Chitosan stimulates root hair callose deposition, endomembrane dynamics, and inhibits root hair growth
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
CZ.02.01.01/00/22_008/0004581
Ministerstvo Školství, Mládeže a Tělovýchovy
8J19FR001
Ministerstvo Školství, Mládeže a Tělovýchovy
LM2023050Czech-BioImaging
Ministerstvo Školství, Mládeže a Tělovýchovy
415322
Grantová Agentura, Univerzita Karlova
287423
Grantová Agentura, Univerzita Karlova
20-11642S
Grantová Agentura České Republiky
803048
European Research Council - International
PubMed
39267452
PubMed Central
PMC11615431
DOI
10.1111/pce.15111
Knihovny.cz E-zdroje
- Klíčová slova
- arabidopsis, cell wall, defence, gene expression, signalling,
- MeSH
- Arabidopsis * růst a vývoj účinky léků metabolismus fyziologie MeSH
- buněčná membrána metabolismus MeSH
- buněčná stěna * metabolismus MeSH
- chitosan * farmakologie MeSH
- glukany * metabolismus MeSH
- glukosyltransferasy metabolismus MeSH
- kořeny rostlin * růst a vývoj metabolismus účinky léků MeSH
- proteiny huseníčku * metabolismus genetika MeSH
- regulace genové exprese u rostlin účinky léků MeSH
- vápník metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- callose MeSH Prohlížeč
- chitosan * MeSH
- glukany * MeSH
- glukosyltransferasy MeSH
- proteiny huseníčku * MeSH
- vápník MeSH
Although angiosperm plants generally react to immunity elicitors like chitin or chitosan by the cell wall callose deposition, this response in particular cell types, especially upon chitosan treatment, is not fully understood. Here we show that the growing root hairs (RHs) of Arabidopsis can respond to a mild (0.001%) chitosan treatment by the callose deposition and by a deceleration of the RH growth. We demonstrate that the glucan synthase-like 5/PMR4 is vital for chitosan-induced callose deposition but not for RH growth inhibition. Upon the higher chitosan concentration (0.01%) treatment, RHs do not deposit callose, while growth inhibition is prominent. To understand the molecular and cellular mechanisms underpinning the responses to two chitosan treatments, we analysed early Ca2+ and defence-related signalling, gene expression, cell wall and RH cellular endomembrane modifications. Chitosan-induced callose deposition is also present in the several other plant species, including functionally analogous and evolutionarily only distantly related RH-like structures such as rhizoids of bryophytes. Our results point to the RH callose deposition as a conserved strategy of soil-anchoring plant cells to cope with mild biotic stress. However, high chitosan concentration prominently disturbs RH intracellular dynamics, tip-localised endomembrane compartments, growth and viability, precluding callose deposition.
Institute of Experimental Botany of the Czech Academy of Sciences Prague 6 Czech Republic
Université Paris Saclay INRAE AgroParisTech Institut Jean Pierre Bourgin Versailles France
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Aslam, S.N. , Erbs, G. , Morrissey, K.L. , Newman, M.‐A. , Chinchilla, D. , Boller, T. et al. (2009) Microbe‐associated molecular pattern (MAMP) signatures, synergy, size and charge: influences on perception or mobility and host defence responses. Molecular Plant Pathology, 10, 375–387. Available from: 10.1111/j.1364-3703.2009.00537.x PubMed DOI PMC
Badri, D.V. , Loyola‐Vargas, V.M. , Du, J. , Stermitz, F.R. , Broeckling, C.D. , Iglesias‐Andreu, L. et al. (2008) Transcriptome analysis of arabidopsis roots treated with signaling compounds: a focus on signal transduction, metabolic regulation and secretion. New Phytologist, 179, 209–223. Available from: 10.1111/j.1469-8137.2008.02458.x PubMed DOI
Baluška, F. , Salaj, J. , Mathur, J. , Braun, M. , Jasper, F. , Šamaj, J. et al. (2000) Root hair formation: F‐actin‐dependent tip growth is initiated by local assembly of profilin‐supported F‐actin meshworks accumulated within expansin‐enriched bulges. Developmental Biology, 227, 618–632. Available from: 10.1006/dbio.2000.9908 PubMed DOI
Baumberger, N. , Steiner, M. , Ryser, U. , Keller, B. & Ringli, C. (2003) Synergistic interaction of the two paralogous arabidopsis genes LRX1 and LRX2 in cell wall formation during root hair development. The Plant Journal, 35, 71–81. Available from: 10.1046/j.1365-313x.2003.01784.x PubMed DOI
Brejšková, L. , Hála, M. , Rawat, A. , Soukupová, H. , Cvrčková, F. , Charlot, F. et al. (2021) SEC6 exocyst subunit contributes to multiple steps of growth and development ofPhyscomitrella(Physcomitrium patens). The Plant Journal, 106, 831–843. Available from: 10.1111/tpj.15205 PubMed DOI
Brost, C. , Studtrucker, T. , Reimann, R. , Denninger, P. , Czekalla, J. , Krebs, M. et al. (2019) Multiple cyclic nucleotide‐gated channels coordinate calcium oscillations and polar growth of root hairs. The Plant Journal, 99, 910–923. Available from: 10.1111/tpj.14371 PubMed DOI
Cai, G. , Faleri, C. , Del Casino, C. , Emons, A.M.C. & Cresti, M. (2011) Distribution of callose synthase, cellulose synthase, and sucrose synthase in tobacco pollen tube is controlled in dissimilar ways by actin filaments and microtubules. Plant Physiology, 155, 1169–1190. Available from: 10.1104/pp.110.171371 PubMed DOI PMC
Carol, R.J. & Dolan, L. (2002) Building a hair: tip growth in Arabidopsis thaliana root hairs. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 357, 815–821. Available from: 10.1098/rstb.2002.1092 PubMed DOI PMC
Cavalier, D.M. , Lerouxel, O. , Neumetzler, L. , Yamauchi, K. , Reinecke, A. , Freshour, G. et al. (2008) Disrupting two Arabidopsis thaliana xylosyltransferase genes results in plants deficient in xyloglucan, a major primary cell wall component. The Plant Cell, 20, 1519–1537. Available from: 10.1105/tpc.108.059873 PubMed DOI PMC
Chin, K. , DeFalco, T.A. , Moeder, W. & Yoshioka, K. (2013) The arabidopsis cyclic nucleotide‐gated ion channels AtCNGC2 and AtCNGC4 work in the same signaling pathway to regulate pathogen defense and floral transition. Plant Physiology, 163, 611–624. Available from: 10.1104/pp.113.225680 PubMed DOI PMC
Chuberre, C. , Plancot, B. , Driouich, A. , Moore, J.P. , Bardor, M. & Gügi, B. et al. (2018) Plant immunity is compartmentalized and specialized in roots. Frontiers in Plant Science, 9, 1692. Available from: 10.3389/fpls.2018.01692 PubMed DOI PMC
Cove, D.J. , Perroud, P.‐F. , Charron, A.J. , McDaniel, S.F. , Khandelwal, A. & Quatrano, R.S. (2009) Culturing the moss physcomitrella patens . Cold Spring Harbor Protocols, 2009, pdb.prot5136. Available from: 10.1101/pdb.prot5136 PubMed DOI
Cui, W. & Lee, J.‐Y. (2016) Arabidopsis callose synthases CalS1/8 regulate plasmodesmal permeability during stress. Nature Plants, 2, 16034. Available from: 10.1038/nplants.2016.34. PubMed DOI
Dehors, J. , Mareck, A. , Kiefer‐Meyer, M.‐C. , Menu‐Bouaouiche, L. , Lehner, A. & Mollet, J.‐C. (2019) Evolution of cell wall polymers in tip‐growing land plant gametophytes: composition, distribution, functional aspects and their remodeling. Frontiers in Plant Science, 10, 441. Available from: 10.3389/fpls.2019.00441 PubMed DOI PMC
Denoux, C. , Galletti, R. , Mammarella, N. , Gopalan, S. , Werck, D. , De Lorenzo, G. et al. (2008) Activation of defense response pathways by OGs and Flg22 elicitors in arabidopsis seedlings. Molecular Plant, 1, 423–445. Available from: 10.1093/mp/ssn019 PubMed DOI PMC
Dolan, L. (1996) Pattern in the root epidermis: an interplay of diffusible signals and cellular geometry. Annals of Botany, 77, 547–553. Available from: 10.1006/anbo.1996.0069 DOI
Epel, B.L. (2009) Plant viruses spread by diffusion on ER‐associated movement‐protein‐rafts through plasmodesmata gated by viral induced host β‐1,3‐glucanases. Seminars in Cell & Developmental Biology, 20, 1074–1081. Available from: 10.1016/j.semcdb.2009.05.010 PubMed DOI
Evans, N. , Hoyne, P. & Stone, B. (1984) Characteristics and specificity of the interaction of a fluorochrome from aniline blue (sirofluor) with polysaccharides. Carbohydrate Polymers, 4, 215–230. Available from: 10.1016/0144-8617(84)90012-2 DOI
Fernandez, A.I. & Beeckman, T. (2020) An MAP kinase cascade downstream of RGF/GLV peptides and their RGI receptors regulates root development. Molecular Plant, 13, 1542–1544. Available from: 10.1016/j.molp.2020.10.009 PubMed DOI
Galway, M.E. , Eng, R.C. , Schiefelbein, J.W. & Wasteneys, G.O. (2011) Root hair‐specific disruption of cellulose and xyloglucan in AtCSLD3 mutants, and factors affecting the post‐rupture resumption of mutant root hair growth. Planta, 233, 985–999. Available from: 10.1007/s00425-011-1355-6 PubMed DOI
Gamborg, O.L. , Miller, R.A. & Ojima, K. (1968) Nutrient requirements of suspension cultures of soybean root cells. Experimental Cell Research, 50, 151–158. Available from: 10.1016/0014-4827(68)90403-5 PubMed DOI
German, L. , Yeshvekar, R. & Benitez‐Alfonso, Y. (2023) Callose metabolism and the regulation of cell walls and plasmodesmata during plant mutualistic and pathogenic interactions. Plant, Cell & Environment, 46, 391–404. Available from: 10.1111/pce.14510 PubMed DOI PMC
Gómez‐Gómez, L. , Felix, G. & Boller, T. (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana . The Plant Journal, 18, 277–284. Available from: 10.1046/j.1365-313x.1999.00451.x PubMed DOI
Herburger, K. & Holzinger, A. (2015) Localization and quantification of callose in the streptophyte Green algae zygnema and klebsormidium: correlation with desiccation tolerance. Plant and Cell Physiology, 56, 2259–2270. Available from: 10.1093/pcp/pcv139 PubMed DOI PMC
Huang, D. , Sherman, B.T. , Tan, Q. , Collins, J.R. , Alvord, W.G. , Roayaei, J. et al. (2007) The DAVID gene functional classification tool: a novel biological module‐centric algorithm to functionally analyze large gene lists. Genome Biology, 8, R183. Available from: 10.1186/gb-2007-8-9-r183 PubMed DOI PMC
Ichikawa, M. , Hirano, T. , Enami, K. , Fuselier, T. , Kato, N. , Kwon, C. et al. (2014) Syntaxin of plant proteins SYP123 and SYP132 mediate root hair tip growth in Arabidopsis thaliana . Plant and Cell Physiology, 55, 790–800. Available from: 10.1093/pcp/pcu048 PubMed DOI
Iriti, M. , Sironi, M. , Gomarasca, S. , Casazza, A.P. , Soave, C. & Faoro, F. (2006) Cell death‐mediated antiviral effect of chitosan in tobacco. Plant Physiology and Biochemistry, 44, 893–900. Available from: 10.1016/j.plaphy.2006.10.009 PubMed DOI
Ishiga, Y. , Ishiga, T. , Uppalapati, S.R. & Mysore, K.S. (2011) Arabidopsis seedling flood‐inoculation technique: a rapid and reliable assay for studying plant‐bacterial interactions. Plant Methods, 7, 32. Available from: 10.1186/1746-4811-7-32 PubMed DOI PMC
Jacobs, A.K. , Lipka, V. , Burton, R.A. , Panstruga, R. , Strizhov, N. , Schulze‐Lefert, P. et al. (2003) An arabidopsis callose synthase, GSL5, is required for wound and papillary callose formation. The Plant Cell, 15, 2503–2513. Available from: 10.1105/tpc.016097 PubMed DOI PMC
Jones, J.D.G. & Dangl, J.L. (2006) The plant immune system. Nature, 444, 323–329. Available from: 10.1038/nature05286 PubMed DOI
Keinath, N.F. , Waadt, R. , Brugman, R. , Schroeder, J.I. , Grossmann, G. , Schumacher, K. et al. (2015) Live cell imaging with R‐GECO1 sheds light on flg22‐ and Chitin‐Induced transient [Ca2+]cyt patterns in arabidopsis. Molecular Plant, 8, 1188–1200. Available from: 10.1016/j.molp.2015.05.006 PubMed DOI PMC
Kemmerling, B. , Schwedt, A. , Rodriguez, P. , Mazzotta, S. , Frank, M. , Qamar, S.A. et al. (2007) The BRI1‐associated kinase 1, BAK1, has a brassinolide‐independent role in plant cell‐death control. Current Biology, 17, 1116–1122. Available from: 10.1016/j.cub.2007.05.046 PubMed DOI
Ks, R. , Ra, L. , Rd, W. , Ha, O. & A, M. (2020) Callose in sporogenesis: novel composition of the inner spore wall in hornworts. Plant systematics and evolution = Entwicklungsgeschichte und Systematik der Pflanzen, 306, 16. Available from: 10.1007/s00606-020-01631-5 PubMed DOI PMC
Kubátová, Z. , Pejchar, P. , Potocký, M. , Sekereš, J. , Žárský, V. & Kulich, I. (2019) Arabidopsis trichome contains two plasma membrane domains with different lipid compositions which attract distinct EXO70 subunits. International Journal of Molecular Sciences, 20, 3803. Available from: 10.3390/ijms20153803 PubMed DOI PMC
Kulich, I. , Vojtíková, Z. , Glanc, M. , Ortmannová, J. , Rasmann, S. & Žárský, V. (2015) Cell wall maturation of arabidopsis trichomes is dependent on exocyst subunit EXO70H4 and involves callose deposition. Plant Physiology, 168, 120–131. Available from: 10.1104/pp.15.00112 PubMed DOI PMC
Ladwig, F. , Dahlke, R.I. , Stührwohldt, N. , Hartmann, J. , Harter, K. & Sauter, M. (2015) Phytosulfokine regulates growth in arabidopsis through a response module at the plasma membrane that includes cyclic nucleotide‐gated channel17, H+‐ATPase, and BAK1. The Plant Cell, 27, 1718–1729. Available from: 10.1105/tpc.15.00306 PubMed DOI PMC
Lopez‐Moya, F. , Escudero, N. , Zavala‐Gonzalez, E.A. , Esteve‐Bruna, D. , Blázquez, M.A. , Alabadí, D. et al. (2017) Induction of auxin biosynthesis and WOX5 repression mediate changes in root development in arabidopsis exposed to chitosan. Scientific Reports, 7, 16813. Available from: 10.1038/s41598-017-16874-5. PubMed DOI PMC
Luna, E. , Pastor, V. , Robert, J. , Flors, V. , Mauch‐Mani, B. & Ton, J. (2011) Callose deposition: a multifaceted plant defense response. Molecular Plant‐Microbe Interactions®, 24, 183–193. Available from: 10.1094/MPMI-07-10-0149 PubMed DOI
Ma, X. , Wu, Y. & Zhang, G. (2021) Formation pattern and regulatory mechanisms of pollen wall in arabidopsis. Journal of Plant Physiology, 260, 153388. Available from: 10.1016/j.jplph.2021.153388. PubMed DOI
Mendrinna, A. & Persson, S. (2015) Root hair growth: it's a one way street. F1000Prime Reports, 7, 23. Available from: 10.12703/P7-23 PubMed DOI PMC
Meyer, D. , Pajonk, S. , Micali, C. , O'Connell, R. & Schulze‐Lefert, P. (2009) Extracellular transport and integration of plant secretory proteins into pathogen‐induced cell wall compartments. The Plant Journal, 57, 986–999. Available from: 10.1111/j.1365-313X.2008.03743.x PubMed DOI
Millet, Y.A. , Danna, C.H. , Clay, N.K. , Songnuan, W. , Simon, M.D. , Werck‐Reichhart, D. et al. (2010) Innate immune responses activated in arabidopsis roots by microbe‐associated molecular patterns. The Plant Cell, 22, 973–990. Available from: 10.1105/tpc.109.069658 PubMed DOI PMC
Miya, A. , Albert, P. , Shinya, T. , Desaki, Y. , Ichimura, K. , Shirasu, K. et al. (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in arabidopsis. Proceedings of the National Academy of Sciences, 104, 19613–19618. Available from: 10.1073/pnas.0705147104 PubMed DOI PMC
Morello, G. , De Iaco, G. , Gigli, G. , Polini, A. & Gervaso, F. (2023) Chitosan and pectin hydrogels for tissue engineering and in vitro modeling. Gels, 9, 132. Available from: 10.3390/gels9020132 PubMed DOI PMC
Motomura, K. , Sugi, N. , Takeda, A. , Yamaoka, S. & Maruyama, D. (2022) Possible molecular mechanisms of persistent pollen tube growth without de novo transcription. Frontiers in Plant Science, 13, 1020306. Available from: 10.3389/fpls.2022.1020306. PubMed DOI PMC
Mravec, J. , Kračun, S.K. , Rydahl, M.G. , Westereng, B. , Miart, F. , Clausen, M.H. et al. (2014) Tracking developmentally regulated post‐synthetic processing of homogalacturonan and chitin using reciprocal oligosaccharide probes. Development, 141, 4841–4850. Available from: 10.1242/dev.113365 PubMed DOI
Müller, K. , Dobrev, P.I. , Pěnčík, A. , Hošek, P. , Vondráková, Z. , Filepová, R. et al. (2021) DIOXYGENASE FOR AUXIN OXIDATION 1 catalyzes the oxidation of IAA amino acid conjugates. Plant Physiology, 187, 103–115. Available from: 10.1093/plphys/kiab242 PubMed DOI PMC
Ngou, B.P.M. , Ahn, H.‐K. , Ding, P. & Jones, J.D.G. (2021) Mutual potentiation of plant immunity by cell‐surface and intracellular receptors. Nature, 592, 110–115. Available from: 10.1038/s41586-021-03315-7 PubMed DOI
Okada, K. , Kubota, Y. , Hirase, T. , Otani, K. , Goh, T. , Hiruma, K. et al. (2021) Uncoupling root hair formation and defence activation from growth inhibition in response to damage‐associated pep peptides in Arabidopsis thaliana . New Phytologist, 229, 2844–2858. Available from: 10.1111/nph.17064 PubMed DOI
Okada, K , Yachi, K , Nguyen, T.A.N. , Kanno, S , Tateda, C , Lee, T‐H et al. (2024) Defense‐related callose synthase PMR4 promotes root hair callose deposition and adaptation to phosphate deficiency in Arabidopsis thaliana . bioRxiv. [Preprint] Available from: 10.1101/2023.07.05.547890 PubMed DOI PMC
Ortmannová, J. , Sekereš, J. , Kulich, I. , Šantrůček, J. , Dobrev, P. , Žárský, V. et al. (2022) Arabidopsis EXO70B2 exocyst subunit contributes to papillae and encasement formation in antifungal defence. Journal of Experimental Botany, 73, 742–755. Available from: 10.1093/jxb/erab457 PubMed DOI
Park, S. , Szumlanski, A.L. , Gu, F. , Guo, F. & Nielsen, E. (2011) A role for CSLD3 during cell‐wall synthesis in apical plasma membranes of tip‐growing root‐hair cells. Nature Cell Biology, 13, 973–980. Available from: 10.1038/ncb2294 PubMed DOI
Parker, J.S. , Cavell, A.C. , Dolan, L. , Roberts, K. & Grierson, C.S. (2000) Genetic interactions during root hair morphogenesis in arabidopsis. The Plant Cell, 12, 1961–1974. Available from: 10.1105/tpc.12.10.1961 PubMed DOI PMC
Paterlini, A. , Sechet, J. , Immel, F. , Grison, M.S. , Pilard, S. , Pelloux, J. et al. (2022) Enzymatic fingerprinting reveals specific xyloglucan and pectin signatures in the cell wall purified with primary plasmodesmata. Frontiers in Plant Science, 13, 1020506. PubMed PMC
Pečenková, T. , Janda, M. , Ortmannová, J. , Hajná, V. , Stehlíková, Z. & Žárský, V. (2017) Early arabidopsis root hair growth stimulation by pathogenic strains of pseudomonas syringae. Annals of Botany, 120, 437–446. Available from: Available from: 10.1093/aob/mcx073 PubMed DOI PMC
Pečenková, T. , Potocká, A. , Potocký, M. , Ortmannová, J. , Drs, M. , Janková Drdová, E. et al. (2020) Redundant and diversified roles among selected Arabidopsis thaliana EXO70 paralogs during biotic stress responses. Frontiers in Plant Science, 11, 960960. Available from: 10.3389/fpls.2020.00960 PubMed DOI PMC
Porter, K. & Day, B. (2016) From filaments to function: the role of the plant actin cytoskeleton in pathogen perception, signaling and immunity. Journal of Integrative Plant Biology, 58, 299–311. Available from: 10.1111/jipb.12445 PubMed DOI
Qi, L. , Kwiatkowski, M. , Kulich, I. , Chen, H. , Gao, Y. , Yun, P. et al. (2023) Guanylate cyclase activity of TIR1/AFB auxin receptors in rapid auxin responses. bioRxiv. Available from: 10.1101/2023.11.18.567481 DOI
Rentel, M.C. , Lecourieux, D. , Ouaked, F. , Usher, S.L. , Petersen, L. , Okamoto, H. et al. (2004) OXI1 kinase is necessary for oxidative burst‐mediated signalling in arabidopsis. Nature, 427, 858–861. [Preprint] Available from: 10.1038/nature02353 PubMed DOI
Rich‐Griffin, C. , Eichmann, R. , Reitz, M.U. , Hermann, S. , Woolley‐Allen, K. , Brown, P.E. et al. (2020) Regulation of cell type‐specific immunity networks in arabidopsis roots. The Plant Cell, 32, 2742–2762. Available from: 10.1105/TPC.20.00154 PubMed DOI PMC
Ringli, C. , Baumberger, N. , Diet, A. , Frey, B. & Keller, B. (2002) ACTIN2 is essential for bulge site selection and tip growth during root hair development of arabidopsis. Plant Physiology, 129, 1464–1472. Available from: 10.1104/pp.005777 PubMed DOI PMC
Rounds, C.M. & Bezanilla, M. (2013) Growth mechanisms in tip‐growing plant cells. Annual review of plant biology, 64, 243–265. Available from: 10.1146/annurev-arplant-050312-120150 PubMed DOI
Schindelin, J. , Arganda‐Carreras, I. , Frise, E. , Kaynig, V. , Longair, M. , Pietzsch, T. et al. (2012) Fiji: an open‐source platform for biological‐image analysis. Nature Methods, 9, 676–682. PubMed PMC
Schoenaers, S. , Lee, H.K. , Gonneau, M. , Faucher, E. , Levasseur, T. , Akary, E. et al. (2024) Rapid alkalinization factor 22 has a structural and signalling role in root hair cell wall assembly. Nature Plants, 10, 494–511. Available from: 10.1038/s41477-024-01637-8 PubMed DOI PMC
Serre, N.B.C. , Kralík, D. , Yun, P. , Slouka, Z. , Shabala, S. & Fendrych, M. (2021) AFB1 controls rapid auxin signalling through membrane depolarization in Arabidopsis thaliana root. Nature Plants, 7, 1229–1238. Available from: 10.1038/s41477-021-00969-z PubMed DOI PMC
Shih, H.W. , Depew, C.L. , Miller, N.D. & Monshausen, G.B. (2015) The cyclic nucleotide‐gated channel CNGC14 regulates root gravitropism in Arabidopsis thaliana . Current Biology, 25, 3119–3125. Available from: 10.1016/j.cub.2015.10.025 PubMed DOI
Sun, H. , Zhu, X. , Li, C. , Ma, Z. , Han, X. , Luo, Y. et al. (2021) Xanthomonas effector XopR hijacks host actin cytoskeleton via complex coacervation. Nature Communications, 12, 4064. Available from: 10.1038/s41467-021-24375-3 PubMed DOI PMC
Suwanchaikasem, P. , Idnurm, A. , Selby‐Pham, J. , Walker, R. & Boughton, B.A. (2022) Root‐TRAPR: a modular plant growth device to visualize root development and monitor growth parameters, as applied to an elicitor response of cannabis sativa . Plant Methods, 18, 46. Available from: 10.1186/s13007-022-00875-1 PubMed DOI PMC
Torres, M.A. , Dangl, J.L. & Jones, J.D. (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proceedings of the National Academy of Sciences of the United States of America, 99, 517–522. Available from: 10.1073/pnas.012452499 PubMed DOI PMC
Toyota, M. , Spencer, D. , Sawai‐Toyota, S. , Jiaqi, W. , Zhang, T. , Koo, A.J. et al. (2018) Glutamate triggers long‐distance, calcium‐based plant defense signaling. Science, 361, 1112–1115. Available from: 10.1126/science.aat7744 PubMed DOI
Uemura, T. , Yoshimura, S.H. , Takeyasu, K. & Sato, M.H. (2002) Vacuolar membrane dynamics revealed by GFP‐AtVam3 fusion protein. Genes to Cells, 7, 743–753. Available from: 10.1046/j.1365-2443.2002.00550.x PubMed DOI
Ušák, D. , Haluška, S. & Pleskot, R. (2023) Callose synthesis at the center point of plant development‐an evolutionary insight. Plant Physiology, 193(1), 54–69. Available from: 10.1093/plphys/kiad274 PubMed DOI
Vaškebová, L. , Šamaj, J. & Ovecka, M. (2018) Single‐point ACT2 gene mutation in the arabidopsis root hair mutant der1‐3 affects overall actin organization, root growth and plant development. Annals of Botany, 122, 889–901. Available from: 10.1093/aob/mcx180 PubMed DOI PMC
Verma, D.P.S. & Hong, Z. (2001) Plant callose synthase complexes. Plant Molecular Biology, 47, 693–701. Available from: 10.1023/a:1013679111111 PubMed DOI
Vissenberg, K. , Claeijs, N. , Balcerowicz, D. & Schoenaers, S. (2020) Hormonal regulation of root hair growth and responses to the environment in arabidopsis. Journal of Experimental Botany, 71, 2412–2427. Available from: 10.1093/JXB/ERAA048 PubMed DOI PMC
Vogel, J. & Somerville, S. (2000) Isolation and characterization of powdery mildew‐resistant arabidopsis mutants. Proceedings of the National Academy of Sciences, 97, 1897–1902. Available from: 10.1073/pnas.030531997 PubMed DOI PMC
Walter, W. , Sánchez‐Cabo, F. & Ricote, M. (2015) GOplot: an R package for visually combining expression data with functional analysis. Bioinformatics, 31, 2912–2914. Available from: 10.1093/bioinformatics/btv300 PubMed DOI
Wan, J. , Tanaka, K. , Zhang, X.‐C. , Son, G.H. , Brechenmacher, L. , Nguyen, T.H.N. et al. (2012) LYK4, a lysin motif receptor‐like kinase, is important for chitin signaling and plant innate immunity in arabidopsis. Plant Physiology, 160, 396–406. Available from: 10.1104/pp.112.201699 PubMed DOI PMC
Wang, X. , Wang, K. , Yin, G. , Liu, X. , Liu, M. , Cao, N. et al. (2018) Pollen‐expressed leucine‐rich repeat extensins are essential for pollen germination and growth. Plant Physiology, 176, 1993–2006. Available from: 10.1104/pp.17.01241 PubMed DOI PMC
Wang, Y.‐S. , Motes, C.M. , Mohamalawari, D.R. & Blancaflor, E.B. (2004) Green fluorescent protein fusions to arabidopsis fimbrin 1 for spatio‐temporal imaging of F‐actin dynamics in roots. Cell Motility, 59, 79–93. Available from: 10.1002/cm.20024 PubMed DOI
Ye, W. , Munemasa, S. , Shinya, T. , Wu, W. , Ma, T. , Lu, J. et al. (2020) Stomatal immunity against fungal invasion comprises not only chitin‐induced stomatal closure but also chitosan‐induced guard cell death. Proceedings of the National Academy of Sciences, 117, 20932–20942. Available from: 10.1073/pnas.1922319117 PubMed DOI PMC
Yoo, S.‐D. , Cho, Y.‐H. & Sheen, J. (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nature Protocols, 2, 1565–1572. Available from: 10.1038/nprot.2007.199 PubMed DOI
Yuan, P. , Jauregui, E. , Du, L. , Tanaka, K. & Poovaiah, B. (2017) Calcium signatures and signaling events orchestrate plant–microbe interactions. Current Opinion in Plant Biology, 38, 173–183. Available from: 10.1016/j.pbi.2017.06.003 PubMed DOI
Zamioudis, C. , Mastranesti, P. , Dhonukshe, P. , Blilou, I. & Pieterse, C.M.J. (2013) Unraveling root developmental programs initiated by beneficial pseudomonas spp. bacteria. Plant Physiology, 162, 304–318. Available from: 10.1104/pp.112.212597 PubMed DOI PMC
Zhang, J. , Li, Y. , Bao, Q. , Wang, H. & Hou, S. (2022) Plant elicitor peptide 1 fortifies root cell walls and triggers a systemic root‐to‐shoot immune signaling in arabidopsis. Plant Signaling & Behavior, 17, 2034270. Available from: 10.1080/15592324.2022.2034270. PubMed DOI PMC
Zhang, M. & Zhang, S. (2022) Mitogen‐activated protein kinase cascades in plant signaling. Journal of Integrative Plant Biology, 64, 301–341. Available from: 10.1111/jipb.13215 PubMed DOI