Reaction wood (RW) formation is an innate physiological response of woody plants to counteract mechanical constraints in nature, reinforce structure and redirect growth toward the vertical direction. Differences and/or similarities between stem and root response to mechanical constraints remain almost unknown especially in relation to phytohormones distribution and RW characteristics. Thus, Populus nigra stem and root subjected to static non-destructive mid-term bending treatment were analyzed. The distribution of tension and compression forces was firstly modeled along the main bent stem and root axis; then, anatomical features, chemical composition, and a complete auxin and cytokinin metabolite profiles of the stretched convex and compressed concave side of three different bent stem and root sectors were analyzed. The results showed that in bent stems RW was produced on the upper stretched convex side whereas in bent roots it was produced on the lower compressed concave side. Anatomical features and chemical analysis showed that bent stem RW was characterized by a low number of vessel, poor lignification, and high carbohydrate, and thus gelatinous layer in fiber cell wall. Conversely, in bent root, RW was characterized by high vessel number and area, without any significant variation in carbohydrate and lignin content. An antagonistic interaction of auxins and different cytokinin forms/conjugates seems to regulate critical aspects of RW formation/development in stem and root to facilitate upward/downward organ bending. The observed differences between the response stem and root to bending highlight how hormonal signaling is highly organ-dependent.

Department of Biosciences and Territory University of Molise Pesche Italy

Department of Biotechnology and Life Science University of Insubria Varese Italy

Department of Chemistry and Biology 'A Zambelli' University of Salerno Fisciano Italy

Laboratory of Growth Regulators Institute of Experimental Botany of the Czech Academy of Sciences and Faculty of Science of Palacký University Olomouc Czechia

Umeå Plant Science Centre Department of Forest Genetics and Plant Physiology Swedish University of Agricultural Sciences Umeå Sweden

Zobrazit více v PubMed

Aloni R., Aloni E., Langhans M., Ullrich C. (2006). Role of cytokinin and auxin in shaping root architecture: regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. Ann. Bot. 97, 883–893. 10.1093/aob/mcl027, PMID: PubMed DOI PMC

Antoniadi I., Placková L., Simonovik B., Doležal K., Turnbull C., Ljung K., et al. . (2015). Cell-type-specific cytokinin distribution within the Arabidopsis primary root apex. Plant Cell 27, 1955–1967. 10.1105/tpc.15.00176, PMID: PubMed DOI PMC

Antonova G. F., Varaksina T. N., Zheleznichenko T. V., Stasova V. V. (2014). Lignin deposition during earlywood and latewood formation in scots pine stems. Wood Sci. Technol. 48, 919–936. 10.1007/s00226-014-0650-3 DOI

Begum S., Nakaba S., Bayramzadeh V., Oribee Y., Kubo T., Funada R. (2008). Temperature responses of cambial reactivation and xylem differentiation in hybrid poplar (Populus sieboldii × P. grandidentata) under natural conditions. Tree Physiol. 28, 1813–1819. 10.1093/treephys/28.12.1813, PMID: PubMed DOI

Bhalerao R. P., Bennett M. J. (2003). The case for morphogens in plants. Nat. Cell Biol. 5, 939–943. 10.1038/ncb1103-939, PMID: PubMed DOI

Bishopp A., Help H., El-Showk S., Weijers D., Scheres B., Friml J., et al. . (2011a). A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Curr. Biol. 21, 917–926. 10.1016/j.cub.2011.04.017, PMID: PubMed DOI

Bishopp A., Lehesranta S., Vaten A., Help H., El-Showk S., Scheres B., et al. . (2011b). Phloem-transported cytokinin regulates polar auxin transport and maintains vascular pattern in the root meristem. Curr. Biol. 21, 927–932. 10.1016/j.cub.2011.04.049, PMID: PubMed DOI

Bowling A. J., Vaughn K. C. (2008). Immunocytochemical characterization of tension wood: gelatinous fibers contain more than just cellulose. Am. J. Bot. 95, 655–663. 10.3732/ajb.2007368, PMID: PubMed DOI

Braam J. (2005). In touch: plant responses to mechanical stimuli. New Phytol. 165, 373–389. 10.1111/j.1469-8137.2004.01263.x, PMID: PubMed DOI

Brunoni F., Collani S., Casanova-Saez R., Simura J., Karady M., Schmid M., et al. . (2020). Conifers exhibit a characteristic inactivation of auxin to maintain tissue homeostasis. New Phytol. 226, 1753–1765. 10.1111/nph.16463, PMID: PubMed DOI

Butterfield B. G., Li G. (2000). Wood properties of glass house grown clonal radiata plantlets. Report to the multiclient seedling group, University of Canterbery, p. 12.

Casanova-Sáez R., Voß U. (2019). Auxin metabolism controls developmental decisions in land plants. Trends Plant Sci. 24, 741–754. 10.1016/j.tplants.2019.05.006, PMID: PubMed DOI

Chiatante D., Scippa G. S., Di Iorio A., Sarnataro M. (2003). The influence of steep slope on root system development. J. Plant Growth Regul. 21, 247–260. 10.1007/s00344-003-0012-0 DOI

Danjon F., Fourcaud T., Bert D. (2005). Root architecture and wind-firmness of mature Pinus pinaster. New Phytol. 168, 387–400. 10.1111/j.1469-8137.2005.01497.x, PMID: PubMed DOI

De Zio E. (2017). The responses of poplar plants to mechanical bending stress. doctoral dissertation. Italy: University of Molise.

De Zio E., Trupiano D., Karady M., Antoniadi I., Montagnoli A., Terzaghi M., et al. . (2019). Tissue-specific hormone profiles from woody poplar roots under bending stress. Physiol. Plant. 165, 101–113. 10.1111/ppl.12830, PMID: PubMed DOI

De Zio E., Trupiano D., Montagnoli A., Terzaghi M., Chiatante D., Grosso A., et al. . (2016). Poplar woody taproot under bending stress: the asymmetric response of the convex and concave sides. Ann. Bot. 118, 865–883. 10.1093/aob/mcw159, PMID: PubMed DOI PMC

Doster M. A., Bostock R. M. (1988). Quantification of lignin formation in almond bark in response to wounding and infection by Phytophthora species. Phytopathology 78, 473–477.

Du S., Uno H., Yamamoto F. (2004). Roles of auxin and gibberellin in gravity induced tension wood formation in Aesculus turbinate seedlings. IAWA J. 25, 337–347. 10.1163/22941932-90000370 DOI

Du S., Yamamoto F. (2007). An overview of the biology of reaction wood formation. J. Integr. Plant Biol. 49, 131–143. 10.1111/j.1744-7909.2007.00427.x DOI

Dumroese R. K., Terzaghi M., Chiatante D., Scippa G. S., Lasserre B., Montagnoli A. (2019). Functional traits of Pinus ponderosa coarse-roots in response to slope conditions. Front. Plant Sci. 10:947. 10.3389/fpls.2019.00947, PMID: PubMed DOI PMC

Fourcaud T., Ji J. N., Zhang Z. Q., Stokes A. (2008). Understanding the impact of root morphology on overturning mechanisms: a modelling approach. Ann. Bot. 101, 1267–1280. 10.1093/aob/mcm245, PMID: PubMed DOI PMC

Funada R., Mizukami E., Kubo T., Fushitani M., Sugiyama T. (1990). Distribution of indole-3-acetic acid and compression wood formation in the stems of inclined Cryptomeria japonica. Holzforschung 44, 331–334.

Gardiner B., Berryd P., Moulia B. (2016). Review: wind impacts on plant growth, mechanics and damage. Plant Sci. 245, 94–118. 10.1016/j.plantsci.2016.01.006, PMID: PubMed DOI

Garner L. C., Björkman T. (1999). Mechanical conditioning of tomato seedlings improves transplant quality without deleterious effects on field performance. HortScience 34, 848–851. 10.21273/hortsci.34.5.848 DOI

Gerber L., Eliasson M., Trygg J., Moritz T., Sundberg B. (2012). Multivariate curve resolution provides a high-throughput data processing pipeline for pyrolysis-gas chromatography/mass spectrometry. J. Anal. Appl. Pyrolysis 95, 95–100. 10.1016/j.jaap.2012.01.011 DOI

Gril J., Jullien D., Bardet S., Yamamoto H. (2017). Tree growth stress and related problems. J. Wood Sci. 63, 411–432. 10.1007/s10086-017-1639-y DOI

Hellgren J. M., Olofsson K., Sundberg B. (2004). Patterns of auxin distribution during gravitational induction of reaction wood in poplar and pine. Plant Physiol. 135, 212–220. 10.1104/pp.104.038927, PMID: PubMed DOI PMC

Husson F., Josse J., Le S., Mazet J. (2014). FactoMineR: multivariate exploratory data analysis and data mining with R. R package version 2.3. Available at: http://cran.r-project.org/package=FactoMineR (Accessed October 20, 2020).

Immanen J., Nieminen K., Smolander O. P., Kojima M., Alonso Serra J., Koskinen P., et al. . (2016). Cytokinin and auxin display distinct but interconnected distribution and signaling profiles to stimulate cambial activity. Curr. Biol. 26, 1990–1997. 10.1016/j.cub.2016.05.053, PMID: PubMed DOI

Jaffe M. J., Forbes S. (1993). Thigmomorphogenesis: the effect of mechanical perturbation on plants. Plant Growth Regul. 12, 313–324. 10.1007/BF00027213, PMID: PubMed DOI

Jones B. J., Ljung K. (2011). Auxin and cytokinin regulate each other’s levels via a metabolic feedback loop. Plant Signal. Behav. 6, 901–904. 10.4161/psb.6.6.15323, PMID: PubMed DOI PMC

Kern K. A., Ewers F. W., Telewski F. W., Koehler L. (2005). Mechanical perturbation affects conductivity, mechanical properties and aboveground biomass of hybrid poplars. Tree Physiol. 25, 1243–1251. 10.1093/treep-hys/25.10.1243, PMID: PubMed DOI

Kieber J. J., Schaller G. E. (2014). Cytokinins. Arabidopsis Book 12:e0168. 10.1199/tab.0168, PMID: PubMed DOI PMC

Koehler L., Telewski F. W. (2006). Biomechanics and transgenic wood. Am. J. Bot. 93, 1433–1438. 10.3732/ajb.93.10.1433, PMID: PubMed DOI

Kollmer I., Novák O., Strnad M., Schmulling T., Werner T. (2014). Overexpression of the cytosolic cytokinin oxidase/dehydrogenase (CKX7) from Arabidopsis causes specific changes in root growth and xylem differentiation. Plant J. 78, 359–371. 10.1111/tpj.12477, PMID: PubMed DOI

Little C. H. A., Pharis R. P. (1995). “Hormonal control of radial and longitudinal growth in the tree stem” in Plant stems: Physiology and functional morphology. ed. Gartner B. L. (San Diego, CA: Academic Press; ), 281–319.

Little C. H. A., Savidge R. A. (1987). The role of plant growth regulators in forest tree cambial growth. Plant Growth Regul. 6, 137–169.

Ljung K. (2013). Auxin metabolism and homeostasis during plant development. Development 140, 943–950. 10.1242/dev.086363, PMID: PubMed DOI

Ludwig-Müller J. (2011). Auxin conjugates their role for plant development and in the evolution of land plants. J. Exp. Bot. 62, 1757–1773. 10.1093/jxb/erq412, PMID: PubMed DOI

Mahonen A. P., Bishopp A., Higuchi M., Nieminen K. M., Kinoshita K., Tormakangas K., et al. . (2006). Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science 311, 94–98. 10.1126/science.1118875, PMID: PubMed DOI

Matsumoto-Kitano M., Kusumoto T., Tarkowski R., Kinoshita-Tsujimura K., Václavíková K., Miyawaki K., et al. . (2008). Cytokinins are central regulators of cambial activity. Proc. Natl. Acad. Sci. U. S. A. 105, 20027–20031. 10.1073/pnas.0805619105, PMID: PubMed DOI PMC

Mecway (2014). Manual-Mecway finite element analysis.

Mellerowicz E. J., Baucher M., Sundberg B., Boerjan W. (2001). Unravelling cell wall formation in the woody dicot stem. Plant Mol. Biol. 47, 239–274. 10.1023/A:1010699919325, PMID: PubMed DOI

Mellerowicz E. J., Gorshkova T. A. (2012). Tensional stress generation in gelatinous fibres: a review and possible mechanism based on cell wall structure and composition. J. Exp. Bot. 63, 551–565. 10.1093/jxb/err339, PMID: PubMed DOI

Miyashima S., Sebastian J., Lee J. Y., Helariuttaa Y. (2013). Stem cell function during plant vascular development. EMBO J. 32, 178–193. 10.1038/emboj.2012.301, PMID: PubMed DOI PMC

Montagnoli A., Lasserre B., Sferra G., Chiatante D., Scippa G. S., Terzaghi M., et al. . (2020). Formation of annual ring eccentricity in coarse roots within the root cage of Pinus ponderosa growing on slopes. Plan. Theory 9:181. 10.3390/plants9020181, PMID: PubMed DOI PMC

Moyle R., Schrader J., Stenberg A., Olsson O., Saxena S., Sandberg G., et al. . (2002). Environmental and auxin regulation of wood formation involves members of the aux/IAA gene family in hybrid Aspen. Plant J. 31, 675–685. 10.1046/j.1365-313x.2002.01386.x, PMID: PubMed DOI

Nishikubo N., Awano T., Banasiak A., Bourquin V., Ibatullin F., Funada R., et al. . (2007). Xyloglucan endotransglycosylase (XET) functions in gelatinous layers of tension wood fibers in poplar: a glimpse into the mechanism of the balancing act of trees. Plant Cell Physiol. 48, 843–855. 10.1093/pcp/pcm055, PMID: PubMed DOI

Novák O., Hauserová E., Amakorová P., Doležal K., Strnad M. (2008). Cytokinin profiling in plant tissues using ultra-performance liquid chromatography-electrospray tandem mass spectrometry. Phytochemistry 69, 2214–2224. 10.1016/j.phytochem.2008.04.022, PMID: PubMed DOI

Novák O., Hényková E., Sairanen I., Kowalczyk M., Pospíšil T., Ljung K. (2012). Tissue-specific profiling of the Arabidopsis thaliana auxin metabolome. Plant J. 72, 523–536. 10.1111/j.1365-313X.2012.05085.x, PMID: PubMed DOI

Parker A. J., Haskins E. F., Deyrup-Olsen I. (1982). Toluidine blue: a simple, effective stain for plant tissues. Am. Biol. Teach. 44, 487–489.

Pencík A., Simonovik B., Petersson S. V., Henyková E., Simon S., Greenham K., et al. . (2013). Regulation of auxin homeostasis and gradients in Arabidopsis roots through the formation of the indole-3-acetic acid catabolite 2-oxindole-3-acetic acid. Plant Cell 25, 3858–3870. 10.1105/tpc.113.114421, PMID: PubMed DOI PMC

Pilate G., Chabbert B., Cathala B., Yoshinaga A., Leplé J. C., Laurans F., et al. . (2004). Lignification and tension wood. C. R. Biol. 327, 889–901. 10.1016/j.crvi.2004.07.006, PMID: PubMed DOI

Plomion C., Leprovost G., Stokes A. (2001). Wood formation in trees. Plant Physiol. 127, 1513–1523. 10.1104/pp.010816, PMID: PubMed DOI PMC

R Core Team (2020). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: https://www.R-project.org/ (Accessed October 20, 2020).

Schafer M., Brutting C., Canales I. M., Großkinsky D. K., Vankova R., Baldwin I. T., et al. . (2015). The role of cis-zeatin-type cytokinins in plant growth regulation and mediating responses to environmental interactions. J. Exp. Bot. 66, 4873–4884. 10.1093/jxb/erv214, PMID: PubMed DOI PMC

Scippa G. S., Trupiano D., Rocco M., Di Iorio A., Chiatante D. (2008). Unravelling the response of poplar (Populus nigra) roots to mechanical stress imposed by bending. Plant Biosyst. 142, 401–413. 10.1080/11263500802151058 DOI

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. 10.1007/s00299-013-1431-4, PMID: PubMed DOI

Spíchal L. (2012). Cytokinins-recent news and views of evolutionarily old molecules. Funct. Plant Biol. 39, 267–284. 10.1071/FP11276, PMID: PubMed DOI

Srivastava L. M. (2002). Plant growth and development. London: Academic Press, 329–339.

Staswick P. E., Serban B., Rowe M., Tiryaki I., Maldonado M. T., Maldonado M. C., et al. . (2005). Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17, 616–627. 10.1105/tpc.104.026690, PMID: PubMed DOI PMC

Sundberg B., Uggla C., Tuominen H. (2000). “Cambial growth and auxin gradients” in Cell and molecular biology of wood formation. eds. Savidge R., Barnett J., Napier R. (Oxford: BIOS Scientific Publishers; ), 169–188.

Svacinová J., Novák O., Placková L., Lenobel R., Holík J., Strnad M., et al. . (2012). A new approach for cytokinin isolation from Arabidopsis tissues using miniaturized purification: pipette tip solid-phase extraction. Plant Methods 8, 17. 10.1186/1746-4811-8-17, PMID: PubMed DOI PMC

Teichmann T., Hamsinah Bolu-Arianto W., Olbrich A., Langenfeld-Heyser R., Göbel C., Grzeganek P., et al. . (2008). GH3::GUS reflects cell-specific developmental patterns and stress-induced changes in wood anatomy in the poplar stem. Tree Physiol. 28, 1305–1315. 10.1093/treephys/28.9.1305, PMID: PubMed DOI

Telewski F. W. (1989). Structure and function of flexure wood in Abies fraseri. Tree Physiol. 5, 113–121. 10.1093/treephys/5.1.113, PMID: PubMed DOI

Tian C., Muto H., Higuchi K., Matamura T., Tatematsu K., Koshiba T., et al. . (2004). Disruption and overexpression of auxin response factor 8 gene of Arabidopsis affect hypocotyl elongation and root growth habit, indicating its possible involvement in auxin homeostasis in light condition. Plant J. 40, 333–343. 10.1111/j.1365-313X.2004.02220.x, PMID: PubMed DOI

Timell T. E. (1986). Compression wood in gymnosperms, Vol. 2 Heidelberg: Springer-Verlag, 983–1262.

Tocquard K., Lopez D., Decourteix M., Thibaut B., Julien J. L., Label P., et al. . (2014). “The molecular mechanisms of reaction wood induction” in The biology of reaction wood. Springer series in wood science. eds. Gardiner B., Barnett J., Saranpää P., Gril J. (Berlin, Heidelberg: Springer; ), 107–138. PMID:

Tran L. S. P., Pal S. (2014). Phytohormones: A window to metabolism, signaling and biotechnological applications. New York: Springer-Verlag.

Trupiano D., Di Iorio A., Montagnoli A., Lasserre B., Rocco M., Grosso A., et al. . (2012b). Involvement of lignin and hormones in the response of woody poplar taproots to mechanical stress. Physiol. Plant. 146, 39–52. 10.1111/j.1399-3054.2012.01601.x, PMID: PubMed DOI

Trupiano D., Rocco M., Renzone G., Scaloni A., Viscosi V., Chiatante D., et al. . (2012a). The proteome of Populus nigra woody root: response to bending. Ann. Bot. 110, 415–432. 10.1093/aob/mcs040, PMID: PubMed DOI PMC

Trupiano D., Rocco M., Scaloni A., Renzoni G., Rossi M., Viscosi V., et al. . (2014). Temporal analysis of poplar woody root response to bending stress. Physiol. Plant. 150, 174–193. 10.1111/ppl.12072, PMID: PubMed DOI

Ursache R., Nieminen K., Helariutta Y. (2013). Genetic and hormonal regulation of cambial development. Physiol. Plant. 147, 36–45. 10.1111/j.1399-3054.2012.01627.x, PMID: PubMed DOI

van Erven G., de Visser R., Merkx D. W. H., Strolenberg W., de Gijsel P., Gruppen H., et al. . (2017). Quantification of lignin and its structural features in plant biomass using 13C lignin as internal standard for pyrolysis-GC-SIM-MS. Anal. Chem. 89, 10907–10916. 10.1021/acs.analchem.7b02632, PMID: PubMed DOI PMC

Vandenbrink J. P., Kiss J. Z., Herranz R., Medina F. J. (2014). Light and gravity signals synergize in modulating plant development. Front. Plant Sci. 5:563. 10.3389/fpls.2014.00563, PMID: PubMed DOI PMC

Vayssières A., Pěnčík A., Felten J., Kohler A., Ljung K., Martin F., et al. . (2015). Development of the poplar-Laccaria bicolor ectomycorrhiza modifies root auxin metabolism, signaling, and response. Plant Physiol. 169, 890–902. 10.1104/pp.114.255620, PMID: PubMed DOI PMC

Waidmann S., Kleine-Vehn J. (2020). Asymmetric cytokinin signaling opposes gravitropism in roots. J. Integr. Plant Biol. 62, 882–886. 10.1111/jipb.12929, PMID: PubMed DOI PMC

Waidmann S., Rosquete M. R., Schöller M., Sarkel E., Lindner H., LaRue T., et al. . (2019). Cytokinin functions as an asymmetric and anti-gravitropic signal in lateral roots. Nat. Commun. 10:3540. 10.1038/s41467-019-11483-4, PMID: PubMed DOI PMC

Yang M., Défossez P., Danjon F., Dupont S., Fourcaud T. (2016). Which root architectural elements contribute the best to anchorage of Pinus species? Insights from in silico experiments. Plant Soil 411, 275–291. 10.1007/s11104-016-2992-0 DOI

Yang M., Défossez P., Danjon F., Fourcaud T. (2014). Tree stability under wind: simulating uprooting with root breakage using a finite element method. Ann. Bot. 114, 695–709. 10.1093/aob/mcu122, PMID: PubMed DOI PMC

Plant Growth Regulators in Tree Rooting