Plant and Soil

, Volume 355, Issue 1–2, pp 1–16 | Cite as

Roles of root border cells in plant defense and regulation of rhizosphere microbial populations by extracellular DNA ‘trapping’

  • Martha C. Hawes
  • Gilberto Curlango-Rivera
  • Zhongguo Xiong
  • John O. Kessler
Marschner Review

Abstract

Background

As roots penetrate soil, specialized cells called ‘border cells’ separate from root caps and contribute a large proportion of exudates forming the rhizosphere. Their function has been unclear. Recent findings suggest that border cells act in a manner similar to that of white blood cells functioning in defense. Histone-linked extracellular DNA (exDNA) and proteins operate as ‘neutrophil extracellular traps’ to attract and immobilize animal pathogens. DNase treatment reverses trapping and impairs defense, and mutation of pathogen DNase results in loss of virulence.

Scope

Histones are among a group of proteins secreted from living border cells. This observation led to the discovery that exDNA also functions in defense of root caps. Experiments revealed that exDNA is synthesized and exported into the surrounding mucilage which attracts, traps and immobilizes pathogens in a host-microbe specific manner. When this plant exDNA is degraded, the normal resistance of the root cap to infection is abolished.

Conclusions

Research to define how exDNA may operate in plant immunity is needed. In the meantime, the specificity and stability of exDNA and its association with distinct microbial species may provide an important new tool to monitor when, where, and how soil microbial populations become established as rhizosphere communities.

Keywords

Root border cells Mucilage Root cap Extracellular DNA (exDNA) Root exudates Rhizosphere colonization 

Abbreviations

exDNA

Extracellular DNA

DAPI

4′,6-diamidino-2-phenylindole

References

  1. Abdallah DS, Lin C, Ball CJ et al (2012) Toxoplasma gondii triggers release of human and mouse neutrophil extracellular traps. Infection Immun 80:768–777CrossRefGoogle Scholar
  2. Amulic B, Hayes G (2011) Neutrophil extracellular traps. Curr Biol 21:R297–R298PubMedCrossRefGoogle Scholar
  3. Atkinson TG, Neal JL, Larson RI (1975) Genetical control of the rhizosphere of wheat. In: Bruehl GW (ed) Biology and control of soil-borne plant pathogens. American Phytopathological Society, St. PaulGoogle Scholar
  4. Bacic A, Moody SF, Clarke AE (1986) Structural analysis of secreted root slime from maize. Plant Physiol 80:771–777PubMedCrossRefGoogle Scholar
  5. Baluska F, Volkmann D, Hauskrecht M, Barlow PW (1996) Root cap mucilage and extracellular calcium as modulators of cellular growth in postmitotic growth zones of the maize root apex. Bot Acta 109:25–34Google Scholar
  6. Bednarek P, Kwon C, Schulze-Lefert P (2010) Not a peripheral issue: secretion in plant-microbe interactions. Curr Opin Plant Biol 13:378–385PubMedCrossRefGoogle Scholar
  7. Bergsson G, Agerberth B, Jornvall H, Gudmundsson GH (2005) Isolation and identification of antimicrobial components from the epidermal mucus of Atlantic cod (Gadus morhua). FEBS J 272:4960–4969PubMedCrossRefGoogle Scholar
  8. Bowen GD, Rovira AD (1976) Microbial colonization of plant roots. Ann Rev Phytopathol 114:121–144CrossRefGoogle Scholar
  9. Bozhkov AI, Kuznetsova YA, Menzyanova NG (2007) Interrelationship between the growth rate of wheat roots, their excretory activity and the number of border cells. Russian J Plant Physiol 54:97–103CrossRefGoogle Scholar
  10. Brady NC, Weil RR (2010) Elements of the nature and properties of soils. Prentice HallGoogle Scholar
  11. Brigham LA, Woo HH, Nicoll SM, Hawes MC (1995) Differential expression of proteins and messenger-RNAs from border cells and root tips of pea. Plant Physiol 109:457–463PubMedGoogle Scholar
  12. 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 118:1223–1231PubMedCrossRefGoogle Scholar
  13. Brigham LA, Michaels PJ, Flores HE (1999) Cell-specific production and antimicrobial activity of naphthoquinones in roots of Lithospermum erythrorhizon. Plant Physiol 119:417–428PubMedCrossRefGoogle Scholar
  14. Brinkmann V, Zychlinsky A (2007) Beneficial suicide: why neutrophils die to make NETs. Nat Rev Microbiol 5:577–582PubMedCrossRefGoogle Scholar
  15. Brinkmann V, Brichard U, Goosmann C et al (2004) Neutrophil extracellular traps kill bacteria. Science 303:1532–1535PubMedCrossRefGoogle Scholar
  16. Brisson RF, Tenhaken R, Lamb C (1994) Function of oxidative cross linking of cell wall structural proteins in plant disease resistance. Plant Cell 6:1703–1712PubMedCrossRefGoogle Scholar
  17. Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco J (2008) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74:738–744PubMedCrossRefGoogle Scholar
  18. Bruehl GW (1987) Soilborne plant pathogens. Macmillan Publishing Company, NY, USAGoogle Scholar
  19. Caffaro MM, Vivanco JM, Gutierrez BFH et al (2011) The effect of root exudates on root architecture in Arabidopsis thaliana. Plant Growth Regul 64:241–249CrossRefGoogle Scholar
  20. Cannesan MA, Gangneux C, Lanoue A et al (2011) Association between border cell responses and localized root infection by pathogenic Aphanomyces euteiches. Ann Bot 108:459–469PubMedCrossRefGoogle Scholar
  21. Caporali L (1983) Cytological study of cultured cells from maize root cap. Plant Sci Lett 31:231–236CrossRefGoogle Scholar
  22. Ceccherini MT, Ascher J, Agnelli A et al (2009) Experimental discrimination and molecular characterization of the extracellular soil DNA fraction. Antonie Van Leeuwenhoek 96:653–657PubMedCrossRefGoogle Scholar
  23. Chaboud A, Rougier M (1990) Comparison of maize root mucilages isolated from root exudates and root surface extracts by complementary cytological and biochemical investigations. Protoplasma 156:163–173CrossRefGoogle Scholar
  24. Chen W, Liu P, Xu G et al (2008) Effects of aluminum on the biological characteristics of cowpea root border cells. Acta Physiol Plant 30:303–308CrossRefGoogle Scholar
  25. Clowes FAL (1971) The proportion of cells that divide in root meristems of Zea mays L. Ann Bot 35:249–261Google Scholar
  26. Compant S, Duffy B, Nowak J et al (2005) Use of plant growth promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action and future prospects. Appl Environ Microbiol 71:4951–4959PubMedCrossRefGoogle Scholar
  27. Cooper JE, Rao JR eds (2006) Molecular approaches to soil, rhizosphere and plant microorganism analysis. CABI, Oxfordshire, UK, Cambridge MA, USAGoogle Scholar
  28. Curl EA, Truelove B (1986) The rhizosphere. Advanced series in agricultural sciences, vol. 15, Springer-Verlag, Berlin-Heidelberg-New York-TokyoGoogle Scholar
  29. Curlango-Rivera G, Hawes MC (2011) Root tips moving through soil: an intrinsic vulnerability. Plant Signal Behavior 6:1–2CrossRefGoogle Scholar
  30. 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 332:267–275CrossRefGoogle Scholar
  31. Darrah PR, Roose T (2001) Modeling the rhizosphere. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface. Marcel Dekker, Inc., New York, pp 327–372Google Scholar
  32. De-la-Pena C, Vivanco JM (2010) Root-microbe interactions: the importance of protein secretion. Curr Proteonomics 7:265–274CrossRefGoogle Scholar
  33. De-la-Pena C, Badri DV, Lei Z et al (2010) Root secretion of defense-related proteins is development-dependent and correlated with flowering time. J Biol Chem 285:30654–30666PubMedCrossRefGoogle Scholar
  34. Dennis PG, Miller AJ, Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol Ecol 72:313–327PubMedCrossRefGoogle Scholar
  35. Donato JJ, Moe LA, Converse BJ et al (2010) Metagenomic analysis of apple orchard soil reveals antibiotic resistance genes encoding predicted bifunctional proteins. Appl Environ Microbiol 76:4396–4401PubMedCrossRefGoogle Scholar
  36. Endo I, Tange T, Osawa H (2011) A cell-type-specific defect in border cell formation in the Acacia mangium root cap developing an extraordinary sheath of sloughed-off cells. Ann Bot 108:279–290PubMedCrossRefGoogle Scholar
  37. Esau K (1967) Plant anatomy. Wiley, New YorkGoogle Scholar
  38. Feldman LJ (1985) Root gravitropism. Physiol Plant 65:341–344PubMedCrossRefGoogle Scholar
  39. Foster RC (1981a) Polysacharrides in soil fabrics. Science 214:665–667PubMedCrossRefGoogle Scholar
  40. Foster RC (1981b) The ultrastructure and histochemistry of the rhizosphere. New Phytol 89:263–273Google Scholar
  41. Foster RC (1982) The fine structure of epidermal cell mucilages of roots. New Phytol 91:727–740CrossRefGoogle Scholar
  42. Foster RC, Rovira AD, Cock TW (1983) Ultrastructure of the root-soil interface. American Phytopathological Society, St. PaulGoogle Scholar
  43. Fries N, Forsman B (1951) Quantitative determination of certain nucleic acid derivatives in pea root exudate. Physiol Plant 4:410–420CrossRefGoogle Scholar
  44. Gamalero E, Lingua G, Capri FG et al (2004) Colonization pattern of primary tomato roots by Pseudomonas fluorescens A6RI characterized by dilution plating, flow cytometry, fluorescence, confocal and scanning electron microscopy. FEMS Microbiol Ecol 48:79–87PubMedCrossRefGoogle Scholar
  45. Gamalero E, Lingua G, Tombolini R et al (2005) Colonization of tomato root seedling by Pseudomonas fluorescens 92rkG5: spatio-temporal dynamics, localization, organization, viability and culturability. Microbial Ecol 50:289–297CrossRefGoogle Scholar
  46. Gautheret MR (1933) Cultures of cells isolated from the root cap. CR Acad Sci 186:638–640Google Scholar
  47. Gilbert GS, Clayton MK, Handelsman J, Parke JL (1996) Use of cluster and discriminant analysis to compare rhizosphere bacterial populations following biological perturbation. Microbial Ecol 32:123–147CrossRefGoogle Scholar
  48. Gochnauer MB, Sealey LJ, McCully ME (1990) Do detached root cap cells influence bacteria associated with maize roots? Plant Cell Environ 13:793–801CrossRefGoogle Scholar
  49. Goldberg NP, Hawes MC, Stanghellini ME (1989) Specific attraction to and infection of cotton root cap cells by zoospores of Pythium dissotocum. Can J Bot 67:1760–1767CrossRefGoogle Scholar
  50. Graham TC (1991) Flavonoid and isoflavonoid distribution in developing soybean seedling tissues and in seed and root exudates. Plant Physiol 95:594–603PubMedCrossRefGoogle Scholar
  51. Griffin GJ, Hale MG, Shay FJ (1975) Nature and quantity of sloughed organic matter produced by roots of axenic peanut plants. Soil Biol Biochem 8:29–32CrossRefGoogle Scholar
  52. Guinel FC, McCully ME (1986) Some water-related physical properties of maize root cap mucilage. Plant Cell Environ 9:657–666CrossRefGoogle Scholar
  53. 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 10:565–578Google Scholar
  54. Gunawardena U, Hawes MC (2002) Tissue specific localization of root infection by fungal pathogens: role of root border cells. Mol Plant Microbe Int 15:1128–1136CrossRefGoogle Scholar
  55. Gunawardena U, Rodriguez M, Straney D et al (2005) Tissue specific localization of root infection by Nectria haematococca: mechanisms and consequences. Plant Physiol 137:1363–1374PubMedCrossRefGoogle Scholar
  56. Hamamoto L, Hawes MC, Rost TL (2006) The production and release of living root cap border cells is a function of root apical meristem type in dicotyledonous angiosperm plants. Ann Bot 97:917–923PubMedCrossRefGoogle Scholar
  57. Handelsman J (2004) Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 68:669–685PubMedCrossRefGoogle Scholar
  58. Handelsman J, Stabb EV (1996) Biocontrol of soilborne plant pathogens. Plant Cell 8:1855–1869PubMedCrossRefGoogle Scholar
  59. Harding M, Kubes P (2012) Innate immunity in the vasculature: interactions with pathogenic bacteria. Curr Opin Microbiol 15:85–91PubMedCrossRefGoogle Scholar
  60. Hawes MC, Wheeler H (1982) Factors affecting victorin-induced cell death: temperature and plasmolysis. Physiol Plant Pathol 20:137–144CrossRefGoogle Scholar
  61. Hawes MC, Pueppke SG (1986) Sloughed peripheral root cap cells: yield from different species and callus formation from single cells. Am J Bot 73:1466–1473CrossRefGoogle Scholar
  62. Hawes MC, Pueppke SG (1987) Correlation between binding of Agrobacterium tumefaciens by root cap cells and susceptibility of plants to crown gall. Plant Cell Rep 6:287–290CrossRefGoogle Scholar
  63. Hawes MC, Smith LY (1989) Requirement for chemotaxis in pathogenicity of Agrobacterium tumefaciens on roots of soil-grown pea plants. J Bacteriol 171:5668–5671PubMedGoogle Scholar
  64. Hawes MC, Brigham LA (1992) Impact of root border cells on microbial populations in the rhizosphere. Adv Plant Pathol 8:119–148Google Scholar
  65. Hawes MC, Smith LY, Howarth AJ (1988) Agrobacterium tumefaciens mutants deficient in chemotaxis to root exudates. Mol Plant Microbe Int 1:182–186CrossRefGoogle Scholar
  66. Hawes MC, Brigham LA, Wen F, Woo HH, Zhu Y (1998) Function of root border cells in plant health: pioneers in the rhizosphere. Ann Rev Phytopathol 36:311–327CrossRefGoogle Scholar
  67. Hawes MC, Gunawardena U, Miyasaka S, Zhao X (2000) The role of root border cells in plant defense. Trends Plant Sci 5:128–133PubMedCrossRefGoogle Scholar
  68. Hawes MC, Bengough G, Cassab G, Ponce G (2003) Root caps and rhizosphere. J Plant Growth Regul 21:352–367CrossRefGoogle Scholar
  69. Hawes MC, Curlango-Rivera G, Wen F et al (2011) Extracellular DNA: the tip of root defenses. Plant Sci 180:741–745PubMedCrossRefGoogle Scholar
  70. Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195CrossRefGoogle Scholar
  71. Hinsinger P, Brauman A, Devau N et al (2011) Acquisition of phosphorus and other poorly mobile nutrients by roots. Where do plant nutrition models fail? Plant Soil 348:29–61CrossRefGoogle Scholar
  72. Hirsch AM (2004) Plant-microbe symbioses: a continuum from commensalism to parasitism. Symbiosis 37:345–363Google Scholar
  73. Humphris SN, Bengough AG, Griffiths BS et al (2005) Root cap influences root colonisation by Pseudomonas fluorescens SBW25 on maize. FEMS Microbiol Ecol 54:123–130PubMedCrossRefGoogle Scholar
  74. Iijima M, Griffiths B, Bengough AG (2000) Sloughing of cap cells and carbon exudation from maize seedling roots in compacted sand. New Phytol 145:477–482CrossRefGoogle Scholar
  75. Iijima M, Sako Y, Rao TP (2003) A new approach for the quantification of root cap mucilage exudation in the soil. Plant Soil 255:399–407CrossRefGoogle Scholar
  76. Izano EA, Amarante MA, Kher WB, Kaplan JB (2008) Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and S. epidermidis biofilms. Appl Environ Microbiol 74:470–476PubMedCrossRefGoogle Scholar
  77. Jaroszuk-Scisel J, Kurek E, Rodzik B, Winiarczyk K (2009) Interactions between rye (Secale cereale) root border cells (RBCs) and pathogenic and nonpathogenic rhizosphere strains of Fusarium culmorum. Mycol Res 113:1053–1061PubMedCrossRefGoogle Scholar
  78. 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 29:68–75CrossRefGoogle Scholar
  79. Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil 321:5–33CrossRefGoogle Scholar
  80. Kawasaki H, Iwamuro S (2008) Potential roles of histones in host defense as antimicrobial agents. Infect Disord Drug Targets 8:195–205PubMedGoogle Scholar
  81. Knee EM, Gong FC, Gao MS et al (2001) Root mucilage from pea and its utilization by rhizosphere bacteria as a sole carbon source. Mol Plant Microbe Int 14:775–784CrossRefGoogle Scholar
  82. Knox OGG, Vadakattu GVSR (2005) Evaluation of border cell number and cry protein expression from root tips of Gossypium hirsutum. In: Cote JC, Otvos IS, Schwartz JL (eds) Pacific rim conference on the biotechnology of Bacillus thuringiensis and its environmental impactGoogle Scholar
  83. Knox OGG, Gupta VVSR, Nehl DB, Stiller WN (2007) Constitutive expression of cry proteins in roots and border cells of transgenic cotton. Euphytica 154:83–90CrossRefGoogle Scholar
  84. Knox OGG, Gupta VVSR, Lardner R (2009) Cotton cultivar selection impacts on microbial diversity and function. Aspects Appl Biol 98:1–8Google Scholar
  85. 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
  86. Knudson L (1919) Viability of detached root cap cells. Am J Bot 6:309–310CrossRefGoogle Scholar
  87. Kraszewska EK, Bjerknes CA, Lamm SS, Van’t Hopf J (1985) Extrachromosomal DNA of pea-root (Pisum sativum) has repeated sequences and ribosomal genes. Plant Mol Biol 5:353–361CrossRefGoogle Scholar
  88. Kubista M, Akerman B, Norden B (1987) Characterization of interaction between DNA and 4,6-diamidino- 2- phenylindole by optical spectroscopy. Biochemistry 26:4545–4553PubMedCrossRefGoogle Scholar
  89. Kuzyakov YV (2001) Tracer studies of carbon translocation by plants from the atmosphere into the soil. Eurasian Soil Sci 34:28–42Google Scholar
  90. Kwon C, Bednarek P, Schulze-Lefert P (2008) Secretory pathways in plant immune responses. Plant Physiol 147:1575–1583PubMedCrossRefGoogle Scholar
  91. Lagopodi AL, Ram AFJ, Lamers GEM et al (2002) Novel aspects of tomato root colonization and infection by Fusarium oxysporum f. sp radicis-lycopersici revealed by confocal laser scanning microscopic analysis using the green fluorescent protein as a marker. Mol Plant Microbe Int 15:172–179CrossRefGoogle Scholar
  92. Lee A, Hirsch AM (2006) Signals and responses: choreographing the complex interaction between legumes and alpha- and beta-rhizobia. Plant Signal Behavior 1:161–168CrossRefGoogle Scholar
  93. Levy-Booth DJ, Campbell RG, Gulden RH et al (2007) Cycling of extracellular DNA in the soil environment. Soil Biol Biochem 39:2977–2991CrossRefGoogle Scholar
  94. Liu B, Zeng Q, Yan F et al (2005) Effects of transgenic plants on soil microorganisms. Plant Soil 271:1–13CrossRefGoogle Scholar
  95. Liu J, Yu M, Wang W, Feng Y (2007) Influence of boron and aluminum on production and viability of root border cells of pea. Adv Plant Animal Boron Nutrition, pp 67–74Google Scholar
  96. Loh J, Pierson EA, Pierson LS III, Stacy G, Chatterjee A (2002) Quorum sensing in plant-associated bacteria. Curr Opin Plant Biol 5:1–5CrossRefGoogle Scholar
  97. Lundegarth H, Stenlid G (1944) On the exudation of nucleotides and flavonone from living roots. Arkiv f Bot 31A:10Google Scholar
  98. Luster J, Gottlein A, Nowack B, Sarret G (2009) Sampling, defining, characterizing and modeling the rhizosphere—the soil science tool box. Plant Soil 321:457–482CrossRefGoogle Scholar
  99. Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10CrossRefGoogle Scholar
  100. Lynch MA, Staehelin LA (1995) Immunocytochemical localization of cell wall polysaccharides in the root tip of Avena sativa. Protoplasma 188:115–127CrossRefGoogle Scholar
  101. Marschner P, Crowley D, Rengel Z (2011) Rhizosphere interactions between microorganisms and plants govern iron phosphorus acquisition along the root axis—model and research methods. Soil Biol Biochem 43:883–894CrossRefGoogle Scholar
  102. Matsuyama T, Satoh H, Yamada Y, Hashimoto T (1999) A maize glycine-rich protein is synthesized in the lateral root cap and accumulates in the mucilage. Plant Physiol 120:665–674PubMedCrossRefGoogle Scholar
  103. Maxwell CA, Phillips DA (1990) Concurrent synthesis and release of nod gene inducing flavonoids from alfalfa roots. Plant Physiol 93:1552–1558PubMedCrossRefGoogle Scholar
  104. McDougall BM, Rovira AD (1970) Sites of exudation of C-14-labelled compounds from wheat roots. New Phytol 69:999CrossRefGoogle Scholar
  105. Medina E (2009) Neutrophil extracellular traps: a strategic tactic to defeat pathogens with potential consequenes for the host. J Innate Immun 1:176–179PubMedCrossRefGoogle Scholar
  106. Miki NK, Clarke KJ, McCully ME (1980) A histological and histochemical comparison of the mucilages on the root tips of several grasses. Can J Bot 58:2581–2593CrossRefGoogle Scholar
  107. Mitroulis I, Kambas K, Chrysanthopoulou A et al (2011) Neutrophil extracellular trap formation is associated with IL-1beta and autophagy-related signaling in gout. PLoS One 6:e29318PubMedCrossRefGoogle Scholar
  108. Miyasaka S, Hawes MC (2001) Possible role of root border cells in detection and avoidance of aluminum toxicity. Plant Physiol 125:1978–1987PubMedCrossRefGoogle Scholar
  109. Moody SF, Clarke AE, Bacic A (1988) Structural analysis of secreted slime from wheat and cowpea roots. Phytochemical 27:2857–2861CrossRefGoogle Scholar
  110. Moore R, Fondren WM (1986) The possible involvement of root-cap mucilage in gravitropism and calcium movement across root tips of Allium cepa L. Ann Bot 58:381–387PubMedGoogle Scholar
  111. Morris CE, Monier J-M (2003) The ecological significance of biofilm formation by plant-associated bacteria. Ann Rev Phytopathol 41:429–453CrossRefGoogle Scholar
  112. Newcomb EH (1967) Fine structure of protein-storing plastids in bean root tips. J Cell Biol 33:143–163PubMedCrossRefGoogle Scholar
  113. Oades JM (1978) Mucilage at the root surface. J Soil Sci 29:1–16CrossRefGoogle Scholar
  114. Odell RE, Dumlao MR, Samar D, Silk WK (2008) Stage-dependent border cell and carbon flow from roots to rhizosphere. Am J Bot 95:441–446PubMedCrossRefGoogle Scholar
  115. Pan J, Ye D, Wang L et al (2004) Root border cell development is a temperature-insensitive and Al-sensitive process in barley. Plant Cell Physiol 45:751–760PubMedCrossRefGoogle Scholar
  116. Park SJ, Pai KS, Kim JH, Shin JI (2012) ANCA-associated glomerulonephritis in a patient with infections endocarditis: the role of neutrophil extracellular traps? Revue Med Int 33:57CrossRefGoogle Scholar
  117. Patat SA, Carnegie RB, Kingsbury C et al (2004) Antimicrobial activity of histones from hemocytes of the pacific white shrimp. Eur J Biochem 271:4825–4833PubMedCrossRefGoogle Scholar
  118. Patel S, Kumar S, Jyoti A et al (2010) Nitric oxide donors release extracellular traps from human neutrophils by augmenting free radical generation. Nitric Oxide 22:226–234PubMedCrossRefGoogle Scholar
  119. Peters NK, Long SR (1988) Alfalfa root exudates and compounds which promote or inhibit induction of Rhizobium meliloti nodulation genes. Plant Physiol 88:396–400PubMedCrossRefGoogle Scholar
  120. Phillips HL, Torrey JG (1971) Deoxyribonucleic acid synthesis in root cap cells of cultured roots of Convolvulus. Plant Physiol 48:213–218PubMedCrossRefGoogle Scholar
  121. Pierson LS III, Pierson EA (2007) Roles of diffusible signals in communication among plant-associated bacteria. Phytopathology 97:227–232PubMedCrossRefGoogle Scholar
  122. Pietramellara G, Ascher J, Borgogni F et al (2009) Extracellular DNA in soil and sediment: fate and ecological relevance. Biol Fertil Soils 45:219–235CrossRefGoogle Scholar
  123. Pilszik FH, Salina D, Poon KK et al (2010) A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. J Immunol 185:7413–7425CrossRefGoogle Scholar
  124. Pinton R, Varanini Z, Nanipieri P, eds (2007) The rhizosphere: biochemistry and organic substances at the soil-plant interface. Marcel Dekker, Inc. New York, BaselGoogle Scholar
  125. 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 28:719–732PubMedCrossRefGoogle Scholar
  126. Read DB, Gregory PJ, Bell AE (1999) Physiological properties of axenic maize root mucilage. Plant Soil 211:87091CrossRefGoogle Scholar
  127. Rogers HT, Pearson RW, Pierre WH (1942) The source and phosphatase activity of exoenzyme systems of corn and tomato roots. Soil Sci 54:353–365CrossRefGoogle Scholar
  128. Rovira AD (1969) Plant root exudates. Bot Rev 35:35–57CrossRefGoogle Scholar
  129. Rovira AD (1991) Rhizosphere research: 85 years of progress and frustration. In: Keister DL, Cregan PB (eds) The rhizosphere and plant growth. Kluwer, Dordrecht, pp 3–13CrossRefGoogle Scholar
  130. Saxena D, Stotzky G (2001) Bacillus thuringiensis (Bt) toxin released from root exudates and biomass of Bt corn has no apparent effect on earthworms, nematodes, protozoa, bacteria, and fungi in soil. Soil Biol Biochem 33:1225–1230CrossRefGoogle Scholar
  131. Schroth MN, Snyder WC (1961) Efect of host exudates on chlamydospore germination of the bean root rot fungus Fusarium solani f sp phaseoli in soil. Phytopathology 52:279–285Google Scholar
  132. Sealey LJ, McCully ME, Canny MJ (1995) The expansion of maize root cap mucilage during hydration. I. Kinetics. Physiol Plant 93:38–46CrossRefGoogle Scholar
  133. Sherwood RT (1987) Papilla formation in corn root cap cells and leaves inoculated with Colletotrichum graminicola. Phytopathology 77:930–934CrossRefGoogle Scholar
  134. Smucker AJM, Erickson AE (1987) Anaerobic stimulation of root exudates and disease of peas. Plant Soil 99:423–433CrossRefGoogle Scholar
  135. Somasundaram S, Fukuzono S, Iijima M (2008) Dynamics of root border cells in rhizosphere soil of Zea mays L.: crushed cells during root penetration, survival in soil, and long term soil compaction effect. Plant Prod Sci 11:440–446CrossRefGoogle Scholar
  136. Stenlid G (1944) Physicochemical properties of the surface of growing plant cells. Nature 153:618–619CrossRefGoogle Scholar
  137. Stubbs VEC, Standing D, Knox OGG et al (2004) Root border cells take up and release glucose-C. Ann Bot 93:221–224PubMedCrossRefGoogle Scholar
  138. Sylvia DM, Fuhrmann JJ, Hartel PG, Zuberer DA (1998) Principles and applications of soil microbiology. Prentice Hall, USAGoogle Scholar
  139. Tamas L, Budikova S, Huttova J et al (2005) Aluminum-induced cell death of barley root border cells is correlated with peroxidase and oxalate oxidase-mediated hydrogen peroxide production. Plant Cell Rep 24:189–194PubMedCrossRefGoogle Scholar
  140. Tapp H, Stotzky G (1997) Monitoring the fate of insecticidal toxins from Bacillus thuringiensis in soil with flow cytometry. Can J Microbiol 43:1074–1078PubMedCrossRefGoogle Scholar
  141. Urban CF, Lourido S, Zychlinsky A (2006) How do microbes evade neutrophil killing? Cell Microbiol 8:1687–1696PubMedCrossRefGoogle Scholar
  142. Uren NC (2001) Types, amounts, and possible functions of compounds released into the rhizosphere by soil-grown plants. In: Pinton R, Varanini P, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface. Marcel Dekker, Inc., New York, Basel. pp 19–40Google Scholar
  143. VanEgeraat 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
  144. Van’t Hopf J, Bjerknes CA (1982) Cells of pea (Pisum sativum) that differentiate from G2 phase have extrachromosomal DNA. Mol Cell Biol 2:339–345Google Scholar
  145. Vermeer J, McCully ME (1982) The rhizosphere in Zea: new insight into its structure and development. Planta 156:45–61CrossRefGoogle Scholar
  146. Vicre M, Santaella C, Blanchet S, Gateau A, Driouich A (2005) Root border like cells of Arabidopsis. Microscopical characterization and role in the interaction with rhizobacteria. Plant Physiol 138:998–1008PubMedCrossRefGoogle Scholar
  147. Vlassov VV, Laktionov PP, Rykova EY (2007) Extracellular nucleic acids. Bioessays 29:654–667PubMedCrossRefGoogle Scholar
  148. Voeller BR, Ledbetter MC, Porter KR (1964) The plant cell: aspects of its form and function. In: Bracket J, Minsky EE (eds) The cell, vol 6. Academic, London, pp 245–312Google Scholar
  149. Wang Y, Li M, Stadler S, Correll S et al (2009) Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J Cell Biol 184:205–213PubMedCrossRefGoogle Scholar
  150. Wardini AB, Guimaraes-Costa AB, Nascimento MT et al (2010) Characterization of neutrophil extracellular traps in cats naturally infected with feline leukemia virus. J Gen Virol 91:259–264PubMedCrossRefGoogle Scholar
  151. Watt M, McCully ME, Jeffree CE (1993) Plant and bacterial mucilages of the maize rhizosphere: comparison of their soil binding properties and histochemistry in a model system. Plant Soil 151:151–165CrossRefGoogle Scholar
  152. Watt M, Silk WK, Passioura J (2006) Rates of root and organism growth, soil conditions and temporal and spatial development of the rhizosphere. Ann Bot 97:839–855PubMedCrossRefGoogle Scholar
  153. Weller DM (1988) Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annu Rev Phytopathol 26:379–407CrossRefGoogle Scholar
  154. 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 11:1129–1140PubMedCrossRefGoogle Scholar
  155. Wen F, Curlango-Rivera G, Hawes MC (2007a) Proteins among the polysaccharides: a new perspective on root cap slime. Plant Signal Behavior 2:1–3CrossRefGoogle Scholar
  156. Wen F, VanEtten HD, Tsaprailis G, Hawes MC (2007b) Extracellular proteins in pea root tip and border cell exudates. Plant Physiol 143:773–783PubMedCrossRefGoogle Scholar
  157. Wen F, Woo HH, Pierson EA et al (2008) 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
  158. Wen F, White GJ, VanEtten HD et al (2009) Extracellular DNA is required for root tip resistance to fungal infection. Plant Physiol 151:820–829PubMedCrossRefGoogle Scholar
  159. Wen F, Shen A, Choi A, Shi J (2012) A xenograft pancreatic cancer mouse model to study the function of extracellular DNA in metastasis. Proceedings, American Association of Cancer ResearchGoogle Scholar
  160. Whipps J, Lynch JM (1983) Substrate flow and utilization in the rhizosphere of cereals. New Phytol 95:605–623CrossRefGoogle Scholar
  161. Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS (2002) Extracellular DNA required for bacterial biofilm formation. Science 295:1487PubMedCrossRefGoogle Scholar
  162. Woo HH, Hirsch AM, Hawes MC (2004) Altered susceptibility to infection by Sinorhizobium meliloti and Nectria haematococca in alfalfa roots with altered cell cycle. Plant Cell Rep 12:967–973Google Scholar
  163. Wood RKS (1967) Physiological plant pathology. Blackwell, OxfordGoogle Scholar
  164. Wuyts N, Maung ZTZ, Swennen R, De Waele D (2006) Banana rhizodeposition: characterization of root border cell production and effects on chemotaxis and motility of the parasitic nematode Radopholus similis. Plant Soil 283:217–228CrossRefGoogle Scholar
  165. Xu J, Zhang X, Pelayo R, Monestier M et al (2009) Extracellular histones are major mediators of death in sepsis. Nat Med 15:1318–1321PubMedCrossRefGoogle Scholar
  166. Yost CC, Cody MJ, Harris ES et al (2009) Impaired NET formation: a novel innate immune deficiency of human neonates. Blood 113:6419–6427PubMedCrossRefGoogle Scholar
  167. Young RL, Malcolm KC, Kret JE, Caceres SM et al (2011) Neutrophil extracellular trap (NET)-mediated killing of Pseudomonas aeruginosa: evidence of acquired resistance within the cystic fibrosis airway, independent of CFTR. PLoS One 6:e23637PubMedCrossRefGoogle Scholar
  168. Zentmyer G (1963) Biological control of Phytophthora root rot of avocado with alfalfa meal. Phytopathology 53:1383Google Scholar
  169. Zhao X, Misaghi IJ, Hawes MC (2000) Stimulation of border cell production in response to increased carbon dioxide levels. Plant Physiol 122:181–188PubMedCrossRefGoogle Scholar
  170. Zhu M, Ahn S, Matsumoto H (2003) Inhibition of growth and development of root border cells in wheat by Al. Physiol Plant 117:359–367PubMedCrossRefGoogle Scholar
  171. Zhu Y, Pierson LS, Hawes MC (1997) Induction of microbial genes for pathogenesis and symbiosis by chemicals from root border cells. Plant Physiol 115:1691–1698PubMedCrossRefGoogle Scholar
  172. Zobel RW, Wright SF (2005) Roots and soil management: interactions between roots and the soil. American Society of Agronomy, Inc., Crop Science Society of America, Inc., Soil Science Society of America, Inc. Madison WI, USAGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Martha C. Hawes
    • 1
  • Gilberto Curlango-Rivera
    • 1
  • Zhongguo Xiong
    • 2
  • John O. Kessler
    • 3
  1. 1.Department of Soil, Water and Environmental SciencesUniversity of ArizonaTucsonUSA
  2. 2.Division of Plant Pathology and Microbiology, School of Plant SciencesUniversity of ArizonaTucsonUSA
  3. 3.Physics DepartmentUniversity of ArizonaTucsonUSA

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