Skip to main content
Log in

Root cap–derived cells and mucilage: a protective network at the root tip

  • Review
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Halverson TWR, Wilton M, Poon KKH, Petri B, Lewenza S (2015) DNA is an antimicrobial component of neutrophil extracellular traps. PLoS Pathog 11:e1004593

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hawes MC, Bengough G, Cassab G, Ponce G (2003) Root caps and rhizosphere. J Plant Growth Regul 21:352–367

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kim YS, Ho SB (2010) Intestinal goblet cells and mucins in health and disease: recent insights and progress. Curr Gastroenterol Rep 12:319–330

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nguema-Ona E, Vicre-Gibouin CMA, Driouich A (2013) Arabinogalactan proteins in root–microbe interactions. Trends Plant Sci 18:440–449

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Papayannopoulos V (2018) Neutrophil extracellular traps in immunity and disease. Nat Rev Immunol 18:134–147

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  Google Scholar 

  • Seifert GJ, Roberts K (2007) The biology of arabinogalactan proteins. Annu Rev Plant Biol 58:137–161

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Wen F, Zhu Y, Hawes MC (1999) Effect of pectin methylesterase gene expression on pea root development. Plant Cell 11:1129–1140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wen F, VanEtten HD, Tsaprailis G, Hawes MC (2007) Extracellular proteins in pea root tip and border cell exudates. Plant Physiol 143:773–783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to acknowledge all the students who contributed (and are contributing) to the research on the structural and functional properties of root cap–derived cells in our laboratory.

Funding

This study received financial support from the University of Rouen Normandy (Fra), the University of Stellenbosh (RSA), and la Région de Normandie.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Azeddine Driouich.

Additional information

Handling Editor: Andreas Holzinger

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

In memory of Ursula Lütz-Meindl

“We believe that there is no structure in plants more wonderful, as far as its functions are concerned, than the tip of the radicle”—Darwin (1880)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Driouich, A., Gaudry, A., Pawlak, B. et al. Root cap–derived cells and mucilage: a protective network at the root tip. Protoplasma 258, 1179–1185 (2021). https://doi.org/10.1007/s00709-021-01660-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-021-01660-y

Keywords

Navigation