Plant and Soil

, Volume 332, Issue 1–2, pp 267–275 | Cite as

Transient exposure of root tips to primary and secondary metabolites: Impact on root growth and production of border cells

  • Gilberto Curlango-Rivera
  • Denise V. Duclos
  • Jean J. Ebolo
  • Martha C. HawesEmail author
Regular Article


Here we describe the use of Pisum sativum L. as a model system to measure how short-term treatment of root tips with soluble metabolites can influence root growth and release of root exudates. The results revealed that even a 3-minute exposure of root tips to metabolites normally released from roots into the rhizosphere (e.g. rhamnose, ferulic acid, salicylic acid) can significantly influence root growth without affecting production of border cells and associated exudates. Conversely, products including caffeine, saccharide lactone, and pisatin alter production of border cells, without affecting root growth. Understanding how root-derived and exogenous metabolites can selectively impact root function may yield benefits in crop production, especially in greenhouse agriculture systems where growing roots can be exposed to a significant accumulation of plant exudates.


Border cells Metabolites Rhizosphere Root cap Root exudates 



analysis of variance








2-phenylethyl 1-thio-beta-D-galactopyranoside


saccharide lactone


2,3,5-triiodobenzoic acid


  1. Bacic A, Moody SF, Clarke AE (1986) Structural analysis of secreted root slime from maize. Plant Physiol 80:771–777CrossRefPubMedGoogle Scholar
  2. Barlow PW (2003) The root cap: cell dynamics, cell differentiation and cap function. J Plant Growth Regul 21:261–286CrossRefGoogle Scholar
  3. Bertin C, Yang XH, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83CrossRefGoogle Scholar
  4. Bhuvaneswari TV, Turgeon BG, Bauer WD (1980) Early events in the infection of soybean (Glycine max L. Merr) by Rhizobium japonicum: I. Localization of infectible root cells. Plant Physiol 66:1027–1031CrossRefPubMedGoogle Scholar
  5. Brigham LA, Woo HH, Hawes MC (1995) Differential expression of proteins and mRNAs from border cells and root tips of pea. Plant Physiol 109:457–460PubMedGoogle Scholar
  6. Brigham LA, Woo HH, Wen F, Hawes MC (1998) Meristem specific suppression of mitosis and a global switch in gene expression in the root cap of pea by endogenous signals. Plant Physiol 118:1223–1231CrossRefPubMedGoogle Scholar
  7. Cruickshank IAM (1962) Studies on phytoalexins IV: the antimicrobial spectrum of pisatin. Aust J Biol Sci 15:147–159Google Scholar
  8. Curl EA, Truelove B (1986) The rhizosphere. Springer-Verlag, BerlinGoogle Scholar
  9. dos Santos WD, Ferrarese MLL, Nakamura CV, Mourão KSM, Mangolin CA, Ferrarese-Filho O (2008) Soybean (Glycine max) root lignification induced by ferulic acid. The possible mode of action. J Chem Ecol 9:1230–1241CrossRefGoogle Scholar
  10. Flaburiari A, Kristen U (1996) The influence of chlorsulfuron and metsulfuron methyl on root growth and on the ultrastructure of root tips of germinating maize seeds. Plant Soil 180:19–28CrossRefGoogle Scholar
  11. Graham TC (1991) Flavonoid and isoflavonoid distribution in developing soybean seedling tissues and in seed and root exudates. Plant Physiol 95:594–603CrossRefPubMedGoogle Scholar
  12. Gregory PJ (2006) Roots, rhizosphere and soil: the route to a better understanding of soil science? Eur J Soil Sci 57:2–12CrossRefGoogle Scholar
  13. Griffin GJ, Hale MG, Shay FJ (1976) Nature and quantity of sloughed organic matter by roots of axenic peanut plants. Soil Biol Biochem 8:29–32CrossRefGoogle Scholar
  14. Gunawardena U, Rodriguez M, Straney D, Romeo JT, VanEtten H, Hawes MC (2005) Tissue specific localization of pea (Pisum sativum L.) root infection by Nectria haematococca: Mechanisms and consequences. Plant Physiol 137:1363–1374CrossRefPubMedGoogle Scholar
  15. Hawes MC, Pueppke SG (1986) Isolated peripheral root cap cells: yield from different plants, and callus formation from single cells. Am J Bot 73:1466–1473CrossRefGoogle Scholar
  16. Hiltner L (1904) Über neurer erfahrungen und probleme auf dem gebiete der bodenbakteriologie unter besonderer berücksichtigung der gründüngung und brache. Arbeiten der Deitschen Landwirtschaftlichen Gesellschaft 98:59–78Google Scholar
  17. Hirsch AA, Bhuvaneswari TV, Torrey JG, Bisseling T (1989) Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proc Natl Acad Sci 86:1244–1248CrossRefPubMedGoogle Scholar
  18. Iijima M, Morita S, Barlow PW (2008) Structure and function of the root cap. Plant Prod Sci 11:17–27CrossRefGoogle Scholar
  19. Jones DD, Morre DJ (1973) Golgi apparatus mediated polysaccharide secretion by outer root cap cells of Zea mays. III. Control by exogenous sugars. Physiol Plant 28:68–72CrossRefGoogle Scholar
  20. Knee EM, Gong FC, Gao MS, Teplitski M, Jones AR, Foxworth A, Mort AJ, Bauer WD (2001) Root mucilage from pea and its utilization by rhizosphere bacteria as a sole carbon source. Mol Plant-Microbe Int 14:775–784CrossRefGoogle Scholar
  21. Knudson L (1917) The toxicity of galactose and mannose for green plants and the antagonistic action of other sugars toward these. Am J Bot 4:430–437CrossRefGoogle Scholar
  22. Levvy GA (1952) Baicalinase, a plant beta-glucuronidase. Biochem J 52:464–469PubMedGoogle Scholar
  23. Pickett-Heaps JD (1967) The effects of colchicine on the ultrastructure of dividing plant cells, xylem wall differentiation and distribution of cytoplasmic microtubules. Dev Biol 15:206–236CrossRefGoogle Scholar
  24. 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 differentiation in maize. Plant Cell Environ 28:719–731CrossRefPubMedGoogle Scholar
  25. Pramanik MHR, Nagai M, Asao T, Matsui Y (2000) Effects of temperature and photoperiod on phytotoxic root exudates of cucumber in hydroponic culture. J Chem Ecol 26:1953–1967CrossRefGoogle Scholar
  26. Rovira AD (1956) Plant root excretions in relation to the rhizosphere effect. I. The nature of root exudate from oats and peas. Plant Soil 7:178–194CrossRefGoogle Scholar
  27. Smith DL, Abbott JA, Gross KC (2002) Down-regulation of tomato beta galactosidase 4 results in decreased fruit softening. Plant Physiol 129:1755–1762CrossRefPubMedGoogle Scholar
  28. Stubbs VEC, Standing D, Knox OGG, Killham K, Bengough AG, Griffiths B (2004) Root border cells take up and release glucose-C. Ann Bot 93:221–224CrossRefPubMedGoogle Scholar
  29. Tsugeki R, Fedoroff NV (1999) Genetic ablation of root cap cells in Arabidopsis. PNAS 96:12941–12946CrossRefPubMedGoogle Scholar
  30. Uren RC (1993) Mucilage secretion and its interaction with soil, and contact reduction. Plant Soil 155:79–82CrossRefGoogle Scholar
  31. Van Egeraat AWSM (1975) Exudation of ninhydrin-positive compounds by pea seedling roots: a study of the sites of exudation and of the composition of the exudate. Plant Soil 42:37–47CrossRefGoogle Scholar
  32. Vanzin GF, Madson M, Carpita NC, Raikhel NV, Keegstra K (2002) The mur2 mutant of Arabidopsis thaliana lacks fucosylated xyloglucan because of a lesion in fucosyltransferase AtFUT1. PNAS 99:3340–3345CrossRefPubMedGoogle Scholar
  33. Wen F, Zhu Y, Brigham LA, Hawes MC (1999) Expression of an inducible pectinmethylesterase gene is required for border cell separation from roots of pea. Plant Cell 11:1129–1140CrossRefPubMedGoogle Scholar
  34. Wen F, Woo HH, Hirsch AM, Hawes MC (2004) Lethality of inducible, meristem-localized ectopic beta- glucuronidase expression in plants. Plant Mol Biol Rep 22:7–14CrossRefGoogle Scholar
  35. Wen F, VanEtten H, Tsaiprailis G, Hawes MC (2007) Extracellular proteins in Pisum sativum L. root tip and border cell exudates. Plant Physiol 143:773–783CrossRefPubMedGoogle Scholar
  36. Wen F, Celoy R, Price I, Ebolo JJ, Woo HH, Hawes MC (2008a) Identification and characterization of a rhizosphere beta-galactosidase from Pisum sativum L. Plant Soil 304:133–144CrossRefGoogle Scholar
  37. Wen F, Celoy R, Nguyen T, Zeng W, Keegstra K, Woo HH, Pauly M, Immerzee P, Hawes MC (2008b) Altered cell wall structure and function in pea hairy roots expressing Pisum sativum xyloglucan fucosyltransferase (Psfut1) antisense mRNA. Plant Cell Rep 27:1125–1135CrossRefPubMedGoogle Scholar
  38. Wen F, White G, VanEtten HD, Xiong Z, Hawes MC (2009a) Extracellular DNA is required for root tip resistance to fungal infection. Plant Physiol 151:820–829CrossRefPubMedGoogle Scholar
  39. Wen F, Woo HH, Pierson EA, Eldhuset TD, Fossdal CG, Nagy NE, Hawes MC (2009b) Synchronous elicitation of development in root caps induces transient gene expression changes common to legume and gymnosperm species. Plant Mol Biol Rep 27:58–68CrossRefGoogle Scholar
  40. Woo HH, Faull KF, Hirsch AM, Hawes MC (2003) Altered life cycle in Arabidopsis plants expressing PsUGT1, a UDP-glucuronosyltransferase-encoding gene from pea. Plant Physiol 133:538–548CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Gilberto Curlango-Rivera
    • 1
  • Denise V. Duclos
    • 1
  • Jean J. Ebolo
    • 1
  • Martha C. Hawes
    • 1
    Email author
  1. 1.Department of Plant Sciences, Division of Plant Pathology and Microbiology and Controlled Environment Agriculture CenterUniversity of ArizonaTucsonUSA

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