Martha C Hawes
Professor, BIO5 Institute
Professor, Environmental Science
Professor, Plant Sciences
Primary Department
Department Affiliations
(520) 621-5490
Work Summary
Martha Hawes is well known for her work on root border cells. Her entire career has focused on changing this perception and now border cells are described in numerous botany textbooks. Dr. Hawes has been very creative in designing experiments to understand the basic biology of this unique cell type especially in light of how border cells fight plant disease. Considering that the root tip serves as one of the major sources of root exudates that can attract microbial pathogens, the fact that this exceptionally vulnerable region of the root is protected from infection by the border cells is a real paradigm shift, especially via the mechanism.
Research Interest
Martha Hawes, PhD, realizes plants of many species systematically shed thousands of healthy cells from each of their root tips daily. Because these cells provide a living interface between the root and the soil, scientists refer to them as root "border" cells. This seemingly wasteful release of living somatic cells into environment is unique among higher organisms, and its function is unknown. Dr. Hawes’ hypothesis is that border cells provide a selective advantage to the plant by releasing specific chemicals that regulate levels of root- associated microorganisms. Soil-borne bacteria and fungi comprise not only pathogens that can destroy roots but also beneficial organisms that are crucial for normal plant development, therefore regulating the balance of such microbial populations is crucial to survival. Border cells act as a reservoir of chemicals that can specifically attract or repel microorganisms, as well as activate microbial genes headed for root infection. Mutants of soil-borne microorganisms have been used to demonstrate that, in some cases, recognition of such chemicals from the cells is required for the establishment of root-microbe associations. Her lab has identified border cell- specific genes cell as well as genes that are expressed among separation of border cells from the root. These plant genes are being used to genetically engineer plants with specific alterations in the production of border cells, and in their biological properties. These transgenic plants can be used test the hypothesis that border cells control the susceptibility of plants to infection by symbiotic and pathogenic bacteria and fungi.

Publications

Hawes, M. C., Bengough, G., Cassab, G., & Ponce, G. (2002). Root caps and rhizosphere. Journal of Plant Growth Regulation, 21(4), 352-367.

Abstract:

In this paper we discuss recent work on the physiological, molecular, and mechanical mechanisms that underlie the capacity of root caps to modulate the properties of the rhizosphere and thereby foster plant growth and development. The root cap initially defines the rhizosphere by its direction of growth, which in turn occurs in response to gradients in soil conditions and gravity. The ability of the root cap to modulate its environment is largely a result of the release of exudates and border cells, and so provides a potential method to engineer the rhizosphere. Factors affecting the release of border cells from the outer surface of the root cap, and function of these cells and their exudates in the rhizosphere, are considered in detail. Release of border cells into the rhizosphere depends on soil matric potential and mechanical impedance, in addition to a host of other environmental conditions. There is good evidence of unidentified feedback signals between border cells and the root cap meristem, and some potential mechanisms are discussed. Root border cells play a significant mechanical role in decreasing frictional resistance to root penetration, and a conceptual model for this function is discussed. Root and border cell exudates influence specific interactions between plant hosts and soil organisms, including pathogenic fungi. The area of exudates and border cell function in soil is an exciting and developing one that awaits the production of appropriate mutant and transgenic lines for further study in the soil environment.

Hawes, M. C., & Pueppke, S. G. (1987). Correlation between binding of Agrobacterium tumefaciens by root cap cells and susceptibility of plants to crown gall. Plant Cell Reports, 6(4), 287-290.

PMID: 24248761;Abstract:

We compared the binding of Agrobacterium tumefaciens by freshly isolated root cap cells with susceptibility of plants to crown gall tumorigenesis. A high binding reaction was strongly correlated with susceptibility to tumorigenesis in a survey of the binding of strain B6 to cells from 48 species in 17 families. In reciprocal experiments with nine virulent A. tumefaciens strains, tumors developed in plant-bacteria combinations that gave a high binding response in the root cap cell assay. Binding was quantified by direct measurement of the number of bacteria bound to the periphery of individual cells. Root cap cells from six susceptible species bound significantly more bacteria than did cells from five resistant species. © 1987 Springer-Verlag.

Hawes, M. C., Curlango-Rivera, G., Xiong, Z., & Kessler, J. O. (2012). Roles of root border cells in plant defense and regulation of rhizosphere microbial populations by extracellular DNA 'trapping'. Plant and Soil, 355(1-2), 1-16.

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. © 2012 Springer Science+Business Media B.V.

Wen, F., Woo, H. H., Pierson, E. A., Eldhuset, T. D., Fossdal, C. G., Nagy, N. E., & Hawes, M. C. (2009). Synchronous elicitation of development in root caps induces transient gene expression changes common to legume and gymnosperm species. Plant Molecular Biology Reporter, 27(1), 58-68.

Abstract:

Root cap development in cereals and legumes is self-regulated by a repressor that accumulates in the extracellular environment, and immersing the root tip into water results in renewed cap development. By exploiting this phenomenon, root cap mitosis and differentiation can be synchronously induced among populations. In Pisum sativum L., messenger RNA (mRNA) differential display revealed changes in expression of approximately 1% of the sample mRNA population within minutes of induced cap turnover. This profile changes sequentially over a period of 30 min, then stabilizes. Microarray analysis of Medicago truncatula root caps confirmed changes in expression of approximately 1% of the target population, within minutes. A cell specific marker for cap turnover exhibited the same temporal and spatial expression profile in the gymnosperm species Norway spruce (Picea abies) as in pea. Induced cap development provides a means to profile cell-specific gene expression among phylogenetically diverse species from the early moments of mitosis and cellular differentiation. © Springer Science + Business Media, LLC 2008.

Wen, F., Celoy, R. M., Nguyen, T., Zeng, W., Keegstra, K., Immerzeel, P., Pauly, M., & Hawes, M. C. (2008). Inducible expression of Pisum sativum xyloglucan fucosyltransferase in the pea root cap meristem, and effects of antisense mRNA expression on root cap cell wall structural integrity. Plant Cell Reports, 27(7), 1125-1135.

PMID: 18347802;PMCID: PMC2755773;Abstract:

Mitosis and cell wall synthesis in the legume root cap meristem can be induced and synchronized by the nondestructive removal of border cells from the cap periphery. Newly synthesized cells can be examined microscopically as they differentiate progressively during cap development, and ultimately detach as a new population of border cells. This system was used to demonstrate that Pisum sativum L. fucosyl transferase (PsFut1) mRNA expression is strongly expressed in root meristematic tissues, and is induced >2-fold during a 5-h period when mitosis in the root cap meristem is increased. Expression of PsFut1 antisense mRNA in pea hairy roots under the control of the CaMV35S promoter, which exhibits meristem localized expression in pea root caps, resulted in a 50-60% reduction in meristem localized endogenous PsFut1 mRNA expression measured using whole mount in situ hybridization. Changes in gross levels of cell wall fucosylated xyloglucan were not detected, but altered surface localization patterns were detected using whole mount immunolocalization with CCRC-M1, an antibody that recognizes fucosylated xyloglucan. Emerging hairy roots expressing antisense PsFut1 mRNA appeared normal macroscopically but scanning electron microscopy of tissues with altered CCRC-M1 localization patterns revealed wrinkled, collapsed cell surfaces. As individual border cells separated from the cap periphery, cell death occurred in correlation with extrusion of cellular contents through breaks in the wall. © 2008 Springer-Verlag.