages of development showed stress defense responses that were more efficient against UV-B exposure.

Zobrazit více v PubMed

Agati G., Tattini M. (2010). Multiple functional roles of flavonoids in photoprotection. New Phytol. 186 786–793. 10.1111/j.1469-8137.2010.03269.x PubMed DOI

Binarová P., Cvikrová M., Havlický T., Eder J., Plevková J. (1994). Changes of shikimate pathway in glyphosate tolerant alfalfa cell lines with reduced embryogenic ability. Biol. Plant. 36 65–73. 10.1007/BF02921271 DOI

Booij-James I. S., Dube S. K., Jansen M. A. K., Edelman M., Mattoo A. K. (2000). Ultraviolet-B radiation impacts light-mediated turnover of the photosystem II reaction center heterodimer in Arabidopsis mutants altered in phenolic metabolism. Plant Physiol. 124 1275–1283. 10.1104/pp.124.3.1275 PubMed DOI PMC

Bouchereau A., Aziz A., Larher F., Martin-Tanguy J. (1999). Polyamines and environmental challenges: recent development. Plant Sci. 140 103–125. 10.1016/S0168-9452(98)00218-0 DOI

Cvikrová M., Gemperlová L., Eder J., Zažímalová E. (2008). Excretion of polyamines in alfalfa and tobacco suspension-cultured cells and its possible role in maintenance of intracellular polyamine contents. Plant Cell Rep. 27 1147–1156. 10.1007/s00299-008-0538-5 PubMed DOI

Cvikrová M., Gemperlová L., Martincová O., Vačková 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. 10.1016/j.plaphy.2013.08.005 PubMed DOI

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. 10.1111/j.1439-0329.2009.00622.x DOI

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. 10.1007/BF00232569 PubMed DOI

Cvikrová M., Vondrákova 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. 10.1007/s00468-015-1280-6 DOI

Eliášová K., Vondráková Z., Malbeck J., Trávníčková A., Pešek B., Vágner M., et al. (2017). Histological and biochemical response of Norway spruce somatic embryos to UV-B irradiation. Trees 31 1279–1293. 10.1007/s00468-017-1547-1 DOI

Filonova L. H., von Arnold S., Daniel G., Bozhkov P. V. (2002). Programmed cell death eliminates all but one embryo in a polyembryonic plant seed. Cell Death Differ. 9 1057–1062. 10.1038/sj.cdd.4401068 PubMed DOI

Fry S. C. (1987). Intracellular feruloylation of pectic polysaccharides. Planta 171 205–211. 10.1007/bf00391095 PubMed DOI

Gemperlová L., Fischerová L., Cvikrová M., Malá J., Vondráková Z., Martincová O., et al. (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. 10.1093/treephys/tpp063 PubMed DOI

Gill S. S., Tuteja N. (2010). Polyamines and abiotic stress tolerance in plants. Plant Signal. Behav. 5 26–33. 10.4161/psb.5.1.10291 PubMed DOI PMC

Gupta P. K., Durzan D. J. (1986). Somatic polyembryogenesis from callus of mature sugar pine embryos. Biotechnology 4 643–645.

Hideg É., Jansen M. A. K., Strid Å. (2013). UV-B exposure, ROS, and stress: inseparable companions or loosely linked associates? Trends Plant. Sci. 18 107–115. 10.1016/j.tplants.2012.09.003 PubMed DOI

Hu X. H., Zhang Y., Shi Y., Zhang Z., Zou Z. R., Zhang H., et al. (2012). Effect of exogenous spermidine on polyamine content and metabolism in tomato exposed to salinity–alkalinity mixed stress. Plant Physiol. Biochem. 57 200–209. 10.1016/j.plaphy.2012.05.015 PubMed DOI

Hussain S. S., Ali M., Ahmad M., Siddique K. H. M. (2011). Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol. Adv. 29 300–311. 10.1016/j.biotechadv.2011.01.003 PubMed DOI

Jansen M. A. K., Babu T. S., Heller D., Gaba V., Mattoo A. K., Edelman M. (1996). Ultraviolet-B effects on Spirodela oligorrhiza: induction of different protection mechanisms. Plant Sci. 115 217–223.

Jansen M. A. K., Gaba V., Greenberg B. M. (1998). Higher plants and UV-B radiation: balancing damage, repair and acclimation. Trends Plant Sci. 3 131–135.

Jansen M. A. K., Hectors K., O’Brien N. M., Guisez Y., Potters G. (2008). Plant stress and human health: do human consumers benefit from UV-B acclimated crops? Plant Sci. 175 449–458. 10.1016/j.plantsci.2008.04.010 DOI

Javelle M., Vernoud V., Rogowsky P. M., Ingram G. C. (2011). Epidermis: the formation and functions of a fundamental plant tissue. New Phytol. 189 17–39. 10.1111/j.1469-8137.2010.03514.x PubMed DOI

Kusano T., Berberich T., Tateda C., Takahashi Y. (2008). Polyamines: essential factors for growth and survival. Planta 228 367–381. 10.1007/s00425-008-0772-7 PubMed DOI

Kuthanová A., Gemperlová L., Zelenková S., Eder J., Macháčková I., Opatrný Z., et al. (2004). Cytological changes and alterations in polyamine contents induced by cadmium in tobacco BY-2 cells. Plant Physiol. Biochem. 42 149–156. 10.1016/j.plaphy.2003.11.003 PubMed DOI

Laakso K., Sullivan J. H., 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. 10.1046/j.1365-3040.2000.00566.x DOI

Lozovaya V., Gorshkova T., Yablokova E., Zabotina O., Ageeva M., Rumyantseva N., et al. (1996). Callus cell wall phenolics and plant regeneration ability. J. Plant Physiol. 148 711–717. 10.1016/S0176-1617(96)80373-7 PubMed DOI

Lütz C., Navakoudis E., Seidlitz H. K., Kotzabasis K. (2005). Simulated solar irradiation with enhanced UV-B adjust plastid- and thylakoid-associated polyamine changes for UV-B protection. Biochim. Biophys. Acta Bioenerg 1710 24–33. 10.1016/j.bbabio.2005.09.001 PubMed DOI

Martin K. P., Madassery J. (2005). Direct and indirect somatic embryogenesis on cotyledon explants of Quassia amara L., an antileukaemic drug plant. In Vitro Cell. Dev. Biol. Plant 41 54–57. 10.1079/IVP2004588 DOI

Martínez-Abaigar J., Monforte L., Del-Castillo-Alonso M. Á., Fabón G., Tomás-Las-Heras R., Núñez-Olivera E. (2015). Ultraviolet-absorbing compounds from the cell walls of an aquatic liverwort are more efficiently extracted by alkaline than by enzymatic digestion. J. Bryol. 37 1–14. 10.1179/1743282014Y.0000000112 DOI

Minocha R., Minocha S. C., Long S. (2004). Polyamines and their biosynthetic enzymes during somatic embryo development in red spruce (Picea rubens sarg.). In Vitro Cell. Dev. Biol. Plant 40 572–580. 10.1079/IVP2004569 DOI

Minocha R., Smith D. R., Reeves C., Steele K. D., Minocha S. C. (1999). Polyamine levels during the development of zygotic and somatic embryos of Pinus radiata. Physiol. Plant. 105 155–164. 10.1034/j.1399-3054.1999.105123.x DOI

Moschou P. N., Paschalidis K. A., Delis I. D., Andriopoulou A. H., Lagiotis G. D., Yakoumakis D. I., et al. (2008). Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. Plant Cell 20 1708–1724. 10.1105/tpc.108.059733 PubMed DOI PMC

Moschou P. N., Wu J., Cona A., Tavladoraki P., Angelini R., Roubelakis-Angelakis K. A. (2012). The polyamines and their catabolic products are significant players in the turnover of nitrogenous molecules in plants. J. Exp. Bot. 63 5003–5015. 10.1093/jxb/ers202 PubMed DOI

Neděla V., Hřib J., Vooková B. (2012). Imaging of early conifer embryogenic tissues with the environmental scanning electron microscope. Biol. Plant. 56 595–598. 10.1007/s10535-012-0062-x DOI

Neděla V., Konvalina I., Oral M., Hudec J. (2015a). The simulation of energy distribution of electrons detected by segmental ionization detector in high pressure conditions of ESEM. Microsc. Microanal. 21 264–269. 10.1017/S1431927615013483 PubMed DOI

Neděla V., Tihlaříková E., Hřib J. (2015b). The low-temperature method for study of coniferous tissues in the environmental scanning electron microscope. Microsc. Res. Tech. 78 13–21. 10.1002/jemt.22439 PubMed DOI

Pál M., Szalai G., Janda T. (2015). Speculation: polyamines are important in abiotic stress signaling. Plant Sci. 237 16–23. 10.1016/j.plantsci.2015.05.003 PubMed DOI

Papadakis A. K., Roubelakis-Angelakis K. A. (2005). Polyamines inhibit NADPH oxidase-mediated superoxide generation and putrescine prevents programmed cell death induced by polyamine oxidase-generated hydrogen peroxide. Planta 220 826–837. 10.1007/s00425-004-1400-9 PubMed DOI

Reifenrath K., Müller C. (2007). Species-specific and leaf-age dependent effects of ultraviolet radiation on two Brassicaceae. Phytochemistry 68 875–885. 10.1016/j.phytochem.2006.12.008 PubMed DOI

Reis E., Batista M. T., Canhoto J. M. (2008). Effect and analysis of phenolic compounds during somatic embryogenesis induction in Feijoa sellowiana berg. Protoplasma 232 193–202. 10.1007/s00709-008-0290-2 PubMed DOI

Santanen A., Simola L. K. (1992). Changes in polyamine metabolism during somatic embryogenesis in Picea abies. J. Plant Physiol. 140 475–480. 10.1016/S0176-1617(11)80828-X DOI

Schenkmayerová A., Bučko M., Gemeiner P., Trel’ová D., Lacík I., Chorvát D., et al. (2014). Physical and bioengineering properties of polyvinyl alcohol lens-shaped particles versus spherical polyelectrolyte complex microcapsules as immobilisation matrices for a whole-cell Baeyer–Villiger monooxygenase. Appl. Biochem. Biotechnol. 174 1834–1849. 10.1007/s12010-014-1174-x PubMed DOI

Schweiger J., Lang M., Lichtenthaler H. K. (1996). Differences in fluorescence excitation spectra of leaves between stressed and non-stressed plants. J. Plant Physiol. 148 536–547. 10.1016/S0176-1617(96)80073-3 DOI

Schweikert K., Sutherland J. E. S., Hurd C. L., Burritt D. J. (2011). UV-B radiation induces changes in polyamine metabolism in the red seaweed Porphyra cinnamomea. Plant Growth Regul. 65 389–399. 10.1007/s10725-011-9614-x PubMed DOI

Semerdjieva S. I., Sheffield E., Phoenix G. K., Gwynn-Jones D., Callaghan T. V., Johnson G. N. (2003). Contrasting strategies for UV-B screening in sub-arctic dwarf shrubs. Plant Cell Environ. 26 957–964. 10.1046/j.1365-3040.2003.01029.x PubMed DOI

Sfichi-Duke L., Ioannidis N. E., 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. 10.1007/s00425-008-0741-1 PubMed DOI

Sheahan J. J. (1996). Sinapate esters provide greater UV-B attenuation than flavonoids in Arabidopsis thaliana (Brassicaceae). Am. J. Bot. 83 679–686. 10.2307/2445845 DOI

Shein I. V., Andreeva O. N., Polyakova G. G., Zrazhevskaya G. K. (2003). Effect of pine callus elicitation by the Fusarium strains of various pathogenicity on the content of phenolic compounds. Russ. J. Plant Physiol. 50 634–639. 10.1023/A:1025688023862 DOI

Shein I. V., Polyakova G. G., Zrazhevskaya G. K., Pashenova N. V., Vetrova V. P. (2001). Accumulation of phenolic compounds in conifer callus cultures in response to wood blue-stain fungi. Russ. J. Plant Physiol. 48 216–221. 10.1023/A:1009056201926 DOI

Shi H., Chan Z. (2014). Improvement of plant abiotic stress tolerance through modulation of the polyamine pathway. J. Integr. Plant Biol. 56 114–121. 10.1111/jipb.12128 PubMed DOI

Silveira V., Floh E. I. S., Handro W., Guerra M. P. (2004). Effect of plant growth regulators on the cellular growth and levels of intracellular protein, starch and polyamines in embryogenic suspension cultures of Pinus taeda. Plant Cell Tissue Organ Cult. 76 53–60. 10.1023/A:1025847515435 DOI

Smith J., Burrit D., Bannister P. (2001). Ultraviolet-B radiation leads to a reduction in free polyamines in Phaseolus vulgaris L. Plant Growth Regul. 35 289–294. 10.1023/A:1014459232710 DOI

Stasolla C., Kong L., Yeung E. C., Thorpe T. A. (2002). Maturation of somatic embryos in conifers: morphogenesis, physiology, biochemistry, and molecular biology. In Vitro Cell. Dev. Biol. Plant 38 93–105. 10.1079/IVP2001262 DOI

Svobodová H., Albrechtová J., Kumstýřová L., Lipavská H., Vágner M., Vondráková Z. (1999). Somatic embryogenesis in Norway spruce: anatomical study of embryo development and influence of polyethylene glycol on maturation process. Plant Physiol. Biochem. 37 209–221. 10.1016/S0981-9428(99)80036-9 DOI

Takahashi T., Kakehi J. I. (2010). Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann. Bot. 105 1–6. 10.1093/aob/mcp259 PubMed DOI PMC

Takshak S., Agrawal S. B. (2015). Defence strategies adopted by the medicinal plant Coleus forskohlii against supplemental ultraviolet-B radiation: augmentation of secondary metabolites and antioxidants. Plant Physiol. Biochem. 97 124–138. 10.1016/j.plaphy.2015.09.018 PubMed DOI

Vondráková Z., Cvikrová M., Eliášová K., Martincová O., Vágner M. (2010). Cryotolerance in Norway spruce and its association with growth rates, anatomical features and polyamines of embryogenic cultures. Tree Physiol. 30 1335–1348. 10.1093/treephys/tpq074 PubMed DOI

Vondráková Z., Eliášová K., Vágner M. (2014). The anti-actin drugs latrunculin and cytochalasin affect the maturation of spruce somatic embryos in different ways. Plant Sci. 221 90–99. 10.1016/j.plantsci.2014.02.006 PubMed DOI

Vondráková Z., Eliášová K., Vágner M., Martincová O., Cvikrová M. (2015). Exogenous putrescine affects endogenous polyamine levels and the development of Picea abies somatic embryos. Plant Growth Regul. 75 405–414. 10.1007/s10725-014-0001-2 DOI

Yiu J.-C., Liu C. W., Fang D. Y. T., Lai Y. S. (2009). Waterlogging tolerance of Welsh onion (Allium fistulosum L.) enhanced by exogenous spermidine and spermine. Plant Physiol. Biochem. 47 710–716. 10.1016/j.plaphy.2009.03.007 PubMed DOI

Zhu T., Moschou P. N., Alvarez J. M., Sohlberg J. J., von Arnold S. (2016). WUSCHEL-RELATED HOMEOBOX 2 is important for protoderm and suspensor development in the gymnosperm Norway spruce. BMC Plant Biol. 16:19. 10.1186/s12870-016-0706-7 PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace