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

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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.

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Abbreviations

exDNA:

Extracellular DNA

DAPI:

4′,6-diamidino-2-phenylindole

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Acknowledgements

We gratefully acknowledge support for our research in this area from the National Science Foundation (NSF# 1032339 to MCH and ZX) and the Department of Energy (DOE DEAC02-06CH11357 to JOK). We thank Dr. Virginia Rich for critical reading of the manuscript.

We dedicate this review to the memory of W. D. ‘Dietz’ Bauer.

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Authors and Affiliations

  1. Department of Soil, Water and Environmental Sciences, University of Arizona, 429 Shantz Building, #38, 1177 E. Fourth St., POB 210038, Tucson, AZ, 85721-0038, USA

    Martha C. Hawes & Gilberto Curlango-Rivera

  2. Division of Plant Pathology and Microbiology, School of Plant Sciences, University of Arizona, Tucson, AZ, 85721, USA

    Zhongguo Xiong

  3. Physics Department, University of Arizona, Building 81, Tucson, AZ, 85721, USA

    John O. Kessler

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  1. Martha C. Hawes
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  2. Gilberto Curlango-Rivera
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  3. Zhongguo Xiong
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  4. John O. Kessler
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Correspondence to Martha C. Hawes.

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Responsible Editor: Philippe Hinsinger.

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Hawes, M.C., Curlango-Rivera, G., Xiong, Z. et al. Roles of root border cells in plant defense and regulation of rhizosphere microbial populations by extracellular DNA ‘trapping’. Plant Soil 355, 1–16 (2012). https://doi.org/10.1007/s11104-012-1218-3

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