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Protein content and antioxidant enzymes activity in reaction wood of poplar and their response to different levels of sustained bending stress

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Abstract

The histogenesis of reaction wood in woody plants is a promising area of exploration for emerging wood technology products and for a generalized understanding of stress physiology. The activity of total protein and antioxidant enzymes were measured during the development of normal and reaction wood (opposite wood and tension wood) in the bole of poplar trees (Populous alba L.) induced by two levels of sustained bending stress to produce moderate and severe reaction wood. Four-year-old poplars were induced to produce reaction wood by sustained bending to 0, 35 and 80° from the vertical position. The activity of antioxidant enzymes was studied with repeated sampling during one growing season. Severe reaction wood showed higher levels of H2O2 and enzymes than moderate reaction wood. Tension wood showed a higher accumulation of total protein than opposite wood at the beginning and end of the bending treatment and opposite wood showed higher enzymatic activity. H2O2 and antioxidant enzymes were also sensitive to mechanical bending stress; compared to normal wood, tension wood and opposite wood which showed higher enzymatic activity coupled with higher amounts of total H2O2. Ascorbate peroxidase was more active than glutathione peroxidase in both tension and opposite wood at some periods of sampling.

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References

  • Adoracion Z, Jesus castro A, Alche, J D, (2018) Identification of novel superoxide dismutase isoenzymes in the olive (Olea europaea L.) pollen. Plant Biol 18:114

    Google Scholar 

  • Alscher RG, Erturk N, Lenwood H (2002) Role of superoxide dismutases in controlling oxidative stress in plants. J Exp Bot 53:1331–1341

    Article  CAS  PubMed  Google Scholar 

  • Anderson D, Prasad K, Stewart R (1995) Changes in isozyme profiles of catalase, peroxidase and glutathione reductase during acclimation to chilling in mesocotyls of mize seedlings. Plant Physiol 109:1247–1257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andersson-Gunneras S, Mellerowicz EJ, Love J, Segerman B, Ohmiya Y, Coutinho PM, Nilsson P, Henrissat B, Moritz T, Sundberg B (2006) Biosynthesis of cellulose-enriched tension wood in Populus: global analysis of transcripts and metabolites identifies biochemical and developmental regulators in secondary wall biosynthesis. Plant J 45(2):144–165

    Article  PubMed  Google Scholar 

  • Anjum A, Aref IM, Duarte AC, Pereira E, Ahmad I, Iqbal M (2014) Glutathione and proline can coordinately make plants withstand the joint attack of metal (loid) and salinity stresses. Front Plant Sci 5:662

    Article  PubMed  PubMed Central  Google Scholar 

  • Anjum A, Ashraf U, Tanveer M, Khan I, Saddam H, Shahzad B, Zohaib A, Abbas F, Saleem M, Iftikhar A, Wang L (2017) Drought induced changes in growth, osmolyte accumulation and antioxidant metabolism of three maize hybrids. Front Plant Sci 8:69

    Article  PubMed  PubMed Central  Google Scholar 

  • Araujo M, Prada J, Mariz-Ponte N, Santos C, Pereira J, Pinto D, Silva A, Dias M (2021) Antioxidant adjustments of olive trees (olea europaea) under field stress conditions. Plants (basel) 10(4):684

    Article  CAS  PubMed  Google Scholar 

  • Azri W, Chambon C, Herbette S, Brunel N, Coutand C, Lepl J, BenRejeb I, Ammar S, Julien J, Roeckel D (2009) Proteome analysis of apical and basal regions of poplar stems under gravitropic stimulation. Physiol Plant 136(2):193–208

    Article  CAS  PubMed  Google Scholar 

  • Bela K, Galle A, Horvath E, Szabados L (2015) Plant glutathione peroxidases: emerging role of the antioxidant enzymes in plant development and stress responses. J Plant Physiol 176C:192–201

    Article  Google Scholar 

  • Bishnupriya B, Anath D, Bhabatosh M (2009) Changes in proteins and antioxidative enzymes in tree mangroves Bruguiera parviflora and Bruguiera gymnorrhiza under high NaCl stress. BioDiCon 2(2):71–77

    Google Scholar 

  • Bradford MM (1976) Arapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Brosche M, Vinocue B, Alatalo ER, Lamminmaki A, Teichmann T, Ottow EA, Djilianov D, Afif D, Bogeat-Tribout MB, Altman A (2005) Gene expression and metabolite profiling of Populus euphratica growing in the Negev desert. Genome Biol 6:R101

    Article  PubMed  PubMed Central  Google Scholar 

  • Bygdell J, Srivastava V, Obudulu O, Srivastava M, Nilsson R, Sundberg B, Trygg J, Mellerowicz E, Wingsle G (2017) Protein expression in tension wood formation monitored at high tissue resolution in Populus. J Exp Bot 68:3405–3417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Chen B, Zhang D (2015) Transcript profiling of Populus tomentosa genes in normal, tension, and opposite wood by RNA-seq. BMC Genomics 16(1):164

    Article  PubMed  PubMed Central  Google Scholar 

  • Christine H, Foyer S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155(1):93–100

    Article  Google Scholar 

  • Clair B, Thibaut B (2014) Physical and Mechanical Properties of Reaction Wood. The Biology of Reaction Wood. Springer Series in Wood Science. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-10814-3_6

  • Dionisio M, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135(1):1–9

    Article  Google Scholar 

  • Du Sh, Yamamoto F (2007) An overview of the biology of reaction wood formation. J Int Plant Biol 49(2):131–143

    Article  CAS  Google Scholar 

  • Ebermann R, Stich K, Kororoi SAA (1995) Wood peroxidase activity dependence on environmental conditions. Conference on peroxidase Biotechnology and Application, Moscow

  • Fernández-Crespo E, Gómez-Pastor R, Scalschi L, Llorens E, Camañes G (2014) NH4 + induces antioxidant cellular machinery and provides resistance to salt stress in citrus plants. Trees 28:1693–1704

    Article  Google Scholar 

  • Groover A (2016) Gravitropisms and reaction woods of forest trees - evolution, functions and mechanisms. New Phytol 3:790–802

    Article  Google Scholar 

  • He X,  Ruan Y, Chen W, Lu T (2006) Responses of the anti-oxidative system in leaves of Ginkgo biloba to elevated ozone concentration in an urban area. Bot Stud 47:409–416

    CAS  Google Scholar 

  • Hincha DK (2008) Effects of alpha-tocopherol (vitamin E) on the stability and lipid dynamics of model membranes mimicking the lipid composition of plant chloroplast membranes. FEBS Lett 582:3687–3692

    Article  CAS  PubMed  Google Scholar 

  • Jia D, Yang J, Cheng-Hao L (2012) Advances in metallotionein studies in forest trees. Plant Omics J 5(1):46–51

    Google Scholar 

  • Jiroutova P, Kovalikova Z, Toman J, Dobrovolna D, Andrys R (2021) Complex analysis of antioxidant activity, abscisic acid level, and accumulation of osmotica in apple and cherry in vitro cultures under osmotic stress. Mole Sci 22:7922

    Article  CAS  Google Scholar 

  • Jourez B, Riboux A, Leclercq A (2001) Anatomical characteristics of tension wood and opposite wood in young inclined stems of poplar (Populus euramericana cv ‘Ghoy’). IAWA J 22:133–157

    Article  Google Scholar 

  • Kehrer JP, Klotz L (2015) Free radicals and related reactive species as mediators of tissue injury and disease: implications for health. Implic Health Crit Rev Toxicol 45(9):765–798

    Article  CAS  Google Scholar 

  • Khelifa S, Hamdi M, Rejeb H, Belbahri L, Souayeh N (2011) Relation between catalase activity, salt stress and urban environments in Citrus aurantium L. J Hortic for 3(6):186–189

    Google Scholar 

  • Lei Y, Yin Ch, Li Ch (2006) Differences in some morphological, physiological, and biochemical responses to drought stress in two contrasting populations of Populus przewalskii. Physiol Plant 127:182–191

    Article  CAS  Google Scholar 

  • Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol 127(4):1781–1787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu S, Sun Y, Shi R, Clark C, Li L, Chiang V (2005) Novel and mechanical stress–responsive microRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell 17:2186–2203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marron N, Maury S, Rinaldi C, Brignolas F (2006) Impact of drought and leaf development stage on enzymatic antioxidant system of two Populus deltoides × nigra clones. Ann Forest Sci Springer Verlag EDP Sci 63(3):323–327

    CAS  Google Scholar 

  • Maruta T, Tanouchi A, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S (2010) Arabidopsis chloroplastic ascorbate peroxidase isoenzymes play a dual role in photoprotection and gene regulation under photooxidative stress. Plant Cell Physiol 51(2):190–200

    Article  CAS  PubMed  Google Scholar 

  • Masoumi A (2013) Study of antioxidant enzymes’ activity in reaction wood of poplar tree (Populus alba L.). M.Sc. Tehran University, Tehran

    Google Scholar 

  • Masoumi A, Bond B (2024) Dimensional stability and equilibrium moisture content of thermally modified hardwoods. BioResources J 19(1):1218–1228. https://doi.org/10.15376/biores.19.1.1218-1228

    Article  CAS  Google Scholar 

  • Masoumi A, Grabosky J (2024) Freezer sampler: a new tools for sampling tree stem tissue in biotechnology studies. Int J Pharm Chem Biol Sci 14(2):01–05. https://doi.org/10.36648/2471-9668-14.2.1

    Article  Google Scholar 

  • Masoumi A, Xavier ZF, Bond B (2023) Adhesive bonding performance of thermally modified yellow poplar. BioResour J 18(4):8151–8162. https://doi.org/10.15376/biores.18.4.8151-8162

    Article  CAS  Google Scholar 

  • Mauriat M, Leplé JC, Claverol S, Bartholomé J, Negroni L, Richet N, Lalanne C, Bonneu M, Coutand C, Plomion C (2015) Quantitative proteomic and phosphoproteomic approaches for deciphering the signaling pathway for tension wood formation in poplar. Proteome Res 14(8):3188–3203

    Article  CAS  Google Scholar 

  • McDowell JM, Dangl JL (2000) Signal transduction in the plant immune response. Trends Biochem Sci 25(2):79–82

    Article  CAS  PubMed  Google Scholar 

  • Mellerowicz E, Gorshkova T (2012) Tensional stress generation in gelatinous fibres: a review and possible mechanism based on cell-wall structure and composition. J Exp Bot 63(2):551–565

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 10:490–498

    Article  Google Scholar 

  • Narendra S, Venkataramani S, Shen G, Wang J, Pasapula V, Lin Y, Kornyeyev D, Holaday AS, Zhang H (2006) The Arabidopsis ascorbate peroxidase 3 is a peroxisomal membrane-bound antioxidant enzyme and is dispensable for Arabidopsis growth and development. J Exp Bot 57:3033–3042

    Article  CAS  PubMed  Google Scholar 

  • Nicol CJ, Zielenski J, Tsui LC (2009) An embryoprotective role for glucose-6-phosphate dehydrogenase in developmental oxidative stress and chemical teratogenesis. FASEB J14:111–127

    Google Scholar 

  • Noctor G, Mhamdi A, Foyer CH (2016) Oxidative stress and antioxidative systems: recipes for successful data collection and interpretation. Plant Cell Environ 39(5):1140–1160

    Article  CAS  PubMed  Google Scholar 

  • Oladi R, Matinibehzad H, Sharifi Z, Masoumi A (2013) Comparing the wood anatomy of the field Elms Ulmus Carpinifolia Borkh native to Gorgan and Komijan. J For Wood Prod (Iran J Nat Resour) 66(1):69–81. https://doi.org/10.22059/JFWP.2013.35342

    Article  Google Scholar 

  • Ozyigit I, Filiz E, Vatansever R, Kurtoglu K, Kok I, Ozturk M, Anjum N (2016) Identification and comparative analysis of H2O2 scavenging enzymes (Ascorbate Peroxidaseand Glutathione Peroxidase) in selected plants employing bioinformatics approaches. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00301

    Article  PubMed  PubMed Central  Google Scholar 

  • Paoletti E, Nicla C, William J, Antonella C, Annamaria R, Francesco T (2008) Protection of ash (Fraxinus excelsior) trees from ozone injury by ethylenediurea (EDU): Roles of biochemical changes and decreased stomatal conductance in enhancement of growth. Environ Pollut 155(3):464–472

    Article  CAS  PubMed  Google Scholar 

  • Paul S, Rakshit A (2022) Evaluating lignification, antioxidative defense, and physiochemical changes in soybean through bio-priming under graded soil fertilization. J Soil Sci Plant Nutr. https://doi.org/10.1007/s42729-022-00809-9

    Article  Google Scholar 

  • Pilate G, Dejardin A, Descauses M, Laurans F (2004) A specific function for arabinogalactan proteins during tension wood formation. Acta Physiol Plant 26:294–295

    Google Scholar 

  • Pitzschke A, Forzani C, Hirt H (2006) Reactive oxygen species signaling in plants. Antioxid Redox Signal 8(9–10):1757–1764

    Article  CAS  PubMed  Google Scholar 

  • Polle A, Rennenberg H (1994) Photooxidative stress in trees. CRC Press Inc, Boca Raton, pp 199–218

    Google Scholar 

  • Rantalainen KI, Uversky VN, Permi P, Kalkkinen N, DunkerA K, Mäkinen K (2008) Potato virus A genome-linked protein VPg is an intrinsically disordered molten globule-like protein with a hydrophobic core. Virology 377(2008):280–288

    Article  CAS  PubMed  Google Scholar 

  • Santos R, Franza T, Laporte M, Sauvage Ch, Touati D, Expert D (2001) Essential role of superoxide dismutase on the pathogenicity of Erwinia chrysanthemi strain 3937. Am Phytopathol Soc 14(6):758–767

    CAS  Google Scholar 

  • Sarvajet G, Narendra T (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plant. Plant Physiol Biochem 48(12):909–930. https://doi.org/10.1016/j.plaphy.2010.08.016

    Article  CAS  Google Scholar 

  • Savchenko T, Tikhonov K (2021) Oxidative stress-induced alteration of plant central metabolism. Life 11:34

    Article  Google Scholar 

  • Schinkel H, Hertzberg M, Wingsle G (2001) A small family of novel CuZn-superoxide dismutases with high isoelectric points in hybrid aspen. Planta 213:272–279

    Article  CAS  PubMed  Google Scholar 

  • Shao H, Chu L, Shao M, Jaleel CA, Mi H (2008) Higher plant antioxidants and redox signaling under environmental stresses. C R Biol 331:433–441

    Article  CAS  PubMed  Google Scholar 

  • Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319

    Article  CAS  PubMed  Google Scholar 

  • Sofo A, Scopa A, Nuzzaci M, Vitti A (2015) Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. Int J Mol Sci 16:13561–13578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Telewski F (2016a) Thigmomorphogenesis: the response of plants to mechanical perturbation. Italus Hortus 23(1):1–16

    Google Scholar 

  • Telewski F (2016b) Flexure wood: mechanical stress induced secondary xylem formation. In: Secondary xylem biology. Academic Press, pp 73–91. https://doi.org/10.1016/B978-0-12-802185-9.00005-X

    Chapter  Google Scholar 

  • Thibaut B, Gril J (2021) Tree growth forces and wood properties. Peer Commun J 1:e46

    Article  Google Scholar 

  • Timell TE (1986) Compression wood in gymnosperms. Springer-Verlag, Berlin

    Book  Google Scholar 

  • Tuteja N (2007) Abscisic acid and abiotic stress signaling. Plant Signal Behav 2(3):135–138

    Article  PubMed  PubMed Central  Google Scholar 

  • Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M, Inzé D, VanCamp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defense in C3 plants. EMBO J 16(16):4806–4816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu N, Li Zh, Wu F, Tang M (2016) Comparative photochemistry activity and antioxidant responses in male and female Populus cathayana cuttings inoculated with arbuscular mycorrhizal fungi under salt. Sci Rep 6:37663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zinkgraf M, TangZhao Sh, Canning C, Gerttula S, Lu M, Filkov V, Groover A (2020) Evolutionary network genomics of wood formation in a phylogenetic survey of angiosperm forest trees. New Phytol 228(6):1811–1823

    Article  CAS  PubMed  Google Scholar 

  • Zolfaghari R, Hosseini SM, Korori SAA (2010) Relationship between peroxidase and catalase with metabolism and environmental factor in Beech (Fagus orientalis Lipsky) in three different elevations. Int J Environ Sci 1:2

    Google Scholar 

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Authors and Affiliations

  1. Department of Sustainable Biomaterials, Virginia Polytechnic Institute and State University, Blacksburg, VA, USA

    Abasali Masoumi

  2. Department of Ecology Evolution and Natural Resources, Rutgers, New Brunswick, NJ, USA

    Jason Grabosky

  3. Department of Plant Biology, W.J. Beal Botanical Garden, Michigan State University, East Lansing, MI, 48824, USA

    Frank W. Telewski

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As secondary author, we have worked extensively with primary author in theory of sampling and method, data interpretation and preparation of the written manuscript. The primary author has sole claim in sampling and laboratory working.

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Correspondence to Abasali Masoumi.

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Masoumi, A., Grabosky, J. & Telewski, F.W. Protein content and antioxidant enzymes activity in reaction wood of poplar and their response to different levels of sustained bending stress. Wood Sci Technol (2024). https://doi.org/10.1007/s00226-024-01553-2

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