Root border cells and secretions as critical elements in plant host defense
Introduction
Maintaining a healthy root within the soil is vitally important for plant growth and crop protection. During root growth, root cap turnover and programmed cell separation from the cap periphery results in the delivery of detached cell populations into the rhizosphere [1, 2]. These are termed root border cells or root border-like cells depending on the pattern of their release and organization [3••, 4]. Border cells are defined as cells that detach from the root cap as individual cells and small aggregates, whereas border-like cells are released as blocks or sheets of cells that remain attached to each other [1, 4].
Interestingly, the production of border cells appears to be correlated to mycorrhizal associations with the root. Plant species that have a higher mycorrhizal propensity release larger numbers of border cells than those with lesser mycorrhizal propensity [5, 6] although the role of border cells in the establishment of mycorrhizal colonization is not known. A number of studies have provided evidence that border cells (Figure 1a,c) can influence root-rhizosphere dynamics at the root tip. First, the number of border cells increases in response to pathogens and other stimuli including carbon dioxide, metals, soil type and secondary metabolites [2, 8, 9]. Second, border cells are capable of attracting or repelling pathogenic microorganisms including nematodes (Figure 1b), bacteria (Figure 1d) and oomycetes (Figure 1e). For example, instantaneous attraction of zoospores to border cells, but not root surfaces, occurs in a host–microbe specific manner (Figure 1e) (see [12], supplementary Figures 1–4). Exposure of pea roots to the pathogen Nectria haematococca results in the formation of a mantle of hyphae, mucilage and border cells that covers the root tip [13]. Remarkably, the moving root tip remains free of infection once the mantle has been detached and left behind. Third, border cells secrete antimicrobial proteins, phytoalexins, arabinogalactan proteins and pectins within the extracellular matrix or ‘slime’ [9, 14, 15, 16••, 17••]. The slime layer and its responses to stimuli can be visualized using India ink, which does not penetrate the matrix (Figure 2). Border cells from pea emerge from the root tip ensheathed within a slime layer measuring several millimeters in diameter (Figure 2b). Individual border cells from maize (Figure 2a) and pea (Figure 2c) respond to the presence of bacteria and germinating fungal spores by increased slime production [18].
It has been recently found that pea root border cells secrete DNA to the matrix (exDNA) much like the NETs ‘neutrophil extracellular traps’ reported by Brinkmann et al. in 2004 [19••] to be released by white blood cells in mammals [19••, 20, 21••, 22]. ExDNA-based extracellular traps have now been shown to underlie critical aspects of mammalian immune responses ranging from infectious disease to lupus and other autoimmune disorders as well as heart attacks, stroke, and skin diseases (summarized in Table 1). These emerging discoveries offer revolutionary insights into previously unrecognized disease processes and offer new avenues for clinical approaches to human health and wellness [31, 32••]. Here, we outline recent advances from studies on the role of these secretions on root health.
Section snippets
Secretion of high molecular weight cell wall glycomolecules, pectin and arabinogalactan proteins
Pectin impacts border cell separation. Release of border cells is dependent on the activity of pectin-degrading enzymes such as methylesterases and polygalacturonases responsible for their separation from the root tip [33, 34]. The cells are released individually or as aggregates, depending on species, genotype, and environmental conditions [3••, 30, 35]. The cell walls of border cells and border-like cells contain significant amounts of pectic polysaccharides including homogalacturonan and
Secretion of Proteins and exDNA by root border cells
In addition to the high molecular weight polysaccharide components of root cap slime, a group of >100 proteins is synthesized and exported into the extracellular matrix [15, 47]. The secretome includes structural and antimicrobial proteins long known to be present within the apoplast of diverse plant tissues [48, 49]. Thus, it was not surprising that adding protease to the root tip at the time of inoculation with a fungal pathogen eliminates resistance to infection, and that antibody to a
Conclusions
In plants and animals, understanding how disease occurs or is circumvented is a fundamental underpinning to developing methods for prevention and control. Microbial trapping by components of the extracellular matrix of higher plants is a mechanism whose significance has been overlooked in the past. Recognition of the process in mammals has yielded new insight into virtually all aspects of human health and disease [31, 32••]. Efforts to utilize these insights to protect patients from death and
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
We gratefully acknowledge support of our research on Root Protection by the University of Arizona and the National Science Foundation (USA), the University of Rouen and Grand Réseau de Recherche VASI « Végétal-Agronomie-Sols et Innovations » de Haute Normandie (France). Jean-Selim Driouich, a student at the faculty of Pharmacy (Rouen University) is acknowledged for stimulating discussion on the diversity of human pathogens and immunity.
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