Skip to main content
SpringerLink
Log in

Rhizosphere humic acid interacts with root cell walls to reduce hydraulic conductivity and plant development

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Humic acids are ubiquitous, organic-end-products of the chemical and microbial degradation of dead biota in soils throughout the world. Humic acids can be transported in soil water as heterogeneous, supra-molecular, colloidal-agglomerates. Humic acid accumulation in the rhizosphere of transpiring plants may chemically stimulate development by increasing root availability of mineral nutrients and/or growth regulatory biomolecules. This report introduces novel, physical mechanisms by which humic acid can also reduce plant development. Effects of humic acid addition to the root media of intact maize plants (Zea mays L.) on their growth, transpiration and resistance to water deficits were assayed, as were the effects of external humic acid on the hydraulic conductivity of excised primary-roots. Humic acid reduced shoot growth, transpiration and resistance to water stress but not root growth. Root hydraulic conductivity was reduced by up to 44% via a time-, concentration- and size-dependent fouling mechanism resulting from humic acid accumulation at root cell-walls. Thus, humic acid is shown, apparently for the first time, to be able to exert novel physical effects in addition to its known chemical effects on plant development.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aguirre E, Lemenager D, Bacaicoa E, Fuentes M, Baigorri R, Angel Z, Jose GM (2009) The root application of a purified leonardite humic acid modifies the transcriptional regulation of the main physiological root responses to Fe deficiency in Fe-sufficient cucumber plants. Plant Physiol Biochem 47:215–223

    Article  CAS  PubMed  Google Scholar 

  • Asli S, Neumann PM (2009) Colloidal suspension of clay or titanium dioxide nanoparticles can inhibit leaf growth and transpiration via physical effects on root water transport. Plant Cell Environ 32:577–584

    Article  CAS  PubMed  Google Scholar 

  • Atiyeh RM, Lee S, Edwards CA, Arancon NQ, Metzger JD (2002) The influence of humic acids derived from earthworm-processed organic wastes on plant growth. Bioresour Technol 84:7–14

    Article  CAS  PubMed  Google Scholar 

  • Arancon NQ, Clive A, Edwards CA, Lee S, Byrne R (2006) Effects of humic acid from vermicompost on plant growth. Eur J Soil Biol 42:565–569

    Article  Google Scholar 

  • Arancon NQ, Lee S, Edwards CA, Atiyeh RM (2003). Effects of humic acid derived from cattle, food and paper-waste vermicomposts on growth of greenhouse plants. Pedobiologia 47:741–744

    Google Scholar 

  • Canellas LP, Olivares FL, Facanha AL, Facanha AR (2002) Humic acid isolated from earthworm compost enhance root elongation, lateral root emergence and plasma membrane H+-ATPase activity in maize roots. Plant Physiol 130:1951–1957

    Article  CAS  PubMed  Google Scholar 

  • Canellas LP, Junior LRLT, Dobbss LB, Silva CA, Medici LO, Zandonadi DB, Facanha AR (2008) Humic acids crossinteractions with root and organic acids. Ann Appl Biol 153:157–166

    CAS  Google Scholar 

  • Canellas LP, Spaccini R, Piccolo A, Dobbss LB, Okorokova-Facanha AL, Santos GD, Olivares FL, Facanha AR (2009) Relationships between chemical characteristics and root growth promotion of humic acids isolated from Brazilian oxisols. Soil Sci 174:611–620

    Article  CAS  Google Scholar 

  • Carpita N, Sabularse D, Montezinos D, Delmer D (1979) Determination of the pore size of cell walls of living plant cells. Science 205:1144–1147

    Article  CAS  PubMed  Google Scholar 

  • Chazen O, Neumann PM (1994) Hydraulic signals from the roots and rapid cell-wall hardening in growing maize (Zea mays L.) leaves are primary responses to polyethylene glycol-induced water deficits. Plant Physiol 104:1385–1392

    CAS  PubMed  Google Scholar 

  • Chazen O, Hartung W, Neumann PM (1995) The different effects of PEG 6000 and NaCl on leaf development are associated with differential inhibition of root water transport. Plant Cell Environ 18:727–735

    Article  CAS  Google Scholar 

  • Chen Y, Aviad T (1990) Effects of humic substances on plant growth. In: MacCarthy P, Clapp CE, Malcolm RL, Bloom PR (eds) Humic substances in soil and crop sciences: selected readings. American Society of Agronomy and Soil Science Society of America, Madison, pp 161–186

    Google Scholar 

  • Chen Y, Katan G, Gamliel A, Aviad T, Schnitzer M (2000) Involvement of soluble organic matter in increased plant growth in solarized soils. Biol Fertil Soils 32:28–34

    Article  CAS  Google Scholar 

  • Cochard H (2002) Xylem embolism and drought-induced stomatal closure in maize. Planta 215:466–471

    Article  CAS  PubMed  Google Scholar 

  • Contreras AE, Kim A, Li Q (2009) Combined fouling of nanofiltration membranes: Mechanisms and effect of organic matter. J Membr Sci 327:87–95

    Article  CAS  Google Scholar 

  • Dobbss LB, Medici LO, Peres LEP, Pino-Nunes LE, Rumjanek VM, Facanha AR, Canellas LP (2007) Changes in root development of Arabidopsis promoted by organic matter from oxisols. Ann Appl Biol 151:1–13

    Article  Google Scholar 

  • Goosen MFA, Sablani SS, Ai-Hinai H, Ai-Obeidani S, Al-Belushi R, Jackson D (2004) Fouling of reverse osmosis and ultrafiltration membranes: a critical review. Sep Sci Technol 39:2261–2297

    Article  CAS  Google Scholar 

  • Haynes RJ, Naidu R (1998) Influence of time fertilizer and manure application on soil organic content and soil physical conditions:a review. Nutr Cycle Agroecosyst 51:123–137

    Article  Google Scholar 

  • Hong S, Elimelech M (1997) Chemical and physical aspects of natural organic matter (NOM) fouling of nanofiltration membranes. J Membr Sci 132:159–181

    Article  CAS  Google Scholar 

  • Hsiao TC, Xu LK (2000) Sensitivity of growth of roots versus leaves to water stress:biophysical analysis and relation to water transport. J Exp Bot 51:1595–1616

    Article  CAS  PubMed  Google Scholar 

  • Kawahigashi M, Sumida H, Yamamoto K (2005) Size and shape of soil humic acids estimated by viscosity and molecular weight. J Colloid Interface Sci 284:463–469

    Article  CAS  PubMed  Google Scholar 

  • Kuga S (1981) Pore size distribution analysis of gel substances by size exclusion chromatography. J Chromatogr A 206:449–461

    Article  CAS  Google Scholar 

  • Lee S, Cho J, Elimelech M (2005) Combined influence of natural organic matter (NOM) and colloidal particles on nanofiltration membrane fouling. J Membr Sci 262:27–41

    Article  CAS  Google Scholar 

  • Lu Z, Neumann PM (1999) Water stress inhibits hydraulic conductance and leaf growth in rice seedling but not the transport of water via mercury-sensitive water channels in the root. Plant Physiol 120:143–151

    Article  CAS  PubMed  Google Scholar 

  • Matyssek R, Tang AC, Boyer JS (1991) Plants can grow on internal water. Plant Cell Environ 14:925–930

    Article  Google Scholar 

  • Money NP (1989) Osmotic pressure of aqueous polyethylene glycols: relationship between molecular weight and vapor pressure deficit. Plant Physiol 91:766–769

    Article  CAS  PubMed  Google Scholar 

  • Muscolo A, Sidari M (2009) Carboxyl and phenolic humic fractions affect Pinus Nigra callus growth and metabolism. Soil Sci Soc Am J 73:1119–1129

    Article  CAS  Google Scholar 

  • Muscolo A, Sidari M, Attina E, Francioso O, Tugnoli V, Nardi S (2007). Biological activity of humic substances is related to their chemical structure. Soil Science Society of America Journal 71:75–85

    Google Scholar 

  • Nardi S, Pizzeghello D, Muscolo A, Vianello A (2002). Physiological effects of humic substances on higher plants. Soil Biology and Biochemistry 34:1527–1536

  • Neumann PM, Weissman R, Stefano G, Mancuso S (2010) Accumulation of xylem transported protein at pit membranes and associated reductions in hydraulic conductance. J Exp Bot 61:1711–1717

    Article  CAS  PubMed  Google Scholar 

  • Piccolo A (2001) The supramolecular structure of humic substances. Soil Sci 166:810–832

    Article  CAS  Google Scholar 

  • Piccolo A, Nardi S, Concheri G (1996) Macromolecular changes of soil humic substances induced by interactions with organic acids. Eur J Soil Sci 47:319–328

    Article  CAS  Google Scholar 

  • Pinton R, Cesco S, Iacolettig G, Astolfi S, Varanini Z (1999) Modulation of NO −3 uptake by water-extractable humic substances: involvement of root plasma membrane H+ATPase. Plant Soil 215:155–161

    Article  CAS  Google Scholar 

  • Quaggiotti S, Ruperti B, Pizzeghello D, Francioso O, Tugnoli V, Nardi S (2004) Effect of low molecular size humic substances on nitrate uptake and expression of genes involved in nitrate transport in maize (Zea mays L.). J Exp Bot 55:803–813

    Article  CAS  PubMed  Google Scholar 

  • Rebhun M, Manka J (1971) Classification of organics in secondary effluents. Environ Sci Technol 5:606–609

    Article  CAS  Google Scholar 

  • Schmidt W, Santi S, Pinton R, Varanini Z (2007) Water-extractable humic substances alter root development and epidermal cell pattern in Arabidopsis. Plant Soil 300:259–267

    Article  CAS  Google Scholar 

  • Sharp RE, Davies WJ (1979) Solute regulation and growth by roots and shoots of water stressed maize plants. Planta 147:43–49

    Article  CAS  Google Scholar 

  • Steinberg CEW, Meinelt T, Timofeyev MA, Bittner M, Menzel R (2008) Humic substances (review series). Part 2: interactions with organisms. Environ Sci Pollut Res 15:128–135

    Article  Google Scholar 

  • Sutton R, Sposito G (2005) Molecular structure in soil humic substances: the new view. Environ Sci Technol 39:9009–9015

    Article  CAS  PubMed  Google Scholar 

  • Tal A (2006) Seeking sustainability: Israel’s evolving water management strategy. Science 313:1081–1084

    Article  CAS  PubMed  Google Scholar 

  • Vallini G, Pera A, Avio L, Valdrighi M, Giovannetti M (1993) Influence of humic acids on laurel growth, associated rhizospheric microorganisms, and mycorrhizal fungi. Biol Fertil Soils 16:1–4

    Article  CAS  Google Scholar 

  • Yuan W, Zydney AL (2000) Humic acid fouling during ultrafiltration. Environ Sci Technol 34:5043–5050

    Article  CAS  Google Scholar 

  • Zandonadi DB, Canellas LP, Facanha AR (2007) Indole acetic and humic acids induce lateral root development through a concerted plasmalemma and tonoplast H+ pumps activation. Planta 225:1583–1595

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Funding by FMW chair (PMN) and Technion graduate school (SA) is gratefully acknowledged.

Author information

Authors and Affiliations

  1. Department of Environmental, Water and Agricultural Engineering, Technion Israel Institute of Technology, Haifa, 32000, Israel

    Sare Asli & Peter M. Neumann

Authors
  1. Sare Asli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter M. Neumann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peter M. Neumann.

Additional information

Responsible Editor: Robert Reid.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Asli, S., Neumann, P.M. Rhizosphere humic acid interacts with root cell walls to reduce hydraulic conductivity and plant development. Plant Soil 336, 313–322 (2010). https://doi.org/10.1007/s11104-010-0483-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-010-0483-2

Keywords

Search

Navigation