Abstract
Figured wood of Karelian birch (Betula pendula Roth var. carelica (Merckl.) Hämet-Ahti) is highly appraised for its ornamental properties. The reasons for its formation remain largely unclear; judging by available data, we are dealing here with auxin inactivation through its interaction with sugars. The aim of this study has been to reveal the correlations between abnormal wood formation in Karelian birch and auxin conjugation producing IAA-glucose. Karelian birch trees with figured and non-figured wood in the trunk were used. Figured plants had a much higher expression of the gene encoding for the enzyme IAA-glucose synthase, which catalyzes IAA-glucose synthesis. The data obtained suggest that auxin conjugation in Karelian birch via a chain of biochemical reactions may be associated with hexoses produced in the apoplast through sucrose cleavage by cell wall invertase. The activity of the enzyme in figured Karelian birch trees is several times higher than in non-figured plants. Vessel differentiation requires free auxin. We assume that a reduced number of vessels in figured wood may be caused by auxin conjugation in the zone of xylem cell growth and differentiation. Figured wood of Karelian birch was found to have an increased transcript level of the PIN3 gene, which encodes for the auxin efflux carrier protein PIN3 responsible for lateral transport of the hormone. In this regard, PIN3 may generate auxin fluxes with a complex configuration. Microscopic analysis provides evidence that PIN3 overexpression in trunk tissues of Karelian birch is associated with active differentiation of parenchyma cells and disruption of wood structure.
Similar content being viewed by others
References
Alekseeva AI (1962) Diagnostic signs of Karelian birch wood. Lesnoi Zhurnal (Forest J) 3:33–37
Aloni R (2010) The induction of vascular tissues by auxin. In: Davis PJ (ed) Plant Hormones. Biosynthesis, signal transduction, action!, 3rd edn edn. Springer, Dordrecht, pp 485–518
Aloni R (2015) Ecophysiological implications of vascular differentiation and plant evolution. Trees 29:1–16. https://doi.org/10.1007/s00468-014-1070-6
Aloni R, Wolf A (1984) Suppressed buds embedded in the bark across the bole and the occurrence of their circular vessels in Ficus religiosa. Am J Bot 71:1060–1066. https://doi.org/10.1002/j.1537-2197.1984.tb11958.x
Aloni R, Zimmermann MH (1983) The control of vessel size and density along the plant axis—a new hypothesis. Differentiation 24:203–208. https://doi.org/10.1111/j.1432-0436.1983.tb01320.x
Aloni R, Alexander JD, Tyree MT (1997) Natural and experimentally altered hydraulic architecture of branch junctions in Acer saccharum Marsh. and Quercus velutina Lam. trees. Trees 11:255–264. https://doi.org/10.1007/PL00009672
Alonso-Serra J, Safronov O, Lim KJ, Fraser-Miller SJ, Blokhina OB, Campilho A, Chong SL, Fagerstedt K, Haavikko R, Helariutta Y et al (2019) Tissue-specific study across the stem reveals the chemistry and transcriptome dynamics of birch bark. New Phytol. https://doi.org/10.1111/nph.15725
Bajguz A, Piotrowska A (2009) Conjugates of auxin and cytokinin. Phytochemistry 70:957–969. https://doi.org/10.1016/j.phytochem.2009.05.006
Barilskaya LA (1979) Comparative structural analysis of the wood of silver birch and Karelian birch. Dissertation, Forest Research Institute of Karelian Branch of the USSR Academy of Sciences
Barratt DHP, Derbyshire P, Findlay K, Pike M, Wellner N, Lunn J, Feil R, Simpson C, Maule AJ, Smith AM (2009) Normal growth of Arabidopsis requires cytosolic invertase but not sucrose synthase. Proc Natl Acad Sci USA 106:13124. https://doi.org/10.1073/pnas.0900689106
Bennett T, Hines G, van Rongen M, Waldie T, Sawchuk MG, Scarpella E, Ljung K, Leyser O (2016) Connective auxin transport in the shoot facilitates communication between shoot apices. PLoS Biol 14:e1002446. https://doi.org/10.1371/journal.pbio.1002446
Carraro N, Tisdale-Orr TE, Clouse RM, Knöller AS, Spicer R (2012) Diversification and expression of the PIN, AUX/LAX, and ABCB families of putative auxin transporters in Populus. Front Plant Sci 3:1–17. https://doi.org/10.3389/fpls.2012.00017
Cho H, Dang TVT, Hwang I (2017) Emergence of plant vascular system: roles of hormonal and non-hormonal regulatory networks. Curr Opin Plant Biol 35:91–97. https://doi.org/10.1016/j.pbi.2016.11.013
De Castro E, Sigrist CJ, Gattiker A, Bulliard V, Langendijk-Genevaux PS, Gasteiger E, Hulo N (2006) ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res 34:W362–W365. https://doi.org/10.1093/nar/gkl124
Dhonukshe P, Kleine-Vehn J, Friml J (2005) Cell polarity, auxin transport, and cytoskeleton-mediated division planes: who comes first? Protoplasma 226:67–73. https://doi.org/10.1007/s00709-005-0104-8
Doley D, Leyton L (1968) Effects of growth regulating substances and water potential on the development of secondary xylem in Fraxinus. New Phytol 67:579–594. https://doi.org/10.1111/j.1469-8137.1968.tb05485.x
Eveland AL, Jackson DP (2012) Sugars, signalling, and plant development. J Exp Bot 63:3367–3377. https://doi.org/10.1093/jxb/err379
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Fonck E, Feigl GG, Fasel J, Sage D, Unser M, Rüfenacht DA, Stergiopulos N (2009) Effect of aging on elastin functionality in human cerebral arteries. Stroke 40:2552–2556. https://doi.org/10.1161/STROKEAHA.108.528091
Friml J, Palme K (2002) Polar auxin transport—old questions and new concepts? Plant Mol Biol 49:273–284. https://doi.org/10.1023/A:1015248926412
Friml J, Wiśniewska J, Benková E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415:806–809. https://doi.org/10.1038/415806a
Galibina NA, Novitskaya LL, Krasavina MS, Moshchenskaya YL (2015a) Activity of sucrose synthase in trunk tissues of Karelian birch during cambial growth. Russ J Plant Physiol 62:381–389. https://doi.org/10.1134/S102144371503005X
Galibina NA, Novitskaya LL, Krasavina MS, Moshchenskaya YL (2015b) Invertase activity in trunk tissues of Karelian birch. Russ J Plant Physiol 62:753–760. https://doi.org/10.1134/S1021443715060060
Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230
Gerttula S, Zinkgraf M, Muday GK, Lewis DR, Ibatullin FM, Brumer H, Hart F, Mansfield SD, Filkov V, Groover A (2015) Transcriptional and hormonal regulation of gravitropism of woody stems in Populus. Plant Cell 27:2800–2813. https://doi.org/10.1105/tpc.15.00531
Hagqvist R, Mikkola A (2008) Visakoivun kasvatus ja käyttö. Metsäkustannus & Visaseurary, Hämeenlinna
Hejnowicz Z (1974) Pulsations of domain length as support for the hypothesis of morphogenetic waves in the cambium. Acta Soc Bot Pol 43:261–271. https://doi.org/10.5586/asbp.1974.025
Hejnowicz Z, Kuczyńska EU (1987) Occurrence of circular vessels above axillary buds in stems of woody plants. Acta Soc Bot Pol 56:415–419. https://doi.org/10.5586/asbp.1987.039
Hejnowicz Z, Romberger JA (1979) The common basis of wood grain figures is the systematically changing orientation of cambial fusiform cells. Wood Sci Technol 13:89–96. https://doi.org/10.1007/BF00368602
Hintikka TJ (1941) Visakoivusta ja niiden anatomista. Suomalaisen kirjallisuuden seuran kirjapainon Oy, Helsinki
Iyer M, Slovin JP, Epstein E, Cohen JD (2005) Transgenic tomato plants with a modified ability to synthesize indole-3-acetyl-β-1-o-d –glucose. J Plant Growth Regul 24:142–152. https://doi.org/10.1007/s00344-004-0007-5
Jackson RG, Lim E-K, Li Y, Kowalczyk M, Sandberg G, Hoggett J, Ashford DA, Bowles DJ (2001) Identification and biochemical characterization of an Arabidopsis indole-3-acetic acid glucosyltransferase. J Biol Chem 276:4350–4356. https://doi.org/10.1074/jbc.M006185200
Jackson RG, Kowalczyk M, Li Y, Higgins G, Ross J, Sandberg G, Bowles DJ (2002) Over-expression of an Arabidopsis gene encoding a glucosyltransferase of indole-3-acetic acid: phenotypic characterisation of transgenic lines. Plant J 32:573–583. https://doi.org/10.1046/j.1365-313X.2002.01445.x
Johnson D, Eckart P, Alsamadisi N, Noble H, Martin C, Spicer R (2018) Polar auxin transport is implicated in vessel differentiation and spatial patterning during secondary growth in Populus. Am J Bot 105:1–11. https://doi.org/10.1002/ajb2.1035
Junghans U, Langenfeld-Heyser R, Polle A, Teichmann T (2004) Effect of auxin transport inhibitors and ethylene on the wood anatomy of poplar. Plant Biol 6:22–29. https://doi.org/10.1055/s-2003-44712
Kleczkowski L, Kunz S, Wilczynska M (2010) Mechanisms of UDP-glucose synthesis in plants. Crit Rev Plant Sci 29:191–203. https://doi.org/10.1080/07352689.2010.483578
Koch KE, Zeng Y (2002) Molecular approaches to altered C partitioning: genes for sucrose metabolism. J Am Soc Hortic Sci 127:474–483
Korovin VV, Novitskaya LL, Kurnosov GA (2003) Structural abnormalities of the stem in woody plants. Moscow State Forest University, Moscow
Kosichenko NE, Shchetinkin SV (1987) Structural aspects of the differentiation and diagnostics of figured wood of Karelian birch. Modern problems of wood science. Siberian Branch of the USSR Academy of Sciences, Krasnoyarsk, pp 27–29
Krabel D (2000) Influence of sucrose on cambial activity. In: Savidge RA, Barnett JR, Napier RR (eds) Cell and molecular biology of wood formation. BIOS Scientific Publishers Limited, Oxford, pp 113–125
Kramer EM (2002) A mathematical model of pattern formation in the vascular cambium of trees. J Theor Biol 216:147–158. https://doi.org/10.1006/jtbi.2002.2551
Kramer EM (2006) Wood grain pattern formation: a brief review. J Plant Growth Regul 25:290–301. https://doi.org/10.1007/s00344-006-0065-y
Krogh A, Larsson B, Von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580. https://doi.org/10.1006/jmbi.2000.4315
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Kurczyńska EU (1992) Vessel differentiation in isolated stem segments of Fraxinus excelsior L. after treatment with auxin. Acta Soc Bot Pol 61:343–357. https://doi.org/10.5586/asbp.1992.030
Kurczyńska EU, Hejnowicz Z (1991) Differentiation of circular vessels in isolated segments of Fraxinus excelsior. Physiol Plant 83:275–280. https://doi.org/10.1111/j.1399-3054.1991.tb02153.x
Kursanov AL (1984) Assimilate transport in plants. Elsevier, Amsterdam
Kursanov AL, Prasolova MF, Pavlinova OA (1989) Ways of enzymatic cleavage of sucrose in the root of sugar beet in connection with its attracting function. Phyziologiya Rasteniy (Russ J Plant Physiol) 36:629–641
Lev-Yadun S, Aloni R (1990) Vascular differentiation in branch junctions of trees: circular patterns and functional significance. Trees 4:49–54
Liu B, Zhang J, Wang L, Li J, Zheng H, Chen J, Lu M (2014) A survey of Populus PIN-FORMED family genes reveals their diversified expression patterns. J Exp Bot 65:2437–2448. https://doi.org/10.1093/jxb/eru129
Ljung K (2013) Auxin metabolism and homeostasis during plant development. Development 140:943–950. https://doi.org/10.1242/dev.086363
Ludwig-Müller J (2011) Auxin conjugates: their role for plant development and in the evolution of land plants. J Exp Bot 62:1757–1773. https://doi.org/10.1093/jxb/erq412
Ludwig-Müller J, Walz A, Slovin JP, Epstein E, Cohen JD, Dong W, Town CD (2005) Overexpression of maize IAGLU in Arabidopsis thaliana alters plant growth and sensitivity to IAA but not IBA and 2,4-D. J Plant Growth Regul 24:127–141. https://doi.org/10.1007/s00344-004-0006-6
Lyubavskaya AY (2006) Karelian birch, 2nd edn. Publishing House of Moscow State Forest University, Moscow
Mahboubi A, Ratke C, Gorzsas A, Kumar M, Mellerowicz EJ, Niittyla T (2013) Aspen SUCROSE TRANSPORTER3 allocates carbon into wood fibers. Plant Physiol 163:1729–1740. https://doi.org/10.1104/pp.113.227603
Marchler-Bauer A, Bryant SH (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32:W327–W331. https://doi.org/10.1093/nar/gkh454
Mazur E, Benková E, Friml J (2016) Vascular cambium regeneration and vessel formation in wounded inflorescence stems of Arabidopsis. Sci Rep 6:33754. https://doi.org/10.1038/srep33754
Michalczuk L, Bandurski RS (1982) Enzymic synthesis of 1-O-indol-3-ylacetyl-β-d-glucose and indol-3-ylacetyl-myo-inositol. Biochem J 207:273–281. https://doi.org/10.1042/bj2070273
Mishra BS, Singh M, Aggrawal P, Laxmi A (2009) Glucose and auxin signaling interaction in controlling Arabidopsis thaliana seedlings root growth and development. PLoS ONE 4:e4502. https://doi.org/10.1371/journal.pone.0004502
Mollenhauer HH (1964) Plastic embedding mixtures for use in electron microscopy. Stain Technol 39:111–114
Moshchenskaya YL, Galibina NA, Topchieva LV, Novitskaya LL (2017) Expression of genes encoding sucrose synthase isoforms during anomalous xylogenesis in Karelian birch. Rus J Plant Physiol 64:616–624. https://doi.org/10.1134/S1021443717030104
Mravec J, Kubeš M, Bielach A, Gaykova V, Petrášek J, Skůpa P, Chand S, Benková E, Zažímalová E, Friml J (2008) Interaction of PIN and PGP transport mechanisms in auxin distribution-dependent development. Development 135:3345–3354. https://doi.org/10.1242/dev.021071
Mravec J, Skůpa P, Bailly A, Hoyerová K, Křeček P, Bielach A, Petrášek J, Zhang J, Gaykova V, Stierhof YD et al (2009) Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459:1136–1140. https://doi.org/10.1038/nature08066
Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York
Normanly J (2010) Approaching cellular and molecular resolution of auxin biosynthesis and metabolism. Cold Spring Harb Perspect Biol 2:a001594–a001594. https://doi.org/10.1101/cshperspect.a001594
Novitskaya LL (2008) Karelian birch: mechanisms of growth and development of structural abnormalities. Verso, Petrozavodsk
Novitskaya LL, Kushnir FV (2006) The role of sucrose in regulation of trunk tissue development in Betula pendula Roth. J Plant Growth Regul 25:18–29. https://doi.org/10.1007/s00344-004-0419-2
Novitskaya L, Nikolaeva N, Galibina N, Tarelkina T, Semenova L (2016a) The greatest density of parenchyma inclusions in Karelian birch wood occurs at confluences of phloem flows. Silva Fenn 50:1461–1478. https://doi.org/10.14214/sf.1461
Novitskaya L, Nikolaeva N, Tarelkina T (2016b) Endogenous variability of the figured wood of Karelian birch. Wulfenia 23:175–188
Novitskaya LL, Shulyakovskaya TA, Galibina NA, Ilyinova MK (2018) Membrane lipid composition upon normal and patterned wood formation in Betula pendula Roth. J Plant Growth Regul 37:958–970. https://doi.org/10.1007/s00344-018-9794-y
Ostrowski M, Jakubowska A (2014) UDP-glycosyltransferases of plant hormones. Adv Cell Biol 4:43–60. https://doi.org/10.2478/acb-2014-0003
Paganova V (2004) Analysis of inheritance and growth of curly birch progenies from controlled hybridisation and possibilities of their utilisation for timber production in agricultural landscape. Czech J Genet Plant Breed 40:51–62. https://doi.org/10.17221/3700-CJGPB
Petrášek J, Mravec J, Bouchard R, Blakeslee J, Abas M, Seifertová D, Wísniewska J, Tadele Z, Kubeš M, Čovanová M et al (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312:914–918. https://doi.org/10.1126/science.1123542
Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper—Excel-based tool using pair-wise correlations. Biotechnol Lett 26:509–515
Pucher GW, Leavenworth CS, Vickery HB (1948) Determination of starch in plant tissues. Anal Chem 20:850–853
Rebrikov DV, Korostin DO, Ushakov VL, Barsova EV, Lukyanov SA (2011) Application of modern methods of molecular biology for the search and cloning of full-length nucleotide sequences of cDNA. Publishing house of the NNIU MEPhI, Moscow
Rende U, Wang W, Gandla ML, Jönsson LJ, Niittylä T (2017) Cytosolic invertase contributes to the supply of substrate for cellulose biosynthesis in developing wood. New Phytol 214:796–807. https://doi.org/10.1111/nph.14392
Roach M, Arrivault S, Mahboubi A, Krohn N, Sulpice R, Stitt M, Niittylä T (2017) Spatially resolved metabolic analysis reveals a central role for transcriptional control in carbon allocation to wood. J Exp Bot 68:3529–3539. https://doi.org/10.1093/jxb/erx200
Sachs T (2000) Integrating cellular and organismic aspects of vascular differentiation. Plant Cell Physiol 41:649–656. https://doi.org/10.1093/pcp/41.6.649
Sachs T, Cohen D (1982) Circular vessels and the control of vascular differentiation in plants. Differentiation 21:22–26. https://doi.org/10.1111/j.1432-0436.1982.tb01189.x
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Salojärvi J, Smolander O-P, Nieminen K et al (2017) Genome sequencing and population genomic analyses provide insights into the adaptive landscape of silver birch. Nat Genet 49:904–912. https://doi.org/10.1038/ng.3862
Sauter JJ (2000) Photosynthate allocation to the vascular cambium: facts and problems. In: Savidge RA, Barnett JR, Napier RR (eds) Cell and molecular biology of wood formation. BIOS Scientific Publishers Limited, Oxford, pp 71–83
Scholz A, Klepsch M, Karimi Z, Jansen S (2013) How to quantify conduits in wood? Front Plant Sci 4:1–11. https://doi.org/10.3389/fpls.2013.00056
Schrader J, Baba K, May ST, Palme K, Bennett M, Bhalerao RP, Sandberg G (2003) Polar auxin transport in the wood-forming tissues of hybrid aspen is under simultaneous control of developmental and environmental signals. Proc Natl Acad Sci USA 100:10096–10101. https://doi.org/10.1073/pnas.1633693100
Shchetinkin SV (1987) Histogenesis of figured wood in birch (Betula pendula Roth var. carelica Merkl. and Betula pendula Roth). Dissertation, Voronezh State University
Sorce C, Giovannelli A, Sebastiani L, Anfodillo T (2013) Hormonal signals involved in the regulation of cambial activity, xylogenesis and vessel patterning in trees. Plant Cell Rep 32:885–898. https://doi.org/10.1007/s00299-013-1431-4
Sturm A, Tang GQ (1999) The sucrose cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci 4:401–407. https://doi.org/10.1016/S1360-1385(99)01470-3
Sundberg B, Uggla C, Tuominen H (2000) Cambial growth and auxin gradients. In: Savidge RA, Barnett JR, Napier R (eds) Cell and molecular biology of wood formation. BIOS Scientific Publishers Limited, Oxford, pp 169–188
Szerszen J, Szczyglowski K, Bandurski R (1994) iaglu, a gene from Zea mays involved in conjugation of growth hormone indole-3-acetic acid. Science 265:1699. https://doi.org/10.1126/science.8085154
Sztein AE, Cohen JD, Slovin JP, Cooke TJ (1995) Auxin metabolism in representative land plants. Am J Bot 82:1514–1521. https://doi.org/10.2307/2446179
Tarelkina TV, Novitskaya LL (2018) Sucrose-caused changes in the frequency and localization of anticlinal divisions in the cambial zone of silver birch. Rus J Dev Biol 49:214–221. https://doi.org/10.1134/S1062360418040045
Tarelkina TV, Novitskaya LL, Nikolaeva NN (2018) Effect of sucrose exposure on the xylem anatomy of three temperate species. IAWA J 39:156–176. https://doi.org/10.1163/22941932-20170198
Unda F, Kim H, Hefer C, Ralph J, Mansfield SD (2017) Altering carbon allocation in hybrid poplar Populus alba × grandidentata impacts cell wall growth and development. Plant Biotechnol J 15:865–878. https://doi.org/10.1111/pbi.12682
Velling P, Vihera-Aarnio A, Hagqvist R, Lehto J (2000) Valuable wood as a result of abnormal cambial activity - the case of Betula pendula var. carelica. In: Savidge RA, Barnett JR, Napier R (eds) Cell and molecular biology of wood formation. BIOS Scientific Publishers Limited, Oxford, pp 377–386
Wang L, Ruan Y-L (2013) Regulation of cell division and expansion by sugar and auxin signaling. Front Plant Sci 4:1–9. https://doi.org/10.3389/fpls.2013.00163
Wheeler EA, Baas P, Gasson PE (1989) IAWA list of microscopic features for hardwood identification. IAWA Bull 10:219–332
Wisniewska J, Xu J, Seifertová D, Brewer PB, Růžička K, Blilou I, Rouquié D, Benková E, Scheres B, Friml J (2006) Polar PIN localization directs auxin flow in plants. Science 312:883. https://doi.org/10.1126/science.1121356
Wodzicki TJ, Abe H, Wodzicki AB, Pharis RP, Cohen JD (1987) Investigations on the nature of the auxin-wave in the cambial region of pine stems. Plant Physiol 84:135–143. https://doi.org/10.1104/pp.84.1.135
Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735. https://doi.org/10.1093/aob/mci083
Yakovlev FS (1949) Anatomy of Karelian birch trunk. Proc Karelo-Finnish Sci Res Base USSR Acad Sci N1:3–19
Yermakov VI (1986) Mechanisms of adaptation of birch in the North. Publishing House, Science, Leningrad
Zagórska-Marek B, Hejnowicz Z (1980) Discontinuous lines on the radial face of wavy-grained xylem as a manifestation of morphogenic waves in the cambium. Acta Soc Bot Pol 49:49–62. https://doi.org/10.5586/asbp.1980.004
Zajączkowska U (2014a) Regeneration of Scots pine stem after wounding. IAWA J 35:270–280. https://doi.org/10.1163/22941932-00000065
Zajączkowska U (2014b) Overgrowth of Douglas fir (Pseudotsuga menziesii Franco) stumps with regenerative tissue as an example of cell ordering and tissue reorganization. Planta 240:1203–1211. https://doi.org/10.1007/s00425-014-2142-y
Zajączkowska U (2015) Ordering of the cellular arrangement and xylogenesis in wounded shoots of willow. IAWA J 36:387–399. https://doi.org/10.1163/22941932-20150109
Zajączkowski S, Wodzicki TJ (1978a) Auxin and plant morphogenesis - a model of regulation. Acta Soc Bot Pol 47:233–243. https://doi.org/10.5586/asbp.1978.021
Zajączkowski S, Wodzicki TJ (1978b) On the question of stem polarity with respect to auxin transport. Physiol Plant 44:122–126. https://doi.org/10.1111/j.1399-3054.1978.tb01625.x
Zakrzewski J (1983) Hormonal control of cambial activity and vessel differentiation in Quercus robur. Physiol Plant 57:537–542. https://doi.org/10.1111/j.1399-3054.1983.tb02782.x
Zakrzewski J (1991) Effect of indole-3-acetic acid (IAA) and sucrose on vessel size and density in isolated stem segments of oak (Quercus robur). Physiol Plant 81:234–238. https://doi.org/10.1111/j.1399-3054.1991.tb02135.x
Acknowledgements
The study was funded by the Russian Foundation for Basic Research, grants N 16-04-01191_a and N 19-04-00622_a; anatomical studies were carried out under state order to the Karelian Research Centre of the Russian Academy of Sciences (Forest Research Institute KRC). We thank D.S. Ivanova for assistance in the preparation of sections for the microscopic analysis of samples.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors certify that they have no conflict of interest to declare.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Novitskaya, L.L., Tarelkina, T.V., Galibina, N.A. et al. The Formation of Structural Abnormalities in Karelian Birch Wood is Associated with Auxin Inactivation and Disrupted Basipetal Auxin Transport. J Plant Growth Regul 39, 378–394 (2020). https://doi.org/10.1007/s00344-019-09989-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-019-09989-8