Generic placeholder image

Protein & Peptide Letters


ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Research Article

Biochemical Aspects of the Spiral Grain Formation in Scots Pine (Pinus Sylvestris L.) Wood. Some Differences and Similarities with Biochemical Indicators of Abnormal Xylogenesis in Karelian Birch (Betula Pendula Roth Var. Carelica (Mercl.) Hämet-Ahti)

Author(s): Kseniya Mihajlovna Nikerova*, Natalia Alekseevna Galibina, Sergey Mihajlovich Sinkevich, Irina Nikolaevna Sofronova, Marina Nikolaevna Borodina, Yuliya Leonidovna Moshchenskaya, Tatiana Vladimirovna Tarelkina and Anna Vladimirovna Klimova

Volume 30, Issue 9, 2023

Published on: 15 September, 2023

Page: [763 - 776] Pages: 14

DOI: 10.2174/0929866530666230824101841

Price: $65


Background: AOS enzymes can be biochemical indicators of abnormal xylogenesis in Scots pine, and this mechanism has similar features with the metabolic base of abnormal xylogenesis in Karelian birch.

Objective: AOS enzymes’ activity in 150-300-year-old Pinus sylvestris L. wood with straight-- grained wood and right-twisted spiral-grained wood, expressed in varying degrees (5-20 angle), grew in three sample plots in lingonberry and blueberry pine forest stands of different ages (100-300 years) in the middle taiga subzone in the Republic of Karelia.

Methods: Plant tissues were ground in liquid nitrogen in a uniform mass and homogenized at 4°C in the buffer containing 50 mM HEPES (pH 7.5), 1 mM EDTA, 1 mM EGTA, 3 mM DTT, 5 mM MgCl2 and 0.5 mM PMSF. After 20 min extraction, the homogenate was centrifuged at 10000 g for 20 min (MPW-351R, Poland). The sediment was washed in the buffer thrice. The pooled supernatant and sediment were dialyzed at 4°C for 18-20 h against a tenfold diluted homogenization buffer. The enzymes' activity was determined spectrophotometrically (Spectrophotometer SF-2000, OKB Spectr, Russia). Proteins in the extracts were quantified by the method of Bradford.

Results: The study showed that the activity of SS, ApInv, CAT, POD and PPO in xylem and PPO in phloem were biochemical indicators for abnormal wood of P. sylvestris. We noticed an increase in sucrose metabolism in the apoplast and the activity of POD and PPO under spiral-grain wood formation like under figured wood formation earlier. We assume that the alternative pathway of sucrose metabolism (an indicator of abnormal xylogenesis in B. pendula var. carelica plants) that lead to restructuring of AOS enzymes have the same biochemical regularities in the spiral-grain wood formation in P. sylvestris.

Conclusion: The study showed that the differences in the AOS enzyme's activity in P. sylvestris during the formation of straight-grained and spiral-grained wood were revealed for the first time. The increased CAT, POD and PPO activities in xylem with a decrease in SS and an increase in Ap- Inv during spiral-grained wood formation can be biochemical markers of these structural anomalies. Metabolic regularities found in the AOS enzyme complex during spiral-grained wood formation do not contradict those found earlier during figured wood formation in B. pendula var. carelica. The identified patterns can form the base for diagnostics of P. sylvestris wood quality in forest seed plantations and in their natural growth, which is necessary both for fundamental science and in various industry areas while high-quality material harvesting.

Keywords: Antioxidant system (AOS) enzymes, carbohydrate metabolism, xylogenesis, spiral-grained wood, figured wood, forest seed plantations.

Graphical Abstract
Paiva, J.A.P.; Garcés, M.; Alves, A.; Garnier-Géré, P.; Rodrigues, J.C.; Lalanne, C.; Porcon, S.; Le Provost, G.; Da Silva Perez, D.; Brach, J.; Frigerio, J.M.; Claverol, S.; Barré, A.; Fevereiro, P.; Plomion, C. Molecular and phenotypic profiling from the base to the crown in maritime pine wood-forming tissue. New Phytol., 2008, 178(2), 283-301.
[] [PMID: 18298434]
Galibina, N.A.; Moshkina, E.V.; Nikerova, K.M.; Moshchenskaya, Yu.L.; Znamenskii, S.R. Peroxydase activity indicates veining of curly birch. Forestry, 2016, 4, 294-304.
Galibina, N.A.; Novitskaya, L.L.; Nikerova, K.M.; Moshkina, E.V.; Moshchenskaya, Y.L.; Borodina, M.N.; Sofronova, I.N.; Nikolaeva, N.N. Labile nitrogen availability in soil influences the expression of wood pattern in karelian birch. Bot. Z., 2019, 104(10), 1598-1609.
Dharanishanthi, V.; Dasgupta, M.G. Construction of co-expression network based on natural expression variation of xylogenesis-related transcripts in Eucalyptus tereticornis. Mol. Biol. Rep., 2016, 43(10), 1129-1146.
[] [PMID: 27465117]
Nikerova, K.M.; Galibina, N.A. The influence of nitrate on the peroxidase activity in tissues of Betula pendula Roth var. pendula and B. pendula var. carelica (Mercklin). Sib. J. For. Sci., 2017, 1, 15-24.
Nikerova, K.M.; Galibina, N.A.; Moshchenskaya, Y.L.; Tarelkina, T.V.; Borodina, M.N.; Sofronova, I.N.; Semenova, L.I.; Ivanova, D.S.; Novitskaya, L.L. Upregulation of antioxidant enzymes is a biochemical indicator of abnormal xylogenesis in Karelian birch. Trees, 2022, 36(2), 517-529.
Kubler, H. Function of spiral grain in trees. Trees, 1991, 5(3), 125-135.
Robertson, D.; Beech, I.; Bolwell, G.P. Regulation of the enzymes of UDP-sugar metabolism during differentiation of French bean. Phytochemistry, 1995, 39(1), 21-28.
Sudachkova, N.E.; Milyutina, I.L.; Romanova, L.I.; Semenova, G.P. The annual dynamics of reserve compounds and hydrolytic enzyme activity in the tissues of Pinus sylvestris L and Larix sibirica Lebed. Eurasian J. For. Res., 2004, 7(1), 1-10.
Foucart, C.; Paux, E.; Ladouce, N.; San-Clemente, H.; Grima-Pettenati, J.; Sivadon, P. Transcript profiling of a xylem vs phloem cDNA subtractive library identifies new genes expressed during xylogenesis in Eucalyptus. New Phytol., 2006, 170(4), 739-752.
[] [PMID: 16684235]
Nomura, T.; Shiozawa, M.; Ogita, S.; Kato, Y. Occurrence of hydroxycinnamoylputrescines in xylogenic bamboo suspension cells. Plant Biotechnol., 2013, 30(5), 447-453.
Galibina, N.A.; Tarelkina, T.V.; Chirva, O.V.; Moshchenskaya, Y.L.; Nikerova, K.M.; Ivanova, D.S.; Semenova, L.I.; Serkova, A.A.; Novitskaya, L.L. Molecular genetic characteristics of different scenarios of xylogenesis on the example of two forms of silver birch differing in the ratio of structural elements in the xylem. Plants, 2021, 10(8), 1593.
[] [PMID: 34451638]
Novitskaya, L.; Nikolaeva, N.; Galibina, N.; Tarelkina, T.; Semenova, L. The greatest density of parenchyma inclusions in Karelian birch wood occurs at confluences of phloem flows. Silva Fenn., 2016, 50(3), 1461-1478.
Novitskaya, L.L.; Tarelkina, T.V.; Galibina, N.A.; Moshchenskaya, Y.L.; Nikolaeva, N.N.; Nikerova, K.M.; Podgornaya, M.N.; Sofronova, I.N.; Semenova, L.I. The formation of structural abnormalities in karelian birch wood is associated with auxin inactivation and disrupted basipetal auxin transport. J. Plant Growth Regul., 2020, 39(1), 378-394.
Nikerova, K.M.; Galibina, NA.; Chirva, O.V. Reactive oxygen species and components of the antioxidant system are participants in plant metabolism. Relationship with phenolic and carbohydrate metabolism. Trans. Karrc. RAS., 2021, 3, 5-20.
Iakimova, E.T.; Woltering, E.J. Xylogenesis in zinnia (Zinnia elegans) cell cultures: Unravelling the regulatory steps in a complex developmental programmed cell death event. Planta, 2017, 245(4), 681-705.
[] [PMID: 28194564]
Tarelkina, T.V.; Galibina, N.A.; Moshchenskaya, Y.L.; Novitskaya, L.L. In silico analysis of regulatory cis-elements in the promoters of genes encoding apoplastic invertase and sucrose synthase in silver birch. Russ. J. Dev. Biol., 2020, 51(5), 323-335.
Tarelkina, T.V.; Novitskaya, L.L.; Galibina, N.A.; Moshchenskaya, Y.L.; Nikerova, K.M.; Nikolaeva, N.N.; Sofronova, I.N.; Ivanova, D.S.; Semenova, L.I. Expression analysis of key auxin biosynthesis, transport, and metabolism genes of Betula pendula with special emphasis on figured wood formation in karelian birch. Plants, 2020, 9(11), 1406.
[] [PMID: 33105649]
Gaspar, T.; Penel, C.; Castillo, F.J.; Greppin, H. A two-step control of basic and acidic peroxidases and its significance for growth and development. Physiol. Plant., 1985, 64(3), 418-423.
Savidge, R.A. Xylogenesis, genetic and environmental regulation. IAWA J., 1996, 17(3), 269-310.
Gabaldón, C.; López-Serrano, M.; Pomar, F.; Merino, F.; Cuello, J.; Pedreño, M.A.; Barceló, A.R. Characterization of the last step of lignin biosynthesis in Zinnia elegans suspension cell cultures. FEBS Lett., 2006, 580(18), 4311-4316.
[] [PMID: 16842784]
Koutaniemi, S.; Warinowski, T.; Kärkönen, A.; Alatalo, E.; Fossdal, C.G.; Saranpää, P.; Laakso, T.; Fagerstedt, K.V.; Simola, L.K.; Paulin, L.; Rudd, S.; Teeri, T.H. Expression profiling of the lignin biosynthetic pathway in Norway spruce using EST sequencing and real-time RT-PCR. Plant Mol. Biol., 2007, 65(3), 311-328.
[] [PMID: 17764001]
Ros-Barceló, A.; Gómez-Ros, L.V. Reactive oxygen species in plant cell walls. In: Reactive Oxygen Species in Plant Signaling. Signaling and Communication in Plants; Rio, L.; Puppo, A., Eds.; Springer: Berlin, Heidelberg, 2009; pp. 73-93.
Novaes, E.; Kirst, M.; Chiang, V.; Winter-Sederoff, H.; Sederoff, R. Lignin and biomass: A negative correlation for wood formation and lignin content in trees. Plant Physiol., 2010, 154(2), 555-561.
[] [PMID: 20921184]
Baril’skaya, L.A. Structural analysis of figured wood of karelian birch. Botanicheskii zhurn., 1978, 63, 805-811.
Korovin, V.V.; Novitskaya, L.L.; Kurnosov, G.A. Structural abnormalities of the stem in woody plants. Moscow state forest University: Moscow., 2003.
Novitskaya, L.L.; Kushnir, F.V. The role of sucrose in regulation of trunk tissue development in Betula pendula Roth. J. Plant Growth Regul., 2006, 25(1), 18-29.
Mashkina, O.S.; Tabatskaya, T.M.; Isakov, Yu.N. Clonal propogation of Karelian birch. 2000. Available from:
Nikerova, K.M.; Galibina, N.A.; Moshchenskaya, Y.L.; Sofronova, I.N.; Borodina, M.N.; Moshkina, E.V.; Novitskaya, L.L. The effect of soil fertility on antioxidant enzymes activity in a subarctic woody species. Czech Polar Rep., 2021, 11(1), 41-66.
Savidge, R.A.; Farrar, J.L. Cellular adjustments in the vascular cambium leading to spiral grain formation in conifers. Can. J. Bot., 1984, 62(12), 2872-2879.
Stant, M.Y.; Philipson, W.R.; Ward, J.M.; Butterfield, B.G. The vascular cambium: Its development and activity. Kew Bull., 1972, 27(1), 210.
Harris, J.M. Spiral grain and wave phenomena in wood formation; Springer: Berlin, Heidelberg, 1989.
Larson, P.R. The vascular cambium: Development and structure; Springer-Verlag: Berlin Heidelberg, 2012.
Thomas, J.; Dijkstra, S.M.; Harrington, J.J.; Collings, D.A. Induction of compression wood inhibits development of spiral grain in radiata pine. IAWA J., 2022, 44(1), 36-62.
Hartig, R. About twisted pine growth. Forst Naturwiss Z, 1985, 4, 313-326.
Jones, B.E.; Jones, B.D. Cell adjustments accompanying the development of spiral grain in a specimen of Pseudotsuga taxifolia Brit. Commonw. For. Rev., 1963, 151-158.
Preston, R.D. Spiral structure and spiral growth: The development of spiral grain in conifers. Forestry, 1950, 23(1), 48-55.
Hejnowicz, Z. Phenomena of orientation in the cambium. The vascular cambium; Research Studies: Taunton, 1990, pp. 127-137.
Harris, J.M. Spiral grain and xylem polarity in radiata pine: Microscopy of cambial reorientation. New Zealand J. Forest. Sci, 1973, 3, 363-378.
Zagórska-Marek, B.; Little, C.H.A. Control of fusiform initial orientation in the vascular cambium of Abies balsamea stems by indol-3-ylacetic acid. Can. J. Bot., 1986, 64(6), 1120-1128.
Harris, J.M. The causes of spiral grain in the corewood of radiata pine. Proc 14th Congr IUFRO, Munich 1967 Pt IX Sect 22/41., 1967, pp. 363-383.
Kubler, H. Silvicultural control of mechanical stresses in trees. Can. J. For. Res., 1988, 18(10), 1215-1225.
Schulgasser, K.; Witztum, A. The mechanism of spiral grain formation in trees. Wood Sci. Technol., 2007, 41(2), 133-156.
Mayer-Wegelin, H. Die biologische, technologische und forstliche Bedeutung des Drehwuchses der Waldbäume. Forstarchi, 1956, 27(12), 265-271.
Vité, J.P.; Rudinsky, J.A. The water-conducting systems in conifers and their importance to the distribution of trunk injected chemicals. Contrib. Boyce Thompson Inst., 1959, 20(1), 27-38.
Northcott, P.L. The effects of spiral grain on the usefulness of wood. Proc Meet Sect 41 IUFRO., Melbourne, 1965, pp. 1-5.
Kozlowski, T.T.; Hughes, J.F.; Leyton, L. Movement of injected dyes in gymnosperm stems in relation to tracheid alignment. Forestry, 1967, 40(2), 207-219.
Kozlowski, T.T.; Pallardy, S.G. CHAPTER 2 - The woody plant body. In: Physiology of Woody Plants, 3rd ed.; Academic Press, 1997; pp. 9-38.
Pope, D.J.; Marcroft, J.P.; Whale, L.R.J. The effect of global slope of grain on the bending strength of scaffold boards. Holz Roh- Werkst., 2005, 63(5), 321-326.
Fukuda, H. Xylogenesis: Initiation, progression, and cell death. Annu. Rev. Plant Physiol. Plant Mol. Biol., 1996, 47(1), 299-325.
[] [PMID: 15012291]
Galibina, N.A.; Novitskaya, L.L.; Krasavina, M.S.; Moshchenskaya, Y.L. Activity of sucrose synthase in trunk tissues of Karelian birch during cambial growth. Russ. J. Plant Physiol., 2015, 62(3), 381-389.
Galibina, N.A.; Novitskaya, L.L.; Krasavina, M.S.; Moshchenskaya, J.L. Invertase activity in trunk tissues of Karelian birch. Russ. J. Plant Physiol., 2015, 62(6), 753-760.
Galibina, N.A.; Novitskaya, L.L.; Nikerova, K.M. Excess of exogenous nitrates inhibits formation of abnormal wood in the Karelian birch. Russ. J. Dev. Biol., 2016, 47(2), 69-76.
Galibina, N.A.; Novitskaya, L.L.; Nikerova, K.M. Source-sink relations in the organs and tissues of silver birch during different scenarios of xylogenesis. Russ. J. Plant Physiol., 2019, 66(2), 308-315.
Galibina, N.A.; Novitskaya, L.L.; Nikerova, K.M.; Moshchenskaya, Y.L.; Borodina, M.N.; Sofronova, I.N. Apoplastic invertase activity regulation in the cambial zone of Karelian birch. Russ. J. Dev. Biol., 2019, 50(1), 20-29.
Moshchenskaya, Y.L.; Galibina, N.A.; Topchieva, L.V.; Novitskaya, L.L. Expression of genes encoding sucrose synthase isoforms during anomalous xylogenesis in Karelian birch. Russ. J. Plant Physiol., 2017, 64(4), 616-624.
Moshchenskaya, Y.L.; Galibina, N.A.; Novitskaya, L.L.; Nikerova, K.M. The role of sucrose synthase in sink organs of woody plants. Russ. J. Plant Physiol., 2019, 66(1), 10-21.
Moschenskaya, Y.L.; Galibina, N.A.; Tarelkina, T.V.; Nikerova, K.M.; Chirva, O.V.; Novitskaya, L.L. Choice reference genes for the normalization of quantitative PCR data in real time in two forms of silver birch. Russ. J. Plant Physiol., 2021, 68(3), 430-439.
Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 1976, 72(1-2), 248-254.
[] [PMID: 942051]
Nikerova, K.M.; Galibina, N.A.; Moshchenskaya, Yu.L.; Novitskaya, L.L.; Podgornaya, M.N.; Sofronova, I.N. The antioxidant enzymes - indicators of different xylogenesis scenarios: In early ontogeny and in adult plants (example of Betula pendula Roth). Trans. Karrc. RAS., 2018, 11, 78-87.
Nikerova, K.M.; Galibina, N.A.; Moshchenskaya, Yu.L.; Novitskaya, L.L.; Podgornaya, M.N.; Sofronova, I.N. Determination of superoxide dismutase and polyphenol oxidase activity in Betula pendula var. carelica (Betulaceae) wood with different degree of xylogenesis disturbance. Rastit. Resur., 2019, 55(2), 213-230.
Nikerova, K.M.; Galibina, N.A.; Moshchenskaya, Yu.L.; Novitskaya, L.L.; Podgornaya, M.N.; Sofronova, I.N. Contribution of catalase and peroxidase to xylogenesis of Karelian birch. Lesovedenie, 2019, 2, 115-127.
Geles, I.S. Woody biomass And the basis of environmentally friendly chemical-mechanical processing technologies; KarNC RAN: Petrozavodsk, 2001.
Tappi (t222 om-11) Acid-insoluble lignin in wood and pulp; Tappi press: Atlanta, 2011.
Dolgodvorova, S.Ya.; Chernyaeva, G.N. Extractive substances of birch tree. In: Extractive substances of woody trees of central Siberia; Krasnoyarsk, 1977; pp. 26-38.
Kolupaev, Y.E.; Karpets, Y.V. Reactive oxygen species and stress signaling in plants. Ukr. Biochem. J., 2014, 86(4), 18-35.
[] [PMID: 25509181]
Mittler, R.; Zilinskas, B.A. Purification and characterization of pea cytosolic ascorbate peroxidase. Plant Physiol., 1991, 97(3), 962-968.
[] [PMID: 16668537]
Creissen, G.P.; Edwards, E.A.; Mullineaux, PM. Glutathione reductase and ascorbate peroxidase. In: Causes of photooxidative stress and amelioration of defense systems in plants; CRC Press: Boca Raton, Florida, 1994; p. 22.
König, J.; Baier, M.; Horling, F.; Kahmann, U.; Harris, G.; Schürmann, P.; Dietz, K.J. The plant-specific function of 2-Cys peroxiredoxin-mediated detoxification of peroxides in the redox-hierarchy of photosynthetic electron flux. Proc. Natl. Acad. Sci., 2002, 99(8), 5738-5743.
[] [PMID: 11929977]
Bi, Y.M.; Kenton, P.; Mur, L.; Darby, R.; Draper, J. Hydrogen peroxide does not function downstream of salicylic acid in the induction of PR protein expression. Plant J., 1995, 8(2), 235-245.
[] [PMID: 7670505]
Pellinen, R.I.; Korhonen, M.S.; Tauriainen, A.A.; Palva, E.T.; Kangasjärvi, J. Hydrogen peroxide activates cell death and defense gene expression in birch. Plant Physiol., 2002, 130(2), 549-560.
[] [PMID: 12376624]
Thipyapong, P.; Hunt, M.D.; Steffens, J.C. Antisense downregulation of polyphenol oxidase results in enhanced disease susceptibility. Planta, 2004, 220(1), 105-117.
[] [PMID: 15300439]
Mayer, A.M. Polyphenol oxidases in plants and fungi: Going places? A review. Phytochemistry, 2006, 67(21), 2318-2331.
[] [PMID: 16973188]
Webb, K.J.; Cookson, A.; Allison, G.; Sullivan, M.L.; Winters, A.L. Polyphenol oxidase affects normal nodule development in red clover (Trifolium pratense L.). Front. Plant Sci., 2014, 5, 700.
[] [PMID: 25566275]
Vaughn, K.C.; Duke, S.O. Function of polyphenol oxidase in higher plants. Physiol. Plant., 1984, 60(1), 106-112.
Constabel, C.P.; Bergey, D.R.; Ryan, C.A. Polyphenol oxidase as a component of the inducible defense response in tomato against herbivores. Phytochemical Diversity and Redundancy in Ecological Interactions. Springer: Boston, MA, 1996; pp. 231-252.
Li, L.; Steffens, J. Overexpression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance. Planta, 2002, 215(2), 239-247.
[] [PMID: 12029473]
Melo, G.A.; Shimizu, M.M.; Mazzafera, P. Polyphenoloxidase activity in coffee leaves and its role in resistance against the coffee leaf miner and coffee leaf rust. Phytochemistry, 2006, 67(3), 277-285.
[] [PMID: 16376392]
Wuyts, N.; De Waele, D.; Swennen, R. Extraction and partial characterization of polyphenol oxidase from banana (Musa acuminata Grande naine) roots. Plant Physiol. Biochem., 2006, 44(5-6), 308-314.
[] [PMID: 16814556]
Humphreys, J.M.; Chapple, C. Rewriting the lignin roadmap. Curr. Opin. Plant Biol., 2002, 5(3), 224-229.
[] [PMID: 11960740]
Karpinska, B.; Karlsson, M.; Schinkel, H.; Streller, S.; Süss, K.H.; Melzer, M.; Wingsle, G. A novel superoxide dismutase with a high isoelectric point in higher plants. expression, regulation, and protein localization. Plant Physiol., 2001, 126(4), 1668-1677.
[] [PMID: 11500564]

Rights & Permissions Print Export Cite as
© 2023 Bentham Science Publishers | Privacy Policy