GDSL-domain proteins have key roles in suberin polymerization and degradation.
Arabidopsis
/ enzymology
Arabidopsis Proteins
/ genetics
Carboxylic Ester Hydrolases
/ genetics
Datasets as Topic
Endoderm
/ metabolism
Gene Knockout Techniques
Indoleacetic Acids
/ metabolism
Lipids
/ genetics
Plant Cells
/ metabolism
Plant Roots
/ metabolism
Polymerization
Protein Domains
Proteolysis
Journal
Nature plants
ISSN: 2055-0278
Titre abrégé: Nat Plants
Pays: England
ID NLM: 101651677
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
received:
17
07
2020
accepted:
25
01
2021
pubmed:
10
3
2021
medline:
30
4
2021
entrez:
9
3
2021
Statut:
ppublish
Résumé
Plant roots acquire nutrients and water while managing interactions with the soil microbiota. The root endodermis provides an extracellular diffusion barrier through a network of lignified cell walls called Casparian strips, supported by subsequent formation of suberin lamellae. Whereas lignification is thought to be irreversible, suberin lamellae display plasticity, which is crucial for root adaptative responses. Although suberin is a major plant polymer, fundamental aspects of its biosynthesis and turnover have remained obscure. Plants shape their root system via lateral root formation, an auxin-induced process requiring local breaking and re-sealing of endodermal lignin and suberin barriers. Here, we show that differentiated endodermal cells have a specific, auxin-mediated transcriptional response dominated by cell wall remodelling genes. We identified two sets of auxin-regulated GDSL lipases. One is required for suberin synthesis, while the other can drive suberin degradation. These enzymes have key roles in suberization, driving root suberin plasticity.
Identifiants
pubmed: 33686223
doi: 10.1038/s41477-021-00862-9
pii: 10.1038/s41477-021-00862-9
pmc: PMC7610369
mid: EMS114910
doi:
Substances chimiques
Arabidopsis Proteins
0
Indoleacetic Acids
0
Lipids
0
suberin
8072-95-5
Carboxylic Ester Hydrolases
EC 3.1.1.-
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
353-364Subventions
Organisme : Swiss National Science Foundation
ID : 157524
Pays : Switzerland
Organisme : Swiss National Science Foundation
ID : 164086
Pays : Switzerland
Organisme : Swiss National Science Foundation
ID : 136278
Pays : Switzerland
Organisme : Swiss National Science Foundation
ID : 156261
Pays : Switzerland
Organisme : European Research Council
ID : 616228
Pays : International
Commentaires et corrections
Type : CommentIn
Références
Castrillo, G. et al. Root microbiota drive direct integration of phosphate stress and immunity. Nature 543, 513–518 (2017).
doi: 10.1038/nature21417
pubmed: 28297714
pmcid: 5364063
Duran, P. et al. Microbial interkingdom interactions in roots promote Arabidopsis survival. Cell 175, 973–983 (2018).
doi: 10.1016/j.cell.2018.10.020
pubmed: 30388454
pmcid: 6218654
Hassani, M. A., Duran, P. & Hacquard, S. Microbial interactions within the plant holobiont. Microbiome 6, 58 (2018).
doi: 10.1186/s40168-018-0445-0
pubmed: 29587885
pmcid: 5870681
Banda, J. et al. Lateral root formation in Arabidopsis: a well-ordered LRexit. Trends Plant Sci. 24, 826–839 (2019).
doi: 10.1016/j.tplants.2019.06.015
pubmed: 31362861
Stoeckle, D., Thellmann, M. & Vermeer, J. E. Breakout-lateral root emergence in Arabidopsis thaliana. Curr. Opin. Plant Biol. 41, 67–72 (2018).
doi: 10.1016/j.pbi.2017.09.005
pubmed: 28968512
Andersen, T. G. et al. Tissue-autonomous phenylpropanoid production is essential for establishment of root barriers. Curr. Biol. (in the press).
Barberon, M. et al. Adaptation of root function by nutrient-induced plasticity of endodermal differentiation. Cell 164, 447–459 (2016).
doi: 10.1016/j.cell.2015.12.021
pubmed: 26777403
Li, B. et al. Role of LOTR1 in nutrient transport through organization of spatial distribution of root endodermal barriers. Curr. Biol. 27, 758–765 (2017).
doi: 10.1016/j.cub.2017.01.030
pubmed: 28238658
Yadav, V. et al. ABCG transporters are required for suberin and pollen wall extracellular barriers in Arabidopsis. Plant Cell 26, 3569–3588 (2014).
doi: 10.1105/tpc.114.129049
pubmed: 25217507
pmcid: 4213157
Vermeer, J. E. et al. A spatial accommodation by neighboring cells is required for organ initiation in Arabidopsis. Science 343, 178–183 (2014).
doi: 10.1126/science.1245871
pubmed: 24408432
Tian, Q., Uhlir, N. J. & Reed, J. W. Arabidopsis SHY2/IAA3 inhibits auxin-regulated gene expression. Plant Cell 14, 301–319 (2002).
doi: 10.1105/tpc.010283
pubmed: 11884676
pmcid: 152914
Fukaki, H., Tameda, S., Masuda, H. & Tasaka, M. Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J. 29, 153–168 (2002).
doi: 10.1046/j.0960-7412.2001.01201.x
pubmed: 11862947
Swarup, K. et al. The auxin influx carrier LAX3 promotes lateral root emergence. Nat. Cell Biol. 10, 946–954 (2008).
doi: 10.1038/ncb1754
pubmed: 18622388
Lewis, D. R. et al. A kinetic analysis of the auxin transcriptome reveals cell wall remodeling proteins that modulate lateral root development in Arabidopsis. Plant Cell 25, 3329–3346 (2013).
doi: 10.1105/tpc.113.114868
pubmed: 24045021
pmcid: 3809535
Voß, U. et al. The circadian clock rephases during lateral root organ initiation in Arabidopsis thaliana. Nat. Commun. 6, 7641 (2015).
doi: 10.1038/ncomms8641
pubmed: 26144255
Bakan, B. & Marion, D. Assembly of the cutin polyester: from cells to extracellular cell walls. Plants 6, 57 (2017).
doi: 10.3390/plants6040057
pubmed: 29156572
pmcid: 5750633
Girard, A. L. et al. Tomato GDSL1 is required for cutin deposition in the fruit cuticle. Plant Cell 24, 3119–3134 (2012).
doi: 10.1105/tpc.112.101055
pubmed: 22805434
pmcid: 3426136
Naseer, S. et al. Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin. Proc. Natl Acad. Sci. USA 109, 10101–10106 (2012).
doi: 10.1073/pnas.1205726109
pubmed: 22665765
pmcid: 3382560
Philippe, G. et al. Ester cross-link profiling of the cutin polymer of wild-type and cutin synthase tomato mutants highlights different mechanisms of polymerization. Plant Physiol. 170, 807–820 (2016).
doi: 10.1104/pp.15.01620
pubmed: 26676255
Yeats, T. H. et al. The identification of cutin synthase: formation of the plant polyester cutin. Nat. Chem. Biol. 8, 609–611 (2012).
doi: 10.1038/nchembio.960
pubmed: 22610035
pmcid: 3434877
Berhin, A. et al. The root cap cuticle: a cell wall structure for seedling establishment and lateral root formation. Cell 176, 1367–1378 (2019).
doi: 10.1016/j.cell.2019.01.005
pubmed: 30773319
Philippe, G. et al. Cutin and suberin: assembly and origins of specialized lipidic cell wall scaffolds. Curr. Opin. Plant Biol. 55, 11–20 (2020).
doi: 10.1016/j.pbi.2020.01.008
pubmed: 32203682
Andersen, T. G. et al. Diffusible repression of cytokinin signalling produces endodermal symmetry and passage cells. Nature 555, 529–533 (2018).
doi: 10.1038/nature25976
pubmed: 29539635
pmcid: 6054302
Doblas, V. G. et al. Root diffusion barrier control by a vasculature-derived peptide binding to the SGN3 receptor. Science 355, 280–284 (2017).
doi: 10.1126/science.aaj1562
pubmed: 28104888
Fujita, S. et al. SCHENGEN receptor module drives localized ROS production and lignification in plant roots. EMBO J. 39, e103894 (2020).
doi: 10.15252/embj.2019103894
pubmed: 32187732
pmcid: 7196915
Lucas, M., Godin, C., Jay-Allemand, C. & Laplaze, L. Auxin fluxes in the root apex co-regulate gravitropism and lateral root initiation. J. Exp. Bot. 59, 55–66 (2008).
doi: 10.1093/jxb/erm171
pubmed: 17720688
Péret, B. et al. Auxin regulates aquaporin function to facilitate lateral root emergence. Nat. Cell Biol. 14, 991–998 (2012).
doi: 10.1038/ncb2573
pubmed: 22983115
Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998).
doi: 10.1046/j.1365-313x.1998.00343.x
pubmed: 10069079
Gasperini, D. et al. Multilayered organization of jasmonate signalling in the regulation of root growth. PLoS Genet. 11, e1005300 (2015).
doi: 10.1371/journal.pgen.1005300
pubmed: 26070206
pmcid: 4466561
Siligato, R. et al. MultiSite Gateway-compatible cell type-specific gene-inducible system for plants. Plant Physiol. 170, 627–641 (2016).
doi: 10.1104/pp.15.01246
pubmed: 26644504
Fauser, F., Schiml, S. & Puchta, H. Both CRISPR–Cas-based nucleases and nickases can be used efficiently for genome engineering in Arabidopsis thaliana. Plant J. 79, 348–359 (2014).
doi: 10.1111/tpj.12554
pubmed: 24836556
Li-Beisson, Y. et al. Acyl-lipid metabolism. Arabidopsis Book 11, e0161 (2013).
doi: 10.1199/tab.0161
pubmed: 23505340
pmcid: 3563272
Ursache, R., Andersen, T. G., Marhavy, P. & Geldner, N. A protocol for combining fluorescent proteins with histological stains for diverse cell wall components. Plant J. 93, 399–412 (2018).
doi: 10.1111/tpj.13784
pubmed: 29171896
Kremer, J. R., Mastronarde, D. N. & McIntosh, J. R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71–76 (1996).
doi: 10.1006/jsbi.1996.0013
pubmed: 8742726
Jan, M., Gobet, N., Diessler, S., Franken, P. & Xenarios, I. A multi-omics digital research object for the genetics of sleep regulation. Sci. Data 6, 258 (2019).
doi: 10.1038/s41597-019-0171-x
pubmed: 31672980
pmcid: 6823400
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
doi: 10.1093/bioinformatics/bts635
pubmed: 23104886
Anders, S., Pyl, P. T. & Huber, W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166–169 (2015).
doi: 10.1093/bioinformatics/btu638
pubmed: 25260700
Li, B. & Dewey, C. N. RSEM: accurate transcript quantification from RNA-seq data with or without a reference genome. BMC Bioinformatics 12, 323 (2011).
doi: 10.1186/1471-2105-12-323
pubmed: 21816040
pmcid: 3163565
Gu, Z., Eils, R. & Schlesner, M. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 32, 2847–2849 (2016).
doi: 10.1093/bioinformatics/btw313
pubmed: 27207943
Alexa, A. & Rahnenfuhrer, J. topGO: enrichment analysis for gene ontology. R package version 2.38.1 (2019).
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
doi: 10.1038/nmeth.2019
pubmed: 22743772