Root cap-derived cells and mucilage: a protective network at the root tip.
Border cells
Mucilage
Plants
Root extracellular trap
Root immunity
Journal
Protoplasma
ISSN: 1615-6102
Titre abrégé: Protoplasma
Pays: Austria
ID NLM: 9806853
Informations de publication
Date de publication:
Nov 2021
Nov 2021
Historique:
received:
30
01
2021
accepted:
27
04
2021
pubmed:
2
7
2021
medline:
18
1
2022
entrez:
1
7
2021
Statut:
ppublish
Résumé
Root cap-derived cells and mucilage provide the first line of defense of the plant against soil microbial pathogens. These cells form a mucilaginous root extracellular trap (RET), which also harbors a range of molecules including exDNA and defensive peptides and proteins much like the neutrophil extracellular trap (NET) of mammalians. Plant RETs resemble mucus structures found in mammalian systems and are rich in arabinogalactan proteins that have similarities to highly glycosylated human mucins. Human mucus and mucins regulate the intestinal flora microbiome through recruiting certain species of microbes and it is plausible that the arabinogalactan protein-rich mucilage found in plant roots fulfills a similar function by attracting specific microbes to the rhizosphere. The role of RETs in root defense functioning is highlighted.
Identifiants
pubmed: 34196784
doi: 10.1007/s00709-021-01660-y
pii: 10.1007/s00709-021-01660-y
doi:
Substances chimiques
Soil
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1179-1185Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Austria, part of Springer Nature.
Références
Allen A, Flemström G (2005) Gastroduodenal mucus bicarbonate barrier: protection against acid and pepsin. Am J Physiol Cell Physiol 288:C1-19. https://doi.org/10.1152/ajpcell.00102.2004
doi: 10.1152/ajpcell.00102.2004
pubmed: 15591243
pmcid: 15591243
An G, Wei B, Xia B, McDaniel MJ, Ju T, Cummings RD, Braun J, Xia L (2007) Increased susceptibility to colitis and colorectal tumors in mice lacking core 3-derived O-glycans. J. Exp Med 204:1417–1429
pubmed: 17517967
pmcid: 2118614
doi: 10.1084/jem.20061929
Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A (2004) Neutrophil extracellular trap traps kill bacteria. Science 303:1532–1535
Cannesan MA, Gangneux C, Lanoue A, Giron D, Laval K, Hawes M, Driouich A, Vicre-Gibouin M (2011) Association between border cell responses and localized root infection by pathogenic Aphanomyces euteiches. Ann Bot 108:459–469
pubmed: 21807690
pmcid: 3158693
doi: 10.1093/aob/mcr177
Cannesan MA, Durand C, Burel C, Gangneux C, Lerouge P, Ishii T, Laval K, Follet-Gueye ML, Driouich A, Vicré-Gibouin M (2012) Effect of arabinogalactan proteins from the root caps of pea and Brassica napus on Aphanomyces euteiches zoospore chemotaxis and germination. Plant Physiol 159:1658–1670
pubmed: 22645070
pmcid: 3425204
doi: 10.1104/pp.112.198507
Chambard M, Plasson C, Tournier I, Leprince J, Kiefer-Meyer M-C, Driouich A, Follet-Gueye M-L, Boulogne I (2021) New insights into plant extracellular DNA. A study in soybean root extracellular trap. Cells. https://doi.org/10.3390/cells10010069
Darwin C (1880) The power of movement in plants. John Murray, London
Del Campillo E, Abdel-Aziz A, Crawford D, Patterson SE (2004) Root cap specific expression of an endo-b-1,4-D D-glucanase (cellulase): a new marker to study root development in Arabidopsis. Annu Rev Plant Biol 56:309–323
Dharmani P, Srivastava V, Kissoon-Singh V et al (2009) Role of intestinal mucins in innate host defense mechanisms against pathogens. J Innate Immun 1:123–213
pubmed: 20375571
doi: 10.1159/000163037
pmcid: 20375571
Driouich A, Durand C, Cannesan MA, Percoco G, Vicré-Gibouin M (2010) Border cells versus border-like cells: are they alike? J Exp Bot 61:3827–3831
pubmed: 20643806
doi: 10.1093/jxb/erq216
pmcid: 20643806
Driouich A, Cannesan MC, Dardelle F, Durand C, Plancot B, Bernard S, Follet-Gueye ML, Vicré-Gibouin M (2012) Unity is strength: the power of border cells and border-like cells in relation with plant defense. Secretions and Exudates in Biological Systems, Signaling and Communication in Plants 12:91–107
doi: 10.1007/978-3-642-23047-9_5
Driouich A, Follet-Gueye ML, Vicré-Gibouin M, Hawes M (2013) Root border cells and secretions as critical elements in plant host defense. Curr Opin Plant Biol 16:489–495
pubmed: 23856080
doi: 10.1016/j.pbi.2013.06.010
pmcid: 23856080
Driouich A, Smith C, Ropitaux M, Chambard M, Boulogne I, Bernard S et al (2019) Root extracellular traps versus neutrophil extracellular traps in host defence, a case of functional convergence? Biol. Rev 94:1685–1700. https://doi.org/10.1111/brv.12522
doi: 10.1111/brv.12522
Durand C, Vicré-Gibouin M, Follet-Gueye ML, Duponchel L, Moreau M, Lerouge L, Driouich A (2009) The organization pattern of root border-like cells of Arabidopsis is dependent on cell wall homogalacturonan. Plant Physiol 150:1411–1421
pubmed: 19448034
pmcid: 2705035
doi: 10.1104/pp.109.136382
Duran-Flores D, Heil M (2018) Extracellular self-DNA as a damage-associated molecular pattern (DAMP) that triggers self-specific immunity induction in plants. Brain Behav Immun 72:78–88. https://doi.org/10.1016/j.bbi.2017.10.010
doi: 10.1016/j.bbi.2017.10.010
pubmed: 29042243
pmcid: 29042243
Galloway AF, Pedersen MJ, Merry B, Marcus SE, Blacker J, Benning LG, Field KJ, Knox JP (2017) Xyloglucan is released by plants and promotes soil particle aggregation. New Phytol 217:1128–1136
pubmed: 29139121
pmcid: 5813166
doi: 10.1111/nph.14897
Gaspar YM, Nam J, Schultz CJ, Lee LY, Gilson PR, Gelvin SB, Bacic A (2004) Characterization of the Arabidopsis lysine-rich arabinogalactan-protein AtAGP17 mutant (rat1) that results in a decreased efficiency of agrobacterium transformation. Plant Physiol 135:2162–2171. https://doi.org/10.1104/pp.104.045542
doi: 10.1104/pp.104.045542
pubmed: 15286287
pmcid: 520787
Gotté M, Ghosh R, Bernard S, Nguema-Ona E, Vicré-Gibouin M, Hara-Nishimura I, Driouich A (2015) Methyl jasmonate affects morphology, number and activity of endoplasmic reticulum bodies in Raphanus sativus root cells. Plant Cell Physiol 56:61–72
pubmed: 25305245
doi: 10.1093/pcp/pcu141
pmcid: 25305245
Gotté M, Bénard M, Kiefer-Meyer MC, Jaber R, Moore JP, Vicré-Gibouin M, Driouich A (2016) Endoplasmic reticulum body–related gene expression in different root zones of Arabidopsis isolated by laser-assisted microdissection. Plant Genome. https://doi.org/10.3835/plantgenome2015.08.0076
doi: 10.3835/plantgenome2015.08.0076
pubmed: 27898830
pmcid: 27898830
Halverson TWR, Wilton M, Poon KKH, Petri B, Lewenza S (2015) DNA is an antimicrobial component of neutrophil extracellular traps. PLoS Pathog 11:e1004593
pubmed: 25590621
pmcid: 4295883
doi: 10.1371/journal.ppat.1004593
Hawes MC, Bengough G, Cassab G, Ponce G (2003) Root caps and rhizosphere. J Plant Growth Regul 21:352–367
doi: 10.1007/s00344-002-0035-y
Hawes MC, Allen C, Turgeon G, Curlango-Rivera G, Tran TM, Huskey DA, Xiong Z (2016) Root border cells and their role in plant defense. Annu Rev Phytopathol 54:1–5
doi: 10.1146/annurev-phyto-080615-100140
Hinsinger P, Plassard C, Tang C et al (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248:43–59
doi: 10.1023/A:1022371130939
Ibáñez de Aldecoa AL, Zafra O, González-Pastor JE (2017) Mechanisms and regulation of extracellular DNA release and its biological roles in microbial communities. Front Microbiol 8:1390. https://doi.org/10.3389/fmicb.2017.01390
doi: 10.3389/fmicb.2017.01390
pubmed: 28798731
pmcid: 5527159
Jacoby RP, Chen L, Schwier M, Koprivova A, Kopriva S (2020) Recent advances in the role of plant metabolites in shaping the root microbiome. F1000Research, (F1000 Faculty Rev):151. https://doi.org/10.12688/f1000research.21796.1
Johansson MEV, Hansson GC (2016) Immunological aspects of intestinal mucus and mucins. Nat Rev Immunol 16:639–644
pubmed: 27498766
pmcid: 6435297
doi: 10.1038/nri.2016.88
Karve R, Suárez-Román F, Iyer-Pascuzzi AS (2016) The transcription factor NIN-LIKE PROTEIN7 controls border-like cell release. Plant Physiol 171:2101–2111
pubmed: 27221617
pmcid: 4936578
doi: 10.1104/pp.16.00453
Kawakubo M, Ito Y, Okimura Y, Kobayashi M, Sakura K, Kasama S, Fukuda MN, Fukuda M, Katsuyama T, Nakayama J (2004) Natural antibiotic function of a human gastric mucin against Helicobacter pylori infection. Science 305:1003–1006
pubmed: 15310903
doi: 10.1126/science.1099250
pmcid: 15310903
Kim YS, Ho SB (2010) Intestinal goblet cells and mucins in health and disease: recent insights and progress. Curr Gastroenterol Rep 12:319–330
pubmed: 20703838
pmcid: 2933006
doi: 10.1007/s11894-010-0131-2
Koroney AS, Plasson C, Pawlak B, Sidikou R, Driouich A, Menu-Bouaouiche L, Vicré-Gibouin M (2016) Root exudate of Solanum tuberosum is enriched in galactose-containing molecules and impacts the growth of Pectobacterium atrosepticum. Ann Bot 4:797–808
doi: 10.1093/aob/mcw128
Kumar N, Iyer-Pascuzzi AS (2020) Shedding the last layer: mechanisms of root cap cell release. Plants 308. https://doi.org/10.3390/plants9030308
Linden S, Sutton P, Karlsson N et al (2008) Mucins in the mucosal barrier to infection. Mucosal Immunol 1:183–197
pubmed: 19079178
pmcid: 7100821
doi: 10.1038/mi.2008.5
Martens EC, Roth R, Heuser JE et al (2009) Coordinate regulation of glycan degradation and polysaccharide capsule biosynthesis by a prominent human gut symbiont. J Biol Chem 284:18445–184575
pubmed: 19403529
pmcid: 2709373
doi: 10.1074/jbc.M109.008094
Meyer-Hoffert U, Hornef MW, Henriques-Normark B, Axelsson LG, Midtvedt T, Pütsep K, Andersson M (2008) Secreted enteric antimicrobial activity localises to the mucus surface layer. Gut 57:764–771
pubmed: 18250125
doi: 10.1136/gut.2007.141481
pmcid: 18250125
Monticolo F, Palomba E, Termolino P, Chiaiese P, De Alteriis E, Mazzoleni S, Chiusano ML (2020) The role of DNA in the extracellular environment: a focus on NETs, RETs and biofilms. Front Plant Sci 11:589837. https://doi.org/10.3389/fpls.2020.589837
doi: 10.3389/fpls.2020.589837
pubmed: 33424885
pmcid: 7793654
Mravec J, Guo X, Hansen AR, Schückel J, Kračun SK, Mikkelsen MD, Mouille G, Johansen IE, Ulvskov P, Domozych DS, Willats WGT (2017) Pea border cell maturation and release involve complex cell wall structural dynamics. Plant Physiol 174:1051–1066
pubmed: 28400496
pmcid: 5462005
doi: 10.1104/pp.16.00097
Nguema-Ona E, Vicre-Gibouin CMA, Driouich A (2013) Arabinogalactan proteins in root–microbe interactions. Trends Plant Sci 18:440–449
pubmed: 23623239
doi: 10.1016/j.tplants.2013.03.006
pmcid: 23623239
Nguema-Ona E, Vicre-Gibouin GM, Plancot B, Lerouge P, Bardor M, Driouich A (2014) Cell wall O-glycoproteins and N-glycoproteins: aspects of biosynthesis and function. Front Plant Sci. https://doi.org/10.3389/fpls.2014.00499
doi: 10.3389/fpls.2014.00499
pubmed: 25324850
pmcid: 4183102
Okshevsky M, Meyer RL (2015) The role of extracellular DNA in the establishment, maintenance and perpetuation of bacterial biofilms. Crit Rev Microbiol 41:341–352
pubmed: 24303798
doi: 10.3109/1040841X.2013.841639
pmcid: 24303798
Pascale A, Proieti S, Pantelides LS, Stringlis IA (2020) Modulation of the root microbiome by plant molecules: the basis for targeted disease suppression and plant growth promotion. Plant Sci Front. https://doi.org/10.3389/fpls.2019.01741
doi: 10.3389/fpls.2019.01741
Papayannopoulos V (2018) Neutrophil extracellular traps in immunity and disease. Nat Rev Immunol 18:134–147
pubmed: 28990587
doi: 10.1038/nri.2017.105
pmcid: 28990587
Plancot B, Santaella C, Jaber R, Kiefer-Meyer MC, Follet-Gueye ML, Leprince J, Gattin I, Souc C, Driouich A, Vicre-Gibouin M (2013) Deciphering the responses of root border-like cells of Arabidopsis and flax to pathogen-derived elicitors. Plant Physiol 163:1584–1597
pubmed: 24130195
pmcid: 3850203
doi: 10.1104/pp.113.222356
Ropitaux M, Bernard S, Follet-Gueye ML, Vicré M, Boulogne I, Driouich A (2019) Xyloglucan and cellulose form molecular cross-bridges connecting root border cells in pea (Pisum sativum). Plant Physiol Biochem 139:191–196
pubmed: 30904720
doi: 10.1016/j.plaphy.2019.03.023
pmcid: 30904720
Ropitaux M, Bernard S, Schapman D, Follet-Gueye ML, Vicré M, Boulogne I, Driouich A (2020) Root border cells and mucilage secretions of soybean, Glycine max (Merr) L.: characterization and role in interactions with the oomycete Phytophthora parasitica. Cells 9:2215. https://doi.org/10.3390/cells9102215
doi: 10.3390/cells9102215
pmcid: 7650559
Seifert GJ, Roberts K (2007) The biology of arabinogalactan proteins. Annu Rev Plant Biol 58:137–161
pubmed: 17201686
doi: 10.1146/annurev.arplant.58.032806.103801
pmcid: 17201686
Silva J, Ferraz R, Dupree P, Showalter AM, Coimbra S (2020) Three decades of advances in arabinogalactan-protein biosynthesis. Front Plant Sci 11:610377. https://doi.org/10.3389/fpls.2020.610377
doi: 10.3389/fpls.2020.610377
pubmed: 33384708
pmcid: 7769824
Stephenson MB, Hawes MC (1994) Correlation of pectin methylesterase activity in root caps of pea with root border cell separation. Plant Physiol 106:739–745
pubmed: 12232366
pmcid: 159582
doi: 10.1104/pp.106.2.739
Tran TM, MacIntyre A, Hawes MC, Allen C (2016) Escaping underground Nets: extracellular DNases degrade plant extracellular traps and contribute to virulence of the plant pathogenic bacterium Ralstonia solanacearum. PLoS Pathog 12:e1005686. https://doi.org/10.1371/journal.ppat.10056
doi: 10.1371/journal.ppat.10056
pubmed: 27336156
pmcid: 4919084
Vicré M, Santaella C, Blanchet S, Gateau A, Driouich A (2005) Root border-like cells of Arabidopsis thaliana: microscopical characterization and role in the interaction with rhizobacteria. Plant Physiol 138:998–1008
pubmed: 15908608
pmcid: 1150414
doi: 10.1104/pp.104.051813
Voiniciuc C, Yang B, Schmidt MH, Günl M, Usadel B (2015) Starting to gel: how arabidopsis seed coat epidermal cells produce specialized secondary cell walls. Int J Mol Sci 16:3452–3473
pubmed: 25658798
pmcid: 4346907
doi: 10.3390/ijms16023452
Wang P, Chen X, Goldbeck C, Chung E, Kang BH (2017) A distinct class of vesicles derived from the trans-Golgi mediates secretion of xylogalacturonan in the root border cell. Plant J 92:596–610
pubmed: 28865155
doi: 10.1111/tpj.13704
pmcid: 28865155
Weiller F, Moore JP, Young P, Driouich A, Vivier MA (2017) The Brassicaceae species Heliophila coronopifolia produces root border-like cells that protect the root tip and secrete defensin peptides. Ann Botany 119:803–813
Wen F, Zhu Y, Hawes MC (1999) Effect of pectin methylesterase gene expression on pea root development. Plant Cell 11:1129–1140
pubmed: 10368183
pmcid: 144245
doi: 10.1105/tpc.11.6.1129
Wen F, VanEtten HD, Tsaprailis G, Hawes MC (2007) Extracellular proteins in pea root tip and border cell exudates. Plant Physiol 143:773–783
pubmed: 17142479
pmcid: 1803736
doi: 10.1104/pp.106.091637
Wen F, White GJ, VanEtten HD, Xiong Z, Hawes MC (2009) Extracellular DNA is required for root tip resistance to fungal infection. Plant Physiol 151:820–829
pubmed: 19700564
pmcid: 2754639
doi: 10.1104/pp.109.142067
Western TL (2012) The sticky tale of seed coat mucilages: production, genetics, and role in seed germination and dispersal. Seed Sci Res 22:1–25
doi: 10.1017/S0960258511000249
Xie F, Williams A, Edwards A, Downie JA (2012) A plant arabinogalactan-like glycoprotein promotes a novel type of polar surface attachment by Rhizobium leguminosarum. Mol Plant Microbe Interact 25:250–258
pubmed: 21995765
doi: 10.1094/MPMI-08-11-0211
pmcid: 21995765
Yakushiji S, Ishiga Y, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y (2009) Bacterial DNA activates immunity in Arabidopsis thaliana. J Gen PlantPathol 75:227–234. https://doi.org/10.1007/s10327-009-0162-4
doi: 10.1007/s10327-009-0162-4
Yamada K, Goto-Yamada S, Nakazaki A et al (2020) Endoplasmic reticulum-derived bodies enable a single-cell chemical defense in Brassicaceae plants. Commun Biol 21. https://doi.org/10.1038/s42003-019-0739-1
Yipp BG, Kubes P (2013) NETosis: how vital is it? Blood 122:2784–2794
pubmed: 24009232
doi: 10.1182/blood-2013-04-457671