Two chemically distinct root lignin barriers control solute and water balance.
Arabidopsis
/ cytology
Arabidopsis Proteins
/ genetics
Cell Membrane
/ metabolism
Cell Wall
/ genetics
Diffusion
Lignin
/ chemistry
Microscopy, Fluorescence
/ methods
Mutation
Phenylpropionates
/ metabolism
Plant Roots
/ cytology
Plants, Genetically Modified
RNA-Seq
/ methods
Transcription Factors
/ genetics
Water
/ metabolism
Xylem
/ genetics
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
19 04 2021
19 04 2021
Historique:
received:
12
10
2020
accepted:
11
03
2021
entrez:
20
4
2021
pubmed:
21
4
2021
medline:
11
5
2021
Statut:
epublish
Résumé
Lignin is a complex polymer deposited in the cell wall of specialised plant cells, where it provides essential cellular functions. Plants coordinate timing, location, abundance and composition of lignin deposition in response to endogenous and exogenous cues. In roots, a fine band of lignin, the Casparian strip encircles endodermal cells. This forms an extracellular barrier to solutes and water and plays a critical role in maintaining nutrient homeostasis. A signalling pathway senses the integrity of this diffusion barrier and can induce over-lignification to compensate for barrier defects. Here, we report that activation of this endodermal sensing mechanism triggers a transcriptional reprogramming strongly inducing the phenylpropanoid pathway and immune signaling. This leads to deposition of compensatory lignin that is chemically distinct from Casparian strip lignin. We also report that a complete loss of endodermal lignification drastically impacts mineral nutrients homeostasis and plant growth.
Identifiants
pubmed: 33875659
doi: 10.1038/s41467-021-22550-0
pii: 10.1038/s41467-021-22550-0
pmc: PMC8055973
doi:
Substances chimiques
Arabidopsis Proteins
0
MYB36 protein, Arabidopsis
0
Phenylpropionates
0
Transcription Factors
0
Water
059QF0KO0R
Lignin
9005-53-2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2320Subventions
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/L027739/1
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/N023927/1
Pays : United Kingdom
Références
Boerjan, W., Ralph, J. & Baucher, M. Lignin biosynthesis. Annu. Rev. Plant Biol. 54, 519–546 (2003).
pubmed: 14503002
doi: 10.1146/annurev.arplant.54.031902.134938
Lee, M. H. et al. Lignin‐based barrier restricts pathogens to the infection site and confers resistance in plants. EMBO J. 38, e1745-17 (2019).
doi: 10.15252/embj.2019101948
Vanholme, R., De Meester, B., Ralph, J. & Boerjan, W. Lignin biosynthesis and its integration into metabolism. Curr. Opin. Biotechnol. 56, 230–239 (2019).
pubmed: 30913460
doi: 10.1016/j.copbio.2019.02.018
Tobimatsu, Y. & Schuetz, M. Lignin polymerization: how do plants manage the chemistry so well? Curr. Opin. Biotechnol. 56, 75–81 (2018).
pubmed: 30359808
doi: 10.1016/j.copbio.2018.10.001
Schuetz, M. et al. Laccases direct lignification in the discrete secondary cell wall domains of protoxylem. Plant Physiol. 166, 798–807 (2014).
pubmed: 25157028
pmcid: 4213109
doi: 10.1104/pp.114.245597
Barros, J., Serk, H., Granlund, I. & Pesquet, E. The cell biology of lignification in higher plants. Ann. Bot. mcv046 https://doi.org/10.1093/aob/mcv046 (2015).
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).
pubmed: 22665765
doi: 10.1073/pnas.1205726109
pmcid: 3382560
Geldner, N. The endodermis. Annu. Rev. Plant Biol. 64, 531–558 (2013).
pubmed: 23451777
doi: 10.1146/annurev-arplant-050312-120050
Pfister, A. et al. A receptor-like kinase mutant with absent endodermal diffusion barrier displays selective nutrient homeostasis defects. Elife 3, e03115 (2014).
pubmed: 25233277
pmcid: 4164916
doi: 10.7554/eLife.03115
Baxter, I. et al. Biodiversity of mineral nutrient and trace element accumulation in Arabidopsis thaliana. PLoS ONE 7, e35121 (2012).
pubmed: 22558123
pmcid: 3338729
doi: 10.1371/journal.pone.0035121
Barbosa, I. C. R., Rojas-Murcia, N. & Geldner, N. The Casparian strip—one ring to bring cell biology to lignification? Curr. Opin. Biotechnol. 56, 121–129 (2018).
pubmed: 30502636
doi: 10.1016/j.copbio.2018.10.004
Roppolo, D. et al. A novel protein family mediates Casparian strip formation in the endodermis. Nature 473, 380–383 (2011).
pubmed: 21593871
doi: 10.1038/nature10070
Lee, Y., Rubio, M. C., Alassimone, J. & Geldner, N. A Mechanism for Localized Lignin Deposition in the Endodermis. Cell 153, 402–412 (2013).
pubmed: 23541512
doi: 10.1016/j.cell.2013.02.045
Rojas-Murcia, N. et al. High-order mutants reveal an essential requirement for peroxidases but not laccases in Casparian strip lignification. Proc. Natl Acad. Sci. USA 117, 29166–29177 (2020).
pubmed: 33139576
doi: 10.1073/pnas.2012728117
pmcid: 7682338
Hosmani, P. S. 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 110, 14498–14503 (2013).
pubmed: 23940370
doi: 10.1073/pnas.1308412110
pmcid: 3761638
Liberman, L. M., Sparks, E. E., Moreno-Risueno, M. A., Petricka, J. J. & Benfey, P. N. MYB36 regulates the transition from proliferation to differentiation in the Arabidopsis root. Proc. Natl Acad. Sci. USA 201515576 https://doi.org/10.1073/pnas.1515576112 (2015).
Kamiya, T. et al. The MYB36 transcription factor orchestrates Casparian strip formation. Proc. Natl Acad. Sci. USA 112, 10533–10538 (2015).
pubmed: 26124109
doi: 10.1073/pnas.1507691112
pmcid: 4547244
Fujita, S. et al. SCHENGEN receptor module drives localized ROS production and lignification in plant roots. EMBO J. 39, e103894 (2020).
pubmed: 32187732
pmcid: 7196915
doi: 10.15252/embj.2019103894
Nakayama, T. et al. A peptide hormone required for Casparian strip diffusion barrier formation in Arabidopsis roots. Science 355, 284–286 (2017).
pubmed: 28104889
doi: 10.1126/science.aai9057
Doblas, V. G. et al. Root diffusion barrier control by a vasculature-derived peptide binding to the SGN3 receptor. Science 355, 280–284 (2017).
pubmed: 28104888
doi: 10.1126/science.aaj1562
Alassimone, J. et al. Polarly localized kinase SGN1 is required for Casparian strip integrity and positioning. Nat. Plants 2, 16113 (2016).
pubmed: 27455051
doi: 10.1038/nplants.2016.113
Li, B. et al. Role of LOTR1 in nutrient transport through organization of spatial distribution of root endodermal barriers. Curr. Biol. 1–9 https://doi.org/10.1016/j.cub.2017.01.030 (2017).
Alassimone, J., Naseer, S. & Geldner, N. A developmental framework for endodermal differentiation and polarity. Proc. Natl Acad. Sci. USA 107, 5214–5219 (2010).
pubmed: 20142472
doi: 10.1073/pnas.0910772107
pmcid: 2841941
Agarwal, U. P., McSweeny, J. D. & Ralph, S. A. FT–Raman investigation of milled-wood lignins: softwood, hardwood, and chemically modified black spruce lignins. J. Wood Chem. Technol. 31, 324–344 (2011).
doi: 10.1080/02773813.2011.562338
Mahonen, A. P. Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science 311, 94–98 (2006).
pubmed: 16400151
doi: 10.1126/science.1118875
Lange, B. M., Lapierre, C. & Sandermann, H. Jr. Elicitor-induced spruce stress lignin (structural similarity to early developmental lignins). Plant Physiol. 108, 1277 (1995).
pubmed: 12228544
pmcid: 157483
doi: 10.1104/pp.108.3.1277
Fukushima, K. & Terashima, N. Heterogeneity in formation of lignin. Wood Sci. Technol. 25, 371–381 (1991).
doi: 10.1007/BF00226177
Westermark, U. The occurrence of p-hydroxyphenylpropane units in the middle-lamella lignin of spruce (Picea abies). Wood Sci. Technol. 19, 223–232 (1985).
doi: 10.1007/BF00392051
Lapierre, C. in Forage Cell Wall Structure and Digestibility 133–166 (John Wiley & Sons, Ltd, 1995). https://doi.org/10.2134/1993.foragecellwall.c6 .
Ride, J. P. Lignification in wounded wheat leaves in response to fungi and its possible rôle in resistance. Physiol. Plant Pathol. 5, 125–134 (1975).
doi: 10.1016/0048-4059(75)90016-8
Hammerschmidt, R., Bonnen, A. M., Bergstrom, G. C. & Baker, K. K. Association of epidermal lignification with nonhost resistance of cucurbits to fungi. Can. J. Bot. 63, 2393–2398 (1985).
doi: 10.1139/b85-342
Doster, M. A. & Bostock, R. M. Quantification of lignin formation in almond bark in response to wounding and infection by Phytophthora species. Phytopathology 78, 473–477 (1988).
doi: 10.1094/Phyto-78-473
Campbell, M. M. & Ellis, B. E. Fungal elicitor-mediated responses in pine cell cultures: cell wall-bound phenolics*. Int. J. Plant Biochem. 31, 737–742 (1992).
Rogers, L. A. et al. Comparison of lignin deposition in three ectopic lignification mutants. N. Phytol. 168, 123–140 (2005).
doi: 10.1111/j.1469-8137.2005.01496.x
Hématy, K. et al. A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr. Biol. 17, 922–931 (2007).
pubmed: 17540573
doi: 10.1016/j.cub.2007.05.018
Cheung, A. Y. & Wu, H.-M. THESEUS 1, FERONIA and relatives: a family of cell wall-sensing receptor kinases? Curr. Opin. Plant Biol. 14, 632–641 (2011).
pubmed: 21963060
doi: 10.1016/j.pbi.2011.09.001
Liu, J., Osbourn, A. & Ma, P. MYB transcription factors as regulators of phenylpropanoid metabolism in plants. Mol. Plant 8, 689–708 (2015).
pubmed: 25840349
doi: 10.1016/j.molp.2015.03.012
Chezem, W. R., Memon, A., Li, F. -S., Weng, J. -K. & Clay, N. K. SG2-Type R2R3-MYB transcription factor MYB15 controls defense-induced lignification and basal immunity in Arabidopsis. Plant Cell Online 29, 1907–1926 (2017).
doi: 10.1105/tpc.16.00954
Kim, S. H. et al. The Arabidopsis R2R3 MYB transcription factor MYB15 is a key regulator of lignin biosynthesis in effector-triggered immunity. Front. Plant Sci. 11, 583153 (2020).
pubmed: 33042196
pmcid: 7527528
doi: 10.3389/fpls.2020.583153
Kai, K. et al. Scopoletin is biosynthesized via ortho-hydroxylation of feruloyl CoA by a 2-oxoglutarate-dependent dioxygenase in Arabidopsis thaliana. Plant J. 55, 989–999 (2008).
pubmed: 18547395
doi: 10.1111/j.1365-313X.2008.03568.x
Vanholme, R. et al. COSY catalyses trans–cis isomerization and lactonization in the biosynthesis of coumarins. Nat. Plants 5, 1066–1075 (2019).
pubmed: 31501530
doi: 10.1038/s41477-019-0510-0
Djébali, N. et al. Partial resistance of Medicago truncatula to Aphanomyces euteiches is associated with protection of the root stele and is controlled by a major QTL rich in proteasome-related genes. MPMI 22, 1043–1055 (2009).
pubmed: 19656040
doi: 10.1094/MPMI-22-9-1043
Turner, M. et al. Dissection of bacterial Wilt on Medicago truncatula revealed two type III secretion system effectors acting on root infection process and disease development. Plant Physiol. 150, 1713–1722 (2009).
pubmed: 19493968
pmcid: 2719136
doi: 10.1104/pp.109.141523
Thomas, R. et al. Soybean root suberin: anatomical distribution, chemical composition, and relationship to partial resistance to Phytophthora sojae. Plant Physiol. 144, 299–311 (2007).
pubmed: 17494920
pmcid: 1913776
doi: 10.1104/pp.106.091090
Holbein, J. et al. Root endodermal barrier system contributes to defence against plant‐parasitic cyst and root‐knot nematodes. Plant J. 100, 221–236 (2019).
pubmed: 31322300
doi: 10.1111/tpj.14459
Kroemer, K. in Wurzelhaut, Hypodermis und Endodermis der Angiospermenwurzel 59 (Bibl Bot, 1903).
Behrisch, R. Zur Kenntnis der Endodermiszelle. Ber. Dtsch. Bot. Ges. 44, 162–164 (1926).
Wang, P. et al. Surveillance of cell wall diffusion barrier integrity modulates water and solute transport in plants. Sci. Rep. 9, 4227 (2019).
pubmed: 30862916
pmcid: 6414709
doi: 10.1038/s41598-019-40588-5
Fernández-Marcos, M. et al. Control of Arabidopsis lateral root primordium boundaries by MYB36. New Phytol. 213, 105–112 (2016).
pubmed: 27891649
pmcid: 5126979
doi: 10.1111/nph.14304
Javot, H. & Maurel, C. The role of aquaporins in root water uptake. Ann. Bot. 90, 301–313 (2002).
pubmed: 12234142
pmcid: 4240399
doi: 10.1093/aob/mcf199
Javot, H. et al. Role of a single aquaporin isoform in root water uptake. Plant Cell 15, 509–522 (2003).
pubmed: 12566588
pmcid: 141217
doi: 10.1105/tpc.008888
Alexandersson, E. et al. Whole gene family expression and drought stress regulation of aquaporins. Plant Mol. Biol. 59, 469–484 (2005).
pubmed: 16235111
doi: 10.1007/s11103-005-0352-1
Olas, J. J., Fichtner, F. & Apelt, F. All roads lead to growth: imaging-based and biochemical methods to measure plant growth. J. Exp. Bot. 71, 11–21 (2019).
pmcid: 6913701
doi: 10.1093/jxb/erz406
Salas-González, I. et al. Coordination between microbiota and root endodermis supports plant mineral nutrient homeostasis. Science 371, eabd0695 (2021).
pubmed: 33214288
doi: 10.1126/science.abd0695
Andersen, T. G. et al. Diffusible repression of cytokinin signalling produces endodermal symmetry and passage cells. Nature 555, 529–533 (2018).
pubmed: 29539635
pmcid: 6054302
doi: 10.1038/nature25976
Barberon, M. et al. Adaptation of root function by nutrient-induced plasticity of endodermal differentiation. Cell 164, 447–459 (2016).
pubmed: 26777403
doi: 10.1016/j.cell.2015.12.021
Vermeer, J. E. M. et al. A spatial accommodation by neighboring cells is required for organ initiation in Arabidopsis. Science 343, 178–183 (2014).
pubmed: 24408432
doi: 10.1126/science.1245871
Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998).
pubmed: 10069079
doi: 10.1046/j.1365-313x.1998.00343.x
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).
pubmed: 29171896
doi: 10.1111/tpj.13784
Beeckman, T. & Viane, R. Embedding thin plant specimens for oriented sectioning. Biotech. Histochem. 75, 1–4 (1999).
Lord, S. J., Velle, K. B., Mullins, R. D. & Fritz-Laylin, L. K. SuperPlots: communicating reproducibility and variability in cell biology. J. Cell Biol. 219,, 94–10 (2020).
doi: 10.1083/jcb.202001064
Logemann, J., Schell, J. & Willmitzer, L. Improved method for the isolation of RNA from plant tissues. Anal. Biochem. 163, 16–20 (1987).
pubmed: 2441623
doi: 10.1016/0003-2697(87)90086-8
Bushnell, B., Rood, J. & Singer, E. BBMerge—accurate paired shotgun read merging via overlap. PLoS ONE 12, e0185056 (2017).
pubmed: 29073143
pmcid: 5657622
doi: 10.1371/journal.pone.0185056
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
pubmed: 23104886
doi: 10.1093/bioinformatics/bts635
Czechowski, T., Stitt, M., Altmann, T., Udvardi, M. K. & Scheible, W.-R. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139, 5–17 (2005).
pubmed: 16166256
pmcid: 1203353
doi: 10.1104/pp.105.063743
Morreel, K. et al. Genetical metabolomics of flavonoid biosynthesis in Populus: a case study. Plant J. 47, 224–237 (2006).
pubmed: 16774647
doi: 10.1111/j.1365-313X.2006.02786.x
Morreel, K. et al. Systematic structural characterization of metabolites in Arabidopsis via candidate substrate-product pair networks. Plant Cell 26, 929–945 (2014).
pubmed: 24685999
pmcid: 4001402
doi: 10.1105/tpc.113.122242
R Core Team. in R: A language and environment for statistical computing (R Foundation for Statistical Computing, R Core Team, 2018).
Burbidge, J. B., Magee, L. & Robb, A. L. Alternative transformations to handle extreme values of the dependent variable. J. Am. Stat. Assoc. 83, 123–127 (1988).
doi: 10.1080/01621459.1988.10478575
Lê, S., Josse, J. & Husson, F. FactoMineR: an R package for multivariate analysis. J. Stat. Softw. 25, 1–18 (2008).
doi: 10.18637/jss.v025.i01
Danku, J. M. C., Lahner, B., Yakubova, E. & Salt, D. E. Large-scale plant ionomics. Methods Mol. Biol. 953, 255–276 (2013).
pubmed: 23073889
Vanholme, B., Houari, El,I. & Boerjan, W. Bioactivity: phenylpropanoids’ best kept secret. Curr. Opin. Biotechnol. 56, 156–162 (2018).
pubmed: 30530240
doi: 10.1016/j.copbio.2018.11.012