Roots: Contribution to the Rhizosphere

Gilberto Curlango‐Rivera, University of Arizona, Tucson, Arizona, USA
Uvini Gunawardena, Cibus, San Diego, California, USA
Fushi Wen, University of Arizona, Tucson, Arizona, USA
Xiaowen Zhao, USDA ARS Tree Fruit Research Lab (TFRL), Wenatchee, Washington, USA
Zhongguo Xiong, University of Arizona, Tucson, Arizona, USA
Martha C Hawes, University of Arizona, Tucson, Arizona, USA

Published online: January 2016

DOI: 10.1002/9780470015902.a0002335.pub3

Abstract

Diverse compounds exuded by different parts of the root system create a unique environment known as the rhizosphere. Interactions among microorganisms found within the rhizosphere and communication between these microorganisms and plant roots play an important role in maintaining plant health. In 2004, the discovery of deoxyribonucleic acid (DNA)‐based neutrophil extracellular traps (NETs) have transformed our understanding of mammalian immune responses. Subsequent studies revealed that plant roots express a similar mechanism in the rhizosphere, where root border cells secrete extracellular DNA together with antibiotic amino acids, enzymes and other proteins, to trap pathogens and prevent their invasion of the root system. As in animals, the defense response is impaired if extracellular proteins and/or extracellular DNA are degraded by protease and/or by DNase at the time of inoculation with fungal or bacterial pathogens. Defining species‐specific mechanisms of plant extracellular trapping may yield new avenues for engineering the rhizosphere to improve crop production.

Key Concepts

  • Extracellular DNA (exDNA) in the rhizosphere has long been observed, and was presumed to result from cell death.
  • Recent studies have revealed that exDNA is a key component of an extracellular matrix involved in trapping and immobilisation of pathogens.
  • The specificity of exDNA‐based trapping may play a critical role in microbial population structure in the rhizosphere.
  • The discovery that DNA‐based extracellular trapping operates in animals and plants suggests that this previously unrecognised process is an ancient underpinning of eukaryotic defence.
  • Efforts to engineer the rhizosphere may be facilitated by a better understanding of how plants control the environment surrounding their roots.

Keywords: mucilage; border cells; root cap; sloughed root cap cells; microbial ecology; root exudates

Figure 1. Functional categories of root exudates.
Figure 2. Sources and effects of root exudates. (a) Regions of the root known to release exudates. (b) Host‐specific interactions of microorganisms with border cells: 1, release of border cells (arrow) into the environment; 2, induction of zoosphere germination by border cells; 3, binding of bacteria to border cells; 4, colonisation of border cells by soil‐borne fungus; 5, attraction of pathogenic nematode to border cells.
Figure 3. Use of rhizosphere interactions for improvement of plant health and the environment.
close

References

Allen MF (ed) (1992) Mycorrhizal Functioning: An Integrative Plant–Fungal Process. New York: Chapman & Hall.

Angus AA and Hirsch AM (2010) Insights into the history of the legume‐betaproteobacterial symbiosis. Molecular Ecology 19: 28–30.

Bacic A, Moody SF and Clarke AE (1986) Structural analysis of secreted root slime from maize (Zea mays L.). Plant Physiology 80: 771–777.

Baetz U and Martinoia E (2014) Root exudates: the hidden part of plant defense. Trends in Plant Science 19: 90–98.

Barlow PW (1975) The root cap. In: Torrey JG and Clarkson DT (eds) The Development and Function of Roots, pp. 21–54. London: Academic Press.

Bednarek P, Kwon C and Schulze‐Lefert P (2010) Not a peripheral issue: secretion in plant‐microbe interactions. Current Opinion in Plant Biology 13: 376–387.

Bolton H Jr and Fredrickson JK (1993) Microbial ecology of the rhizosphere. In: Meeting FB Jr (ed) Soil Microbial Ecology, pp. 27–57. New York: Marcel Dekker.

Brinkmann V, Reichard U, Goosmann C, et al. (2004) Neutrophil extracellular traps kill bacteria. Science 303: 1532–1535.

Buchanan JT, Simpson A, Aziz R, et al. (2006) DNase expression allows the pathogen Group A Streptococcus to escape killing in NETs. Current Biology 16: 396–400.

Clowes FAL (1968) The DNA content of the cells of the quiescent center and root cap of Zea mays. New Phytologist 67: 631–639.

Curl EA and Truelove B (1986) The Rhizosphere. Berlin: Springer.

Curlango‐Rivera G and Hawes MC (2011) Root tips moving through soil: an intrinsic vulnerability. Plant Signaling and Behavior 6: 1–2.

Curlango‐Rivera G, Cho I, Huskey DA, Xiong Z and Hawes MC (2014) Signals controlling extracellular trap formation in plant and animal immune responses. Clinical Microbiology 3: 5–8.

Curlango‐Rivera G, Huskey DA, Mostafa A, et al. (2013) Intraspecies variation in cotton border cell production: rhizosphere microbiome implications. American Journal of Botany 100: 9–15.

De Coninck B, Timmermans P, Bos C, Cammue BPA and Kazan K (2015) What lies beneath: belowground defense strategies in plants. Trends in Plant Science 20: 91–101.

De‐la‐Pena C and Vivanco JM (2010) Root‐microbe interactions: the importance of protein secretion. Current Proteomics 7: 265–274.

Dennis PG, Miller AJ and Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiology Ecology 72: 313–321.

Driouich A, Follet‐Gueye M, Vicre‐Gibouin M and Hawes MC (2013) Root border cells and secretions as critical elements in plant host defense. Current Opinion in Plant Biology 16: 1–5.

Flores HE, Weber C and Puffett J (1996) Underground plant metabolism: the biosynthetic potential of roots. In: Waisel Y, Eshel A and Kafkafi U (eds) Plant Roots, The Hidden Half, pp. 931–956. New York: Marcel Dekker.

Gerke J (2015) The acquisition of phosphate by higher plants: effect of carboxylate release by the roots. Journal of Plant Nutrition and Soil Science 178: 351–364.

Gunawardena U, Van Etten H and Hawes MC (2005) Tissue‐specific localization of pea (Pisum sativum L.) root infection by Nectria haematococca: mechanisms and consequences. Plant Physiology 137: 1363–1374.

Gunawardena V, Miyasaka S, Zhao X and Hawes MC (2000) Function of root border cells in plant defence. Trends in Plant Sciences 5: 128–133.

Haichar F, Santaella C, Heulin T and Wafa A (2014) Root exudates mediated interactions belowground. Soil Biology and Biochemistry 77: 69–80.

Halverson TWR, Wilton M, Poon KKH, Petri B and Lewenze S (2015) DNA is an antimicrobial component of neutrophil extracellular traps. PLoS Pathogens 11 (1):e1004593.

Hawes MC, Bengough GA, Cassab G and Ponce G (2003) Root caps and rhizosphere. Journal of Plant Growth Regulation 21: 352–367.

Hawes MC, Brigham LA, Wen F, Woo HH and Zhu Y (1998) Function of root border cells in plant health: pioneers in the rhizosphere. Annual Review of Phytopathology 36: 311–327.

Hawes MC, Curlango‐Rivera G, Wen F, et al. (2011) Extracellular DNA: the tip of root defenses? Plant Science 180: 741–745.

Hawes MC, Curlango‐Rivera G, Xiong Z and Kessler JO (2012) Marschner review. Roles of root border cells in plant defense and regulation of rhizosphere microbial populations by extracellular DNA 'trapping'. Plant and Soil 355: 1–15.

Hawes MC, Wen F and Elquza E (2015) Extracellular DNA: a bridge to cancer. Cancer Research 75 (20): 4260–4264.

Iijima M, Griffiths B and Bengough AG (2000) Sloughing of cap cells and carbon exudation from maize seedling roots in compacted sand. New Phytologist 145: 477–482.

Janczarek M, Rachwal K, Marzec A, Grzadziel J and Palusinska‐Szysc M (2015) Signal molecules and cell‐surface components involved in early stages of the legume‐rhizobium interactions. Applied Soil Ecology 85: 94–113.

Jones DL, Nguyen C and Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil‐root interface. Plant and Soil 321: 5–33.

Kennedy AC (1998) The rhizosphere and spermosphere. In: Sylvia DM, Fuhrman JJ, Hartel PG and Zuberer DA (eds) Principles and Applications of Soil Microbiology, pp. 389–407. Englewood Cliffs, NJ: Prentice‐Hall.

Kim YC, Leveau J, McSpadden Gardener BB, et al. (2011) The multifactorial basis for plant health promotion by plant‐associated bacteria. Applied and Environmental Microbiology 77: 1548–1555.

Kloepper JW, Zablotowicz RM, Tipping EM and Lifshitz R (1991) Growth promotion mediated by bacterial rhizosphere colonizers. In: Keister DL and Cregan PB (eds) The Rhizosphere and Plant Growth, pp. 315–326. Dordrecht, The Netherlands: Kluwer.

Lambers H, Mougel C, Jaillard B and Hinsinger P (2009) Plant‐microbe‐soil interactions in the rhizosphere: an evolutionary perspective. Plant and Soil 32: 83–115.

Lynch JM and Whipps JM (1991) Substrate flow in the rhizosphere. In: Keister DL and Cregan PB (eds) The Rhizosphere and Plant Growth, pp. 15–24. Dordrecht, The Netherlands: Kluwer.

Lynn DG and Chang M (1990) Phenolic signals in cohabitation: implications for plant development. Annual Review of Plant Physiology and Plant Molecular Biology 41: 497–526.

Metzler KD, Goosmann C, Lubojemska A, Zychlinsky A and Papayanopoulos VA (2014) A myeloperoxidase‐containing complex regulates neutrophil elastase release and actin dynamics during NETosis. Cell Reports 8: 883–896.

Nasser W, Beres SB, Olsen RJ, et al. (2014) Evolutionary pathway to increased virulence Group A Streptococcus disease derived from 3,615 genome sequences. Proceedings of the National Academy of Science 111: E1768–E1776.

Nelson EB (1991) Exudate molecules initiating fungal responses to seeds and roots. In: Keister DL and Cregan PB (eds) The Rhizosphere and Plant Growth, pp. 197–209. Dordrecht, The Netherlands: Kluwer.

O'Connell KP, Goodman RM and Handelsman J (1996) Engineering the rhizosphere: expressing a bias. Trends in Biotechnology 14: 83–88.

Pii Y, Mimmo T, Tomasi N, et al. (2015) Microbial interactions in the rhizosphere: beneficial influences of plant growth‐promoting rhizobacteria on nutrient acquisition process. A review. Biology and Fertility of Soils 51: 403–415.

Rovira AD (1969) Plant root exudate. Botanical Review 35: 35–57.

Rovira AD (1991) Rhizosphere research – 85 years of progress and frustration. In: Keister DL and Cregan PB (eds) The Rhizosphere and Plant Growth, pp. 3–13. Dordrecht, The Netherlands: Kluwer.

Tollefson SJ, Curlango‐Rivera G, Huskey DA, et al. (2015) Altered carbon delivery from roots: rapid, sustained inhibition of border cell dispersal in response to compost water extracts. Plant and Soil 378: 145–156.

Tran TM, Hawes MC and Allen C (2013) Extracellular DNases contribute to virulence of Ralstonia solanacearum. Phytopathology 103: 147–148.

Watt M, Silk WK and Passioura JB (2006) Rates of root and organism growth, soil conditions, and temporal and spatial development of the rhizosphere. Annals of Botany 97: 839–855.

Wen F, VanEtten HD, Tsaprailis G and Hawes MC (2007) Extracellular proteins in pea root tip and border cell exudates. Plant Physiology 143: 773–785.

Wen F, White G, VanEtten HD and Hawes MC (2009) Extracellular DNA is required for root tip resistance to infection. Plant Physiology 151: 820–829.

Zhang Y, Ruyter‐Spira C and Bouwmeester HJ (2015) Engineering the plant rhizosphere. Current Opinion in Biotechnology 32: 136–142.

Further Reading

Fitter A (1996) Characteristics and functions of root systems. In: Waisel Y, Eshel A and Kafkafi U (eds) Plant Roots, The Hidden Half, pp. 1–20. New York: Marcel Dekker.

Klein DA, Salzwedel JL and Dazzo FB (1990) Microbial colonization of plant roots. In: Nakes JP and Hagedorn C (eds) Biotechnology of Plant–Microbe Interactions, pp. 189–225. New York: McGraw‐Hill.

Ogoshi A, Kobayashi K, Homma Y, et al. (eds) (1997) Plant Growth‐Promoting Rhizobacteria – Present Status and Future Prospects. The 4th PGPR International Workshop Organizing Committee 1997. Sapporo, Japan: Nakanishi Printing.

Pierson LS III Wood DW and Pierson EA (1998) Homoserine lactone‐mediated gene regulation in plant‐associated bacteria. Annual Review of Phytopathology 36: 207–225.

Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C and Moinne‐Loccoz Y (2009) The rhizosphere: a playground and battlefield for soil‐borne pathogens and beneficial microorganisms. Plant and Soil 321: 341–361.

Stacey G, Mullin B and Gresshoff M (eds) (1996) Biology of Plant–Microbe Interactions. St. Paul, MN: International Society for Molecular Plant–Microbe Interactions.

Vance CP (1991) Root–bacteria interaction: symbiotic nitrogen fixation. In: Waisel Y, Eshel A and Kafkafi U (eds) Plant Roots, The Hidden Half, pp. 723–767. New York: Marcel Dekker.

Wilcox HE (1991) Mycorrhizae. In: Waisel Y, Eshel A and Kafkafi U (eds) Plant Roots, The Hidden Half, pp. 689–721. New York: Marcel Dekker.

Related Sub-Topics:

Physiological Ecology | Microbial Interactions and Communities | Mutualism and Symbiosis | Environmental Microbiology | Roots and Root Systems | Plant Secondary Metabolism | Biomes and Ecosystems
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Roots: Contribution to the Rhizosphere
 
How to Cite close
Curlango‐Rivera, Gilberto, Gunawardena, Uvini, Wen, Fushi, Zhao, Xiaowen, Xiong, Zhongguo, and Hawes, Martha C(Jan 2016) Roots: Contribution to the Rhizosphere. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0002335.pub3]