Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Altered carbon delivery from roots: rapid, sustained inhibition of border cell dispersal in response to compost water extracts

  • 357 Accesses

  • 4 Citations


Background and aims

In a previous study, a compost water extract (CWE) applied to pea seedlings resulted in >95 % protection against root infection. The protection was correlated with retention of a sheath of root border cells surrounding each root tip. A transient exposure to CWE was correlated with 80 % reduction in infection, and with retention of border cell sheaths. Early effects of CWE on border cell dispersal therefore were examined.

Materials and methods

Temporal and spatial dynamics of pea, maize, cotton, and cucumber border cell dispersal into water or CWE were measured.


Border cells formed a mass surrounding root tips within seconds after exposure to water, and most cells dispersed into suspension spontaneously. In CWE, >90 % of the border cell population instead remained appressed to the root surface, even after vigorous agitation. In cotton, for example, >25,000 border cells dispersed within seconds of immersion in water, but <100 border cells dispersed after >24 h in CWE.


Border cells can contribute >90 % of carbon released from young roots, and a single border cell can trap hundreds of bacteria within minutes. The impact of altered border cell dispersal on soil properties, plant nutrition, and root disease development warrants further study.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7



Compost water extract


Analysis of variance




  1. Baetz U, Martinoia E (2013) Root exudates: the hidden part of plant defense. Trends Plant Sci 19:90–98

  2. Bailey K, Lazarovits G (2003) Suppressing soil-borne diseases with residue management and organic amendments. Soil Tillage Res 72:169–180

  3. Ben-Yephet Y, Nelson EB (1999) Differential suppression of damping-off caused by Pythium aphananidermatum, P. irregulare, and P. myriotylum in composts at different temperatures. Plant Dis 83:356–360

  4. Brigham LA, Woo H, Nicoll SM, Hawes MC (1995) Differential expression of proteins and mRNAs from border cells and root tips of pea. Plant Physiol 109:457–463

  5. Brinkmann V, Reichard U, Goosman C, Fauler B, Uuhleman DS, Weiss Y, Weinrauch Y, Zuchlinsky A (2004) Neutrophil extracellular traps kill bacteria. Science 303:1532–1535

  6. Brinkmann V, Zychlinsky A (2012) NETs: is immunity the second function of chromatin? J Cell Biol 198:773–784

  7. Cai M, Wang N, Xing C, Wang F, Wu K, Du X (2013) Immobilization of aluminum with mucilage secreted by root cap and root border cells is related to aluminum resistance in Glycine max L. Pollut Res Int 12:8924–8933

  8. Carballo T, Gil MV, Calvo LF, Moran A (2009) The influence of aeration system, temperature, and compost origin on the phytotoxicity of compost tea. Compost Sci Util 17:127–139

  9. Chalk PM, Alberto MT, Magalhaes T, Ciao T (2012) Towards an understanding of the dynamics of compost N in the soil-plant-atmosphere system using 15N tracer. Plant Soil 362:373–388

  10. Chen MH, Nelson EB (2008) Seed-colonizing microbes from municipal biosolids compost suppress Pythium ultimum damping-off on different plant species. Phytopathology 98:1012–1018

  11. Craft CM, Nelson EB (1996) Microbial properties of composts that suppress damping-off and root rot of creeping bentgrass caused by Pythium graminicola. Appl Environ Microbiol 62:1550–1557

  12. Cummings JA, Miles CA, du Toit LJ (2009) Greenhouse evaluation of seed and drench treatments for organic management of soilborne pathogens of spinach. Plant Dis 93:1281–1929

  13. Curlango-Rivera G, Duclos DV, Ebolo JJ, Hawes MC (2010) Transient exposure of root tips to primary and secondary metabolites: impact on root growth and production of border cells. Plant Soil 332:267–275

  14. Curlango-Rivera G, Huskey DA, Mostafa A, Kessler JO, Xiong Z, Hawes MC (2013a) Intraspecies variation in cotton border cell production: rhizosphere microbiome implications. Am J Bot 100:9–15

  15. Curlango-Rivera G, Pew T, VanEtten HD, Xiong Z, Yu N, Hawes MC (2013b) Measuring root disease suppression in response to a compost water extract. Phytopathology 103:255–260

  16. Duong TTT, Pnefold C, Marschner P (2012) Amending soils of different texture with six compost types: impact on soil nutrient availability, plant growth and nutrient uptake. Plant Soil 354:197–209

  17. Ebid A, Ueno H, Ghoneim A, Asagi N (2008) Uptake of carbon and nitrogen derived from carbon-13 and nitrogen-15 dual-labeled maize residue compost applied to radish, komatsuna, and chingensai for three consecutive croppings. Plant Soil 304:241–248

  18. Elmer WH, McGovern RJ (2004) Efficacy of integrating biologicals with fungicides for the suppression of Fusarium wilt of cyclamen. Crop Prot 23:909–914

  19. Everts KL, Sardanelli S, Kratochvil RJ, Armentrout DK, Gallagher LE (2006) Root-knot and root-lesion nematode suppression by cover crops, poultry litter, and poultry litter compost. Plant Dis 90:487–492

  20. Fichtner DJ, Benson DM, Diab HG, Shew HD (2004) Abiotic and biological suppression of Phytophthora parasitica in a horticultural medium containing composted swine waste. Phytopathology 94:780–788

  21. Gochnauer MB, Sealey LJ, McCully ME (1990) Do detached root cap cells influence bacteria associated with maize roots? Plant Cell Environ 13:793–801

  22. Griffin GJ, Hale MG, Shay FJ (1976) Nature and quantity of sloughed organic matter produced by roots of axenic peanut plants. Soil Biol Biochem 8:29–32

  23. Guinel FC, McCully ME (1987) The cells shed by the root cap of Zea: their origin and some structural and physiological properties. Plant Cell Environ 10:565–578

  24. Hawes MC, Brigham LA (1992) Impact of root border cells on microbial populations in the rhizosphere. Adv Plant Pathol 8:119–148

  25. Hawes MC, Curlango-Rivera G, Wen F, White GJ, VanEtten HD, Xiong Z (2011) Extracellular DNA: the tip of root defenses? Plant Sci 180:741–745

  26. Hawes MC, Curlango-Rivera G, Xiong Z, Kessler JO (2012) Roles of root border cells in plant defense and regulation of rhizosphere microbial populations by extracellular trapping. Plant Soil 355:1–16

  27. Hawes MC, Wheeler H (1982) Factors affecting victorin-induced root cap cell death: temperature and plasmolysis. Physiol Plant Pathol 20:137–144

  28. Iverson S, Maier RM (2009) Effects of compost on colonization of roots of plants grown in metalliferous mine tailings, as examined by fluorescence in situ hybridization. Appl Environ Microbiol 75:842–847

  29. Kavroulakis N, Ntougias S, Besi MI, Katsou P, Damaskinou A, Ehaliotis C, Zervakis GI, Papadopoulou KK (2010) Antagonistic bacteria of composted agro-industrial residues exhibit antibiosis against soil-borne fungal plant pathogens and protection of tomato plants from Fusarium oxysporum f.sp radicis-lycopersici. Plant Soil 333:233–247

  30. Knudson L (1919) Viability of detached root cap cells. Am J Bot 6:309–310

  31. Larkin RP (2008) Relative effects of biological amendments and crop rotations on soil microbial communities and soilborne diseases of potato. Soil Biol Biochem 40:1341–1351

  32. Litterick AM, Harrier L, Wallace P, Watson CA, Wood M (2002) The role of uncomposted materials, composts, manures, and compost extracts in reducing pest and disease incidence and severity in sustainable temperate agricultural and horticultural crop production–a review. Crit Rev Plant Sci 23:453–479

  33. Marin F, Santos M, Dianez F, Carretero F, Gea FJ, Yau JA, Navarro MJ (2013) Characters of compost teas from different sources and their suppreessive effect on fungal phytopathogens. World J Microbiol Biotechnol 29:1371–1382

  34. Marks EAN, Alcaniz JM, Domene X (2014) Unintended effects of biochars on short-term plant growth in a calcareous soil. Plant Soil 385:87–105

  35. McKellar ME, Nelson EB (2003) Compost-induced suppression of Pythium damping-off is mediated by fatty-acid-metabolizing seed-colonizing microbial communities. Appl Environ Microbiol 69:452–460

  36. Noble R, Coventry E (2005) Suppression of soil-borne plant diseases with composts: a review. Biocontrol Sci Technol 15:3–20

  37. Odell RE, Dumlao MR, Samar D, Silk WK (2008) Stage-dependent border cell and carbon flow from roots to rhizosphere. Am J Bot 95:441–446

  38. Pausch J, Tian J, Riederer M, Kuzyakov Y (2013) Estimation of rhizodeposition at field scale: upscaling of a 14C labeling study. Plant Soil 364:273–285

  39. Perez-Esteban J, Escolastico C, Moliner A, Masaguer A, Ruiz-Fernandez J (2014) Phytostabilization of metals in mine soils using Brassica juncea in ombination with organic amendments. Plant Soil 377:97–109

  40. Pharand B, Carisse O, Benhamou N (2002) Cytological aspects of compost-mediated induced resistance against Fusarium crown and root rot in tomato. Phytopathology 92:424–438

  41. Ponce G, Barlow PW, Feldman LJ, Cassab GI (2005) Auxin and ethylene interactions control mitotic activity of the quiescent centre, root cap size, and pattern of cap cell differentiation in maize. Plant Cell Environ 28:719–732

  42. Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moenne-Loccoz Y (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321:341–361

  43. Rogers HT, Pearson RW, Pierre WH (1942) The source and phosphatase activity of exoenzyme systems of corn and tomato roots. Soil Sci 54:353–365

  44. Rovira AD (1991) Rhizosphere research--85 years of progress and frustration. In: Keister DL, Cregan PB (eds) The rhizosphere and plant growth. Kluwer Academic Publishers, Boston, pp 3–14

  45. Sabeh NC, Giacomelli GA, Kubota C (2011) Water use in a greenhouse in a semi-arid climate. Trans ASABE 54:1069–1077

  46. Sang MK, Kim KD (2011) Biocontrol activity and primed systemic resistance by compost water extracts against anthracnoses of pepper and cucumber. Phytopathology 101:732–740

  47. Scheuerell SJ, Mahaffee WF (2004) Compost tea as a container medium drench for suppressing seedling damping-off caused by Pythium ultimum. Phytopathology 94:1156–1163

  48. Singh PK, Vias D (2009) Biocontrol of plant diseases and sustainable agriculture. PNAS India Sect B Biol Sci 79:110–128

  49. Somasundaram S, Bonkowski M, Iijima M (2008) Functional role of mucilage-border cells: a complex facilitating protozoan effects on plant growth. Plant Prod Sci 11:344–351

  50. Tits M, Elsen A, Bries J, Vandendriessche H (2014) short-term and long-term effects of vegetable, fruit and garden waste compost applications in an arable crop rotation in Flanders. Plant Soil 376:43–59

  51. Vermeer J, McCully ME (1982) The rhizosphere in Zea: new insight into its structure and development. Planta 156:45–61

  52. 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

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

  54. Xu D, Raza W, Yu G, Zhao Q, Shen Q, Huang Q (2012) Phytotoxicity analysis of extracts from compost and their ability to inhibit soil-borne pathogenic fungi and reduce root-knot nematodes. World J Microbiol Biotechnol 28:1193–1201

  55. Zhang W, Dick WA, Hoitink HAJ (1996) Compost-induced acquired resistance in cucumber to Pythium root rot and anthracnose. Phytopathology 86:1066–1070

  56. Zhao X, Schmitt M, Hawes MC (2000) Species-dependent effects of border cells and root tip exudates on nematode behaviour. Phytopathology 90:1239–1245

  57. Zhu Y, Pierson LSIII, Hawes MC (1997) Induction of microbial genes for pathogenesis and symbiosis by chemicals from root border cells. Plant Physiol 115:1691–1698

Download references


We thank the National Science Foundation and the University of Arizona College of Agriculture and Life Science for support of studies defining border cell extracellular trapping phenomena, and we thank Chris Allen, North Central Instruments, for microscopy assistance.

Author information

Correspondence to Martha C. Hawes.

Additional information

Stacy Joy Tollefson and Gilberto Curlango-Rivera contributed equally to this study.

Responsible Editor: Tim S. George.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Tollefson, S.J., Curlango-Rivera, G., Huskey, D.A. et al. Altered carbon delivery from roots: rapid, sustained inhibition of border cell dispersal in response to compost water extracts. Plant Soil 389, 145–156 (2015). https://doi.org/10.1007/s11104-014-2350-z

Download citation


  • Root border cells
  • Rhizosphere microbiome
  • Carbon deposition
  • Belowground C
  • Root-derived C
  • Compost