• This record comes from PubMed

Surveillance of cell wall diffusion barrier integrity modulates water and solute transport in plants

. 2019 Mar 12 ; 9 (1) : 4227. [epub] 20190312

Language English Country England, Great Britain Media electronic

Document type Journal Article, Research Support, Non-U.S. Gov't

Grant support
BB/N023927/1 Biotechnology and Biological Sciences Research Council - United Kingdom

Links

PubMed 30862916
PubMed Central PMC6414709
DOI 10.1038/s41598-019-40588-5
PII: 10.1038/s41598-019-40588-5
Knihovny.cz E-resources

The endodermis is a key cell layer in plant roots that contributes to the controlled uptake of water and mineral nutrients into plants. In order to provide such functionality the endodermal cell wall has specific chemical modifications consisting of lignin bands (Casparian strips) that encircle each cell, and deposition of a waxy-like substance (suberin) between the wall and the plasma membrane. These two extracellular deposits provide control of diffusion enabling the endodermis to direct the movement of water and solutes into and out of the vascular system in roots. Loss of integrity of the Casparian strip-based apoplastic barrier is sensed by the leakage of a small peptide from the stele into the cortex. Here, we report that such sensing of barrier integrity leads to the rebalancing of water and mineral nutrient uptake, compensating for breakage of Casparian strips. This rebalancing involves both a reduction in root hydraulic conductivity driven by deactivation of aquaporins, and downstream limitation of ion leakage through deposition of suberin. These responses in the root are also coupled to a reduction in water demand in the shoot mediated by ABA-dependent stomatal closure.

See more in PubMed

Geldner N. The endodermis. Annu. Rev. Plant Biol. 2013;64:531–558. doi: 10.1146/annurev-arplant-050312-120050. PubMed DOI

Andersen TG, Barberon M, Geldner N. Suberization — the second life of an endodermal cell. Current Opinion in Plant Biology. 2015;28:9–15. doi: 10.1016/j.pbi.2015.08.004. PubMed DOI

Hosmani PS, et al. Dirigent domain-containing protein is part of the machinery required for formation of the lignin-based Casparian strip in the root. Proc. Natl. Acad. Sci. USA. 2013;110:14498–14503. doi: 10.1073/pnas.1308412110. PubMed DOI PMC

Pfister, A. et al. A receptor-like kinase mutant with absent endodermal diffusion barrier displays selective nutrient homeostasis defects. Elife3 (2014). PubMed PMC

Kamiya, T. et al. The MYB36 transcription factor orchestrates Casparian strip formation. Proc. Natl. Acad. Sci. USA 201507691, 10.1073/pnas.1507691112 (2015). PubMed PMC

Barberon, M. et al. Adaptation of Root Function by Nutrient-Induced Plasticity of Endodermal Differentiation. Cell 1–35, 10.1016/j.cell.2015.12.021 (2016). PubMed

Li, B. et al. Role of LOTR1 in Nutrient Transport through Organization of Spatial Distribution of Root Endodermal Barriers. Curr. Biol. 1–9, 10.1016/j.cub.2017.01.030 (2017). PubMed

Kalmbach, L. et al. Transient cell-specific EXO70A1 activity in the CASP domain and Casparian strip localization. NaturePlants 1–9, 10.1038/nplants.2017.58 (2017). PubMed

Lee Y, Rubio MC, Alassimone J, Geldner N. A Mechanism for Localized Lignin Deposition in the Endodermis. Cell. 2013;153:402–412. doi: 10.1016/j.cell.2013.02.045. PubMed DOI

Baxter I, et al. Root Suberin Forms an Extracellular Barrier That Affects Water Relations and Mineral Nutrition in Arabidopsis. PLoS Genet. 2009;5:e1000492. doi: 10.1371/journal.pgen.1000492. PubMed DOI PMC

Doblas VG, et al. Root diffusion barrier control by a vasculature-derived peptide binding to the SGN3 receptor. Science. 2017;355:280–284. doi: 10.1126/science.aaj1562. PubMed DOI

Nakayama T, et al. A peptide hormone required for Casparian strip diffusion barrier formation in Arabidopsis roots. Science. 2017;355:284–286. doi: 10.1126/science.aai9057. PubMed DOI

Nawrath C, et al. Apoplastic Diffusion Barriers in Arabidopsis. The Arabidopsis Book. 2013;11:e0167–36. doi: 10.1199/tab.0167. PubMed DOI PMC

Ranathunge K, Schreiber L. Water and solute permeabilities of Arabidopsis roots in relation to the amount and composition of aliphatic suberin. Journal of Experimental Botany. 2011;62:1961–1974. doi: 10.1093/jxb/erq389. PubMed DOI PMC

Péret B, et al. Auxin regulates aquaporin function to facilitate lateral root emergence. Nature Cell Biology. 2012;14:991–998. doi: 10.1038/ncb2573. PubMed DOI

Santoni, V. In Plant Aquaporins285, 83–105 (Springer, Cham, 2017).

Bellati J, et al. Novel Aquaporin Regulatory Mechanisms Revealed by Interactomics. Mol Cell Proteomics. 2016;15:3473–3487. doi: 10.1074/mcp.M116.060087. PubMed DOI PMC

Maurel C, et al. Aquaporins in Plants. Physiological Reviews. 2015;95:1321–1358. doi: 10.1152/physrev.00008.2015. PubMed DOI

Koornneef M, Jorna ML, Brinkhorst-van der Swan DL, Karssen CM. The isolation of abscisic acid (ABA) deficient mutants by selection of induced revertants in non-germinating gibberellin sensitive lines of Arabidopsis thaliana (L.) heynh. Theor. Appl. Genet. 1982;61:385–393. doi: 10.1007/BF00272861. PubMed DOI

Di Laurenzio L, et al. The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell. 1996;86:423–433. doi: 10.1016/S0092-8674(00)80115-4. PubMed DOI

Shatil-Cohen A, Attia Z, Moshelion M. Bundle-sheath cell regulation of xylem-mesophyll water transport via aquaporins under drought stress: a target of xylem-borne ABA? The Plant Journal. 2011;67:72–80. doi: 10.1111/j.1365-313X.2011.04576.x. PubMed DOI

Takahashi F, et al. A small peptide modulates stomatal control via abscisic acid in long-distance signalling. Nature. 2018;556:235–238. doi: 10.1038/s41586-018-0009-2. PubMed DOI

Vermeer JEM, et al. A Spatial Accommodation by Neighboring Cells Is Required for Organ Initiation in Arabidopsis. Science. 2014;343:178–183. doi: 10.1126/science.1245871. PubMed DOI

Domergue F, et al. Three Arabidopsis Fatty Acyl-Coenzyme A Reductases, FAR1, FAR4, and FAR5, Generate Primary Fatty Alcohols Associated with Suberin Deposition. Plant Physiology. 2010;153:1539–1554. doi: 10.1104/pp.110.158238. PubMed DOI PMC

Naseer S, et al. Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin. Proc. Natl. Acad. Sci. USA. 2012;109:10101–10106. doi: 10.1073/pnas.1205726109. PubMed DOI PMC

Marsch-Martínez N, et al. An efficient flat-surface collar-free grafting method for Arabidopsis thaliana seedlings. Plant Methods. 2013;9:14. doi: 10.1186/1746-4811-9-14. PubMed DOI PMC

Malamy JE, Benfey PN. Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development. 1997;124:33–44. PubMed

Lux A, MORITA S, Abe J, ITO K. An Improved Method for Clearing and Staining Free-hand Sections and Whole-mount Samples*. Annals of Botany. 2005;96:989–996. doi: 10.1093/aob/mci266. PubMed DOI PMC

Ursache R, Andersen TG, Marhavy P, Geldner N. A protocol for combining fluorescent proteins with histological stains for diverse cell wall components. The Plant Journal. 2018;93:399–412. doi: 10.1111/tpj.13784. PubMed DOI

Livak KJ, Schmittgen TD. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method. Methods. 2001;25:402–408. doi: 10.1006/meth.2001.1262. PubMed DOI

Hilu KW, Taxon JR. 1984. Convenient method for studying grass leaf epidermis. JSTOR. 1984;33:413.

Javot H. The Role of Aquaporins in Root Water Uptake. Annals of Botany. 2002;90:301–313. doi: 10.1093/aob/mcf199. PubMed DOI PMC

Sutka M, et al. Natural variation of root hydraulics in Arabidopsis grown in normal and salt-stressed conditions. Plant Physiology. 2011;155:1264–1276. doi: 10.1104/pp.110.163113. PubMed DOI PMC

Novák O, et al. Tissue-specific profiling of the Arabidopsis thaliana auxin metabolome. The Plant Journal. 2012;72:523–536. doi: 10.1111/j.1365-313X.2012.05085.x. PubMed DOI

Floková K, et al. UHPLC-MS/MS based target profiling of stress-induced phytohormones. Phytochemistry. 2014;105:147–157. doi: 10.1016/j.phytochem.2014.05.015. PubMed DOI

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...