Wood of trees: Cellular structure, molecular formation, and genetic engineering

Abstract

Wood is an invaluable asset to human society due to its renewable nature, making it suitable for both sustainable energy production and material manufacturing. Additionally, wood derived from forest trees plays a crucial role in sequestering a significant portion of the carbon dioxide fixed during photosynthesis by terrestrial plants. Nevertheless, with the expansion of the global population and ongoing industrialization, forest coverage has been substantially decreased, resulting in significant challenges for wood production and supply. Wood production practices have changed away from natural forests toward plantation forests. Thus, understanding the underlying genetic mechanisms of wood formation is the foundation for developing high-quality, fast-growing plantation trees. Breeding ideal forest trees for wood production using genetic technologies has attracted the interest of many. Tremendous studies have been carried out in recent years on the molecular, genetic, and cell-biological mechanisms of wood formation, and considerable progress and findings have been achieved. These studies and findings indicate enormous possibilities and prospects for tree improvement. This review will outline and assess the cellular and molecular mechanisms of wood formation, as well as studies on genetically improving forest trees, and address future development prospects.

Keywords

cambium / cell wall / Populus / wood formation / xylem

References

[1] Abbas, M., Peszlen, I., Shi, R., Kim, H., Katahira, R., Kafle, K., Xiang, Z., Huang, X., Min, D., Mohamadamin, M., et al. (2020). Involvement of CesA4, CesA7-A/B and CesA8-A/B in secondary wall formation in Populus trichocarpa wood. Tree Physiol. 40: 73-89.

[2] Van Acker, R., Déjardin, A., Desmet, S., Hoengenaert, L., Vanholme, R., Morreel, K., Laurans, F., Kim, H., Santoro, N., Foster, C., et al. (2017). Different routes for conifer- and sinapaldehyde and higher saccharification upon deficiency in the dehydrogenase CAD1. Plant Physiol. 175: 1018-1039.

[3] Van Acker, R., Leplé, J.-C., Aerts, D., Storme, V., Goeminne, G., Ivens, B., Légée, F., Lapierre, C., Piens, K., Van Montagu, M.C., et al. (2014). Improved saccharification and ethanol yield from field-grown transgenic poplar deficient in cinnamoyl-CoA reductase. Proc. Natl. Acad. Sci. U.S.A. 111: 845-850.

[4] Ahlawat, Y.K., Nookaraju, A., Harman-Ware, A.E., Doeppke, C., Biswal, A.K., and Joshi, C.P. (2021). Genetic modification of KNAT7 transcription factor expression enhances saccharification and reduces recalcitrance of woody biomass in poplars. Front. Plant Sci. 12: 12.

[5] Allario, T., Tixier, A., Awad, H., Lemaire, C., Brunel, N., Badel, E., Barigah, T.S., Julien, J.-L., Peyret, P., Mellerowicz, E.J., et al. (2018). PtxtPME1 and homogalacturonans influence xylem hydraulic properties in poplar. Physiol. Plant. 163: 502-515.

[6] Allwood, E.G., Davies, D.R., Gerrish, C., Ellis, B.E., and Bolwell, G.P. (1999). Phosphorylation of phenylalanine ammonia-lyase: Evidence for a novel protein kinase and identification of the phosphorylated residue. FEBS Lett. 457: 47-52.

[7] Baas, P., Blokhina, N., Fujii, T., Gasson, P., Grosser, D., Heinz, I., Ilic, J., Xiaomei, J., Miller, R., Newsom, L., et al. (2004). IAWA list of microscopic features for softwood identification. IAWA J. 25: 1-70.

[8] Badmi, R., Payyavula, R.S., Bali, G., Guo, H.-B., Jawdy, S.S., Gunter, L.E., Yang, X., Winkeler, K.A., Collins, C., Rottmann, W.H., et al. (2018). A new Calmodulin-binding protein expresses in the context of secondary cell wall biosynthesis and impacts biomass properties in populus. Front. Plant Sci. 9: 1669.

[9] Bar-On, Y.M., Phillips, R., and Milo, R. (2018). The biomass distribution on Earth. Proc. Natl. Acad. Sci. U.S.A. 115: 6506-6511.

[10] Baucher, M., Chabbert, B., Pilate, G., Van Doorsselaere, J., Tollier, M.T., Petit-Conil, M., Cornu, D., Monties, B., Van Montagu, M., Inze, D., et al. (1996). Red xylem and higher lignin extractability by down-regulating a cinnamyl alcohol dehydrogenase in poplar. Plant Physiol. 112: 1479-1490.

[11] Benová-Kákosová, A., Digonnet, C., Goubet, F., Ranocha, P., Jauneau, A., Pesquet, E., Barbier, O., Zhang, Z., Capek, P., Dupree, P., et al. (2006). Galactoglucomannans increase cell population density and alter the protoxylem/metaxylem tracheary element ratio in xylogenic cultures of Zinnia. Plant Physiol. 142: 696-709.

[12] Berglund, J., Mikkelsen, D., Flanagan, B.M., Dhital, S., Gaunitz, S., Henriksson, G., Lindström, M.E., Yakubov, G.E., Gidley, M.J., and Vilaplana, F. (2020). Wood hemicelluloses exert distinct biomechanical contributions to cellulose fibrillar networks. Nat. Commun. 11: 4692.

[13] Biswal, A.K., Atmodjo, M.A., Li, M., Baxter, H.L., Yoo, C.G., Pu, Y., Lee, Y.-C., Mazarei, M., Black, I.M., Zhang, J.-Y., et al. (2018a). Sugar release and growth of biofuel crops are improved by downregulation of pectin biosynthesis. Nat. Biotechnol. 36: 249-257.

[14] Biswal, A.K., Atmodjo, M.A., Pattathil, S., Amos, R.A., Yang, X., Winkeler, K., Collins, C., Mohanty, S.S., Ryno, D., Tan, L., et al. (2018b). Working towards recalcitrance mechanisms: Increased xylan and homogalacturonan production by overexpression of GAlactUronosylTransferase12 (GAUT12) causes increased recalcitrance and decreased growth in Populus. Biotechnol. Biofuels 11: 9.

[15] Biswal, A.K., Hao, Z., Pattathil, S., Yang, X., Winkeler, K., Collins, C., Mohanty, S.S., Richardson, E.A., Gelineo-Albersheim, I., Hunt, K., et al. (2015). Downregulation of GAUT12 in populus deltoides by RNA silencing results in reduced recalcitrance, increased growth and reduced xylan and pectin in a woody biofuel feedstock. Biotechnol. Biofuels 8: 41.

[16] Biswal, A.K., Soeno, K., Gandla, M.L., Immerzeel, P., Pattathil, S., Lucenius, J., Serimaa, R., Hahn, M.G., Moritz, T., Jönsson, L.J., et al. (2014). Aspen pectate lyase PtxtPL1-27 mobilizes matrix polysaccharides from woody tissues and improves saccharification yield. Biotechnol. Biofuels 7: 11.

[17] Bjurhager, I., Olsson, A.-M., Zhang, B., Gerber, L., Kumar, M., Berglund, L.A., Burgert, I., Sundberg, B., and Salmén, L. (2010). Ultrastructure and mechanical properties of populus wood with reduced lignin content caused by transgenic down-regulation of cinnamate 4-hydroxylase. Biomacromolecules 11: 2359-2365.

[18] Blokhina, O., Laitinen, T., Hatakeyama, Y., Delhomme, N., Paasela, T., Zhao, L., Street, N.R., Wada, H., Kärkönen, A., and Fagerstedt, K. (2019). Ray parenchymal cells contribute to lignification of tracheids in developing xylem of Norway spruce. Plant Physiol. 181: 1552-1572.

[19] Boerjan, W., Ralph, J., and Baucher, M. (2003). Lignin biosynthesis. Annu. Rev. Plant Biol. 54: 519-546.

[20] Bollhöner, B., Jokipii-Lukkari, S., Bygdell, J., Stael, S., Adriasola, M., Muñiz, L., Van Breusegem, F., Ezcurra, I., Wingsle, G., and Tuominen, H. (2018). The function of two type II metacaspases in woody tissues of populus trees. New Phytol. 217: 1551-1565.

[21] Bollhöner, B., Prestele, J., and Tuominen, H. (2012). Xylem cell death: Emerging understanding of regulation and function. J. Exp. Bot. 63: 1081-1094.

[22] Bollhöner, B., Zhang, B., Stael, S., Denancé, N., Overmyer, K., Goffner, D., Van Breusegem, F., and Tuominen, H. (2013). Post mortem function of AtMC9 in xylem vessel elements. New Phytol. 200: 498-510.

[23] Bomal, C., Bedon, F., Caron, S., Mansfield, S.D., Levasseur, C., Cooke, J.E., Blais, S., Tremblay, L., Morency, M.-J., Pavy, N., et al. (2008). Involvement of Pinus taeda MYB1 and MYB8 in phenylpropanoid metabolism and secondary cell wall biogenesis: A comparative in planta analysis. J. Exp. Bot. 59: 3925-3939.

[24] Borthakur, D., Busov, V., Cao, X.H., Du, Q., Gailing, O., Isik, F., Ko, J.-H., Li, C., Li, Q., Niu, S., et al. (2022). Current status and trends in forest genomics. For Res. 2: 11.

[25] Bossinger, G., and Spokevicius, A.V. (2018). Sector analysis reveals patterns of cambium differentiation in poplar stems. J. Exp. Bot. 69: 4339-4348.

[26] Bryan, A.C., Jawdy, S., Gunter, L., Gjersing, E., Sykes, R., Hinchee, M.A., Winkeler, K.A., Collins, C.M., Engle, N., Tschaplinski, T.J., et al. (2016). Knockdown of a laccase in populus deltoides confers altered cell wall chemistry and increased sugar release. Plant Biotechnol. J. 14: 2010-2020.

[27] Bugos, R.C., Chiang, V.L., and Campbell, W.H. (1991). cDNA cloning, sequence analysis and seasonal expression of lignin-bispecific caffeic acid/5-hydroxyferulic acid O-methyltransferase of aspen. Plant Mol. Biol. 17: 1203-1215.

[28] Butterfield, B. (2003). Wood anatomy in relation to wood quality. In Wood quality and its biological basis. eds J.R. Barnett, G. Jeronimidis (CRC Press, UK). pp. 30-52.

[29] Cai, Y., Zhang, K., Kim, H., Hou, G., Zhang, X., Yang, H., Feng, H., Miller, L., Ralph, J., and Liu, C.-J. (2016). Enhancing digestibility and ethanol yield of Populus wood via expression of an engineered monolignol 4-O-methyltransferase. Nat. Commun. 7: 11989.

[30] Cao, S., Guo, M., Cheng, J., Cheng, H., Liu, X., Ji, H., Liu, G., Cheng, Y., and Yang, C. (2022). Aspartic proteases modulate programmed cell death and secondary cell wall synthesis during wood formation in poplar. J. Exp. Bot. 73: 6876-6890.

[31] Cao, S., Huang, C., Luo, L., Zheng, S., Zhong, Y., Sun, J., Gui, J., and Li, L. (2020). Cell-specific suppression of 4-coumarate-CoA ligase gene reveals differential effect of lignin on cell physiological function in populus. Front. Plant Sci. 11: 589729.

[32] Chai, G., Qi, G., Cao, Y., Wang, Z., Yu, L., Tang, X., Yu, Y., Wang, D., Kong, Y., and Zhou, G. (2014). Poplar PdC3H17 and PdC3H18 are direct targets of PdMYB3 and PdMYB21, and positively regulate secondary wall formation in Arabidopsis and poplar. New Phytol. 203: 520-534.

[33] Chanoca, A., de Vries, L., and Boerjan, W. (2019). Lignin engineering in forest trees. Front. Plant Sci. 10: 912.

[34] Chen, H., Wang, J.P., Liu, H., Li, H., Lin, Y.J., Shi, R., Yang, C., Gao, J., Zhou, C., Li, Q., et al. (2019). Hierarchical transcription factor and chromatin binding network for wood formation in Populus trichocarpa. Plant Cell 31: 602-626.

[35] Chen, Y., Tong, S., Jiang, Y., Ai, F., Feng, Y., Zhang, J., Gong, J., Qin, J., Zhang, Y., Zhu, Y., et al. (2021). Transcriptional landscape of highly lignified poplar stems at single-cell resolution. Genome Biol. 22: 319.

[36] Cho, J.-S., Kim, M.-H., Bae, E.-K., Choi, Y.-I., Jeon, H.-W., Han, K.-H., and Ko, J.-H. (2021). Field evaluation of transgenic hybrid poplars with desirable wood properties and enhanced growth for biofuel production by bicistronic expression of PdGA20ox1 and PtrMYB3 in wood-forming tissue. Biotechnol. Biofuels 14: 177.

[37] Cho, J.S., Jeon, H.W., Kim, M.H., Vo, T.K., Kim, J., Park, E.J., Choi, Y.I., Lee, H., Han, K.H., and Ko, J.H. (2019). Wood forming tissue-specific bicistronic expression of PdGA20ox1 and PtrMYB221 improves both the quality and quantity of woody biomass production in a hybrid poplar. Plant Biotechnol. J. 17: 1-10.

[38] Christensen, J.H., Bauw, G., Welinder, K.G., Van Montagu, M., and Boerjan, W. (1998). Purification and characterization of peroxidases correlated with lignification in poplar xylem. Plant Physiol. 118: 125-135.

[39] Chu, L., He, X., Shu, W., Wang, L., and Tang, F. (2021). Knockdown of miR393 promotes the growth and biomass production in poplar. Front. Plant Sci. 12: 714907.

[40] Coleman, H.D., Park, J.-Y., Nair, R., Chapple, C., and Mansfield, S.D. (2008). RNAi-mediated suppression of p-coumaroyl-CoA 3’-hydroxylase in hybrid poplar impacts lignin deposition and soluble secondary metabolism. Proc. Natl. Acad. Sci. U.S.A. 105: 4501-4506.

[41] Coleman, H.D., Yan, J., and Mansfield, S.D. (2009). Sucrose synthase affects carbon partitioning to increase cellulose production and altered cell wall ultrastructure. Proc. Natl. Acad. Sci. U.S.A. 106: 13118-13123.

[42] Courtois-Moreau, C.L., Pesquet, E., Sjödin, A., Muñiz, L., Bollhöner, B., Kaneda, M., Samuels, L., Jansson, S., and Tuominen, H. (2009). A unique program for cell death in xylem fibers of Populus stem. Plant J. 58: 260-274.

[43] Cui, G., Li, Y., Yi, X., Wang, J., Lin, P., Lu, C., Zhang, Q., Gao, L., and Zhong, G. (2023). Meliaceae genomes provide insights into wood development and limonoids biosynthesis. Plant Biotechnol. J. 21: 574-590.

[44] Daneva, A., Gao, Z., Van Durme, M., and Nowack, M.K. (2016). Functions and regulation of programmed cell death in plant development. Annu. Rev. Cell Dev. Biol. 32: 441-468.

[45] Derba-Maceluch, M., Amini, F., Donev, E.N., Pawar, P.M.-A., Michaud, L., Johansson, U., Albrectsen, B.R., and Mellerowicz, E.J. (2020) Cell wall acetylation in hybrid aspen affects field performance, foliar phenolic composition and resistance to biological stress factors in a construct-dependent fashion. Front. Plant Sci. 11: 651.

[46] Derba-Maceluch, M., Sivan, P., Donev, E.N., Gandla, M.L., Yassin, Z., Vaasan, R., Heinonen, E., Andersson, S., Amini, F., Scheepers, G., et al. (2023). Impact of xylan on field productivity and wood saccharification properties in aspen. Front. Plant Sci. 14: 1218302.

[47] Desprez, T., Juraniec, M., Crowell, E.F., Jouy, H., Pochylova, Z., Parcy, F., Höfte, H., Gonneau, M., and Vernhettes, S. (2007). Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 104: 15572-15577.

[48] Van Doorsselaere, J., Baucher, M., Chognot, E., Chabbert, B., Tollier, M.-T., Petit-Conil, M., Leplé, J.-C., Pilate, G., Cornu, D., Monties, B., et al. (1995). A novel lignin in poplar trees with a reduced caffeic acid/5-hydroxyferulic acid O-methyltransferase activity. Plant J. 8: 855-864.

[49] Du, J., Gerttula, S., Li, Z., Zhao, S.-T., Liu, Y.-L., Liu, Y., Lu, M.-Z., and Groover, A.T. (2020). Brassinosteroid regulation of wood formation in poplar. New Phytol. 225: 1516-1530.

[50] Du, J., and Groover, A. (2010). Transcriptional regulation of secondary growth and wood formation. J. Integr. Plant Biol. 52: 17-27.

[51] Du, J., Miura, E., Robischon, M., Martinez, C., and Groover, A. (2011). The Populus Class III HD ZIP transcription factor POPCORONA affects cell differentiation during secondary growth of woody stems. PLoS ONE 6: e17458.

[52] Du, J., Wang, Y., Chen, W., Xu, M., Zhou, R., Shou, H., and Chen, J. (2023). High-resolution anatomical and spatial transcriptome analyses reveal two types of meristematic cell pools within the secondary vascular tissue of poplar stem. Mol. Plant 16: 809-828.

[53] Edmunds, C.W., Peralta, P., Kelley, S.S., Chiang, V.L., Sharma-Shivappa, R.R., Davis, M.F., Harman-Ware, A.E., Sykes, R.W., Gjersing, E., Cunningham, M.W., et al. (2017). Characterization and enzymatic hydrolysis of wood from transgenic Pinus taeda engineered with syringyl lignin or reduced lignin content. Cellulose 24: 1901-1914.

[54] Eriksson, M.E., Israelsson, M., Olsson, O., and Moritz, T. (2000). Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Nat. Biotechnol. 18: 784-788.

[55] Escamez, S., and Tuominen, H. (2014). Programmes of cell death and autolysis in tracheary elements: When a suicidal cell arranges its own corpse removal. J. Exp. Bot. 65: 1313-1321.

[56] Etchells, J.P., Mishra, L.S., Kumar, M., Campbell, L., and Turner, S.R. (2015). Wood formation in trees is increased by manipulating PXY-regulated cell division. Curr. Biol. 25: 1050-1055.

[57] Fan, C., Zhang, W., Guo, Y., Sun, K., Wang, L., and Luo, K. (2022). Overexpression of PtoMYB115 improves lignocellulose recalcitrance to enhance biomass digestibility and bioethanol yield by specifically regulating lignin biosynthesis in transgenic poplar. Biotechnol. Biofuels Bioprod. 15: 119.

[58] Fan, D., Li, C., Fan, C., Hu, J., Li, J., Yao, S., Lu, W., Yan, Y., and Luo, K. (2020). MicroRNA6443-mediated regulation of FERULATE 5-HYDROXYLASE gene alters lignin composition and enhances saccharification in Populus tomentosa. New Phytol. 226: 410-425.

[59] Filer, D., and Farjon, A. (2013). An atlas of the world's conifers: An analysis of their distribution, biogeography, diversity and conservation status. (Leiden, Netherlands: Brill).

[60] Fischer, U., Kucukoglu, M., Helariutta, Y., and Bhalerao, R.P. (2019). The dynamics of cambial stem cell activity. Annu. Rev. Plant Biol. 70: 293-319.

[61] Franke, R., McMichael, C.M., Meyer, K., Shirley, A.M., Cusumano, J.C., and Chapple, C. (2000). Modified lignin in tobacco and poplar plants over-expressing the Arabidopsis gene encoding ferulate 5-hydroxylase. Plant J. 22: 223-234.

[62] Friedrichsen, D.M., Nemhauser, J., Muramitsu, T., Maloof, J.N., Alonso, J., Ecker, J.R., Furuya, M., and Chory, J. (2002). Three redundant brassinosteroid early response genes encode putative bHLH transcription factors required for normal growth. Genetics 162: 1445-1456.

[63] Fu, X., Su, H., Liu, S., Du, X., Xu, C., and Luo, K. (2021). Cytokinin signaling localized in phloem noncell-autonomously regulates cambial activity during secondary growth of Populus stems. New Phytol. 230: 1476-1488.

[64] Gerber, L., Zhang, B., Roach, M., Rende, U., Gorzsás, A., Kumar, M., Burgert, I., Niittylä, T., and Sundberg, B. (2014). Deficient sucrose synthase activity in developing wood does not specifically affect cellulose biosynthesis, but causes an overall decrease in cell wall polymers. New Phytol. 203: 1220-1230.

[65] Gouwentak C.A. (1941) Cambial activity as dependent on the presence of growth hormone and the non-resting condition of stems. Protoplasma 36: 454.

[66] Gray-Mitsumune, M., Blomquist, K., McQueen-Mason, S., Teeri, T.T., Sundberg, B., and Mellerowicz, E.J. (2008). Ectopic expression of a wood-abundant expansin PttEXPA1 promotes cell expansion in primary and secondary tissues in aspen. Plant Biotechnol. J. 6: 62-72.

[67] Griscom, B.W., Adams, J., Ellis, P.W., Houghton, R.A., Lomax, G., Miteva, D.A., Schlesinger, W.H., Shoch, D., Siikamäki, J.V., Smith, P., et al. (2017). Natural climate solutions. Proc. Natl. Acad. Sci. U.S.A. 114: 11645-11650.

[68] Gui, J., Lam, P.Y., Tobimatsu, Y., Sun, J., Huang, C., Cao, S., Zhong, Y., Umezawa, T., and Li, L. (2020). Fibre-specific regulation of lignin biosynthesis improves biomass quality in Populus. New Phytol. 226: 1074-1087.

[69] Gui, J., Luo, L., Zhong, Y., Sun, J., Umezawa, T., and Li, L. (2019). Phosphorylation of LTF1, an MYB transcription factor in populus, acts as a sensory switch regulating lignin biosynthesis in wood cells. Mol. Plant 12: 1325-1337.

[70] Guo, Y., Wang, S., Yu, K., Wang, H.-L., Xu, H., Song, C., Zhao, Y., Wen, J., Fu, C., Li, Y., et al. (2023). Manipulating microRNA miR408 enhances both biomass yield and saccharification efficiency in poplar. Nat. Commun. 14: 4285.

[71] Halpin, C. (2019). Lignin engineering to improve saccharification and digestibility in grasses. Curr. Opin. Biotechnol. 56: 223-229.

[72] Han, J.-J., Lin, W., Oda, Y., Cui, K.-M., Fukuda, H., and He, X.-Q. (2012). The proteasome is responsible for caspase-3-like activity during xylem development. Plant J. 72: 129-141.

[73] Hao, Z., and Mohnen, D. (2014). A review of xylan and lignin biosynthesis: Foundation for studying Arabidopsis irregular xylem mutants with pleiotropic phenotypes. Crit. Rev. Biochem. Mol. Biol. 49: 212-241.

[74] Hoffmann, N., Benske, A., Betz, H., Schuetz, M., and Samuels, A.L. (2020). Laccases and peroxidases co-localize in lignified secondary cell walls throughout stem development. Plant Physiol. 184: 806-822.

[75] Hori, C., Takata, N., Lam, P.Y., Tobimatsu, Y., Nagano, S., Mortimer, J.C., and Cullen, D. (2020). Identifying transcription factors that reduce wood recalcitrance and improve enzymatic degradation of xylem cell wall in Populus. Sci. Rep. 10: 22043.

[76] Hou, J., Xu, H., Fan, D., Ran, L., Li, J., Wu, S., Luo, K., and He, X.-Q. (2020). MiR319a-targeted PtoTCP20 regulates secondary growth via interactions with PtoWOX4 and PtoWND6 in Populus tomentosa. New Phytol. 228: 1354-1368.

[77] Hu, J., Hu, X., Yang, Y., He, C., Hu, J., and Wang, X. (2022a). Strigolactone signaling regulates cambial activity through repression of WOX4 by transcription factor BES1. Plant Physiol. 188: 255-267.

[78] Hu, S., Kamimura, N., Sakamoto, S., Nagano, S., Takata, N., Liu, S., Goeminne, G., Vanholme, R., Uesugi, M., Yamamoto, M., et al. (2022b). Rerouting of the lignin biosynthetic pathway by inhibition of cytosolic shikimate recycling in transgenic hybrid aspen. Plant J. 110: 358-376.

[79] Hu, W.J., Harding, S.A., Lung, J., Popko, J.L., Ralph, J., Stokke, D.D., Tsai, C.J., and Chiang, V.L. (1999). Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees. Nat. Biotechnol. 17: 808-812.

[80] Huntley, S.K., Ellis, D., Gilbert, M., Chapple, C., and Mansfield, S.D. (2003). Significant increases in pulping efficiency in C4H-F5H-transformed poplars: Improved chemical savings and reduced environmental toxins. J. Agric. Food Chem. 51: 6178-6183.

[81] Immanen, J., Nieminen, K., Smolander, O.-P., Kojima, M., Alonso Serra, J., Koskinen, P., Zhang, J., Elo, A., Mähönen, A.P., Street, N., et al. (2016). Cytokinin and auxin display distinct but interconnected distribution and signaling profiles to stimulate cambial activity. Curr. Biol. 26: 1990-1997.

[82] Israelsson, M., Sundberg, B., and Moritz, T. (2005). Tissue-specific localization of gibberellins and expression of gibberellin-biosynthetic and signaling genes in wood-forming tissues in aspen. Plant J. 44: 494-504.

[83] Jang, H.-A., Bae, E.-K., Kim, M.-H., Park, S.-J., Choi, N.-Y., Pyo, S.-W., Lee, C., Jeong, H.-Y., Lee, H., Choi, Y.-I., et al. (2021). CRISPR-knockout of CSE gene improves saccharification efficiency by reducing lignin content in hybrid poplar. Int. J. Mol. Sci. 22: 9750.

[84] Jeon, H.-W., Cho, J.-S., Park, E.-J., Han, K.-H., Choi, Y.-I., and Ko, J.-H. (2016). Developing xylem-preferential expression of PdGA20ox1, a gibberellin 20-oxidase 1 from Pinus densiflora, improves woody biomass production in a hybrid poplar. Plant Biotechnol. J. 14: 1161-1170.

[85] Jia, C., Zhao, H., Wang, H., Xing, Z., Du, K., Song, Y., and Wei, J. (2004). Obtaining the transgenic poplars with low lignin content through down-regulation of4CL. Chin. Sci. Bull. 49: 905-909.

[86] Jiang, C., Li, B., Song, Z., Zhang, Y., Yu, C., Wang, H., Wang, L., and Zhang, H. (2021). PtBRI1.2 promotes shoot growth and wood formation through a brassinosteroid-mediated PtBZR1-PtWNDs module in poplar. J. Exp. Bot. 72: 6350-6364.

[87] Jiang, P.-F., Lin, X.-Y., Bian, X.-Y., Zeng, Q.-Y., and Liu, Y.-J. (2022). Ectopic expression of Populus MYB10 promotes secondary cell wall thickening and inhibits anthocyanin accumulation. Plant Physiol. Biochem. 172: 24-32.

[88] Jiao, B., Zhao, X., Lu, W., Guo, L., and Luo, K. (2019). The R2R3 MYB transcription factor MYB189 negatively regulates secondary cell wall biosynthesis in Populus. Tree Physiol. 39: 1187-1200.

[89] Jin, Y.-L., Tang, R.-J., Wang, H.-H., Jiang, C.-M., Bao, Y., Yang, Y., Liang, M.-X., Sun, Z.-C., Kong, F.-J., Li, B., et al. (2017). Overexpression of Populus trichocarpa CYP85A3 promotes growth and biomass production in transgenic trees. Plant Biotechnol. J. 15: 1309-1321.

[90] Joshi, C.P., Thammannagowda, S., Fujino, T., Gou, J.-Q., Avci, U., Haigler, C.H., McDonnell, L.M., Mansfield, S.D., Mengesha, B., Carpita, N.C., et al. (2011). Perturbation of wood cellulose synthesis causes pleiotropic effects in transgenic aspen. Mol. Plant 4: 331-345.

[91] Jouanin, L., Goujon, T., de Nadaï, V., Martin, M.T., Mila, I., Vallet, C., Pollet, B., Yoshinaga, A., Chabbert, B., Petit-Conil, M., et al. (2000). Lignification in transgenic poplars with extremely reduced caffeic acid O-methyltransferase activity. Plant Physiol. 123: 1363-1374.

[92] Kalluri, U.C., Payyavula, R.S., Labbé, J.L., Engle, N., Bali, G., Jawdy, S.S., Sykes, R.W., Davis, M., Ragauskas, A., Tuskan, G.A., et al. (2016). Down-regulation of KORRIGAN-like endo-β-1,4-glucanase genes impacts carbon partitioning, mycorrhizal colonization and biomass production in populus. Front. Plant Sci. 7: 1455.

[93] Kieber, J.J., and Polko, J. (2019). The regulation of cellulose biosynthesis in plants. Plant Cell 31: 282-296.

[94] Kim, H., Li, Q., Karlen, S. D., and Smith, R. A. (2020) Monolignol benzoates incorporate into the lignin of transgenic Populus trichocarpa depleted in C3H and C4H. ACS Sustainable Chem. Eng. 8: 3644-3654.

[95] Kim, H.B., Kwon, M., Ryu, H., Fujioka, S., Takatsuto, S., Yoshida, S., An, C.S., Lee, I., Hwang, I., and Choe, S. (2006). The regulation of DWARF4 expression is likely a critical mechanism in maintaining the homeostasis of bioactive brassinosteroids in Arabidopsis. Plant Physiol. 140: 548-557.

[96] Kim, K.H., Dutta, T., Ralph, J., Mansfield, S.D., Simmons, B.A., and Singh, S. (2017). Impact of lignin polymer backbone esters on ionic liquid pretreatment of poplar. Biotechnol. Biofuels 10: 101.

[97] Kim, M.-H., Cho, J.-S., Bae, E.-K., Choi, Y.-I., Eom, S.H., Lim, Y.J., Lee, H., Park, E.-J., and Ko, J.-H. (2021). PtrMYB120 functions as a positive regulator of both anthocyanin and lignin biosynthetic pathway in a hybrid poplar. Tree Physiol. 41: 2409-2423.

[98] Kim, M.-H., Cho, J.-S., Tran, T.N.A., Nguyen, T.T.T., Park, E.-J., Im, J.-H., Han, K.-H., Lee, H., and Ko, J.-H. (2023). Comparative functional analysis of PdeNAC2 and AtVND6 in the tracheary element formation. Tree Physiol. 43: 1201-1217.

[99] Kirui, A., Zhao, W., Deligey, F., Yang, H., Kang, X., Mentink-Vigier, F., and Wang, T. (2022). Carbohydrate-aromatic interface and molecular architecture of lignocellulose. Nat. Commun. 13: 538.

[100] Kubo, M., Udagawa, M., Nishikubo, N., Horiguchi, G., Yamaguchi, M., Ito, J., Mimura, T., Fukuda, H., and Demura, T. (2005). Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev. 19: 1855-1860.

[101] Kucukoglu, M., Chaabouni, S., Zheng, B., Mähönen, A.P., Helariutta, Y., and Nilsson, O. (2020). Peptide encoding Populus CLV3/ESR-RELATED 47 (PttCLE47) promotes cambial development and secondary xylem formation in hybrid aspen. New Phytol. 226: 75-85.

[102] Kucukoglu, M., Nilsson, J., Zheng, B., Chaabouni, S., and Nilsson, O. (2017). WUSCHEL-RELATED HOMEOBOX 4 (WOX4)-like genes regulate cambial cell division activity and secondary growth in Populus trees. New Phytol. 215: 642-657.

[103] Lapierre, C., Pollet, B., Petit-Conil, M., Toval, G., Romero, J., Pilate, G., Leple, J.C., Boerjan, W., Ferret, V., De Nadai, V., et al. (1999). Structural alterations of lignins in transgenic poplars with depressed cinnamyl alcohol dehydrogenase or caffeic acid O-methyltransferase activity have an opposite impact on the efficiency of industrial kraft pulping. Plant Physiol. 119: 153-164.

[104] Lapierre, C., Sibout, R., Laurans, F., Lesage-Descauses, M.-C., Déjardin, A., and Pilate, G. (2021). p-Coumaroylation of poplar lignins impacts lignin structure and improves wood saccharification. Plant Physiol. 187: 1374-1386.

[105] Larson, P.R. (1994). Defining the Cambium BT. In The Vascular Cambium: Development and Structure. Larson, P.R., ed. (Springer Berlin Heidelberg: Berlin, Heidelberg), pp. 33-97.

[106] Lee, C., Teng, Q., Huang, W., Zhong, R., and Ye, Z.-H. (2009). Down-regulation of PoGT47C expression in poplar results in a reduced glucuronoxylan content and an increased wood digestibility by cellulase. Plant Cell Physiol. 50: 1075-1089.

[107] Lee, C., Teng, Q., Zhong, R., and Ye, Z.-H. (2011). Molecular dissection of xylan biosynthesis during wood formation in poplar. Mol. Plant 4: 730-747.

[108] Lei, L., Li, S., and Gu, Y. (2012). Cellulose synthase complexes: Composition and regulation. Front. Plant Sci. 3: 3.

[109] Leplé, J.-C., Dauwe, R., Morreel, K., Storme, V., Lapierre, C., Pollet, B., Naumann, A., Kang, K.-Y., Kim, H., Ruel, K., et al. (2007). Downregulation of cinnamoyl-coenzyme A reductase in poplar: Multiple-level phenotyping reveals effects on cell wall polymer metabolism and structure. Plant Cell 19: 3669-3691.

[110] Lewis, S.L., Wheeler, C.E., Mitchard, E.T.A., and Koch, A. (2019). Restoring natural forests is the best way to remove atmospheric carbon. Nature 568: 25-28.

[111] Li, C., Li, D., Zhou, H., Li, J., and Lu, S. (2019). Analysis of the laccase gene family and miR397-/miR408-mediated posttranscriptional regulation in Salvia miltiorrhiza. PeerJ 7: e7605.

[112] Li, H., Dai, X., Huang, X., Xu, M., Wang, Q., Yan, X., Sederoff, R.R., and Li, Q. (2021a). Single-cell RNA sequencing reveals a high-resolution cell atlas of xylem in Populus. J. Integr. Plant Biol. 63: 1906-1921.

[113] Li, L., Lu, S., and Chiang, V. (2006). A genomic and molecular view of wood formation. CRC Crit. Rev. Plant. Sci. 25: 215-233.

[114] Li, L., Zhou, Y., Cheng, X., Sun, J., Marita, J.M., Ralph, J., and Chiang, V.L. (2003). Combinatorial modification of multiple lignin traits in trees through multigene cotransformation. Proc. Natl. Acad. Sci. U.S.A. 100: 4939-4944.

[115] Li, M., Yang, Y., Xu, R., Mu, W., Li, Y., Mao, X., Zheng, Z., Bi, H., Hao, G., Li, X., et al. (2021b). A chromosome-level genome assembly for the tertiary relict plant Tetracentron sinense oliv. (trochodendraceae). Mol. Ecol. Resour. 21: 1186-1199.

[116] Li, Q., Min, D., Wang, J.P.-Y., Peszlen, I., Horvath, L., Horvath, B., Nishimura, Y., Jameel, H., Chang, H.-M., and Chiang, V.L. (2011). Down-regulation of glycosyltransferase 8D genes in Populus trichocarpa caused reduced mechanical strength and xylan content in wood. Tree Physiol. 31: 226-236.

[117] Li, R., Wang, Z., Wang, J., and Li, L. (2023). Combining single-cell RNA sequencing with spatial transcriptome analysis reveals dynamic molecular maps of cambium differentiation in the primary and secondary growth of trees. Plant Commun. 4: 100665.

[118] Liao, R.-Y., and Wang, J.-W. (2023). Analysis of meristems and plant regeneration at single-cell resolution. Curr. Opin. Plant Biol. 74: 102378.

[119] Lin, Y.-C., Li, W., Sun, Y.-H., Kumari, S., Wei, H., Li, Q., Tunlaya-Anukit, S., Sederoff, R.R., and Chiang, V.L. (2013). SND1 transcription factor-directed quantitative functional hierarchical genetic regulatory network in wood formation in Populus trichocarpa. Plant Cell 25: 4324-4341.

[120] Liu, B., Liu, J., Yu, J., Wang, Z., Sun, Y., Li, S., Lin, Y.-C.J., Chiang, V.L., Li, W., and Wang, J.P. (2021a). Transcriptional reprogramming of xylem cell wall biosynthesis in tension wood. Plant Physiol. 186: 250-269.

[121] Liu, H., Gao, J., Sun, J., Li, S., Zhang, B., Wang, Z., Zhou, C., Sulis, D.B., Wang, J.P., Chiang, V.L., et al. (2022). Dimerization of PtrMYB074 and PtrWRKY19 mediates transcriptional activation of PtrbHLH186 for secondary xylem development in Populus trichocarpa. New Phytol. 234: 918-933.

[122] Liu, H., Wang, X., Wang, G., Cui, P., Wu, S., Ai, C., Hu, N., Li, A., He, B., Shao, X., et al. (2021b). The nearly complete genome of Ginkgo biloba illuminates gymnosperm evolution. Nat. Plants 7: 748-756.

[123] Liu, P.-L., Zhang, X., Mao, J.-F., Hong, Y.-M., Zhang, R.-G., E, Y., Nie, S., Jia, K., Jiang, C.-K., He, J., et al. (2020). The Tetracentron genome provides insight into the early evolution of eudicots and the formation of vessel elements. Genome Biol. 21: 291.

[124] Lu, J., Zhao, H., Wei, J., He, Y., Shi, C., Wang, H., and Song, Y. (2004). Lignin reduction in transgenic poplars by expressing antisense CCoAOMT gene. Prog. Nat. Sci. 14: 1060-1063.

[125] Lu, S., Li, Q., Wei, H., Chang, M.-J., Tunlaya-Anukit, S., Kim, H., Liu, J., Song, J., Sun, Y.-H., Yuan, L., et al. (2013). Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa. Proc. Natl. Acad. Sci. U.S.A. 110: 10848-10853.

[126] Luo, L., and Li, L. (2022). Molecular understanding of wood formation in trees. For. Res. 2: 5.

[127] Mahon, E.L., de Vries, L., Jang, S.-K., Middar, S., Kim, H., Unda, F., Ralph, J., and Mansfield, S.D. (2022). Exogenous chalcone synthase expression in developing poplar xylem incorporates naringenin into lignins. Plant Physiol. 188: 984-996.

[128] Maloney, V.J., and Mansfield, S.D. (2010). Characterization and varied expression of a membrane-bound endo-beta-1,4-glucanase in hybrid poplar. Plant Biotechnol. J. 8: 294-307.

[129] Maloney, V.J., Samuels, A.L., and Mansfield, S.D. (2012). The endo-1,4-β-glucanase Korrigan exhibits functional conservation between gymnosperms and angiosperms and is required for proper cell wall formation in gymnosperms. New Phytol. 193: 1076-1087.

[130] Mauriat, M., and Moritz, T. (2009). Analyses of GA20ox- and GID1-over-expressing aspen suggest that gibberellins play two distinct roles in wood formation. Plant J. 58: 989-1003.

[131] McNamara, J.T., Morgan, J.L.W., and Zimmer, J. (2015). A molecular description of cellulose biosynthesis. Annu. Rev. Biochem. 84: 895-921.

[132] Meents, M.J., Watanabe, Y., and Samuels, A.L. (2018). The cell biology of secondary cell wall biosynthesis. Ann. Bot. 121: 1107-1125.

[133] De Meester, B., Madariaga Calderón, B., de Vries, L., Pollier, J., Goeminne, G., Van Doorsselaere, J., Chen, M., Ralph, J., Vanholme, R., and Boerjan, W. (2020). Tailoring poplar lignin without yield penalty by combining a null and haploinsufficient CINNAMOYL-CoA REDUCTASE2 allele. Nat. Commun. 11: 5020.

[134] De Meester, B., Oyarce, P., Vanholme, R., Van Acker, R., Tsuji, Y., Vangeel, T., Van den Bosch, S., Van Doorsselaere, J., Sels, B., Ralph, J., et al. (2022a). Engineering curcumin biosynthesis in poplar affects lignification and biomass yield. Front. Plant Sci. 13: 943349.

[135] De Meester, B., Vanholme, R., Mota, T., and Boerjan, W. (2022b). Lignin engineering in forest trees: From gene discovery to field trials. Plant Commun. 3: 100465.

[136] De Meester, B., Vanholme, R., de Vries, L., Wouters, M., Van Doorsselaere, J., and Boerjan, W. (2021). Vessel- and ray-specific monolignol biosynthesis as an approach to engineer fiber-hypolignification and enhanced saccharification in poplar. Plant J. 108: 752-765.

[137] Meyermans, H., Morreel, K., Lapierre, C., Pollet, B., De Bruyn, A., Busson, R., Herdewijn, P., Devreese, B., Van Beeumen, J., Marita, J.M., et al. (2000). Modifications in lignin and accumulation of phenolic glucosides in poplar xylem upon down-regulation of caffeoyl-coenzyme A O-methyltransferase, an enzyme involved in lignin biosynthesis. J. Biol. Chem. 275: 36899-36909.

[138] Micheli, F., Sundberg, B., Goldberg, R., and Richard, L. (2000). Radial distribution pattern of pectin methylesterases across the cambial region of hybrid aspen at activity and dormancy. Plant Physiol. 124: 191-199.

[139] Min, D., Li, Q., Jameel, H., Chiang, V., and Chang, H. (2012). The cellulase-mediated saccharification on wood derived from transgenic low-lignin lines of black cottonwood (Populus trichocarpa). Appl. Biochem. Biotechnol. 168: 947-955.

[140] Mitsuda, N., Iwase, A., Yamamoto, H., Yoshida, M., Seki, M., Shinozaki, K., and Ohme-Takagi, M. (2007). NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of arabidopsis. Plant Cell 19: 270-280.

[141] Morris, H., Gillingham, M.A.F., Plavcová, L., Gleason, S.M., Olson, M.E., Coomes, D.A., Fichtler, E., Klepsch, M.M., Martínez-Cabrera, H.I., McGlinn, D.J., et al. (2018). Vessel diameter is related to amount and spatial arrangement of axial parenchyma in woody angiosperms. Plant Cell Environ. 41: 245-260.

[142] Mottiar, Y., Karlen, S.D., Goacher, R.E., Ralph, J., and Mansfield, S.D. (2023). Metabolic engineering of p-hydroxybenzoate in poplar lignin. Plant Biotechnol. J. 21: 176-188.

[143] Myburg, A.A., Grattapaglia, D., Tuskan, G.A., Hellsten, U., Hayes, R.D., Grimwood, J., Jenkins, J., Lindquist, E., Tice, H., Bauer, D., et al. (2014). The genome of Eucalyptus grandis. Nature 510: 356-362.

[144] Nakaba, S., Sano, Y., Kubo, T., and Funada, R. (2006). The positional distribution of cell death of ray parenchyma in a conifer, Abies sachalinensis. Plant Cell Rep. 25: 1143-1148.

[145] Nakano, Y., Endo, H., Gerber, L., Hori, C., Ihara, A., Sekimoto, M., Matsumoto, T., Kikuchi, J., Ohtani, M., and Demura, T. (2022). Enhancement of secondary cell wall formation in poplar xylem using a self-reinforced system of secondary cell wall-related transcription factors. Front. Plant Sci. 13: 13.

[146] Nayeri, S., Baghban Kohnehrouz, B., Ahmadikhah, A., and Mahna, N. (2022). CRISPR/Cas9-mediated P-CR domain-specific engineering of CESA4 heterodimerization capacity alters cell wall architecture and improves saccharification efficiency in poplar. Plant Biotechnol. J. 20: 1197-1212.

[147] Nieminen, K., Immanen, J., Laxell, M., Kauppinen, L., Tarkowski, P., Dolezal, K., Tähtiharju, S., Elo, A., Decourteix, M., Ljung, K., et al. (2008). Cytokinin signaling regulates cambial development in poplar. Proc. Natl. Acad. Sci. U.S.A. 105: 20032-20037.

[148] Nilsson, J., Karlberg, A., Antti, H., Lopez-Vernaza, M., Mellerowicz, E., Perrot-Rechenmann, C., Sandberg, G., and Bhalerao, R.P. (2008). Dissecting the molecular basis of the regulation of wood formation by auxin in hybrid aspen. Plant Cell 20: 843-855.

[149] Nishikubo, N., Takahashi, J., Roos, A.A., Derba-Maceluch, M., Piens, K., Brumer, H., Teeri, T.T., Stålbrand, H., and Mellerowicz, E.J. (2011). Xyloglucan endo-transglycosylase-mediated xyloglucan rearrangements in developing wood of hybrid aspen. Plant Physiol. 155: 399-413.

[150] Niu, S., Li, J., Bo, W., Yang, W., Zuccolo, A., Giacomello, S., Chen, X., Han, F., Yang, J., Song, Y., et al. (2022). The Chinese pine genome and methylome unveil key features of conifer evolution. Cell 185: 204-217.

[151] Noh, S.A., Choi, Y.-I., Cho, J.-S., and Lee, H. (2015). The poplar basic helix-loop-helix transcription factor BEE3 - Like gene affects biomass production by enhancing proliferation of xylem cells in poplar. Biochem. Biophys. Res. Commun. 462: 64-70.

[152] Nuoendagula, T.sujiY., Takata, N., Sakamoto, S., Nakagawa-Izumi, A., Taniguchi, T., Ralph, J., Mitsuda, N., and Kajita, S. (2018). Change in lignin structure, but not in lignin content, in transgenic poplar overexpressing the rice master regulator of secondary cell wall biosynthesis. Physiol. Plant. 163: 170-182.

[153] Nystedt, B., Street, N.R., Wetterbom, A., Zuccolo, A., Lin, Y.-C., Scofield, D.G., Vezzi, F., Delhomme, N., Giacomello, S., Alexeyenko, A., et al. (2013). The Norway spruce genome sequence and conifer genome evolution. Nature 497: 579-584.

[154] Osakabe, K., Tsao, C.C., Li, L., Popko, J.L., Umezawa, T., Carraway, D.T., Smeltzer, R.H., Joshi, C.P., and Chiang, V.L. (1999). Coniferyl aldehyde 5-hydroxylation and methylation direct syringyl lignin biosynthesis in angiosperms. Proc. Natl. Acad. Sci. U.S.A. 96: 8955-8960.

[155] Park, E.-J., Kim, H.-T., Choi, Y.-I., Lee, C., Nguyen, V.P., Jeon, H.-W., Cho, J.-S., Funada, R., Pharis, R.P., Kurepin, L.V., et al. (2015). Overexpression of gibberellin 20-oxidase1 from Pinus densiflora results in enhanced wood formation with gelatinous fiber development in a transgenic hybrid poplar. Tree Physiol. 35: 1264-1277.

[156] Pawar, P.M., Derba-Maceluch, M., Chong, S.-L., Gandla, M.L., Bashar, S.S., Sparrman, T., Ahvenainen, P., Hedenström, M., Özparpucu, M., Rüggeberg, M., et al. (2017a). In muro deacetylation of xylan affects lignin properties and improves saccharification of aspen wood. Biotechnol. Biofuels 10: 98.

[157] Pawar, P.M.-A., Ratke, C., Balasubramanian, V.K., Chong, S.-L., Gandla, M.L., Adriasola, M., Sparrman, T., Hedenström, M., Szwaj, K., Derba-Maceluch, M., et al. (2017b). Downregulation of RWA genes in hybrid aspen affects xylan acetylation and wood saccharification. New Phytol. 214: 1491-1505.

[158] Pedersen, G.B., Blaschek, L., Frandsen, K.E.H., Noack, L.C., and Persson, S. (2023). Cellulose synthesis in land plants. Mol. Plant 16: 206-231.

[159] Persson, S., Paredez, A., Carroll, A., Palsdottir, H., Doblin, M., Poindexter, P., Khitrov, N., Auer, M., and Somerville, C.R. (2007). Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 104: 15566-15571.

[160] Pilate, G., Guiney, E., Holt, K., Petit-Conil, M., Lapierre, C., Leplé, J.-C., Pollet, B., Mila, I., Webster, E.A., Marstorp, H.G., et al. (2002). Field and pulping performances of transgenic trees with altered lignification. Nat. Biotechnol. 20: 607-612.

[161] Pramod, S., Gandla, M.L., Derba-Maceluch, M., Jönsson, L.J., Mellerowicz, E.J., and Winestrand, S. (2021). Saccharification potential of transgenic greenhouse- and field-grown aspen engineered for reduced xylan acetylation. Front. Plant Sci. 12: 704960.

[162] Project, A.G., Albert, V.A., Barbazuk, W.B., dePamphilis, C.W., Der, J.P., Leebens-Mack, J., Ma, H., Palmer, J.D., Rounsley, S., Sankoff, D., et al. (2013). The amborella genome and the evolution of flowering plants. Science 342: 1241089.

[163] Qin, S., Fan, C., Li, X., Li, Y., Hu, J., Li, C., and Luo, K. (2020). LACCASE14 is required for the deposition of guaiacyl lignin and affects cell wall digestibility in poplar. Biotechnol. Biofuels 13: 197.

[164] Ralph, J., Akiyama, T., Coleman, H.D., and Mansfield, S.D. (2012). Effects on lignin structure of coumarate 3-hydroxylase downregulation in poplar. Bioenergy Res. 5: 1009-1019.

[165] Ranocha, P., Chabannes, M., Chamayou, S., Danoun, S., Jauneau, A., Boudet, A.-M., and Goffner, D. (2002). Laccase down-regulation causes alterations in phenolic metabolism and cell wall structure in poplar. Plant Physiol. 129: 145-155.

[166] Rastogi, S., and Dwivedi, U.N. (2006). Down-regulation of lignin biosynthesis in transgenic Leucaena leucocephala harboring O-methyltransferase gene. Biotechnol. Prog. 22: 609-616.

[167] Ratke, C., Pawar, P.M.-A., Balasubramanian, V.K., Naumann, M., Duncranz, M.L., Derba-Maceluch, M., Gorzsás, A., Endo, S., Ezcurra, I., and Mellerowicz, E.J. (2015). Populus GT43 family members group into distinct sets required for primary and secondary wall xylan biosynthesis and include useful promoters for wood modification. Plant Biotechnol. J. 13: 26-37.

[168] Ratke, C., Terebieniec, B.K., Winestrand, S., Derba-Maceluch, M., Grahn, T., Schiffthaler, B., Ulvcrona, T., Özparpucu, M., Rüggeberg, M., Lundqvist, S.-O., et al. (2018). Downregulating aspen xylan biosynthetic GT43 genes in developing wood stimulates growth via reprograming of the transcriptome. New Phytol. 219: 230-245.

[169] Ren, L.-L., Liu, Y.-J., Liu, H.-J., Qian, T.-T., Qi, L.-W., Wang, X.-R., and Zeng, Q.-Y. (2014). Subcellular relocalization and positive selection play key roles in the retention of duplicate genes of populus class III peroxidase family. Plant Cell 26: 2404-2419.

[170] Ren, M., Zhang, Y., Wang, R., Liu, Y., Li, M., Wang, X., Chen, X., Luan, X., Zhang, H., Wei, H., et al. (2022). PtrHAT22, as a higher hierarchy regulator, coordinately regulates secondary cell wall component biosynthesis in Populus trichocarpa. Plant Sci. 316: 111170.

[171] Ribeiro, C.L., Conde, D., Balmant, K.M., Dervinis, C., Johnson, M.G., McGrath, A.P., Szewczyk, P., Unda, F., Finegan, C.A., Schmidt, H.W., et al. (2020). The uncharacterized gene EVE contributes to vessel element dimensions in Populus. Proc. Natl. Acad. Sci. U.S.A. 117: 5059-5066.

[172] Riefler, M., Brügmann, T., Fladung, M., and Schmülling, T. (2022). A constitutively active cytokinin receptor variant increases cambial activity and stem growth in poplar. Int. J. Mol. Sci. 23: 8321.

[173] Robischon, M., Du, J., Miura, E., and Groover, A. (2011). The Populus class III HD ZIP, popREVOLUTA, influences cambium initiation and patterning of woody stems. Plant Physiol. 155: 1214-1225.

[174] Sahu, S.K., Liu, M., Chen, Y., Gui, J., Fang, D., Chen, X., Yang, T., He, C., Cheng, L., Yang, J., et al. (2023). Chromosome-scale genomes of commercial timber trees (Ochroma pyramidale, Mesua ferrea, and Tectona grandis). Sci. Data 10: 512.

[175] Sakamoto, S., Takata, N., Oshima, Y., Yoshida, K., Taniguchi, T., and Mitsuda, N. (2016). Wood reinforcement of poplar by rice NAC transcription factor. Sci. Rep. 6: 19925.

[176] Saleme, M., Cesarino, I., Vargas, L., Kim, H., Vanholme, R., Goeminne, G., Van Acker, R., Fonseca, F., Pallidis, A., Voorend, W., et al. (2017). Silencing CAFFEOYL SHIKIMATE ESTERASE affects lignification and improves saccharification in poplar. Plant Physiol. 175: 1040-1057.

[177] Salmén, L. (2022). On the organization of hemicelluloses in the wood cell wall. Cellulose 29: 1349-1355.

[178] Sampedro, J., Carey, R.E., and Cosgrove, D.J. (2006). Genome histories clarify evolution of the expansin superfamily: New insights from the poplar genome and pine ESTs. J. Plant Res. 119: 11-21.

[179] Scheller, H.V., and Ulvskov, P. (2010). Hemicelluloses. Annu. Rev. Plant Biol. 61: 263-289.

[180] Schrader, J., Baba, K., May, S.T., Palme, K., Bennett, M., Bhalerao, R.P., and 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. U.S.A. 100: 10096-10101.

[181] Seyfferth, C., Wessels, B., Jokipii-Lukkari, S., Sundberg, B., Delhomme, N., Felten, J., and Tuominen, H. (2018). Ethylene-related gene expression networks in wood formation. Front. Plant Sci. 9: 272.

[182] Seyfferth, C., Wessels, B.A., Vahala, J., Kangasjärvi, J., Delhomme, N., Hvidsten, T.R., Tuominen, H., and Lundberg-Felten, J. (2021). PopulusPtERF85 balances xylem cell expansion and secondary cell wall formation in hybrid Aspen. Cells 10: 1971.

[183] Shen, Y., Li, Y., Xu, D., Yang, C., Li, C., and Luo, K. (2018). Molecular cloning and characterization of a brassinosteriod biosynthesis-related gene PtoDWF4 from Populus tomentosa. Tree Physiol. 38: 1424-1436.

[184] Shi, D., Lebovka, I., López-Salmerón, V., Sanchez, P., and Greb, T. (2019). Bifacial cambium stem cells generate xylem and phloem during radial plant growth. Development 146: dev171355.

[185] Shimada, Y., Fujioka, S., Miyauchi, N., Kushiro, M., Takatsuto, S., Nomura, T., Yokota, T., Kamiya, Y., Bishop, G.J., and Yoshida, S. (2001). Brassinosteroid-6-oxidases from Arabidopsis and tomato catalyze multiple C-6 oxidations in brassinosteroid biosynthesis. Plant Physiol. 126: 770-779.

[186] Shimada, Y., Goda, H., Nakamura, A., Takatsuto, S., Fujioka, S., and Yoshida, S. (2003). Organ-specific expression of brassinosteroid-biosynthetic genes and distribution of endogenous brassinosteroids in Arabidopsis. Plant Physiol. 131: 287-297.

[187] Siedlecka, A., Wiklund, S., Péronne, M.-A., Micheli, F., Lesniewska, J., Sethson, I., Edlund, U., Richard, L., Sundberg, B., and Mellerowicz, E.J. (2008). Pectin methyl esterase inhibits intrusive and symplastic cell growth in developing wood cells of Populus. Plant Physiol. 146: 554-565.

[188] Słupianek, A., Dolzblasz, A., and Sokołowska, K. (2021). Xylem parenchyma-role and relevance in wood functioning in trees. Plants 10: 1247.

[189] Smith, P.J., Wang, H.-T., York, W.S., Peña, M.J., and Urbanowicz, B.R. (2017). Designer biomass for next-generation biorefineries: Leveraging recent insights into xylan structure and biosynthesis. Biotechnol. Biofuels 10: 286.

[190] Soler, M., Plasencia, A., Larbat, R., Pouzet, C., Jauneau, A., Rivas, S., Pesquet, E., Lapierre, C., Truchet, I., and Grima-Pettenati, J. (2017). The Eucalyptus linker histone variant EgH1.3 cooperates with the transcription factor EgMYB1 to control lignin biosynthesis during wood formation. New Phytol. 213: 287-299.

[191] Song, C., Guo, Y., Shen, W., Yao, X., Xu, H., Zhao, Y., Li, R., and Lin, J. (2023). PagUNE12 encodes a basic helix-loop-helix transcription factor that regulates the development of secondary vascular tissue in poplar. Plant Physiol. 192: 1046-1062.

[192] Song, D., Gui, J., Liu, C., Sun, J., and Li, L. (2016). Suppression of PtrDUF579-3 expression causes structural changes of the glucuronoxylan in populus. Front. Plant Sci. 7: 493.

[193] Song, D., Shen, J., and Li, L. (2010). Characterization of cellulose synthase complexes in Populus xylem differentiation. New Phytol. 187: 777-790.

[194] Stewart, J.J., Akiyama, T., Chapple, C., Ralph, J., and Mansfield, S.D. (2009). The effects on lignin structure of overexpression of ferulate 5-hydroxylase in hybrid poplar. Plant Physiol. 150: 621-635.

[195] Stout, A.T., Davis, A.A., Domec, J.-C., Yang, C., Shi, R., and King, J.S. (2014). Growth under field conditions affects lignin content and productivity in transgenic Populus trichocarpa with altered lignin biosynthesis. Biomass Bioenergy 68: 228-239.

[196] Stratilová, B., Kozmon, S., Stratilová, E., and Hrmova, M. (2020). Plant xyloglucan xyloglucosyl transferases and the cell wall structure: Subtle but significant. Molecules 25: 5619.

[197] Su, M., Liu, Y., Lyu, J., Zhao, S., and Wang, Y. (2021). Chemical and structural responses to downregulated p-hydroxycinnamoyl-coenzyme A: Quinate/Shikimate p-hydroxycinnamoyltransferase in poplar cell walls. Front. Plant Sci. 12: 679230.

[198] Sulis, D.B., Jiang, X., Yang, C., Marques, B.M., Matthews, M.L., Miller, Z., Lan, K., Cofre-Vega, C., Liu, B., Sun, R., et al. (2023). Multiplex CRISPR editing of wood for sustainable fiber production. Science 381: 216-221.

[199] Sun, C., Xie, Y.-H., Li, Z., Liu, Y.-J., Sun, X.-M., Li, J.-J., Quan, W.-P., Zeng, Q.-Y., Van de Peer, Y., and Zhang, S.-G. (2022). The Larix kaempferi genome reveals new insights into wood properties. J. Integr. Plant Biol. 64: 1364-1373.

[200] Sun, Y., Ren, S., Ye, S., Tian, Q., and Luo, K. (2020). Identification and functional characterization of PtoMYB055 involved in the regulation of the lignin biosynthesis pathway in Populus tomentosa. Int. J. Mol. Sci. 21: 4857.

[201] Sundell, D., Street, N.R., Kumar, M., Mellerowicz, E.J., Kucukoglu, M., Johnsson, C., Kumar, V., Mannapperuma, C., Delhomme, N., Nilsson, O., et al. (2017). AspWood: High-spatial-resolution transcriptome profiles reveal uncharacterized modularity of wood formation in Populus tremula. Plant Cell 29: 1585-1604.

[202] Suzuki, S., Li, L., Sun, Y.-H., and Chiang, V.L. (2006). The cellulose synthase gene superfamily and biochemical functions of xylem-specific cellulose synthase-like genes in Populus trichocarpa. Plant Physiol. 142: 1233-1245.

[203] Sykes, R.W., Gjersing, E.L., Foutz, K., Rottmann, W.H., Kuhn, S.A., Foster, C.E., Ziebell, A., Turner, G.B., Decker, S.R., Hinchee, M.A., et al. (2015). Down-regulation of p-coumaroyl quinate/shikimate 3′-hydroxylase (C3′H) and cinnamate 4-hydroxylase (C4H) genes in the lignin biosynthetic pathway of Eucalyptus urophylla × E. grandis leads to improved sugar release. Biotechnol. Biofuels 8: 128.

[204] Tai, H.-C., Chang, C.-H., Cai, W., Lin, J.-H., Huang, S.-J., Lin, Q.-Y., Yuan, E.C., Li, S.-L., Lin, Y.J., Chan, J.C.C., et al. (2023). Wood cellulose microfibrils have a 24-chain core-shell nanostructure in seed plants. Nat. Plants 9: 1154-1168.

[205] Takata, N., Awano, T., Nakata, M.T., Sano, Y., Sakamoto, S., Mitsuda, N., and Taniguchi, T. (2019). Populus NST/SND orthologs are key regulators of secondary cell wall formation in wood fibers, phloem fibers and xylem ray parenchyma cells. Tree Physiol. 39: 514-525.

[206] Tang, X., Wang, C., Chai, G., Wang, D., Xu, H., Liu, Y., He, G., Liu, S., Zhang, Y., Kong, Y., et al. (2022). Ubiquitinated DA1 negatively regulates vascular cambium activity through modulating the stability of WOX4 in Populus. Plant Cell 34: 3364-3382.

[207] Tang, X., Wang, D., Liu, Y., Lu, M., Zhuang, Y., Xie, Z., Wang, C., Wang, S., Kong, Y., Chai, G., et al. (2020). Dual regulation of xylem formation by an auxin-mediated PaC3H17-PaMYB199 module in Populus. New Phytol. 225: 1545-1561.

[208] Tian, X., Xie, J., Zhao, Y., Lu, H., Liu, S., Qu, L., Li, J., Gai, Y., and Jiang, X. (2013). Sense-, antisense- and RNAi-4CL1 regulate soluble phenolic acids, cell wall components and growth in transgenic Populus tomentosa Carr. Plant Physiol. Biochem. 65: 111-119.

[209] Tsai, C.-J., Popko, J.L., Mielke, M.R., Hu, W.-J., Podila, G.K., and Chiang, V.L. (1998). Suppression of O-methyltransferase gene by homologous sense transgene in quaking aspen causes red-brown wood phenotypes1. Plant Physiol. 117: 101-112.

[210] Tsai, C.-J., Xu, P., Xue, L.-J., Hu, H., Nyamdari, B., Naran, R., Zhou, X., Goeminne, G., Gao, R., Gjersing, E., et al. (2020). Compensatory guaiacyl lignin biosynthesis at the expense of syringyl lignin in 4CL1-knockout poplar. Plant Physiol. 183: 123-136.

[211] Tung, C.-C., Kuo, S.-C., Yang, C.-L., Yu, J.-H., Huang, C.-E., Liou, P.-C., Sun, Y.-H., Shuai, P., Su, J.-C., Ku, C., et al. (2023). Single-cell transcriptomics unveils xylem cell development and evolution. Genome Biol. 24: 3.

[212] Tuominen, H., Puech, L., Fink, S., and Sundberg, B. (1997). A radial concentration gradient of indole-3-acetic acid is related to secondary xylem development in hybrid aspen. Plant Physiol. 115: 577-585.

[213] Uggla, C., Mellerowicz, E.J., and Sundberg, B. (1998). Indole-3-acetic acid controls cambial growth in scots pine by positional signaling. Plant Physiol. 117: 113-121.

[214] Unda, F., Mottiar, Y., Mahon, E.L., Karlen, S.D., Kim, K.H., Loqué, D., Eudes, A., Ralph, J., and Mansfield, S.D. (2022). A new approach to zip-lignin: 3,4-dihydroxybenzoate is compatible with lignification. New Phytol. 235: 234-246.

[215] Vain, T., Crowell, E.F., Timpano, H., Biot, E., Desprez, T., Mansoori, N., Trindade, L.M., Pagant, S., Robert, S., Höfte, H., et al. (2014). The cellulase KORRIGAN is part of the cellulose synthase complex. Plant Physiol. 165: 1521-1532.

[216] Vanholme, R., De Meester, B., Ralph, J., and Boerjan, W. (2019). Lignin biosynthesis and its integration into metabolism. Curr. Opin. Biotechnol. 56: 230-239.

[217] Voelker, S.L., Lachenbruch, B., Meinzer, F.C., Jourdes, M., Ki, C., Patten, A.M., Davin, L.B., Lewis, N.G., Tuskan, G.A., Gunter, L., et al. (2010). Antisense down-regulation of 4CL expression alters lignification, tree growth, and saccharification potential of field-grown poplar. Plant Physiol. 154: 874-886.

[218] de Vries, L., Brouckaert, M., Chanoca, A., Kim, H., Regner, M.R., Timokhin, V.I., Sun, Y., De Meester, B., Van Doorsselaere, J., Goeminne, G., et al. (2021). CRISPR-Cas9 editing of CAFFEOYL SHIKIMATE ESTERASE 1 and 2 shows their importance and partial redundancy in lignification in Populus tremula × P. alba. Plant Biotechnol. J. 19: 2221-2234.

[219] de Vries, L., MacKay, H.A., Smith, R.A., Mottiar, Y., Karlen, S.D., Unda, F., Muirragui, E., Bingman, C., Vander Meulen, K., Beebe, E.T., et al. (2022). pHBMT1, a BAHD-family monolignol acyltransferase, mediates lignin acylation in poplar. Plant Physiol. 188: 1014-1027.

[220] Wadenbäck, J., von Arnold, S., Egertsdotter, U., Walter, M.H., Grima-Pettenati, J., Goffner, D., Gellerstedt, G., Gullion, T., and Clapham, D. (2008). Lignin biosynthesis in transgenic Norway spruce plants harboring an antisense construct for cinnamoyl CoA reductase (CCR). Transgenic Res. 17: 379-392.

[221] Wagner, A., Donaldson, L., Kim, H., Phillips, L., Flint, H., Steward, D., Torr, K., Koch, G., Schmitt, U., and Ralph, J. (2009). Suppression of 4-coumarate-CoA ligase in the coniferous gymnosperm Pinus radiata. Plant Physiol. 149: 370-383.

[222] Wang, C., Liu, N., Geng, Z., Ji, M., Wang, S., Zhuang, Y., Wang, D., He, G., Zhao, S., Zhou, G., et al. (2022a). Integrated transcriptome and proteome analysis reveals brassinosteroid-mediated regulation of cambium initiation and patterning in woody stem. Hortic. Res. 9: uhab048.

[223] Wang, H., Jiang, C., Wang, C., Yang, Y., Yang, L., Gao, X., and Zhang, H. (2015a). Antisense expression of the fasciclin-like arabinogalactan protein FLA6 gene in Populus inhibits expression of its homologous genes and alters stem biomechanics and cell wall composition in transgenic trees. J. Exp. Bot. 66: 1291-1302.

[224] Wang, H., Xue, Y., Chen, Y., Li, R., and Wei, J. (2012). Lignin modification improves the biofuel production potential in transgenic Populus tomentosa. Ind. Crops Prod. 37: 170-177.

[225] Wang, J.P., Chuang, L., Loziuk, P.L., Chen, H., Lin, Y.-C., Shi, R., Qu, G.-Z., Muddiman, D.C., Sederoff, R.R., and Chiang, V.L. (2015b). Phosphorylation is an on/off switch for 5-hydroxyconiferaldehyde O-methyltransferase activity in poplar monolignol biosynthesis. Proc Natl Acad Sci. U.S.A. 112: 8481-8486.

[226] Wang, J.P., Matthews, M.L., Williams, C.M., Shi, R., Yang, C., Tunlaya-Anukit, S., Chen, H.-C., Li, Q., Liu, J., Lin, C.-Y., et al. (2018). Improving wood properties for wood utilization through multi-omics integration in lignin biosynthesis. Nat. Commun. 9: 1579.

[227] Wang, L., Lu, W., Ran, L., Dou, L., Yao, S., Hu, J., Fan, D., Li, C., and Luo, K. (2019). R2R3-MYB transcription factor MYB6 promotes anthocyanin and proanthocyanidin biosynthesis but inhibits secondary cell wall formation in Populus tomentosa. Plant J. 99: 733-751.

[228] Wang, X.-Q., and Ran, J.-H. (2014). Evolution and biogeography of gymnosperms. Mol. Phylogenet. Evol. 75: 24-40.

[229] Wang, X., Yao, S., Htet, W.P.P.M., Yue, Y., Zhang, Z., Sun, K., Chen, S., Luo, K., and Fan, D. (2022b). MicroRNA828 negatively regulates lignin biosynthesis in stem of Populus tomentosa through MYB targets. Tree Physiol. 42: 1646-1661.

[230] Wang, Z., Mao, Y., Guo, Y., Gao, J., Liu, X., Li, S., Lin, Y.-C.J., Chen, H., Wang, J.P., Chiang, V.L., et al. (2020a). MYB transcription factor161 mediates feedback regulation of secondary wall-associated NAC-domain1 family genes for wood formation. Plant Physiol. 184: 1389-1406.

[231] Wang, Z., Pawar, P.M.-A., Derba-Maceluch, M., Hedenström, M., Chong, S.-L., Tenkanen, M., Jönsson, L.J., and Mellerowicz, E.J. (2020b). Hybrid aspen expressing a carbohydrate esterase family 5 acetyl xylan esterase under control of a wood-specific promoter shows improved saccharification. Front. Plant Sci. 11: 380.

[232] Wei, J., Wang, Y., Wang, H., Li, R., Lin, N., Ma, R., Qu, L., and Song, Y. (2008). Pulping performance of transgenic poplar with depressed Caffeoyl-CoA O-methyltransferase. Chin. Sci. Bull. 53: 3553-3558.

[233] Weng, J.-K., and Chapple, C. (2010). The origin and evolution of lignin biosynthesis. New Phytol. 187: 273-285.

[234] Wessels, B., Seyfferth, C., Escamez, S., Vain, T., Antos, K., Vahala, J., Delhomme, N., Kangasjärvi, J., Eder, M., Felten, J., et al. (2019). An AP2/ERF transcription factor ERF139 coordinates xylem cell expansion and secondary cell wall deposition. New Phytol. 224: 1585-1599.

[235] Wilkerson, C.G., Mansfield, S.D., Lu, F., Withers, S., Park, J.-Y., Karlen, S.D., Gonzales-Vigil, E., Padmakshan, D., Unda, F., Rencoret, J., et al. (2014). Monolignol ferulate transferase introduces chemically labile linkages into the lignin backbone. Science 344: 90-93.

[236] Xi, W., Song, D., Sun, J., Shen, J., and Li, L. (2017). Formation of wood secondary cell wall may involve two type cellulose synthase complexes in Populus. Plant Mol. Biol. 93: 419-429.

[237] Xiang, Z., Sen, S.K., Min, D., Savithri, D., Lu, F., Jameel, H., Chiang, V., and Chang, H. (2017). Field-grown transgenic hybrid poplar with modified lignin biosynthesis to improve enzymatic saccharification efficiency. ACS Sustainable Chem. Eng. 5: 2407-2414.

[238] Xie, J., Li, M., Zeng, J., Li, X., and Zhang, D. (2022). Single-cell RNA sequencing profiles of stem-differentiating xylem in poplar. Plant Biotechnol. J. 20: 417-419.

[239] Xie, M., Muchero, W., Bryan, A.C., Yee, K., Guo, H.-B., Zhang, J., Tschaplinski, T.J., Singan, V.R., Lindquist, E., Payyavula, R.S., et al. (2018). A 5-Enolpyruvylshikimate 3-phosphate synthase functions as a transcriptional repressor in populus. Plant Cell 30: 1645-1660.

[240] Xie, Z., Gui, J., Zhong, Y., Li, B., Sun, J., Shen, J., and Li, L. (2023). Screening genome-editing knockouts reveals the receptor-like kinase ASX role in regulations of secondary xylem development in Populus. New Phytol. 238: 1972-1985.

[241] Xu, C., Shen, Y., He, F., Fu, X., Yu, H., Lu, W., Li, Y., Li, C., Fan, D., Wang, H.C., et al. (2019). Auxin-mediated Aux/IAA-ARF-HB signaling cascade regulates secondary xylem development in Populus. New Phytol. 222: 752-767.

[242] Xu, W., Cheng, H., Zhu, S., Cheng, J., Ji, H., Zhang, B., Cao, S., Wang, C., Tong, G., Zhen, C., et al. (2021). Functional understanding of secondary cell wall cellulose synthases in Populus trichocarpa via the Cas9/gRNA-induced gene knockouts. New Phytol. 231: 1478-1495.

[243] Yamaguchi, M., Goué, N., Igarashi, H., Ohtani, M., Nakano, Y., Mortimer, J.C., Nishikubo, N., Kubo, M., Katayama, Y., Kakegawa, K., et al. (2010). VASCULAR-RELATED NAC-DOMAIN6 and VASCULAR-RELATED NAC-DOMAIN7 effectively induce transdifferentiation into xylem vessel elements under control of an induction system. Plant Physiol. 153: 906-914.

[244] Yan, X., Liu, J., Kim, H., Liu, B., Huang, X., Yang, Z., Lin, Y.J., Chen, H., Yang, C., Wang, J.P., et al. (2019). CAD1 and CCR2 protein complex formation in monolignol biosynthesis in Populus trichocarpa. New Phytol. 222: 244-260.

[245] Yang, Y., Yoo, C.G., Rottmann, W., Winkeler, K.A., Collins, C.M., Gunter, L.E., Jawdy, S.S., Yang, X., Pu, Y., Ragauskas, A.J., et al. (2019). PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus. BMC Plant Biol. 19: 486.

[246] Yang, Y., Yoo, C.G., Winkeler, K.A., Collins, C.M., Hinchee, M.A.W., Jawdy, S.S., Gunter, L.E., Engle, N.L., Pu, Y., Yang, X., et al. (2017). Overexpression of a domain of unknown function 231-containing protein increases O-xylan acetylation and cellulose biosynthesis in Populus. Biotechnol. Biofuels 10: 311.

[247] Ye, Z.-H., and Zhong, R. (2015). Molecular control of wood formation in trees. J. Exp. Bot. 66: 4119-4131.

[248] Yin, Z., Zhou, F., Chen, Y., Wu, H., and Yin, T. (2023). Genome-wide analysis of the expansin gene family in populus and characterization of expression changes in response to phytohormone (abscisic acid) and abiotic (low-temperature) stresses. Int. J. Mol. Sci. 24: 7759.

[249] Yu, L., Chen, H., Sun, J., and Li, L. (2014). PtrKOR1 is required for secondary cell wall cellulose biosynthesis in Populus. Tree Physiol. 34: 1289-1300.

[250] Zhang, B., Gao, Y., Zhang, L., and Zhou, Y. (2021). The plant cell wall: Biosynthesis, construction, and functions. J. Integr. Plant Biol. 63: 251-272.

[251] Zhang, J., Liu, Y., Li, C., Yin, B., Liu, X., Guo, X., Zhang, C., Liu, D., Hwang, I., Li, H., et al. (2022). PtomtAPX is an autonomous lignification peroxidase during the earliest stage of secondary wall formation in Populus tomentosa Carr. Nat. Plants 8: 828-839.

[252] Zhang, J., Wang, X., Wang, H.-T., Qiao, Z., Yao, T., Xie, M., Urbanowicz, B.R., Zeng, W., Jawdy, S.S., Gunter, L.E., et al. (2023). Overexpression of reduced wall acetylation C increases xylan acetylation and biomass recalcitrance in Populus. Plant Physiol. 194: 243-257.

[253] Zhang, X., Dominguez, P.G., Kumar, M., Bygdell, J., Miroshnichenko, S., Sundberg, B., Wingsle, G., and Niittylä, T. (2018). Cellulose synthase stoichiometry in aspen differs from Arabidopsis and Norway spruce. Plant Physiol. 177: 1096-1107.

[254] Zhao, C., Lasses, T., Bako, L., Kong, D., Zhao, B., Chanda, B., Bombarely, A., Cruz-Ramírez, A., Scheres, B., Brunner, A.M., et al. (2017). XYLEM NAC DOMAIN1, an angiosperm NAC transcription factor, inhibits xylem differentiation through conserved motifs that interact with retinoblastoma-related. New Phytol. 216: 76-89.

[255] Zhao, X., Jiang, X., Li, Z., Song, Q., Xu, C., and Luo, K. (2023). Jasmonic acid regulates lignin deposition in poplar through JAZ5-MYB/NAC interaction. Front. Plant Sci. 14: 1232880.

[256] Zhao, Y., Song, D., Sun, J., and Li, L. (2013). Populus endo-beta-mannanase PtrMAN6 plays a role in coordinating cell wall remodeling with suppression of secondary wall thickening through generation of oligosaccharide signals. Plant J. 74: 473-485.

[257] Zhao, Y., Song, X., Zhou, H., Wei, K., Jiang, C., Wang, J., Cao, Y., Tang, F., Zhao, S., and Lu, M.-Z. (2020). KNAT2/6b, a class I KNOX gene, impedes xylem differentiation by regulating NAC domain transcription factors in poplar. New Phytol. 225: 1531-1544.

[258] Zhao, Y., Sun, J., Xu, P., Zhang, R., and Li, L. (2014). Intron-mediated alternative splicing of WOOD-ASSOCIATED NAC TRANSCRIPTION FACTOR1B regulates cell wall thickening during fiber development in Populus species. Plant Physiol. 164: 765-776.

[259] Zhao, Y., Yu, X., Lam, P.-Y., Zhang, K., Tobimatsu, Y., and Liu, C.-J. (2021). Monolignol acyltransferase for lignin p-hydroxybenzoylation in Populus. Nat. Plants 7: 1288-1300.

[260] Zhen, C., Hua, X., Jiang, X., Tong, G., Li, C., Yang, C., and Cheng, Y. (2022). Cas9/gRNA-mediated mutations in PtrFLA40 and PtrFLA45 reveal redundant roles in modulating wood cell size and SCW synthesis in poplar. Int. J. Mol. Sci. 24: 427.

[261] Zheng, L., Chen, Y., Ding, D., Zhou, Y., Ding, L., Wei, J., and Wang, H. (2019). Endoplasmic reticulum-localized UBC34 interaction with lignin repressors MYB221 and MYB156 regulates the transactivity of the transcription factors in Populus tomentosa. BMC Plant Biol. 19: 97.

[262] Zheng, S., He, J., Lin, Z., Zhu, Y., Sun, J., and Li, L. (2021). Two MADS-box genes regulate vascular cambium activity and secondary growth by modulating auxin homeostasis in Populus. Plant Commun. 2: 100134.

[263] Zhong, R., Cui, D., and Ye, Z.-H. (2019). Secondary cell wall biosynthesis. New Phytol. 221: 1703-1723.

[264] Zhong, R., Demura, T., and Ye, Z.-H. (2006). SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of arabidopsis. Plant Cell 18: 3158-3170.

[265] Zhong, R., Morrison, 3rd, W.H., Himmelsbach, D.S., and Poole, 2nd, F.L., Ye, Z.H. (2000). Essential role of caffeoyl coenzyme A O-methyltransferase in lignin biosynthesis in woody poplar plants. Plant Physiol. 124: 563-578.

[266] Zhong, R., Richardson, E.A., and Ye, Z.-H. (2007). Two NAC domain transcription factors, SND1 and NST1, function redundantly in regulation of secondary wall synthesis in fibers of Arabidopsis. Planta 225: 1603-1611.

[267] Zhou, X., Jacobs, T.B., Xue, L.-J., Harding, S.A., and Tsai, C.-J. (2015). Exploiting SNPs for biallelic CRISPR mutations in the outcrossing woody perennial Populus reveals 4-coumarate:CoA ligase specificity and redundancy. New Phytol. 208: 298-301.

[268] Zhou, X., Ren, S., Lu, M., Zhao, S., Chen, Z., Zhao, R., and Lv, J. (2018). Preliminary study of cell wall structure and its mechanical properties of C3H and HCT RNAi transgenic poplar sapling. Sci. Rep. 8: 10508.

[269] Zhu, Y., and Li, L. (2021). Multi-layered regulation of plant cell wall thickening. Plant Cell Physiol. 62: 1867-1873.

[270] Zhu, Y., Song, D., Sun, J., Wang, X., and Li, L. (2013). PtrHB7, a class III HD-Zip gene, plays a critical role in regulation of vascular cambium differentiation in Populus. Mol. Plant 6: 1331-1343.

[271] Zhu, Y., Song, D., Xu, P., Sun, J., and Li, L. (2018). A HD-ZIP III gene, PtrHB4, is required for interfascicular cambium development in Populus. Plant Biotechnol. J. 16: 808-817.

[272] Zhu, Y., Song, D., Zhang, R., Luo, L., Cao, S., Huang, C., Sun, J., Gui, J., and Li, L. (2020). A xylem-produced peptide PtrCLE20 inhibits vascular cambium activity in Populus. Plant Biotechnol. J. 18: 195-206.

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