[en] The remarkable desiccation tolerance of the vegetative tissues in the resurrection species Craterostigma plantagineum (Hochst.) is favored by its unique cell wall folding mechanism that allows the ordered and reversible shrinking of the cells without damaging neither the cell wall nor the underlying plasma membrane. The ability to withstand extreme drought is also maintained in abscisic acid pre-treated calli, which can be cultured both on solid and in liquid culture media. Cell wall research has greatly advanced, thanks to the use of inhibitors affecting the biosynthesis of e.g., cellulose, since they allowed the identification of the compensatory mechanisms underlying habituation. Considering the innate cell wall plasticity of C. plantagineum, the goal of this investigation was to understand whether habituation to the cellulose biosynthesis inhibitors dichlobenil and isoxaben entailed or not identical mechanisms as known for non-resurrection species and to decipher the cell wall proteome of habituated cells. The results showed that exposure of C. plantagineum calli/cells triggered abnormal phenotypes, as reported in non-resurrection species. Additionally, the data demonstrated that it was possible to habituate Craterostigma cells to dichlobenil and isoxaben and that gene expression and protein abundance did not follow the same trend. Shotgun and gel-based proteomics revealed a common set of proteins induced upon habituation, but also identified candidates solely induced by habituation to one of the two inhibitors. Finally, it is hypothesized that alterations in auxin levels are responsible for the increased abundance of cell wall-related proteins upon habituation.
Guerriero, Gea ; Environmental Research and Innovation Department, Luxembourg Institute of Science and Technology, 5, Rue Bommel, L-4940 Hautcharage, Luxembourg
Achen, Charles; Environmental Research and Innovation Department, Luxembourg Institute of Science and Technology, 41, Rue du Brill, L-4422 Belvaux, Luxembourg
Xu, Xuan ; Environmental Research and Innovation Department, Luxembourg Institute of Science and Technology, 5, Rue Bommel, L-4940 Hautcharage, Luxembourg
Planchon, Sébastien ; Environmental Research and Innovation Department, Luxembourg Institute of Science and Technology, 41, Rue du Brill, L-4422 Belvaux, Luxembourg
Leclercq, Céline C ; Environmental Research and Innovation Department, Luxembourg Institute of Science and Technology, 41, Rue du Brill, L-4422 Belvaux, Luxembourg
Sergeant, Kjell ; Environmental Research and Innovation Department, Luxembourg Institute of Science and Technology, 5, Rue Bommel, L-4940 Hautcharage, Luxembourg
Berni, Roberto ; Université de Liège - ULiège > TERRA Research Centre > Echanges Eau - Sol - Plantes
Hausman, Jean-Francois ; Environmental Research and Innovation Department, Luxembourg Institute of Science and Technology, 5, Rue Bommel, L-4940 Hautcharage, Luxembourg
Renaut, Jenny ; Environmental Research and Innovation Department, Luxembourg Institute of Science and Technology, 41, Rue du Brill, L-4422 Belvaux, Luxembourg
Legay, Sylvain; Environmental Research and Innovation Department, Luxembourg Institute of Science and Technology, 5, Rue Bommel, L-4940 Hautcharage, Luxembourg
Language :
English
Title :
The Cell Wall Proteome of Craterostigma plantagineum Cell Cultures Habituated to Dichlobenil and Isoxaben.
Bartels, D.; Hussain, S.S. Resurrection Plants: Physiology and molecular biology. In Plant Desiccation Tolerance; Ecological Studies; Lüttge, U., Beck, E., Bartels, D., Eds.; Springer: Berlin/Heidelberg, Germany, 2011; pp. 139–156, ISBN 978‐3‐642‐19106‐0.
Chen, P.; Jung, N.U.; Giarola, V.; Bartels, D. The Dynamic Responses of Cell Walls in Resurrection Plants during Dehydration and Rehydration. Front. Plant Sci. 2020, 10, 1698, doi:10.3389/fpls.2019.01698.
Bartels, D.; Schneider, K.; Terstappen, G.; Piatkowski, D.; Salamini, F. Molecular cloning of abscisic acid‐modulated genes which are induced during desiccation of the resurrection plant Craterostigma plantagineum. Planta 1990, 181, 27–34, doi:10.1007/bf00202321.
Vicré, M.; Sherwin, H.; Driouich, A.; Jaffer, M.; Farrant, J. Cell Wall Characteristics and Structure of Hydrated and Dry leaves of the Resurrection Plant Craterostigma wilmsii, a Microscopical Study. J. Plant Physiol. 1999, 155, 719–726, doi:10.1016/s0176‐ 1617(99)80088‐1.
Vicre, M.; Lerouxel, O.; Farrant, J.; Lerouge, P.; Driouich, A. Composition and desiccation‐induced alterations of the cell wall in the resurrection plant Craterostigma wilmsii. Physiol. Plant. 2004, 120, 229–239, doi:10.1111/j.0031‐9317.2004.0234.x.
Moore, J.; Nguema‐Ona, E.; Chevalier, L.; Lindsey, G.G.; Brandt, W.F.; Lerouge, P.; Farrant, J.; Driouich, A. Response of the Leaf Cell Wall to Desiccation in the Resurrection Plant Myrothamnus flabellifolius. Plant Physiol. 2006, 141, 651–662, doi:10.1104/pp.106.077701.
Moore, J.P.; Farrant, J.; Driouich, A. A role for pectin‐associated arabinans in maintaining the flexibility of the plant cell wall during water deficit stress. Plant Signal. Behav. 2008, 3, 102–104, doi:10.4161/psb.3.2.4959.
Jung, N.U.; Giarola, V.; Chen, P.; Knox, J.P.; Bartels, D. Craterostigma plantagineum cell wall composition is remodelled during desiccation and the glycine‐rich protein CpGRP1 interacts with pectins through clustered arginines. Plant J. 2019, 100, 661–676, doi:10.1111/tpj.14479.
Moore, J.P.; Nguema‐Ona, E.E.; Vicré‐Gibouin, M.; Sørensen, I.; Willats, W.; Driouich, A.; Farrant, J. Arabinose‐rich polymers as an evolutionary strategy to plasticize resurrection plant cell walls against desiccation. Planta 2012, 237, 739–754, doi:10.1007/s00425‐012‐1785‐9.
Le Gall, H.; Philippe, F.; Domon, J.‐M.; Gillet, F.; Pelloux, J.; Rayon, C. Cell Wall Metabolism in Response to Abiotic Stress. Plants 2015, 4, 112–166, doi:10.3390/plants4010112.
Tenhaken, R. Cell wall remodeling under abiotic stress. Front. Plant Sci. 2015, 5, 771–771, doi:10.3389/fpls.2014.00771.
Willats, W.; Orfila, C.; Limberg, G.; Buchholt, H.C.; van Alebeek, G.‐J.W.M.; Voragen, A.G.J.; Marcus, S.E.; Christensen, T.M.I.E.; Mikkelsen, J.D.; Murray, B.S.; et al. Modulation of the degree and pattern of methyl‐esterification of Pectic Homogalacturonan in plant cell walls: Implications for pectin methyl esterase action, matrix properties, and cell adhesion. J. Biol. Chem. 2001, 276, 19404–19413, doi:10.1074/jbc.m011242200.
Wu, H.‐C.; Bulgakov, V.; Jinn, T.‐L. Pectin Methylesterases: Cell Wall Remodeling Proteins Are Required for Plant Response to Heat Stress. Front. Plant Sci. 2018, 9, 1612, doi:10.3389/fpls.2018.01612.
Moura, J.C.M.S.; Bonine, C.A.V.; Viana, J.D.O.F.; Dornelas, M.C.; Mazzafera, P. Abiotic and Biotic Stresses and Changes in the Lignin Content and Composition in Plants. J. Integr. Plant Biol. 2010, 52, 360–376, doi:10.1111/j.1744‐7909.2010.00892.x.
Hamann, T. The Plant Cell Wall Integrity Maintenance Mechanism—Concepts for Organization and Mode of Action. Plant Cell Physiol. 2014, 56, 215–223, doi:10.1093/pcp/pcu164.
Rui, Y.; Dinneny, J.R. A wall with integrity: Surveillance and maintenance of the plant cell wall under stress. New Phytol. 2019, 225, 1428–1439, doi:10.1111/nph.16166.
Duval, I.; Beaudoin, N. Transcriptional profiling in response to inhibition of cellulose synthesis by thaxtomin A and isoxaben in Arabidopsis thaliana suspension cells. Plant Cell Rep. 2009, 28, 811–830, doi:10.1007/s00299‐009‐0670‐x.
Wormit, A.; Butt, S.M.; Chairam, I.; McKenna, J.; Nunes‐Nesi, A.; Kjaer, L.; O’Donnelly, K.; Fernie, A.R.; Woscholski, R.; Barter, M.L.; et al. Osmosensitive Changes of Carbohydrate Metabolism in Response to Cellulose Biosynthesis Inhibition. Plant Physiol. 2012, 159, 105–117, doi:10.1104/pp.112.195198.
Mélida, H.; Encina, A.; Álvarez, J.; Acebes, J.‐L.; Caparrós‐Ruiz, D. Unraveling the Biochemical and Molecular Networks Involved in Maize Cell Habituation to the Cellulose Biosynthesis Inhibitor Dichlobenil. Mol. Plant 2010, 3, 842–853, doi:10.1093/mp/ssq027.
De Castro, M.; Largo‐Gosens, A.; Alvarez, J.M.; García‐Angulo, P.; Acebes, J.L. Early cell‐wall modifications of maize cell cultures during habituation to dichlobenil. J. Plant Physiol. 2014, 171, 127–135, doi:10.1016/j.jplph.2013.10.010.
Encina, A.; Moral, R.M.; Acebes, J.‐L.; Álvarez, J.M. Characterization of cell walls in bean (Phaseolus vulgaris L.) callus cultures tolerant to dichlobenil. Plant Sci. 2001, 160, 331–339, doi:10.1016/s0168‐9452(00)00397‐6.
Encina, A.; Sevillano, J.M.; Acebes, J.‐L.; Alvarez, J. Cell wall modifications of bean (Phaseolus vulgaris) cell suspensions during habituation and dehabituation to dichlobenil. Physiol. Plant. 2002, 114, 182–191, doi:10.1034/j.1399‐3054.2002.1140204.x.
Tateno, M.; Brabham, C.; DeBolt, S. Cellulose biosynthesis inhibitors—A multifunctional toolbox. J. Exp. Bot. 2015, 67, 533–542, doi:10.1093/jxb/erv489.
DeBolt, S.; Gutierrez, R.; Ehrhardt, D.W.; Somerville, C. Nonmotile Cellulose Synthase Subunits Repeatedly Accumulate within Localized Regions at the Plasma Membrane in Arabidopsis Hypocotyl Cells following 2,6‐Dichlorobenzonitrile Treatment. Plant Physiol. 2007, 145, 334–338, doi:10.1104/pp.107.104703.
Anderson, J.R.; Barnes, W.S.; Bedinger, P. 2,6‐Dichlorobenzonitrile, a cellulose biosynthesis inhibitor, affects morphology and structural integrity of Petunia and lily pollen tubes. J. Plant Physiol. 2002, 159, 61–67, doi:10.1078/0176‐1617‐00651.
Lazzaro, M.D.; Donohue, J.M.; Soodavar, F.M. Disruption of cellulose synthesis by isoxaben causes tip swelling and disorgan-izes cortical microtubules in elongating conifer pollen tubes. Protoplasma 2003, 220, 201–207, doi:10.1007/s00709‐002‐0042‐7.
Díaz‐Cacho, P.; Moral, R.; Encina, A.; Acebes, J.‐L.; Alvarez, J. Cell wall modifications in bean (Phaseolus vulgaris) callus cultures tolerant to isoxaben. Physiol. Plant. 1999, 107, 54–59, doi:10.1034/j.1399‐3054.1999.100108.x.
Mélida, H.; García‐Angulo, P.; Alonso‐Simón, A.; Encina, A.; Alvarez, J.; Acebes, J.L. Novel type II cell wall architecture in dichlobenil‐habituated maize calluses. Planta 2008, 229, 617–631, doi:10.1007/s00425‐008‐0860‐8.
Murashige, T.; Skoog, F. A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures. Physiol. Plant. 1962, 15, 473–497, doi:10.1111/j.1399‐3054.1962.tb08052.x.
O., T.; S., T.; T., P.; P., S. An effective and reproducible transformation protocol for the model resurrection plant Craterostigma plantagineum Hochst. Plant Cell Rep. 2002, 21, 63–69, doi:10.1007/s00299‐002‐0479‐3.
Pettolino, F.; Walsh, C.; Fincher, G.B.; Bacic, A. Determining the polysaccharide composition of plant cell walls. Nat. Protoc. 2012, 7, 1590–1607, doi:10.1038/nprot.2012.081.
Xu, X.; Backes, A.; Legay, S.; Berni, R.; Faleri, C.; Gatti, E.; Hausman, J.‐F.; Cai, G.; Guerriero, G. Cell wall composition and transcriptomics in stem tissues of stinging nettle (Urtica dioica L.): Spotlight on a neglected fibre crop. Plant Direct 2019, 3, e00151, doi:10.1002/pld3.151.
Behr, M.; Sergeant, K.; Leclercq, C.C.; Planchon, S.; Guignard, C.; Lenouvel, A.; Renaut, J.; Hausman, J.‐F.; Lutts, S.; Guerriero, G. Insights into the molecular regulation of monolignol‐derived product biosynthesis in the growing hemp hypocotyl. BMC Plant Biol. 2018, 18, 1–18, doi:10.1186/s12870‐017‐1213‐1.
Backes, A.; Behr, M.; Xu, X.; Gatti, E.; Legay, S.; Predieri, S.; Hausman, J.‐F.; Deyholos, M.K.; Cai, G.; Guerriero, G. Sucrose synthase gene expression analysis in the fibre nettle (Urtica dioica L.) cultivar “clone 13”. Ind. Crop. Prod. 2018, 123, 315–322, doi:10.1016/j.indcrop.2018.06.090.
Sergeant, K.; Printz, B.; Guerriero, G.; Renaut, J.; Lutts, S.; Hausman, J.‐F. The Dynamics of the Cell Wall Proteome of Developing Alfalfa Stems. Biology 2019, 8, 60, doi:10.3390/biology8030060.
Xu, X.; Legay, S.; Sergeant, K.; Zorzan, S.; Leclercq, C.C.; Charton, S.; Giarola, V.; Liu, X.; Challabathula, D.; Renaut, J.; et al. Molecular insights into plant desiccation tolerance: Transcriptomics, proteomics and targeted metabolite profiling in Craterostigma plantagineum. Plant J. 2021, doi:10.1111/tpj.15294.
Armenteros, J.J.A.; Sønderby, C.K.; Sønderby, S.K.; Nielsen, H.; Winther, O. DeepLoc: Prediction of protein subcellular localization using deep learning. Bioinformatics 2017, 33, 3387–3395, doi:10.1093/bioinformatics/btx431.
Vizcaíno, J.A.; Csordas, A.; Del‐Toro, N.; Dianes, J.A.; Griss, J.; Lavidas, I.; Mayer, G.; Perez‐Riverol, Y.; Reisinger, F.; Ternent, T.; et al. 2016 update of the PRIDE database and its related tools. Nucleic Acids Res. 2015, 44, D447–D456, doi:10.1093/nar/gkv1145.
Untergasser, A.; Nijveen, H.; Rao, X.; Bisseling, T.; Geurts, R.; Leunissen, J.A.M. Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res. 2007, 35, W71–W74, doi:10.1093/nar/gkm306.
Giarola, V.; Challabathula, D.; Bartels, D. Quantification of expression of dehydrin isoforms in the desiccation tolerant plant Craterostigma plantagineum using specifically designed reference genes. Plant Sci. 2015, 236, 103–115, doi:10.1016/j.plantsci.2015.03.014.
Printz, B.; Morais, R.D.S.; Wienkoop, S.; Sergeant, K.; Lutts, S.; Hausman, J.‐F.; Renaut, J. An improved protocol to study the plant cell wall proteome. Front. Plant Sci. 2015, 6, 237, doi:10.3389/fpls.2015.00237.
Metsalu, T.; Vilo, J. ClustVis: A web tool for visualizing clustering of multivariate data using Principal Component Analysis and heatmap. Nucleic Acids Res. 2015, 43, W566–W570, doi:10.1093/nar/gkv468.
Alonso‐Simón, A.; García‐Angulo, P.; Encina, A.; Acebes, J.L.; Álvarez, J. Habituation of Bean (Phaseolus vulgaris) Cell Cultures to Quinclorac and Analysis of the Subsequent Cell Wall Modifications. Ann. Bot. 2008, 101, 1329–1339, doi:10.1093/aob/mcn051.
Brochu, V.; Girard‐Martel, M.; Duval, I.; Lerat, S.; Grondin, G.; Domingue, O.; Beaulieu, C.; Beaudoin, N. Habituation to thax-tomin A in hybrid poplar cell suspensions provides enhanced and durable resistance to inhibitors of cellulose synthesis. BMC Plant Biol. 2010, 10, 1–16, doi:10.1186/1471‐2229‐10‐272.
Menna, A.; Fischer‐Stettler, M.; Pfister, B.; Andrés, G.S.; Holbrook‐Smith, D.; Sánchez‐Rodríguez, C. Single‐run HPLC Quanti-fication of Plant Cell Wall Monosaccharides. Bio‐Protocol 2020, 10, doi:10.21769/bioprotoc.3546.
Lagrimini, L.M.; Burkhart, W.; Moyer, M.; Rothstein, S. Molecular cloning of complementary DNA encoding the lignin‐forming peroxidase from tobacco: Molecular analysis and tissue‐specific expression. Proc. Natl. Acad. Sci. USA 1987, 84, 7542–7546, doi:10.1073/pnas.84.21.7542.
Kukavica, B.M.; Veljovicć‐Jovanovicć, S.D.; Menckhoff, L.; Lüthje, S. Cell wall‐bound cationic and anionic class III isoperoxi-dases of pea root: Biochemical characterization and function in root growth. J. Exp. Bot. 2012, 63, 4631–4645, doi:10.1093/jxb/ers139.
Tegg, R.S.; Shabala, S.N.; Cuin, T.; Davies, N.W.; Wilson, C.R. Enhanced resistance to the cellulose biosynthetic inhibitors, thax-tomin A and isoxaben in Arabidopsis thaliana mutants, also provides specific co‐resistance to the auxin transport inhibitor, 1‐ NPA. BMC Plant Biol. 2013, 13, 1–10, doi:10.1186/1471‐2229‐13‐76.
Carpin, S.; Crèvecoeur, M.; Greppin, H.; Penel, C. Molecular Cloning and Tissue‐Specific Expression of an Anionic Peroxidase in Zucchini1. Plant Physiol. 1999, 120, 799–810, doi:10.1104/pp.120.3.799.
Lagrimini, L.M.; Gingas, V.; Finger, F.; Rothstein, S.; Liu, T. Characterization of Antisense Transformed Plants Deficient in the Tobacco Anionic Peroxidase. Plant Physiol. 1997, 114, 1187–1196, doi:10.1104/pp.114.4.1187.
Cosio, C.; Vuillemin, L.; De Meyer, M.; Kevers, C.; Penel, C.; Dunand, C. An anionic class III peroxidase from zucchini may regulate hypocotyl elongation through its auxin oxidase activity. Planta 2009, 229, 823–836, doi:10.1007/s00425‐008‐0876‐0.
Lehman, T.A.; Sanguinet, K. Auxin and Cell Wall Crosstalk as Revealed by the Arabidopsis thaliana Cellulose Synthase Mutant Radially Swollen 1. Plant Cell Physiol. 2019, 60, 1487–1503, doi:10.1093/pcp/pcz055.
Lagrimini, L.M. Wound‐Induced Deposition of Polyphenols in Transgenic Plants Overexpressing Peroxidase. Plant Physiol. 1991, 96, 577–583, doi:10.1104/pp.96.2.577.
Yang, Y.; Jiang, R.; Wang, H.; Tian, Z.; Xie, C. StPOPA, encoding an anionic peroxidase, enhances potato resistance against Phytophthora infestans. Mol. Breed. 2020, 40, 16, doi:10.1007/s11032‐019‐1093‐1.
Gigli‐Bisceglia, N.; Engelsdorf, T.; Hamann, T. Plant cell wall integrity maintenance in model plants and crop species‐relevant cell wall components and underlying guiding principles. Cell. Mol. Life Sci. 2019, 77, 2049–2077, doi:10.1007/s00018‐019‐03388‐ 8.
Rayle, D.L.; Cleland, R. The Acid Growth Theory of auxin‐induced cell elongation is alive and well. Plant Physiol. 1992, 99, 1271– 1274, doi:10.1104/pp.99.4.1271.
Hensel, A.; Brummell, D.; Hanna, R.; MacLachlan, G. Auxin‐dependent breakdown of xyloglucan in cotyledons of germinating Nasturtium seeds. Planta 1991, 183, 321–326, doi:10.1007/bf00197728.
Du, M.; Spalding, E.P.; Gray, W. Rapid Auxin‐Mediated Cell Expansion. Annu. Rev. Plant Biol. 2020, 71, 379–402, doi:10.1146/an-nurev‐arplant‐073019‐025907.
Majda, M.; Robert, S. The Role of Auxin in Cell Wall Expansion. Int. J. Mol. Sci. 2018, 19, 951, doi:10.3390/ijms19040951.
Rodriguez, M.C.S.; Edsgard, S.D.; Hussain, S.S.; Alquezar, D.; Rasmussen, M.; Gilbert, M.; Nielsen, H.B.; Bartels, D.; Mundy, J. Transcriptomes of the desiccation‐tolerant resurrection plant Craterostigma plantagineum. Plant J. 2010, 63, 212–228, doi:10.1111/j.1365‐313x.2010.04243.x.
Solomon, M.; Belenghi, B.; Delledonne, M.; Menachem, E.; Levine, A. The Involvement of Cysteine Proteases and Protease Inhibitor Genes in the Regulation of Programmed Cell Death in Plants. Plant Cell 1999, 11, 431–443, doi:10.1105/tpc.11.3.431.
Giarola, V.; Krey, S.; Frerichs, A.; Bartels, D. Taxonomically restricted genes of Craterostigma plantagineum are modulated in their expression during dehydration and rehydration. Planta 2014, 241, 193–208, doi:10.1007/s00425‐014‐2175‐2.
Hamann, T.; Bennett, M.; Mansfield, J.; Somerville, C. Identification of cell‐wall stress as a hexose‐dependent and osmosensitive regulator of plant responses. Plant J. 2009, 57, 1015–1026, doi:10.1111/j.1365‐313x.2008.03744.x.
Li, W.; Zhao, F.; Fang, W.; Xie, D.; Hou, J.; Yang, X.; Zhao, Y.; Tang, Z.; Nie, L.; Lv, S. Identification of early salt stress responsive proteins in seedling roots of upland cotton (Gossypium hirsutum L.) employing iTRAQ‐based proteomic technique. Front. Plant Sci. 2015, 6, 732, doi:10.3389/fpls.2015.00732.
Giarola, V.; Jung, N.U.; Singh, A.; Satpathy, P.; Bartels, D. Analysis of pcC13‐62 promoters predicts a link between cis‐element variations and desiccation tolerance in Linderniaceae. J. Exp. Bot. 2018, 69, 3773–3784, doi:10.1093/jxb/ery173.
Giarola, V.; Chen, P.; Dulitz, S.J.; König, M.; Manduzio, S.; Bartels, D. The dehydration‐ and ABA‐inducible germin‐like protein CpGLP1 from Craterostigma plantagineum has SOD activity and may contribute to cell wall integrity during desiccation. Planta 2020, 252, 1–13, doi:10.1007/s00425‐020‐03485‐0.
Sánchez‐Cortés, J.; Mrksich, M. The Platelet Integrin αIIbβ3 Binds to the RGD and AGD Motifs in Fibrinogen. Chem. Biol. 2009, 16, 990–1000, doi:10.1016/j.chembiol.2009.08.012.
Nakagawa, N.; Sakurai, N. Increase in the amount of celA1 protein in tobacco BY‐2 cells by a cellulose biosynthesis inhibitor, 2,6‐dichlorobenzonitrile.. Plant Cell Physiol. 1998, 39, 779–785, doi:10.1093/oxfordjournals.pcp.a029434.
Gutierrez, R.; Lindeboom, J.J.; Paredez, A.; Emons, A.M.C.; Ehrhardt, D.W. Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat. Cell Biol. 2009, 11, 797–806, doi:10.1038/ncb1886.
Wu, J.; Steinebrunner, I.; Sun, Y.; Butterfield, T.; Torres, J.; Arnold, D.; Gonzalez, A.; Jacob, F.; Reichler, S.; Roux, S.J. Apyrases (Nucleoside Triphosphate‐Diphosphohydrolases) Play a Key Role in Growth Control in Arabidopsis. Plant Physiol. 2007, 144, 961–975, doi:10.1104/pp.107.097568.
Lim, M.H.; Wu, J.; Yao, J.; Gallardo, I.F.; Dugger, J.; Webb, L.J.; Huang, J.; Salmi, M.; Song, J.; Clark, G.; et al. Apyrase Suppres-sion Raises Extracellular ATP Levels and Induces Gene Expression and Cell Wall Changes Characteristic of Stress Responses. Plant Physiol. 2014, 164, 2054–2067, doi:10.1104/pp.113.233429.
Maeda, M.; Kimura, Y. Structural features of free N‐glycans occurring in plants and functional features of de‐N‐glycosylation enzymes, ENGase, and PNGase: The presence of unusual plant complex type N‐glycans. Front. Plant Sci. 2014, 5, 429, doi:10.3389/fpls.2014.00429.
Chang, T.; Kuo, M.‐C.; Khoo, K.‐H.; Inoue, S.; Inoue, Y. Developmentally Regulated Expression of a Peptide:N‐Glycanase during Germination of Rice Seeds (Oryza sativa) and Its Purification and Characterization. J. Biol. Chem. 2000, 275, 129–134, doi:10.1074/jbc.275.1.129.
Herger, A.; Dünser, K.; Kleine‐Vehn, J.; Ringli, C. Leucine‐Rich Repeat Extensin Proteins and Their Role in Cell Wall Sensing. Curr. Biol. 2019, 29, R851–R858, doi:10.1016/j.cub.2019.07.039.
Liu, F.; Zhang, X.; Lu, C.; Zeng, X.; Li, Y.; Fu, D.; Wu, G. Non‐specific lipid transfer proteins in plants: Presenting new advances and an integrated functional analysis. J. Exp. Bot. 2015, 66, 5663–5681, doi:10.1093/jxb/erv313.
Engelen, F.A.; Hartog, M.V.; Thomas, T.L.; Taylor, B.; Sturm, A.; Van Kammen, A.; Vries, S.C. The carrot secreted glycoprotein gene EP1 is expressed in the epidermis and has sequence homology to Brassica S‐locus glycoproteins. Plant J. 1993, 4, 855–862, doi:10.1046/j.1365‐313x.1993.04050855.x.
Hove, C.A.T.; Bochdanovits, Z.; Jansweijer, V.M.A.; Koning, F.G.; Berke, L.; Sanchez‐Perez, G.; Scheres, B.; Heidstra, R. Probing the roles of LRR RLK genes in Arabidopsis thaliana roots using a custom T‐DNA insertion set. Plant Mol. Biol. 2011, 76, 69–83, doi:10.1007/s11103‐011‐9769‐x.
Wang, J.; Kucukoglu, M.; Zhang, L.; Chen, P.; Decker, D.; Nilsson, O.; Jones, B.; Sandberg, G.; Zheng, B. The Arabidopsis LRR‐ RLK, PXC1, is a regulator of secondary wall formation correlated with the TDIF‐PXY/TDR‐WOX4 signaling pathway. BMC Plant Biol. 2013, 13, 1–11, doi:10.1186/1471‐2229‐13‐94.
