Wood of broad-leaf tree species is a valued source of renewable biomass for biorefinery and a target for genetic improvement efforts to reduce its recalcitrance. Glucuronoxylan (GX) plays a key role in recalcitrance through its interactions with cellulose and lignin. To reduce recalcitrance, we modified wood GX by expressing GH10 and GH11 endoxylanases from Aspergillus nidulans in hybrid aspen (Populus tremula L. × tremuloides Michx.) and targeting the enzymes to cell wall. The xylanases reduced tree height, modified cambial activity by increasing phloem and reducing xylem production, and reduced secondary wall deposition. Xylan molecular weight was decreased, and the spacing between acetyl and MeGlcA side chains was reduced in transgenic lines. The transgenic trees produced hypolignified xylem having thin secondary walls and deformed vessels. Glucose yields of enzymatic saccharification without pretreatment almost doubled indicating decreased recalcitrance. The transcriptomics, hormonomics and metabolomics data provided evidence for activation of cytokinin and ethylene signalling pathways, decrease in ABA levels, transcriptional suppression of lignification and a subset of secondary wall biosynthetic program, including xylan glucuronidation and acetylation machinery. Several candidate genes for perception of impairment in xylan integrity were detected. These candidates could provide a new target for uncoupling negative growth effects from reduced recalcitrance. In conclusion, our study supports the hypothesis that xylan modification generates intrinsic signals and evokes novel pathways regulating tree growth and secondary wall biosynthesis.

Department of Chemical Engineering and Applied Chemistry University of Toronto Toronto Ontario Canada

Department of Chemistry Umeå University Umeå Sweden

Division of Glycoscience Department of Chemistry KTH Royal Institute of Technology AlbaNova University Centre Stockholm Sweden

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

RISE Research Institutes of Sweden Stockholm Sweden

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

Wallenberg Wood Science Centre KTH Royal Institute of Technology Stockholm Sweden

Zobrazit více v PubMed

Abreu, I.N. , Johansson, A.I. , Sokołowska, K. , Niittylä, T. , Sundberg, B. , Hvidsten, T.R. , Street, N.R. PubMed

Albersheim, P. , Darvill, A. , Roberts, K. , Sederoff, R. and Staehelin, A. (2010) Plant Cell Walls. New York: Garland Science, Taylor & Francis Group LLC.

Anderson, J.P. , Badruzsaufari, E. , Schenk, P.M. , Manners, J.M. , Desmond, O.J. , Ehlert, C. , Maclean, D.J. PubMed PMC

Bacete, L. and Hamann, T. (2020) The role of mechanoperception in plant cell wall integrity maintenance. Plan. Theory 9, 574. PubMed PMC

Bacete, L. , Mélida, H. , López, G. , Dabos, P. , Tremousaygue, D. , Denancé, N. , Miedes, E. PubMed

Bacete, L. , Schulz, J. , Engelsdorf, T. , Bartosova, Z. , Vaahtera, L. , Yan, G. , Gerhold, J.M. PubMed PMC

Barbut, F.R. , Cavel, E. , Donev, E.N. , Gaboreanu, I. , Urbancsok, J. , Pandey, G. , Demailly, H. PubMed PMC

Bar‐On, Y.M. , Phillips, R. and Milo, R. (2018) The biomass distribution on Earth. Proc. Natl. Acad. Sci. USA 115, 6506–6511. PubMed PMC

Bauer, S. , Vasu, P. , Persson, S. , Mort, A.J. and Somerville, C.R. (2006) Development and application of a suite of polysaccharide‐degrading enzymes for analyzing plant cell walls. Proc. Natl. Acad. Sci. USA 103, 11417–11422. PubMed PMC

Bavnhøj, L. , Paulsen, P.A. , Flores‐Canales, J.C. , Schiøtt, B. and Pedersen, B.P. (2021) Molecular mechanism of sugar transport in plants unveiled by structures of glucose/H PubMed

Bi, G. , Su, M. , Li, N. , Liang, Y. , Dang, S. , Xu, J. , Hu, M. PubMed

Biely, P. , Vrsanská, M. , Tenkanen, M. and Kluepfel, D. (1997) Endo‐beta‐1,4‐xylanase families: differences in catalytic properties. J. Biotechnol. 57, 151–166. PubMed

Biely, P. , Singh, S. and Puchart, V. (2016) Towards enzymatic breakdown of complex plant xylan structures: state of the art. Biotechnol. Adv. 34, 1260–1274. PubMed

Bishopp, A. , Benková, E. and Helariutta, Y. (2011) Sending mixed messages: auxin‐cytokinin crosstalk in roots. Curr. Opin. Plant Biol. 14, 10–16. PubMed

Biswal, A.K. , Hao, Z. , Pattathil, S. , Yang, X. , Winkeler, K. , Collins, C. , Mohanty, S.S. PubMed PMC

Bromley, J.R. , Busse‐Wicher, M. , Tryfona, T. , Mortimer, J.C. , Zhang, Z. , Brown, D.M. and Dupree, P. (2013) GUX1 and GUX2 glucuronyltransferases decorate distinct domains of glucuronoxylan with different substitution patterns. Plant J. 74, 423–434. PubMed

Brown, D.M. , Zeef, L.A. , Ellis, J. , Goodacre, R. and Turner, S.R. (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17, 2281–2295. PubMed PMC

Busse‐Wicher, M. , Gomes, T.C.F. , Tryfona, T. , Nikolovski, N. , Stott, K. , Grantham, N.J. , Bolam, D.N. PubMed PMC

Cantarel, B.L. , Coutinho, P.M. , Rancurel, C. , Bernard, T. , Lombard, V. and Henrissat, B. (2009) The Carbohydrate‐Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res. 37, D233–D238. PubMed PMC

Cavalier, D.M. and Keegstra, K. (2006) Two xyloglucan xylosyltransferases catalyze the addition of multiple xylosyl residues to cellohexaose. J. Biol. Chem. 281, 34197–34207. PubMed

Chang, S. , Puryear, J. and Cairney, J. (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol. Biol. Report. 11, 113–116.

Chang, N. , Sun, Q. , Li, Y. , Mu, Y. , Hu, J. , Feng, Y. , Liu, X. PubMed

Chen, H. , Wang, J.P. , Liu, H. , Li, H. , Lin, Y.J. , Shi, R. , Yang, C. PubMed PMC

Chong, S.L. , Koutaniemi, S. , Virkki, L. , Pynnönen, H. , Tuomainen, P. and Tenkanen, M. (2013) Quantitation of 4‐ PubMed

DeMartini, J.D. , Pattathil, S. , Miller, J.S. , Li, H. , Hahn, M.G. and Wyman, C.E. (2013) Investigating plant cell wall components that affect biomass recalcitrance in poplar and switchgrass. Energy Environ. Sci. 6, 898–909.

Derba‐Maceluch, M. , Awano, T. , Takahashi, J. , Lucenius, J. , Ratke, C. , Kontro, I. , Busse‐Wicher, M. PubMed

Derba‐Maceluch, M. , Sivan, P. , Donev, E.N. , Gandla, M.L. , Yassin, Z. , Vaasan, R. , Heinonen, E. PubMed PMC

Dewangan, B.P. , Gupta, A. , Sah, R.K. , Das, S. , Kumar, S. , Bhattacharjee, S. and Pawar, P.A. (2023) Xylobiose treatment triggers a defense‐related response and alters cell wall composition. Plant Mol. Biol. 113, 383–400. PubMed

Donaldson, L.A. (1992) Lignin distribution during late wood formation in

Donev, E. , Gandla, M.L. , Jönsson, L.J. and Mellerowicz, E.J. (2018) Engineering non‐cellulosic polysaccharides of wood for the biorefinery. Front. Plant Sci. 9, 1537. PubMed PMC

Escalante, A. , Gonçalves, A. , Bodin, A. , Stepan, A. , Sandström, C. , Toriz, G. and Gatenholm, P. (2012) Flexible oxygen barrier films from spruce xylan. Carbohydr. Polym. 87, 2381–2387.

Faria‐Blanc, N. , Mortimer, J.C. and Dupree, P. (2018) A transcriptomic analysis of xylan mutants does not support the existence of a secondary cell wall integrity system in PubMed PMC

Gandla, L.M. , Derba‐Maceluch, M. , Liu, X. , Gerber, L. , Master, E.R. , Mellerowicz, E.J. and Jönsson, L.J. (2015) Expression of a fungal glucuronoyl esterase in Populus: effects on wood properties and saccharification efficiency. Phytochemistry 112, 210–220. PubMed

Gandla, M.L. , Mähler, N. , Escamez, S. , Skotare, T. , Obudulu, O. , Möller, L. , Abreu, I.N. PubMed PMC

Garapati, P. , Xue, G.P. , Munné‐Bosch, S. and Balazadeh, S. (2015) Transcription factor ATAF1 in PubMed PMC

Gerber, L. , Eliasson, M. , Trygg, J. , Moritz, T. and 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.

Grantham, N.J. , Wurman‐Rodrich, J. , Terrett, O.M. , Lyczakowski, J.J. , Stott, K. , Iuga, D. , Simmons, T.J. PubMed

Gui, J. , Luo, L. , Zhong, Y. , Sun, J. , Umezawa, T. and Li, L. (2019) Phosphorylation of LTF1, an MYB transcription factor in PubMed

Gupta, M. , Rawal, T.B. , Dupree, P. , Smith, J.C. and Petridis, L. (2021) Spontaneous rearrangement of acetylated xylan on hydrophilic cellulose surfaces. Cellulose 28, 3327–3345.

Haas, A.S. , Shi, D. and Greb, T. (2022) Cell fate decisions within the vascular cambium–initiating wood and bast formation. Front. Plant Sci. 13, 864422. PubMed PMC

Hao, Z. , Avci, U. , Tan, L. , Zhu, X. , Glushka, J. , Pattathil, S. , Eberhard, S. PubMed PMC

Hartley, R.D. , Morrison, W.H. , Himmelsbach, D.S. and Borneman, W.S. (1990) Cross‐linking of cell wall phenolic arabinoxylans in graminaceous plants. Phytochemistry 29, 3705–3709.

Hernández‐Blanco, C. , Feng, D.X. , Hu, J. , Sánchez‐Vallet, A. , Deslandes, L. , Llorente, F. , Berrocal‐Lobo, M. PubMed PMC

Hoang, N.V. , Choe, G. , Zheng, Y. , Aliaga Fandino, A.C. , Sung, I. , Hur, J. , Kamran, M. PubMed

Immanen, J. , Nieminen, K. , Smolander, O.‐P. , Kojima, M. , Alonso Serra, J. , Koskinen, P. , Zhang, J. PubMed

Jones, L. , Ennos, A.R. and Turner, S.R. (2001) Cloning and characterization of irregular xylem4 (irx4): a severely lignin‐deficient mutant of PubMed

Kaida, R. , Kaku, T. , Baba, K. , Oyadomari, M. , Watanabe, T. , Nishida, K. , Kanaya, T. PubMed

Karady, M. , Hladík, P. , Cermanová, K. , Jiroutová, P. , Antoniadi, I. , Casanova‐Sáez, R. , Ljung, K. PubMed PMC

Karimi, M. , Inzé, D. and Depicker, A. (2002) GATEWAY vectors for Agrobacterium‐mediated plant transformation. Trends Plant Sci. 7, 193–195. PubMed

Keegan, D. , Kretschmer, B. , Elbersen, B. and Panoutsou, C. (2013) Cascading use: a systematic approach to biomass beyond the energy sector. Biofuels Bioprod. Biorefin. 7, 193–206.

Kim, J.H. , Nguyen, N.H. , Jeong, C.Y. , Nguyen, N.T. , Hong, S.W. and Lee, H. (2013) Loss of the R2R3 MYB, PubMed

Kitin, P. , Nakaba, S. , Hunt, C.G. , Lim, S. and Funada, R. (2020) Direct fluorescence imaging of lignocellulosic and suberized cell walls in roots and stems. AoB Plants 12, plaa032. PubMed PMC

Kojima, K. , Sunagawa, N. , Yoshimi, Y. , Tryfona, T. , Samejima, M. , Dupree, P. and Igarashi, K. (2022) Acetylated xylan degradation by glycoside hydrolase family 10 and 11 xylanases from the white‐rot fungus PubMed PMC

Kolenová, K. , Vrsanská, M. and Biely, P. (2006) Mode of action of endo‐beta‐1,4‐xylanases of families 10 and 11 on acidic xylooligosaccharides. J. Biotechnol. 121, 338–345. PubMed

Kumar, V. , Hainaut, M. , Delhomme, N. , Mannapperuma, C. , Immerzeel, P. , Street, N.R. , Henrissat, B. PubMed PMC

Lee, C. , Teng, Q. , Huang, W. , Zhong, R. and Ye, Z.‐H. (2009) Down‐regulation of PubMed

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. PubMed

Li, Q. , Lin, Y.C. , Sun, Y.H. , Song, J. , Chen, H. , Zhang, X.H. , Sederoff, R.R. PubMed PMC

Li, Q. , Min, D. , Wang, J.P. , Peszlen, I. , Horvath, L. , Horvath, B. , Nishimura, Y. PubMed

Liu, C. , Yu, H. , Rao, X. , Li, L. and Dixon, R.A. (2021) Abscisic acid regulates secondary cell‐wall formation and lignin deposition in PubMed PMC

Maris, A. , Kaewthai, N. , Eklöf, J.M. , Miller, J.G. , Brumer, H. , Fry, S.C. , Verbelen, J.P. PubMed

Markwalder, H.U. and Neukom, H. (1976) Diferulic acid as a possible crosslink in hemicelluloses from wheat germ. Phytochemistry 15, 836–837.

Martínez‐Abad, A. , Giummarella, N. , Lawoko, M. and Vilaplana, F. (2018) Differences in extractability under subcritical water reveal interconnected hemicellulose and lignin recalcitrance in birch hardwoods. Green Chem. 20, 2534–2546.

McKee, L.S. , Sunner, H. , Anasontzis, G.E. , Toriz, G. , Gatenholm, P. , Bulone, V. , Vilaplana, F. PubMed PMC

Mertz, R.A. , Olek, A.T. and Carpita, N.C. (2012) Alterations in cell‐wall glycosyl linkage structure of Arabidopsis murus mutants. Carbohydr. Polym. 89, 331–339. PubMed

Mischnick, P. (2012) Mass spectrometric characterization of oligo‐ and polysaccharides and their derivatives. In Advances in Polymer Science, Vol. 248 ( Hakkarainen, M. , ed), pp. 105–174. Berlin, Heidelberg: Springer.

Mori, K. , Renhu, N. , Naito, M. , Nakamura, A. , Shiba, H. , Yamamoto, T. , Suzaki, T. PubMed PMC

Murthy, S.E. , Dubin, A.E. , Whitwam, T. , Jojoa‐Cruz, S. , Cahalan, S.M. , Mousavi, S.A.R. , Ward, A.B. PubMed PMC

Ohtani, M. , Nishikubo, N. , Xu, B. , Yamaguchi, M. , Mitsuda, N. , Goué, N. , Shi, F. PubMed

Papdi, C. , ÁbrahÁm, E. , Joseph, M.P. , Popescu, C. , Koncz, C. and Szabados, L.S. (2008) Functional identification of PubMed PMC

Pauly, M. and Keegstra, K. (2008) Cell‐wall carbohydrates and their modification as a resource for biofuels. Plant J. 54, 559–568. PubMed

Pauly, M. and Keegstra, K. (2010) Plant cell wall polymers as precursors for biofuels. Curr. Opin. Plant Biol. 13, 305–312. PubMed

Pawar, P.M. , Derba‐Maceluch, M. , Chong, S.L. , Gómez, L.D. , Miedes, E. , Banasiak, A. , Ratke, C. PubMed PMC

Pawar, P.M.‐A. , Derba‐Maceluch, M. , Chong, S.‐L. , Gandla, M.L. , Bashar, S.S. , Sparrman, T. , Ahvenainen, P. PubMed PMC

Pell, G. , Taylor, E.J. , Gloster, T.M. , Turkenburg, J.P. , Fontes, C.M. , Ferreira, L.M. , Nagy, T. PubMed

Persson, S. , Caffall, K.H. , Freshour, G. , Hilley, M.T. , Bauer, S. , Poindexter, P. , Hahn, M.G. PubMed PMC

Petersen, P.D. , Lau, J. , Ebert, B. , Yang, F. , Verhertbruggen, Y. , Kim, J.S. , Varanasi, P. PubMed PMC

Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real‐time RT‐PCR. Nucleic Acids Res. 29, e45. PubMed PMC

Pogorelko, G. , Fursova, O. , Lin, M. , Pyle, E. , Jass, J. and Zabotina, O.A. (2011) Post‐synthetic modification of plant cell walls by expression of microbial hydrolases in the apoplast. Plant Mol. Biol. 77, 433–445. PubMed

Pollet, A. , Delcour, J.A. and Courtin, C.M. (2010) Structural determinants of the substrate specificities of xylanases from different glycoside hydrolase families. Crit. Rev. Biotechnol. 30, 176–191. PubMed

Potikha, T. and Delmer, D.P. (1995) A mutant of

Pramod, S. , Patel, V.R. , Rajput, K.S. and Rao, K.S. (2014) Distribution of tension wood like gelatinous fibres in the roots of PubMed

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. PubMed PMC

Ralph, J. , Grabber, J.H. and Hatfield, R.D. (1995) Lignin‐ferulate cross‐links in grasses: active incorporation of ferulate polysaccharide esters into ryegrass lignins. Carbohydr. Res. 275, 167–178.

Ramírez, V. and Pauly, M. (2019) Genetic dissection of cell wall defects and the strigolactone pathway in Arabidopsis. Plant Direct 3, e00149. PubMed PMC

Ratke, C. , Pawar, P.M. , Balasubramanian, V.K. , Naumann, M. , Duncranz, M.L. , Derba‐Maceluch, M. , Gorzsás, A. PubMed

Ratke, C. , Terebieniec, B.K. , Winestrand, S. , Derba‐Maceluch, M. , Grahn, T. , Schiffthaler, B. , Ulvcrona, T. PubMed

Reilly, P.J. (1981) Xylanases: structure and function. Basic Life Sci. 18, 111–129. PubMed

Richmond, B.L. , Coelho, C.L. , Wilkinson, H. , McKenna, J. , Ratchinski, P. , Schwarze, M. , Frost, M. PubMed PMC

Rivero, R.M. , Mittler, R. , Blumwald, E. and Zandalinas, S.I. (2022) Developing climate‐resilient crops: improving plant tolerance to stress combination. Plant J. 109, 373–389. PubMed

Romano, J.M. , Dubos, C. , Prouse, M.B. , Wilkins, O. , Hong, H. , Poole, M. , Kang, K.‐Y. PubMed

Rudsander, U.J. , Denman, S. , Raza, S. and Teeri, T.T. (2003) Molecular features of family GH9 cellulases in hybrid aspen and the filamentous fungus

Ruel, K. , Chevalier‐billosta, V. , Guillemin, F. , Sierra, J.B. and Joseleau, J.‐P. (2006) The wood cell wall at the ultrastructural scale – formation and topochemical organization. Maderas Cienc.Tecnol. 8, 107–116.

Saeman, J.F. , Moore, W.E. , Mitchell, R.L. and Millett, M.A. (1954) Technique for the determination of pulp constituents by quantitative paper chromatography. TAPPI J. 37, 336–343.

Sapouna, I. , Kärkönen, A. and McKee, L.S. (2023) The impact of xylan on the biosynthesis and structure of extracellular lignin produced by a Norway spruce tissue culture. Plant Direct 7, e500. PubMed PMC

Schuetz, M. , Smith, R. and Ellis, B. (2013) Xylem tissue specification, patterning, and differentiation mechanisms. J. Exp. Bot. 64, 11–31. PubMed

Simmons, T.J. , Mortimer, J.C. , Bernardinelli, O.D. , Pöppler, A.‐C. , Brown, S.P. , deAzevedo, E.R. , Dupree, R. PubMed PMC

Simura, J. , Antoniadi, I. , Siroka, J. , Tarkowska, D. , Strnad, M. , Ljung, K. and Novak, O. (2018) Plant hormonomics: multiple phytohormone profiling by targeted metabolomics. Plant Physiol. 177, 476–489. PubMed PMC

Sivan, P. , Heinonen, E. , Escudero, L. , Gandla, M.L. , Jiménez‐Quero, A. , Jönsson, L.J. , Mellerowicz, E.J. PubMed

Sivan, P. , Heinonen, E. , Latha Gandla, M. , Jiménez‐Quero, A. , Özeren, H.D. , Jönsson, L.J. , Mellerowicz, E.J.

Somerville, C.R. and Bonetta, D. (2001) Plants as factories for technical materials. Plant Physiol. 125, 168–171. PubMed PMC

Sundell, D. , Mannapperuma, C. , Netotea, S. , Delhomme, N. , Lin, Y.C. , Sjödin, A. , Van de Peer, Y. PubMed

Sundell, D. , Street, N.R. , Kumar, M. , Mellerowicz, E.J. , Kucukoglu, M. , Johnsson, C. , Kumar, V. PubMed PMC

Takata, N. , Awano, T. , Nakata, M.T. , Sano, Y. , Sakamoto, S. , Mitsuda, N. and Taniguchi, T. (2019) PubMed

Taylor‐Teeples, M. , Lin, L. , de Lucas, M. , Turco, G. , Toal, T.W. , Gaudinier, A. , Young, N.F. PubMed PMC

Teh, O.K. and Moore, I. (2007) An ARF‐GEF acting at the Golgi and in selective endocytosis in polarized plant cells. Nature 448, 493–496. PubMed

Timell, T.E. (1961) Isolation of galactoglucomannans from the wood of gymnosperms. Tappi 44, 88–96.

Tipper, E. , Leitão, N. , Dangeville, P. , Lawson, D.M. and Charpentier, M. (2023) A novel mutant allele of PubMed PMC

Turner, S.R. and Somerville, C.R. (1997) Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. Plant Cell 9, 689–701. PubMed PMC

Turner, S.R. , Taylor, N. and Jones, L. (2001) Mutations of the secondary cell wall. Plant Mol. Biol. 47, 209–219. PubMed

Urbancsok, J. , Donev, E.N. , Sivan, P. , van Zalen, E. , Barbut, F.R. , Derba‐Maceluch, M. , Šimura, J. PubMed

Van Norman, J.M. and Sieburth, L.E. (2007) Dissecting the biosynthetic pathway for the bypass1 root‐derived signal. Plant J. 49, 619–628. PubMed

Vandesompele, J. , De Preter, K. , Pattyn, F. , Poppe, B. , Van Roy, N. , De Paepe, A. PubMed PMC

Vardakou, M. , Dumon, C. , Murray, J.W. , Christakopoulos, P. , Weiner, D.P. , Juge, N. , Lewis, R.J. PubMed

Wang, Z. , Winestrand, S. , Gillgren, T. and Jönsson, L.J. (2018) Chemical and structural factors influencing enzymatic saccharification of wood from aspen, birch and spruce. Biomass Bioenergy 109, 125–134.

Wang, Z. , Mao, Y. , Guo, Y. , Gao, J. , Liu, X. , Li, S. , Lin, Y.J. PubMed PMC

Wang, L. , Wang, B. , Yu, H. , Guo, H. , Lin, T. , Kou, L. , Wang, A. PubMed

Wang, X. , Niu, Y. and Zheng, Y. (2021) Multiple functions of MYB transcription factors in abiotic stress responses. Int. J. Mol. Sci. 22, 6125. PubMed PMC

Wang, W. , Talide, L. , Viljamaa, S. and Niittylä, T. (2022) Aspen growth is not limited by starch reserves. Curr. Biol. 32, 3619–3627. PubMed

Wenkel, S. , Emery, J. , Hou, B.H. , Evans, M.M. and Barton, M.K. (2007) A feedback regulatory module formed by LITTLE ZIPPER and HD‐ZIPIII genes. Plant Cell 19, 3379–3390. PubMed PMC

Windram, O. , Madhou, P. , McHattie, S. , Hill, C. , Hickman, R. , Cooke, E. , Jenkins, D.J. PubMed PMC

Wu, F. , Chi, Y. , Jiang, Z. , Xu, Y. , Xie, L. , Huang, F. , Wan, D. PubMed

Yang, Y. , Tang, R.J. , Li, B. , Wang, H.H. , Jin, Y.L. , Jiang, C.M. , Bao, Y. PubMed

Yuan, F. , Yang, H. , Xue, Y. , Kong, D. , Ye, R. , Li, C. , Zhang, J. PubMed

Yuan, Y. , Teng, Q. , Zhong, R. , Haghighat, M. , Richardson, E.A. and Ye, Z.H. (2016a) Mutations of Arabidopsis TBL32 and TBL33 affect xylan acetylation and secondary wall deposition. PLoS One 11, e0146460. PubMed PMC

Yuan, Y. , Teng, Q. , Zhong, R. and Ye, Z.H. (2016b) TBL3 and TBL31, Two PubMed

Yuan, Y. , Teng, Q. , Zhong, R. and Ye, Z.H. (2016c) Roles of Arabidopsis TBL34 and TBL35 in xylan acetylation and plant growth. Plant Sci. 243, 120–130. PubMed

Zhang, X. , Gou, M. and Liu, C.J. (2013) Arabidopsis Kelch repeat F‐box proteins regulate phenylpropanoid biosynthesis via controlling the turnover of phenylalanine ammonia‐lyase. Plant Cell 25, 4994–5010. PubMed PMC

Zhao, Y. , Song, D. , Sun, J. and Li, L. (2013) PubMed

Zheng, K. , Wang, X. , Weighill, D.A. , Guo, H.B. , Xie, M. , Yang, Y. , Yang, J. PubMed PMC

Zhong, R. , Peña, M.J. , Zhou, G.K. , Nairn, C.J. , Wood‐Jones, A. , Richardson, E.A. , Morrison, W.H., 3rd PubMed PMC

Zhong, R. , Lee, C. , Zhou, J. , McCarthy, R.L. and Ye, Z.‐H. (2008) A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in PubMed PMC

Zhong, R. , Lee, C. and Ye, Z.H. (2010) Functional characterization of poplar wood‐associated NAC domain transcription factors. Plant Physiol. 152, 1044–1055. PubMed PMC

Zhong, R. , McCarthy, R.L. , Lee, C. and Ye, Z.H. (2011) Dissection of the transcriptional program regulating secondary wall biosynthesis during wood formation in poplar. Plant Physiol. 157, 1452–1468. PubMed PMC

Zhu, L. , Zhang, X.Q. , Ye, D. and Chen, L.Q. (2021) The MILDEW RESISTANCE LOCUS O 4 interacts with CaM/CML and is involved in root gravity response. Int. J. Mol. Sci. 22, 5962. PubMed PMC

Wood-specific modification of glucuronoxylan can enhance growth in Populus