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The impact of UV-B irradiation applied at different phases of somatic embryo development in Norway spruce on polyamine metabolism

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Abstract

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Higher polyamine levels of fully developed embryos had positive effects on their ability to tolerate UV-B irradiation when compared with induced responses of early embryos.

Abstract

The aim of this work was to test the hypothesis that the higher levels of polyamines (PAs) might be involved in the response of Norway spruce somatic embryos to UV-B irradiation. We compare here the effects of 0.1, 0.6 and 6 W m−2 h−1 UV-B irradiation on polyamine metabolism in early and fully developed Norway spruce somatic embryos. The impact of UV-B treatment on irradiated embryogenic suspensor mass (ESM, consisting of early somatic embryos) and matured somatic embryos was assessed by measuring changes in the content of PAs and the activities of enzymes involved in their biosynthesis. Under control conditions, developmental stages of embryos are characterized not only by clear differences in their histological structure, but also by the levels of free PAs, which are several fold higher in fully developed embryos than those of early embryos. The decrease in the PA content and the decline in PA biosynthetic enzyme activities in irradiated ESMs were dependent on the doses of UV-B irradiation applied and the length of time after the exposure. The viability of ESM and its histological structure changed depending on the dose applied. The effect was much more pronounced in ESM treated with higher UV-B doses (0.6 W m−2 h−1), where the embryos were seriously damaged or killed, and irradiation with 6 W m−2 h−1 was lethal to the culture. No marked differences in PA contents were observed between control and UV-B irradiated fully developed embryos. The effect of UV-B irradiation on fully developed embryos was marginal when compared with that on proliferating tissue. The increase in malondialdehyde (MDA) levels in irradiated ESM was correlated with the decrease in their PA contents. Neither significant increases in MDA levels nor significant changes in PA content were observed in the fully developed embryos after irradiation; this may indicate that the plants’ defence mechanisms are particularly active in these tissues. The accumulation of higher levels of PAs in fully developed somatic embryos may be causally linked to their better tolerance to UV-B irradiation.

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Abbreviations

ADC:

Arginine decarboxylase

ESM:

Embryogenic suspensor mass

MDA:

Malondialdehyde

ODC:

Ornithine decarboxylase

PAs:

Polyamines

Put:

Putrescine

ROS:

Reactive oxygen species

Spd:

Spermidine

Spm:

Spermine

References

  • Alcazar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249

    Article  PubMed  CAS  Google Scholar 

  • An LZ, Liu GX, Zhang MX, Chen T, Liu YH, Feng HY, Xu SJ, Qiang WY, Wang XL (2004) Effect of enhanced UV-B radiation on polyamine content and membrane permeability in Cucumber Leaves. Russ J Plant Physiol 51:658–662

    Article  CAS  Google Scholar 

  • Bagni N, Tassoni A (2001) Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids 20:301–317

    Article  PubMed  CAS  Google Scholar 

  • Bandurska H, Niedziela J, Chadzinikolau T (2013) Separate and combined responses to water deficit and UV-B radiation. Plant Sci 213:98–105

    Article  PubMed  CAS  Google Scholar 

  • Bouchereau A, Aziz A, Lahrer F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125

    Article  CAS  Google Scholar 

  • Brosche M, Strid A (2003) Molecular events following perception of ultraviolet-B radiation by plants. Physiol Plant 117:1–10

    Article  CAS  Google Scholar 

  • Cvikrova M, Gemperlova L, Martincova O, Vankova 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

    Article  PubMed  CAS  Google Scholar 

  • De Ascensao ARFDC, Dubery IA (2003) Soluble and wall-bound phenolics and phenolic polymers in Musa acuminata roots exposed to elicitors from Fusarium oxysporum f. sp cubens. Phytochemistry 63:679–686

    Article  PubMed  CAS  Google Scholar 

  • Esteban E, Moreno E, Penalosa J, Cabrero JI, Millan R, Zornoza P (2008) Short and long-term uptake of Hg in white lupin plants: kinetics and stress indicators. Environ Exp Bot 62:316–322

    Article  CAS  Google Scholar 

  • Fagerberg WR, Bornman JF (2005) Modification of leaf cytology and anatomy in Brassica napus grown under above ambient levels of supplemental UV-B radiation. Photochem Photobiol Sci 4:275–279

    Article  PubMed  CAS  Google Scholar 

  • Farooq M, Aziz T, Cheema ZA, Hussain M, Khaliq A (2008) Activation of antioxidant system by KCl improves the shilling tolerance in hybrid maize. J Agr Crop Sci 194:438–448

    Google Scholar 

  • Frohnmeyer H, Staiger D (2003) Ultraviolet-B radiation-mediated responses in plants. Balancing damage and protection. Plant Physiol 133:1420–1428

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gemperlova L, Fischerova L, Cvikrova M, Mala J, Vondrakova Z, Martincova O, Vagner 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

    Article  PubMed  CAS  Google Scholar 

  • Gupta PK, Durzan DJ (1986) Somatic polyembryogenesis from casus of mature sugar pine embryos. Bio-technol 4:643–645

    Article  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 53:463–499

    Article  Google Scholar 

  • Hectors K, Prinsen E, Coen WD, Jansen MAK, Guisez Y (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 175:255–270  

    Article  PubMed  CAS  Google Scholar 

  • Hideg E, Jansen MAK, Strid A (2013) UV-B exposure, ROS, and stress: inseparable companions or loosely linked associates? Trends Plant Sci 18:107–115

    Article  PubMed  CAS  Google Scholar 

  • Hussain SS, Ali M, Ahmad M, Siddiquw KHM (2011) Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol Adv 29:300–311

    Article  PubMed  CAS  Google Scholar 

  • Jansen MAK (2002) Ultraviolet-B radiation effects on plants: induction of morph genic responses. Physiol Plant 116:423–429

    Article  CAS  Google Scholar 

  • Jansen MAK, Batu TS, Heller D, Gaba V, Mattoo AK, Edelman M (1996) Ultraviolet-B effects on Spirodela oligorrhiza: induction of different protection mechanisms. Plant Sci 115:217–223

    Article  CAS  Google Scholar 

  • Jantaro S, Baebprasert W, Piyamawadee Ch, Sodsuay O, Incharoensakdi A (2014) Exogenous spermidine alleviates UV-induced growth inhibition of Synechocystis sp. PCC 6803 via reduction of hydrogen peroxide and malonaldehyde levels. Appl Biochem Biotechnol 173:1145–1156

    Article  PubMed  CAS  Google Scholar 

  • Jenkins GI (2009) Signal transduction in responses to UV-B radiation. An Rev Plant Biol 60:407–431

    Article  CAS  Google Scholar 

  • Kramer GF, Krizek DT, Mirecki RM (1992) Influence of photosynthetically active radiation and spectral quality on UV-B-induced polyamine accumulation in soybean. Phytochemistry 31:1119–1125

    Article  CAS  Google Scholar 

  • Krishnamurthy R, Bhagwat KA (1998) Polyamines as modulators of salt tolerance in rice cultivars. Plant Physiol 91:500–504

    Article  Google Scholar 

  • Kuthanova A, Gemperlova L, Zelenkova S, Eder J, Machackova I, Opatrny Z, Cvikrova M (2004) Cytological changes and alterations in polyamine contents induced by cadmium in tobacco BY-2 cells. Plant Physiol Biochem 42:149–156

    Article  PubMed  CAS  Google Scholar 

  • Lutz 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. Biochim Biophys Acta 1710:24–33

    Article  PubMed  CAS  Google Scholar 

  • Noble RE (2002) Effects of UV-irradiance on seed germination. Sci Tot Environ 299:173–176

    Article  CAS  Google Scholar 

  • Papadakis AK, Roubelakis-Angelakis KA (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

    Article  PubMed  CAS  Google Scholar 

  • Rakitin VY, Prudnikova ON, Karyagin VV, Rakitina TY, Vlasov PV, Borisova TA, Novikova GV, Moshkov IE (2008) Ethylene evolution and ABA and polyamine contents in Arabidopsis thaliana during UV-B Stress. Russ J Plant Physiol 55:321–327

    Article  CAS  Google Scholar 

  • Rakitin VY, Prudnikova ON, Rakitina TY, Karyagin VV, Vlasov PV, Novikova GV, Moshkov IE (2009) Interaction between ethylene and ABA in the regulation of polyamine level in Arabidopsis thaliana during UV-B stress. Russ J Plant Physiol 56:147–153

    Article  CAS  Google Scholar 

  • Reifenrath K, Muller C (2007) Species-specific and leaf-age dependent effects of ultraviolet radiation on two Brassicaceae. Phytochemistry 68:875–885

    Article  PubMed  CAS  Google Scholar 

  • Ruhland CT, Xiong FS, Clark WD, Day TA (2005) The influence of ultraviolet-B radiation on hydroxycinnamic acids, flavonoids and growth of Deschampsia antarctica during the springtime ozone depletion season in Antarctica. Photochem Photobiol 81:1086–1093

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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 89:316–322

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Svobodova H, Albrechtova J, Kumštýřova L, Lipavska H, Vagner M, Vondrákova 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

    Article  CAS  Google Scholar 

  • Tassoni A, Van Buuren M, Franceschetti M, Fornale S, Bagni N (2000) Polyamine content and metabolism in Arabidopsis thaliana and effect of spermidine on plant development. Plant Physiol Biochem 38:383–393

    Article  CAS  Google Scholar 

  • Tegelberg R, Turtola S, Rousi M, Meier B, Julkunen-Tiitto R (2006) Soluble polyamines in Salix myrsinifolia and S. myrsinites × S. myrsinifolia plantlets exposed to increased UV-B irradiation and decreased watering. Trees 20:299–303

    Article  CAS  Google Scholar 

  • Vondrakova Z, Cvikrova M, Eliasova K, Martincova O, Vagner M (2010) Cryotolerance in Norway spruce and its association with growth rates, anatomical features and polyamines of embryogenic cultures. Tree Physiol 30:1335–1348

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wen XP, Pang XM, Matsuda N, Kita M, Inoue H, Hao YJ, Honda C, Moriguchi T (2008) Over-expression of the apple spermidine synthase gene in pear confers multiple abiotic stress tolerance by altering polyamine titers. Transgenic Res 17:251–263

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

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. LD13051 and COST No. LD13050).

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Correspondence to M. Cvikrova.

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Communicated by J. Lin.

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Cvikrova, M., Vondrakova, Z., Eliasova, K. et al. The impact of UV-B irradiation applied at different phases of somatic embryo development in Norway spruce on polyamine metabolism. Trees 30, 113–124 (2016). https://doi.org/10.1007/s00468-015-1280-6

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