Abstract
Plants possess an outer cell layer called the cell wall. This matrix comprises various molecules, such as polysaccharides and proteins, and serves a wide array of physiologically important functions. This structure is not static but rather flexible in response to the environment. One of the factors responsible for this plasticity is the xyloglucan endotransglucosylase/hydrolase (XTH) family, which cleaves and reconnects xyloglucan molecules. Since xyloglucan molecules have been hypothesised to tether cellulose microfibrils forming the main load-bearing network in the primary cell wall, XTHs have been thought to play a central role in cell wall loosening for plant cell expansion. However, multiple lines of recent evidence have questioned this classic model. Nevertheless, reverse genetic analyses have proven the biological importance of XTHs; therefore, a major challenge at present is to reconsider the role of XTHs in planta. Recent advances in analytical techniques have allowed for gathering rich information on the structure of the primary cell wall. Thus, the integration of accumulated knowledge in current XTH studies may offer a turning point for unveiling the precise functions of XTHs. In the present review, we redefine the biological function of the XTH family based on the recent architectural model of the cell wall. We highlight three key findings regarding this enzyme family: (1) XTHs are not strictly required for cell wall loosening during plant cell expansion but play vital roles in response to specific biotic or abiotic stresses; (2) in addition to their transglycosylase activity, the hydrolase activity of XTHs is involved in physiological benefits; and (3) XTHs can recognise a wide range of polysaccharides other than xyloglucans.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Akiyama T, Jin S, Yoshida M, Hoshino T, Opassiri R, Ketudat Cairns JR (2009) Expression of an endo-(1,3;1,4)-beta-glucanase in response to wounding, methyl jasmonate, abscisic acid and ethephon in rice seedlings. J Plant Physiol 166:1814–1825. https://doi.org/10.1016/j.jplph.2009.06.002
Baumann MJ, Eklof JM, Michel G, Kallas AM, Teeri TT, Czjzek M, Brumer H III (2007) Structural evidence for the evolution of xyloglucanase activity from xyloglucan endo-transglycosylases: biological implications for cell wall metabolism. Plant Cell 19:1947–1963. https://doi.org/10.1105/tpc.107.051391
Becnel J, Natarajan M, Kipp A, Braam J (2006) Developmental expression patterns of Arabidopsis xth genes reported by transgenes and genevestigator. Plant Mol Biol 61:451–467. https://doi.org/10.1007/s11103-006-0021-z
Behar H, Graham SW, Brumer H (2018) Comprehensive cross-genome survey and phylogeny of glycoside hydrolase family 16 members reveals the evolutionary origin of eg16 and xth proteins in plant lineages. Plant J 95:1114–1128. https://doi.org/10.1111/tpj.14004
Berry EA, Tran ML, Dimos CS, Budziszek MJ Jr, Scavuzzo-Duggan TR, Roberts AW (2016) Immuno and affinity cytochemical analysis of cell wall composition in the moss Physcomitrella patens. Front Plant Sci 7:248. https://doi.org/10.3389/fpls.2016.00248
Bogaert F, Marmonier A, Pichon E, Boissinot S, Ziegler-Graff V, Chesnais Q, Villeroy C, Drucker M, Brault V (2020) Impact of mutations in Arabidopsis thaliana metabolic pathways on polerovirus accumulation, aphid performance, and feeding behavior. Viruses 12:146. https://doi.org/10.3390/v12020146
Bowman JL, Kohchi T, Yamato KT et al (2017) Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171:287–304. https://doi.org/10.1016/j.cell.2017.09.030
Cao J, Lv YQ, Li X (2019) Interspaced repeat sequences confer the regulatory functions of AtXTH10, important for root growth in Arabidopsis. Plants 8:130. https://doi.org/10.3390/plants8050130
Carey AT, Holt K, Picard S, Wilde R, Tucker GA, Bird CR, Schuch W, Seymour GB (1995) Tomato exo-(1→4)-. β-D-galactanase: isolation, changes during ripening in normal and mutant tomato fruit, and characterization of a related cDNA clone. Plant Physiol 108:1099–1107. https://doi.org/10.1104/pp.108.3.1099
Cavalier DM, Keegstra K (2006) Two xyloglucan xylosyltransferases catalyze the addition of multiple xylosyl residues to cellohexaose. J Biol Chem 281:3419–34207. https://doi.org/10.1074/jbc.M606379200
Cavalier DM, Lerouxel O, Neumetzler L et al (2008) Disrupting two Arabidopsis thaliana xylosyltransferase genes results in plants deficient in xyloglucan, a major primary cell wall component. Plant Cell 20:1519–1537. https://doi.org/10.1105/tpc.108.059873
Cosgrove DJ (2014) Re-constructing our models of cellulose and primary cell wall assembly. Curr Opin Plant Biol 22:122–131. https://doi.org/10.1016/j.pbi.2014.11.001
Cosgrove DJ (2018) Nanoscale structure, mechanics and growth of epidermal cell walls. Curr Opin Plant Biol 46:77–86. https://doi.org/10.1016/j.pbi.2018.07.016
Culbertson AT, Ehrlich JJ, Choe JY, Honzatko RB, Zabotina OA (2018) Structure of xyloglucan xylosyltransferase 1 reveals simple steric rules that define biological patterns of xyloglucan polymers. Proc Natl Acad Sci USA 115:6064–6069. https://doi.org/10.1073/pnas.1801105115
Dick-Pérez M, Zhang Y, Hayes J, Salazar A, Zabotina OA, Hong M (2011) Structure and interactions of plant cell-wall polysaccharides by two- and three-dimensional magic-angle-spinning solid-state NMR. Biochemistry 50:989–1000. https://doi.org/10.1021/bi101795q
Dick-Perez M, Wang T, Salazar A, Zabotina OA, Hong M (2012) Multidimensional solid-state NMR studies of the structure and dynamics of pectic polysaccharides in uniformly 13C-labeled Arabidopsis primary cell walls. Magn Reson Chem 50:539–550. https://doi.org/10.1002/mrc.3836
Ding SY, Liu YS, Zeng Y, Himmel ME, Baker JO, Bayer EA (2012) How does plant cell wall nanoscale architecture correlate with enzymatic digestibility? Science 338:1055–1160. https://doi.org/10.1126/science.1227491
Divol F, Vilaine F, Thibivilliers S, Kusiak C, Sauge MH, Dinant S (2007) Involvement of the xyloglucan endotransglycosylase/hydrolases encoded by celery XTH1 and Arabidopsis XTH33 in the phloem response to aphids. Plant Cell Environ 30:187–201. https://doi.org/10.1111/j.1365-3040.2006.01618.x
Eklöf JM, Brumer H (2010) The XTH gene family: an update on enzyme structure, function, and phylogeny in xyloglucan remodeling. Plant Physiol 153:456–466. https://doi.org/10.1104/pp.110.156844
Eklöf JM, Shojania S, Okon M, McIntosh LP, Brumer H (2013) Structure-function analysis of a broad specificity Populus trichocarpa endo-β-glucanase reveals an evolutionary link between bacterial licheninases and plant XTH gene products. J Biol Chem 288:15786–15799. https://doi.org/10.1074/jbc.M113.462887
Endo A, Tatematsu K, Hanada K et al (2012) Tissue-specific transcriptome analysis reveals cell wall metabolism, flavonol biosynthesis and defense responses are activated in the endosperm of germinating Arabidopsis thaliana seeds. Plant Cell Physiol 53:16–27. https://doi.org/10.1093/pcp/pcr171
Fry SC (2011) Plant cell walls. From chemistry to biology. Ann Bot. https://doi.org/10.1093/aob/mcr128
Galstyan A, Nemhauser JL (2019) Auxin promotion of seedling growth via ARF5 is dependent on the brassinosteroid-regulated transcription factors BES1 and BEH4. Plant Direct 3:e00166. https://doi.org/10.1002/pld3.166
Genovesi V, Fornalé S, Fry SC, Ruel K, Ferrer P, Encina A, Sonbol FM, Bosch J, Puigdomènech P, Rigau J, Caparrós-Ruiz D (2008) ZmXTH1, a new xyloglucan endotransglucosylase/hydrolase in maize, affects cell wall structure and composition in Arabidopsis thaliana. J Exp Bot 59:875–889. https://doi.org/10.1093/jxb/ern013
Grantham NJ, Wurman-Rodrich J, Terrett OM et al (2017) An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls. Nat Plants 3:859–865. https://doi.org/10.1038/s41477-017-0030-8
Haas KT, Wightman R, Meyerowitz EM, Peaucelle A (2020) Pectin homogalacturonan nanofilament expansion drives morphogenesis in plant epidermal cells. Science 367:1003–1007. https://doi.org/10.1126/science.aaz5103
Han Y, Wang W, Sun J et al (2013) Populus Euphratica XTH overexpression enhances salinity tolerance by the development of leaf succulence in transgenic tobacco plants. J Exp Bot 64:4225–4238. https://doi.org/10.1093/jxb/ert229
Han Y, Ban Q, Li H et al (2016) DkXTH8, a novel xyloglucan endotransglucosylase/hydrolase in persimmon, alters cell wall structure and promotes leaf senescence and fruit postharvest softening. Sci Rep 6:39155. https://doi.org/10.1038/srep39155
Höfte H, Voxeur A (2017) Plant cell walls. Curr Biol 27:R865-870. https://doi.org/10.1016/j.cub.2017.05.025
Hrmova M, MacGregor EA, Biely P, Stewart RJ, Fincher GB (1998) Substrate binding and catalytic mechanism of a barley β-D-glucosidase/(1, 4)-β-D-glucan exohydrolase. J Biol Chem 273:11134–11143. https://doi.org/10.1074/jbc.273.18.11134
Ivakov A, Persson S (2013) Plant cell shape: modulators and measurements. Front Plant Sci 4:439. https://doi.org/10.3389/fpls.2013.00439
Jensen JK, Schultink A, Keegstra K, Wilkerson CG, Pauly M (2012) RNA-Seq analysis of developing nasturtium seeds (Tropaeolum majus): identification and characterization of an additional, galactosyltransferase involved in xyloglucan biosynthesis. Mol Plant 5:984–992. https://doi.org/10.1093/mp/sss032
Johansson P, Brumer H, Baumann MJ, Kallas ÅM, Henriksson H, Denman SE, Teeri TT, Jones TA (2004) Crystal structures of a poplar xyloglucan endotransglycosylase reveal details of transglycosylation acceptor binding. Plant Cell 16:874–886. https://doi.org/10.1105/tpc.020065
Kaewthai N, Gendre D, Eklöf JM, Ibatullin FM, Ezcurra I, Bhalerao RP, Brumer H (2013) Group III-A XTH genes of Arabidopsis encode predominant xyloglucan endohydrolases that are dispensable for normal growth. Plant Physiol 161:440–454. https://doi.org/10.1104/pp.112.207308
Kaku T, Tabuchi A, Wakabayashi K, Hoson T (2004) Xyloglucan oligosaccharides cause cell wall loosening by enhancing xyloglucan endotransglucosylase/hydrolase activity in azuki bean epicotyls. Plant Cell Physiol 45:77–82. https://doi.org/10.1093/pcp/pch007
Keegstra K (2010) Plant cell walls. Plant Physiol 154:483–486. https://doi.org/10.1104/pp.110.161240
Keegstra K, Talmadge KW, Bauer WD, Albersheim P (1973) The structure of plant cell walls: III. A model of the walls of suspension-cultured sycamore cells based on the interconnections of the macromolecular components. Plant Physiol 51:188–197. https://doi.org/10.1104/pp.51.1.188
Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJE (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845–858. https://doi.org/10.1038/nprot.2015.053
Kuki H, Yokoyama R, Kuroha T, Nishitani K (2020) Xyloglucan is not essential for the formation and integrity of the cellulose network in the primary cell wall regenerated from Arabidopsis protoplasts. Plants 9:629. https://doi.org/10.3390/plants9050629
Kurasawa K, Matsui A, Yokoyama R, Kuriyama T, Yoshizumi T, Matsui M, Suwabe K, Watanabe M, Nishitani K (2009) The AtXTH28 gene, a xyloglucan endotransglucosylase/hydrolase, is involved in automatic self-pollination in Arabidopsis thaliana. Plant Cell Physiol 50:413–422. https://doi.org/10.1093/pcp/pcp003
Kushwah S, Banasiak A, Nishikubo N et al (2020) Arabidopsis XTH4 and XTH9 contribute to wood cell expansion and secondary wall formation. Plant Physiol 182:1946–1965. https://doi.org/10.1104/pp.19.01529
Le MQ, Pagter M, Hincha DK (2015) Global changes in gene expression, assayed by microarray hybridization and quantitative RT-PCR, during acclimation of three Arabidopsis thaliana accessions to sub-zero temperatures after cold acclimation. Plant Mol Biol 87:1–15. https://doi.org/10.1007/s11103-014-0256-z
Lee D, Polisensky DH, Braam J (2005) Genome-wide identification of touch- and darkness-regulated Arabidopsis genes: a focus on calmodulin-like and XTH genes. New Phytol 165:429–444. https://doi.org/10.1111/j.1469-8137.2004.01238.x
Lima DU, Loh W, Buckeridge MS (2004) Xyloglucan–cellulose interaction depends on the sidechains and molecular weight of xyloglucan. Plant Physiol Biochem 42:389–394. https://doi.org/10.1016/j.plaphy.2004.03.003
Liu YB, Lu SM, Zhang JF, Liu S, Lu YT (2007) A xyloglucan endotransglucosylase/hydrolase involves in growth of primary root and alters the deposition of cellulose in Arabidopsis. Planta 226:1547–1560. https://doi.org/10.1007/s00425-007-0591-2
Madson M, Dunand C, Li XM, Verma R, Vanzin GF, Calplan J, Shoue DA, Carpita NC, Reiter WD (2003) The MUR3 gene of Arabidopsis encodes a xyloglucan galactosyltransferase that is evolutionarily related to animal exostosins. Plant Cell 15:1662–1670. https://doi.org/10.1105/tpc.009837
Maris A, Suslov D, Fry SC, Verbelen JP, Vissenberg K (2009) Enzymic characterization of two recombinant xyloglucan endotransglucosylase/hydrolase (XTH) proteins of Arabidopsis and their effect on root growth and cell wall extension. J Exp Bot 60:3959–3397. https://doi.org/10.1093/jxb/erp229
Maris A, Kaewthai N, Eklöf JM, Miller JG, Brumer H, Fry SC, Verbelen JP, Vissenberg K (2011) Differences in enzymic properties of five recombinant xyloglucan endotransglucosylase/hydrolase (XTH) proteins of Arabidopsis thaliana. J Exp Bot 62:261–271. https://doi.org/10.1093/jxb/erq263
Matsui A, Yokoyama R, Seki M, Ito T, Shinozaki K, Takahashi T, Komeda Y, Nishitani K (2005) AtXTH27 plays an essential role in cell wall modification during the development of tracheary elements. Plant J 42:525–534. https://doi.org/10.1111/j.1365-313X.2005.02395.x
McGregor N, Yin V, Tung CC, Van Petegem F, Brumer H (2017) Crystallographic insight into the evolutionary origins of xyloglucan endotransglycosylases and endohydrolases. Plant J 89:651–670. https://doi.org/10.1111/tpj.13421
Miedes E, Suslov D, Vandenbussche F, Kenobi K, Ivakov A, Van Der Straeten D, Lorences EP, Mellerowicz EJ, Verbelen JP, Vissenberg K (2013) Xyloglucan endotransglucosylase/hydrolase (XTH) overexpression affects growth and cell wall mechanics in etiolated Arabidopsis hypocotyls. J Exp Bot 64:2481–2497. https://doi.org/10.1093/jxb/ert107
Myśliwiec D, Chylińska M, Szymańska-Chargot M, Chibowski S, Zdunek A (2016) Revision of adsorption models of xyloglucan on microcrystalline cellulose. Cellulose 23:2819–2829. https://doi.org/10.1007/s10570-016-0995-x
Niraula PM, Lawrence KS, Klink VP (2020) The heterologous expression of a soybean (Glycine max) xyloglucan endotransglycosylase/hydrolase (XTH) in cotton (Gossypium hirsutum) suppresses parasitism by the root knot nematode Meloidogyne incognita. PLOS ONE 15:e0235344. https://doi.org/10.1371/journal.pone.0235344
Nishitani K, Demura T (2015) Editorial: an emerging view of plant cell walls as an apoplastic intelligent system. Plant Cell Physiol 56:177–179. https://doi.org/10.1093/pcp/pcv001
Notaguchi M, Kurotani K, Sato Y et al (2020) Cell-cell adhesion in plant grafting is facilitated by β-1,4-glucanases. Science 369:698–702. https://doi.org/10.1126/science.abc3710
Oehme DP, Doblin MS, Wagner J, Bacic A, Downton MT, Gidley MJ (2015) Gaining insight into cell wall cellulose macrofibril organisation by simulating microfibril adsorption. Cellulose 22:3501–3520. https://doi.org/10.1007/s10570-015-0778-9
One Thousand Plant Transcriptomes Initiative (2019) One thousand plant transcriptomes and the phylogenomics of green plants. Nature 574:679–685. https://doi.org/10.1038/s41586-019-1693-2
Osato Y, Yokoyama R, Nishitani K (2006) A principal role for AtXTH18 in Arabidopsis thaliana root growth: a functional analysis using RNAi plants. J Plant Res 119:153–162. https://doi.org/10.1007/s10265-006-0262-6
Park YB, Cosgrove DJ (2012) A revised architecture of primary cell walls based on biomechanical changes induced by substrate-specific endoglucanases. Plant Physiol 158:1933–1943. https://doi.org/10.1104/pp.111.192880
Pauly M, Keegstra K (2016) Biosynthesis of the plant cell wall matrix polysaccharide xyloglucan. Annu Rev Plant Biol 67:235–259. https://doi.org/10.1146/annurev-arplant-043015-112222
Pauly M, Vicente R (2018) New insights into wall polysaccharide O-acetylation. Front Plant Sci 9:1210. https://doi.org/10.3389/fpls.2018.01210
Peña MJ, Darvill AG, Eberhard S, York WS, O’Neill MA (2008) Moss and liverwort xyloglucans contain galacturonic acid and are structurally distinct from the xyloglucans synthesized by hornworts and vascular plants. Glycobiology 18:891–904. https://doi.org/10.1093/glycob/cwn078
Peña MJ, Kong Y, York WS, O’Neill MA (2012) A galacturonic acid–containing xyloglucan is involved in Arabidopsis root hair tip growth. Plant Cell 24:4511–4524. https://doi.org/10.1105/tpc.112.103390
Peng JS, Zhang BC, Chen H et al (2021) Galactosylation of rhamnogalacturonan-II for cell wall pectin biosynthesis is critical for root apoplastic iron reallocation in Arabidopsis. Mol Plant 14:1–12. https://doi.org/10.1016/j.molp.2021.06.016
Perrin RM, DeRocher AE, Bar-Peled M, Zeng W, Norambuena L, Orellana A, Raikhel NV, Keegstra K (1999) Xyloglucan fucosyltransferase, an enzyme involved in plant cell wall biosynthesis. Science 284:1976–1979. https://doi.org/10.1126/science.284.5422.1976
Pitaksaringkarn W, Matsuoka K, Asahina M et al (2014) XTH20 and XTH19 regulated by ANAC071 under auxin flow are involved in cell proliferation in incised Arabidopsis inflorescence stems. Plant J 80:604–614. https://doi.org/10.1111/tpj.12654
Pressey R (1983) Beta-galactosidases in ripening tomatoes. Plant Physiol 71:132–135. https://doi.org/10.1104/pp.71.1.132
Rose JK, Braam J, Fry SC, Nishitani K (2002) The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Plant Cell Physiol 43:1421–1435. https://doi.org/10.1093/pcp/pcf171
Sasidharan R, Chinnappa CC, Staal M, Elzenga JT, Yokoyama R, Nishitani K, Voesenek LACJ, Pieriket R (2010) Light quality-mediated petiole elongation in Arabidopsis during shade avoidance involves cell wall modification by xyloglucan endotransglucosylase/hydrolases. Plant Physiol 154:978–990. https://doi.org/10.1104/pp.110.162057
Schultink A, Cheng K, Park YB, Cosgrove DJ, Pauly M (2013) The identification of two arabinosyltransferases from tomato reveals functional equivalency of xyloglucan side chain substituents. Plant Physiol 163:86–94. https://doi.org/10.1104/pp.113.221788
Seven M, Derman ÜC, Harvey AJ (2021) Enzymatic characterization of ancestral/group-IV clade xyloglucan endotransglycosylase/hydrolase enzymes reveals broad substrate specificities. Plant J 106:1660–1673. https://doi.org/10.1111/tpj.15262
Shi H, Ye T, Zhong B, Liu X, Jin R, Chan Z (2014) AtHAP5A modulates freezing stress resistance in Arabidopsis through binding to CCAAT motif of AtXTH21. New Phytol 203:554–567. https://doi.org/10.1111/nph.12812
Shi YZ, Zhu XF, Miller JG, Gregson T, Zheng SJ, Fry SC (2015) Distinct catalytic capacities of two aluminium-repressed Arabidopsis thaliana xyloglucan endotransglucosylase/hydrolases, XTH15 and XTH31, heterologously produced in Pichia. Phytochemistry 112:160–169. https://doi.org/10.1016/j.phytochem.2014.09.020
Shinohara N, Nishitani K (2021) Cryogenian origin and subsequent diversification of the plant cell-wall enzyme XTH family. Plant Cell Physiol. https://doi.org/10.1093/pcp/pcab093
Shinohara N, Sunagawa N, Tamura S, Yokoyama R, Ueda M, Igarashi K, Nishitani K (2017) The plant cell-wall enzyme AtXTH3 catalyses covalent cross-linking between cellulose and cello-oligosaccharide. Sci Rep 7:1–10. https://doi.org/10.1038/srep46099
Simmons TJ, Mortimer JC, Bernardinelli OD, Pöppler AC, Brown SP, deAzevedo ER, Dupree R, Dupree P (2016) Folding of Xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR. Nature Commun 7:13902. https://doi.org/10.1038/ncomms13902
Takahashi D, Johnson KL, Hao P et al (2021) Cell wall modification by the xyloglucan endotransglucosylase/hydrolase XTH19 influences freezing tolerance after cold and sub-zero acclimation. Plant Cell Environ 44:915–930. https://doi.org/10.1111/pce.13953
Thimm JC, Burritt DJ, Ducker WA, Melton LD (2009) Pectins influence microfibril aggregation in celery cell walls: an atomic force microscopy study. J Struct Biol 168:337–344. https://doi.org/10.1016/j.jsb.2009.06.017
Van Sandt VS, Suslov D, Verbelen JP, Vissenberg K (2007) Xyloglucan endotransglucosylase activity loosens a plant cell wall. Ann Bot 100:1467–1473. https://doi.org/10.1093/aob/mcm248
Vissenberg K, Oyama M, Osato Y, Yokoyama R, Verbelen JP, Nishitani K (2005) Differential expression of AtXTH17, AtXTH18, AtXTH19 and AtXTH20 genes in Arabidopsis roots. Physiological roles in specification in cell wall construction. Plant Cell Physiol 46:192–200. https://doi.org/10.1093/pcp/pci013
Wang T, Hong M (2016) Solid-state NMR investigations of cellulose structure and interactions with matrix polysaccharides in plant primary cell walls. J Exp Bot 67:503–514. https://doi.org/10.1093/jxb/erv416
Wang T, Phyo P, Hong M (2016a) Multidimensional solid-state NMR spectroscopy of plant cell walls. Solid State Nucl Magn Reson 78:56–63. https://doi.org/10.1016/j.ssnmr.2016.08.001
Wang T, Yang H, Kubicki JD, Hong M (2016b) Cellulose structural polymorphism in plant primary cell walls investigated by high-field 2d solid-state NMR spectroscopy and density functional theory calculations. Biomacromol 17:2210–2222. https://doi.org/10.1021/acs.biomac.6b00441
Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An ‘electronic fluorescent pictograph’ browser for exploring and analyzing large-scale biological data sets. PLOS ONE 2:e718. https://doi.org/10.1371/journal.pone.0000718
Xu P, Cai W (2019) Nitrate-responsive OBP4-XTH9 regulatory module controls lateral root development in Arabidopsis thaliana. PLoS Genet 15:e1008465. https://doi.org/10.1371/journal.pgen.1008465
Xu H, Ding A, Chen S et al (2018) Genome-wide analysis of sorghum GT47 family reveals functional divergences of MUR3-like genes. Front Plant Sci 9:1773. https://doi.org/10.3389/fpls.2018.01773
Xu P, Fang S, Chen H, Cai W (2020) The brassinosteroid-responsive xyloglucan endotransglucosylase/hydrolase 19 (XTH19) and XTH23 genes are involved in lateral root development under salt stress in Arabidopsis. Plant J 104:59–75. https://doi.org/10.1111/tpj.14905
Yan J, Huang Y, He H et al (2019) Xyloglucan endotransglucosylase-hydrolase30 negatively affects salt tolerance in Arabidopsis. J Exp Bot 70:5495–5506. https://doi.org/10.1093/jxb/erz311
Yokoyama R, Nishitani K (2001) A comprehensive expression analysis of all members of a gene family encoding cell-wall enzymes allowed us to predict cis-regulatory regions involved in cell-wall construction in specific organs of Arabidopsis. Plant Cell Physiol 42:1025–1033. https://doi.org/10.1093/pcp/pce154
Yokoyama R, Rose JKC, Nishitani K (2004) A surprising diversity and abundance of xyloglucan endotransglucosylase/hydrolases in rice. Classification and expression analysis. Plant Physiol 134:1088–1099. https://doi.org/10.1104/pp.103.035261
Yokoyama R, Uwagaki Y, Sasaki H, Harada T, Hiwatashi Y, Hasebe M, Nishitani K (2010) Biological implications of the occurrence of 32 members of the XTH (xyloglucan endotransglucosylase/hydrolase) family of proteins in the bryophyte Physcomitrella patens. Plant J 64:645–656. https://doi.org/10.1111/j.1365-313X.2010.04351.x
York WS, Darvill AG, McNeil M, Stevenson TT, Albersheim P (1986) Isolation and characterization of plant cell walls and cell wall components. Methods Enzymol 118:3–40. https://doi.org/10.1016/0076-6879(86)18062-1
Zabotina OA, van de Ven WT, Freshour G et al (2008) Arabidopsis XXT5 gene encodes a putative α-1,6-xylosyltransferase that is involved in xyloglucan biosynthesis. Plant J 56:101–115. https://doi.org/10.1111/j.1365-313X.2008.03580.x
Zhang Y, Yu J, Wang X, Durachko DM, Zhang S, Cosgrove DJ (2021) Molecular insights into the complex mechanics of plant epidermal cell walls. Science 372:706–711. https://doi.org/10.1126/science.abf2824
Zheng Y, Wang X, Chen Y, Wagner E, Cosgrove DJ (2018) Xyloglucan in the primary cell wall: assessment by FESEM, selective enzyme digestions and nanogold affinity tags. Plant J 93:211–226. https://doi.org/10.1111/tpj.13778
Zheng S, Ren P, Zhai M, Li C, Chen Q (2021) Identification of genes involved in root growth inhibition under lead stress by transcriptome profiling in Arabidopsis. Plant Mol Biol Rep 39:50–59. https://doi.org/10.1007/s11105-020-01233-y
Zhu XF, Shi YZ, Lei GJ et al (2012) XTH31, encoding an in-vitro XEH/XET-active enzyme, controls Al sensitivity by modulating in-vivo XET action, cell wall xyloglucan content and Al binding capacity in Arabidopsis. Plant Cell 24:4731–4747. https://doi.org/10.1105/tpc.112.106039
Zhu L, Dama M, Pauly M (2018) Identification of an arabinopyranosyltransferase from Physcomitrella patens involved in the synthesis of the hemicellulose xyloglucan. Plant Direct 2:e00046. https://doi.org/10.1002/pld3.46
Zhu XF, Jiang XW, Ying S, Yuan ZS, Janet B, Gui XL, Shao JZ (2014) Xyloglucan Endotransglucosylase-Hydrolase17 Interacts with Xyloglucan Endotransglucosylase-Hydrolase31 to Confer Xyloglucan Endotransglucosylase Action and Affect Aluminum Sensitivity in Arabidopsis. Plant Physiol 165:1566–1574. https://doi.org/10.1104/pp.114.243790
Acknowledgements
We thank Dr. Yoshihisa Yoshimi and Dr. Paul Dupree at University of Cambridge for reading the manuscript critically and giving us valuable comments. K.I. also would like to thank Yuki Hata at Tohoku University for encouraging to write this manuscript. This work was supported by the Masayoshi-Son foundation (K.I.).
Author information
Authors and Affiliations
Contributions
KI and RY conceptualized and wrote this manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest associated with this manuscript.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ishida, K., Yokoyama, R. Reconsidering the function of the xyloglucan endotransglucosylase/hydrolase family. J Plant Res 135, 145–156 (2022). https://doi.org/10.1007/s10265-021-01361-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-021-01361-w