SYNERGISTIC ON AUXIN AND CYTOKININ 1 positively regulates growth and attenuates soil pathogen resistance
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
32358503
PubMed Central
PMC7195429
DOI
10.1038/s41467-020-15895-5
PII: 10.1038/s41467-020-15895-5
Knihovny.cz E-zdroje
- MeSH
- Arabidopsis genetika růst a vývoj metabolismus MeSH
- buněčná stěna chemie metabolismus MeSH
- cytokininy metabolismus MeSH
- endozomy metabolismus MeSH
- geneticky modifikované rostliny metabolismus MeSH
- Golgiho aparát metabolismus MeSH
- kořeny rostlin metabolismus mikrobiologie MeSH
- kyseliny indoloctové metabolismus MeSH
- membránové proteiny genetika metabolismus MeSH
- odolnost vůči nemocem genetika MeSH
- Plasmodiophorida patogenita MeSH
- proteiny huseníčku genetika metabolismus MeSH
- půda MeSH
- regulace genové exprese u rostlin genetika MeSH
- regulátory růstu rostlin metabolismus MeSH
- sekreční dráha genetika MeSH
- stanovení celkové genové exprese MeSH
- transkriptom genetika MeSH
- vezikulární transportní proteiny metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- AT2G18840 protein, Arabidopsis MeSH Prohlížeč
- AT4G30260 protein, Arabidopsis MeSH Prohlížeč
- cytokininy MeSH
- ECHIDNA protein, Arabidopsis MeSH Prohlížeč
- kyseliny indoloctové MeSH
- membránové proteiny MeSH
- proteiny huseníčku MeSH
- půda MeSH
- regulátory růstu rostlin MeSH
- SYAC1 protein, Arabidopsis MeSH Prohlížeč
- vezikulární transportní proteiny MeSH
Plants as non-mobile organisms constantly integrate varying environmental signals to flexibly adapt their growth and development. Local fluctuations in water and nutrient availability, sudden changes in temperature or other abiotic and biotic stresses can trigger changes in the growth of plant organs. Multiple mutually interconnected hormonal signaling cascades act as essential endogenous translators of these exogenous signals in the adaptive responses of plants. Although the molecular backbones of hormone transduction pathways have been identified, the mechanisms underlying their interactions are largely unknown. Here, using genome wide transcriptome profiling we identify an auxin and cytokinin cross-talk component; SYNERGISTIC ON AUXIN AND CYTOKININ 1 (SYAC1), whose expression in roots is strictly dependent on both of these hormonal pathways. We show that SYAC1 is a regulator of secretory pathway, whose enhanced activity interferes with deposition of cell wall components and can fine-tune organ growth and sensitivity to soil pathogens.
Departamento de Biología de Organismos y Sistemas Universidad de Oviedo Oviedo Spain
Department of Chemistry Umeå University Linnaeus väg 6 SE 901 87 Umeå Sweden
Department of Plant Biotechnology and Bioinformatics Ghent University Ghent Belgium
Institut für Botanik Technische Universität Dresden Dresden Germany
Institut Jean Pierre Bourgin INRAE AgroParisTech Université Paris Saclay 78000 Versailles France
Institute of Biophysics The Czech Academy of Sciences Královopolská 135 61265 Brno Czech Republic
Institute of Science and Technology Klosterneuburg Austria
Mendel Centre for Plant Genomics and Proteomics CEITEC Masaryk University Brno Czech Republic
Zobrazit více v PubMed
Schaller GE, Bishopp A, Kieber JJ. The yin-yang of hormones: cytokinin and auxin interactions in plant development. Plant Cell Online. 2015;27:44–63. doi: 10.1105/tpc.114.133595. PubMed DOI PMC
Wang YH, Irving HR. Developing a model of plant hormone interactions. Plant Signal. Behav. 2011;6:494–500. doi: 10.4161/psb.6.4.14558. PubMed DOI PMC
Dello Ioio R, et al. A genetic framework for the control of cell division and differentiation in the root meristem. Science. 2008;322:1380–1384. doi: 10.1126/science.1164147. PubMed DOI
Zhao Z, et al. Hormonal control of the shoot stem-cell niche. Nature. 2010;465:1089–1092. doi: 10.1038/nature09126. PubMed DOI
Bielach A, et al. Spatiotemporal regulation of lateral root organogenesis in Arabidopsis by cytokinin. Plant Cell. 2012;24:3967–3981. doi: 10.1105/tpc.112.103044. PubMed DOI PMC
Müller D, et al. Cytokinin is required for escape but not release from auxin mediated apical dominance. Plant J. 2015;82:874–886. doi: 10.1111/tpj.12862. PubMed DOI PMC
Skoog F, Miller CO. Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp. Soc. Exp. Biol. 1957;11:118–130. PubMed
Yang Z, et al. Synergistic action of auxin and cytokinin mediates aluminum-induced root growth inhibition in Arabidopsis. EMBO Rep. 2017;18:1213–1230. doi: 10.15252/embr.201643806. PubMed DOI PMC
Dharmasiri N, Dharmasiri S, Estelle M. The F-box protein TIR1 is an auxin receptor. Nature. 2005;435:441–445. doi: 10.1038/nature03543. PubMed DOI
Hwang I, Sheen J. Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature. 2001;413:383–389. doi: 10.1038/35096500. PubMed DOI
Inoue T, et al. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature. 2001;409:35059117. doi: 10.1038/35059117. PubMed DOI
Kepinski S, Leyser O. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature. 2005;435:446–451. doi: 10.1038/nature03542. PubMed DOI
Ueguchi C, Koizumi H, Suzuki T, Mizuno T. Novel family of sensor histidine kinase genes in Arabidopsis thaliana. Plant Cell Physiol. 2001;42:231–235. doi: 10.1093/pcp/pce015. PubMed DOI
Schlereth A, et al. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature. 2010;464:nature08836. doi: 10.1038/nature08836. PubMed DOI
Marhavý P, et al. Cytokinin modulates endocytic trafficking of PIN1 auxin efflux carrier to control plant organogenesis. Dev. Cell. 2011;21:796–804. doi: 10.1016/j.devcel.2011.08.014. PubMed DOI
Marhavý P, et al. Auxin reflux between the endodermis and pericycle promotes lateral root initiation. EMBO J. 2013;32:149–158. doi: 10.1038/emboj.2012.303. PubMed DOI PMC
Růžička K, et al. Cytokinin regulates root meristem activity via modulation of the polar auxin transport. Proc. Natl Acad. Sci. USA. 2009;106:4284–4289. doi: 10.1073/pnas.0900060106. PubMed DOI PMC
Šimášková M, et al. Cytokinin response factors regulate PIN-FORMED auxin transporters. Nat. Commun. 2015;6:8717. doi: 10.1038/ncomms9717. PubMed DOI
Vanstraelen M, Benková E. Hormonal interactions in the regulation of plant development. Annu. Rev. Cell Dev. Biol. 2012;28:463–487. doi: 10.1146/annurev-cellbio-101011-155741. PubMed DOI
Krouk G, et al. A framework integrating plant growth with hormones and nutrients. Trends Plant Sci. 2011;16:178–182. doi: 10.1016/j.tplants.2011.02.004. PubMed DOI
Sánchez-Rodríguez C, Rubio-Somoza I, Sibout R, Persson S. Phytohormones and the cell wall in Arabidopsis during seedling growth. Trends Plant Sci. 2010;15:291–301. doi: 10.1016/j.tplants.2010.03.002. PubMed DOI
Verma V, Ravindran P, Kumar PP. Plant hormone-mediated regulation of stress responses. BMC Plant Biol. 2016;16:86. doi: 10.1186/s12870-016-0771-y. PubMed DOI PMC
Hurný, A. & Benková, E. Methodological advances in auxin and cytokinin biology. in Auxins and Cytokinins in Plant Biology 1–29 (Humana Press, New York, NY, 2017). 10.1007/978-1-4939-6831-2_1. PubMed
Denancé N, Sánchez-Vallet A, Goffner D, Molina A. Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front. Plant Sci. 2013;4:1–12. doi: 10.3389/fpls.2013.00155. PubMed DOI PMC
Huot B, Yao J, Montgomery BL, He SY. Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Mol. Plant. 2014;7:1267–1287. doi: 10.1093/mp/ssu049. PubMed DOI PMC
Boivin S, Fonouni-Farde C, Frugier F. How auxin and cytokinin phytohormones modulate root microbe interactions. Front. Plant Sci. 2016;7:1240. doi: 10.3389/fpls.2016.01240. PubMed DOI PMC
Sabatini S, et al. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell. 1999;99:463–472. doi: 10.1016/S0092-8674(00)81535-4. PubMed DOI
Zürcher E, Liu J, di Donato M, Geisler M, Müller B. Plant development regulated by cytokinin sinks. Science. 2016;353:1027–1030. doi: 10.1126/science.aaf7254. PubMed DOI
Chae HS, Faure F, Kieber JJ. The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein. Plant Cell. 2003;15:545–559. doi: 10.1105/tpc.006882. PubMed DOI PMC
Raz V, Ecker JR. Regulation of differential growth in the apical hook of Arabidopsis. Development. 1999;126:3661–3668. PubMed
Žádníková P, et al. Role of PIN-mediated auxin efflux in apical hook development of Arabidopsis thaliana. Development. 2010;137:607–617. doi: 10.1242/dev.041277. PubMed DOI
Gendreau E, et al. Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol. 1997;114:295–305. doi: 10.1104/pp.114.1.295. PubMed DOI PMC
Geldner N, et al. Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J. 2009;59:169–178. doi: 10.1111/j.1365-313X.2009.03851.x. PubMed DOI PMC
Drakakaki G, et al. Isolation and proteomic analysis of the SYP61 compartment reveal its role in exocytic trafficking in Arabidopsis. Cell Res. 2012;22:413–424. doi: 10.1038/cr.2011.129. PubMed DOI PMC
Gendre D, et al. Trans-Golgi network localized ECHIDNA/Ypt interacting protein complex is required for the secretion of cell wall polysaccharides in Arabidopsis. Plant Cell. 2013;25:2633–2646. doi: 10.1105/tpc.113.112482. PubMed DOI PMC
Bassham DC, Brandizzi F, Otegui MS, Sanderfoot AA. The secretory system of Arabidopsis. Arab. Book. 2008;6:e0116. doi: 10.1199/tab.0116. PubMed DOI PMC
Früholz, S. & Pimpl, P. Analysis of nanobody–epitope interactions in living cells via quantitative protein transport assays. in Plant Protein Secretion 171–182 (Humana Press, New York, NY, 2017). 10.1007/978-1-4939-7262-3_15. PubMed
Wolf S, Greiner S. Growth control by cell wall pectins. Protoplasma. 2012;249:169–175. doi: 10.1007/s00709-011-0371-5. PubMed DOI
Young RE, et al. Analysis of the Golgi apparatus in Arabidopsis seed coat cells during polarized secretion of pectin-rich mucilage. Plant Cell. 2008;20:1623–1638. doi: 10.1105/tpc.108.058842. PubMed DOI PMC
Mouille G, Robin S, Lecomte M, Pagant S, Höfte H. Classification and identification of Arabidopsis cell wall mutants using fourier-transform infrared (FT-IR) microspectroscopy. Plant J. Cell Mol. Biol. 2003;35:393–404. doi: 10.1046/j.1365-313X.2003.01807.x. PubMed DOI
Derbyshire P, McCann MC, Roberts K. Restricted cell elongation in Arabidopsis hypocotyls is associated with a reduced average pectin esterification level. BMC Plant Biol. 2007;7:31. doi: 10.1186/1471-2229-7-31. PubMed DOI PMC
Bethke, G. & Glazebrook, J. Measuring pectin properties to track cell wall alterations during plant–pathogen interactions. in Plant Innate Immunity: Methods and Protocols (ed. Gassmann, W.) 55–60 (Springer, 2019). 10.1007/978-1-4939-9458-8_6. PubMed
Cosgrove DJ. Catalysts of plant cell wall loosening. F1000Research. 2016;5:119. doi: 10.12688/f1000research.7180.1. PubMed DOI PMC
Daher FB, Braybrook SA. How to let go: pectin and plant cell adhesion. Front. Plant Sci. 2015;3:523. PubMed PMC
Ando S, et al. Increase in BrAO1 gene expression and aldehyde oxidase activity during clubroot development in Chinese cabbage (Brassica rapa L.) Mol. Plant Pathol. 2006;7:223–234. doi: 10.1111/j.1364-3703.2006.00333.x. PubMed DOI
Devos S, Vissenberg K, Verbelen J-P, Prinsen E. Infection of Chinese cabbage by Plasmodiophorabrassicae leads to a stimulation of plant growth: impacts on cell wall metabolism and hormone balance. New Phytol. 2005;166:241–250. doi: 10.1111/j.1469-8137.2004.01304.x. PubMed DOI
Schuller A, Ludwig-Müller J. A family of auxin conjugate hydrolases from Brassica rapa: characterization and expression during clubroot disease. New Phytol. 2006;171:145–157. doi: 10.1111/j.1469-8137.2006.01727.x. PubMed DOI
Siemens J, et al. Transcriptome analysis of Arabidopsis clubroots indicate a key role for cytokinins in disease development. Mol. Plant. Microbe Interact. 2006;19:480–494. doi: 10.1094/MPMI-19-0480. PubMed DOI
Knaust A, Ludwig-Müller J. The ethylene signaling pathway is needed to restrict root gall growth in Arabidopsis after infection with the obligate biotrophic protist Plasmodiophora brassicae. J. Plant Growth Regul. 2013;32:9–21. doi: 10.1007/s00344-012-9271-y. DOI
Siemens J, Nagel M, Ludwig‐Müller J, Sacristán MD. The interaction of Plasmodiophora brassicae and Arabidopsis thaliana: parameters for disease quantification and screening of mutant lines. J. Phytopathol. 2002;150:592–605. doi: 10.1046/j.1439-0434.2002.00818.x. DOI
Müller B, Sheen J. Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature. 2008;453:1094–1097. doi: 10.1038/nature06943. PubMed DOI PMC
Dello Ioio R, et al. Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr. Biol. 2007;17:678–682. doi: 10.1016/j.cub.2007.02.047. PubMed DOI
Argyros RD, et al. Type B response regulators of Arabidopsis play key roles in cytokinin signaling and plant development. Plant Cell. 2008;20:2102–2116. doi: 10.1105/tpc.108.059584. PubMed DOI PMC
Dharmasiri N, et al. Plant development is regulated by a family of auxin receptor F box proteins. Dev. Cell. 2005;9:109–119. doi: 10.1016/j.devcel.2005.05.014. PubMed DOI
Hutchison CE, et al. The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell. 2006;18:3073–3087. doi: 10.1105/tpc.106.045674. PubMed DOI PMC
Mason MG. Multiple type-B response regulators mediate cytokinin signal transduction in Arabidopsis. Plant Cell. 2005;17:3007–3018. doi: 10.1105/tpc.105.035451. PubMed DOI PMC
Nishimura C, et al. Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell. 2004;16:1365–1377. doi: 10.1105/tpc.021477. PubMed DOI PMC
To JPC, Kieber JJ. Cytokinin signaling: two-components and more. Trends Plant Sci. 2008;13:85–92. doi: 10.1016/j.tplants.2007.11.005. PubMed DOI
Petersson SV, et al. An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell. 2009;21:1659–1668. doi: 10.1105/tpc.109.066480. PubMed DOI PMC
Brenner WG, Schmülling T. Transcript profiling of cytokinin action in Arabidopsis roots and shoots discovers largely similar but also organ-specific responses. BMC Plant Biol. 2012;12:112. doi: 10.1186/1471-2229-12-112. PubMed DOI PMC
Polko JK, Kieber JJ. The regulation of cellulose biosynthesis in plants. Plant Cell. 2019;31:282–296. doi: 10.1105/tpc.18.00760. PubMed DOI PMC
Saffer AM. Expanding roles for pectins in plant development. J. Integr. Plant Biol. 2018;60:910–923. doi: 10.1111/jipb.12662. PubMed DOI
Bouton S, et al. QUASIMODO1 encodes a putative membrane-bound glycosyltransferase required for normal pectin synthesis and cell adhesion in Arabidopsis. Plant Cell. 2002;14:2577–2590. doi: 10.1105/tpc.004259. PubMed DOI PMC
Krupková E, Immerzeel P, Pauly M, Schmülling T. The TUMOROUS SHOOT DEVELOPMENT2 gene of Arabidopsis encoding a putative methyltransferase is required for cell adhesion and co-ordinated plant development. Plant J. Cell Mol. Biol. 2007;50:735–750. doi: 10.1111/j.1365-313X.2007.03123.x. PubMed DOI
Mouille G, et al. Homogalacturonan synthesis in Arabidopsisthaliana requires a Golgi-localized protein with a putative methyltransferase domain. Plant J. Cell Mol. Biol. 2007;50:605–614. doi: 10.1111/j.1365-313X.2007.03086.x. PubMed DOI
Peaucelle A, Wightman R, Höfte H. The control of growth symmetry breaking in the Arabidopsis hypocotyl. Curr. Biol. 2015;25:1746–1752. doi: 10.1016/j.cub.2015.05.022. PubMed DOI
Phyo P, et al. Gradients in wall mechanics and polysaccharides along growing inflorescence stems. Plant Physiol. 2017;175:1593–1607. doi: 10.1104/pp.17.01270. PubMed DOI PMC
Kim S-J, Brandizzi F. The plant secretory pathway: an essential factory for building the plant cell wall. Plant Cell Physiol. 2014;55:687–693. doi: 10.1093/pcp/pct197. PubMed DOI
Atmodjo MA, Hao Z, Mohnen D. Evolving views of pectin biosynthesis. Annu. Rev. Plant Biol. 2013;64:747–779. doi: 10.1146/annurev-arplant-042811-105534. PubMed DOI
Ogawa M, Kay P, Wilson S, Swain SM. ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE1 (ADPG1), ADPG2, and QUARTET2 are polygalacturonases required for cell separation during reproductive development in Arabidopsis. Plant Cell. 2009;21:216–233. doi: 10.1105/tpc.108.063768. PubMed DOI PMC
Peñarrubia L, et al. Temporal aspects of copper homeostasis and its crosstalk with hormones. Front. Plant Sci. 2015;6:255. doi: 10.3389/fpls.2015.00255. PubMed DOI PMC
Karasov TL, Chae E, Herman JJ, Bergelson J. Mechanisms to mitigate the trade-off between growth and defense. Plant Cell. 2017;29:666–680. doi: 10.1105/tpc.16.00931. PubMed DOI PMC
Lahlali R, et al. Evaluating changes in cell-wall components associated with clubroot resistance using fourier transform infrared spectroscopy and RT-PCR. Int. J. Mol. Sci. 2017;18:2058. doi: 10.3390/ijms18102058. PubMed DOI PMC
Gendre D, et al. Conserved Arabidopsis ECHIDNA protein mediates trans-Golgi-network trafficking and cell elongation. Proc. Natl Acad. Sci. USA. 2011;108:8048–8053. doi: 10.1073/pnas.1018371108. PubMed DOI PMC
Higuchi M, et al. In planta functions of the Arabidopsis cytokinin receptor family. Proc. Natl Acad. Sci. USA. 2004;101:8821–8826. doi: 10.1073/pnas.0402887101. PubMed DOI PMC
Parry G, et al. Complex regulation of the TIR1/AFB family of auxin receptors. Proc. Natl Acad. Sci. USA. 2009;106:22540–22545. doi: 10.1073/pnas.0911967106. PubMed DOI PMC
Ruegger M, et al. The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast grr1p. Genes Dev. 1998;12:198–207. doi: 10.1101/gad.12.2.198. PubMed DOI PMC
Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. Cell Mol. Biol. 1998;16:735–743. doi: 10.1046/j.1365-313x.1998.00343.x. PubMed DOI
Laplaze L, et al. GAL4-GFP enhancer trap lines for genetic manipulation of lateral root development in Arabidopsis thaliana. J. Exp. Bot. 2005;56:2433–2442. doi: 10.1093/jxb/eri236. PubMed DOI
Birnbaum K, et al. Cell type–specific expression profiling in plants via cell sorting of protoplasts from fluorescent reporter lines. Nat. Methods. 2005;2:615–619. doi: 10.1038/nmeth0805-615. PubMed DOI
Irizarry RA, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostat. Oxf. Engl. 2003;4:249–264. doi: 10.1093/biostatistics/4.2.249. PubMed DOI
Naouar N, et al. Quantitative RNA expression analysis with Affymetrix Tiling 1.0R arrays identifies new E2F target genes. Plant J. 2009;57:184–194. doi: 10.1111/j.1365-313X.2008.03662.x. PubMed DOI
Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 2004;3:Article3. doi: 10.2202/1544-6115.1027. PubMed DOI
Storey JD, Tibshirani R. Statistical significance for genomewide studies. Proc. Natl Acad. Sci. USA. 2003;100:9440–9445. doi: 10.1073/pnas.1530509100. PubMed DOI PMC
Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible W-R. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 2005;139:5–17. doi: 10.1104/pp.105.063743. PubMed DOI PMC
Zhu Q, Žádníková P, Smet D, Van Der Straeten D, Benková E. Real-time analysis of the apical hook development. Methods Mol. Biol. 2017;1497:1–8. doi: 10.1007/978-1-4939-6469-7_1. PubMed DOI
Malamy JE, Benfey PN. Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development. 1997;124:33–44. PubMed
Sauer M, Paciorek T, Benkova E, Friml J. Immunocytochemical techniques for whole-mount in situ protein localization in plants. Nat. Protoc. 2006;1:98–103. doi: 10.1038/nprot.2006.15. PubMed DOI
Sanderfoot AA, Kovaleva V, Bassham DC, Raikhel NV. Interactions between syntaxins identify at least five SNARE complexes within the Golgi/prevacuolar system of the Arabidopsis cell. Mol. Biol. Cell. 2001;12:3733–3743. doi: 10.1091/mbc.12.12.3733. PubMed DOI PMC
Haas TJ, et al. The Arabidopsis AAA ATPase SKD1 is involved in multivesicular endosome function and interacts with its positive regulator LYST-INTERACTING PROTEIN5. Plant Cell. 2007;19:1295–1312. doi: 10.1105/tpc.106.049346. PubMed DOI PMC
Paciorek T, et al. Auxin inhibits endocytosis and promotes its own efflux from cells. Nature. 2005;435:1251–1256. doi: 10.1038/nature03633. PubMed DOI
Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22:4673–4680. doi: 10.1093/nar/22.22.4673. PubMed DOI PMC
Wu FH, et al. Tape-Arabidopsis sandwich-a simpler Arabidopsis protoplast isolation method. Plant Methods. 2009;5:16. doi: 10.1186/1746-4811-5-16. PubMed DOI PMC
Ischebeck T, Stenzel I, Heilmann I. Type B phosphatidylinositol-4-phosphate 5-kinases mediate Arabidopsis and Nicotiana tabacum pollen tube growth by regulating apical pectin secretion. Plant Cell. 2008;20:3312–3330. doi: 10.1105/tpc.108.059568. PubMed DOI PMC
Hempel F, et al. MAPKs influence pollen tube growth by controlling the formation of phosphatidylinositol 4,5-bisphosphate in an apical plasma membrane domain. Plant Cell. 2017;29:3030–3050. doi: 10.1105/tpc.17.00543. PubMed DOI PMC
Ischebeck T, et al. Functional cooperativity of enzymes of phosphoinositide conversion according to synergistic effects on pectin secretion in tobacco pollen tubes. Mol. Plant. 2010;3:870–881. doi: 10.1093/mp/ssq031. PubMed DOI
Cruz-Ramírez A, et al. A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cues to inform asymmetric stem cell division. Cell. 2012;150:1002–1015. doi: 10.1016/j.cell.2012.07.017. PubMed DOI PMC
Van Leene J, et al. An improved toolbox to unravel the plant cellular machinery by tandem affinity purification of Arabidopsis protein complexes. Nat. Protoc. 2014;10:169–187. doi: 10.1038/nprot.2014.199. PubMed DOI
Neumetzler L, et al. The FRIABLE1 gene product affects cell adhesion in Arabidopsis. PLoS ONE. 2012;7:e42914. doi: 10.1371/journal.pone.0042914. PubMed DOI PMC
Blumenkrantz N, Asboe-Hansen G. New method for quantitative determination of uronic acids. Anal. Biochem. 1973;54:484–489. doi: 10.1016/0003-2697(73)90377-1. PubMed DOI
Klavons JA, Bennett RD. Determination of methanol using alcohol oxidase and its application to methyl ester content of pectins. J. Agric. Food Chem. 1986;34:597–599. doi: 10.1021/jf00070a004. DOI
Fang L, et al. Loss of inositol phosphorylceramide sphingolipid mannosylation induces plant immune responses and reduces cellulose content in Arabidopsis. Plant Cell. 2016;28:2991–3004. doi: 10.1105/tpc.16.00186. PubMed DOI PMC
Eilers PHC. Parametric time warping. Anal. Chem. 2004;76:404–411. doi: 10.1021/ac034800e. PubMed DOI
Savitzky Abraham, Golay MJE. Smoothing and differentiation of data by simplified least squares procedures. Anal. Chem. 1964;36:1627–1639. doi: 10.1021/ac60214a047. DOI
Fähling M, Graf H, Siemens J. Pathotype separation of Plasmodiophora brassicae by the host plant. J. Phytopathol. 2003;151:425–430. doi: 10.1046/j.1439-0434.2003.00744.x. DOI
Expansin-mediated developmental and adaptive responses: A matter of cell wall biomechanics?
Xyloglucan Remodeling Defines Auxin-Dependent Differential Tissue Expansion in Plants