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Root Border Cells and Their Role in Plant Defense PY54CH05-Hawes ARI 13 May 2016 11:31 V I E Review in Advance first posted online E W on May 23, 2016. (Changes may R S still occur before final publication online and in print.) I E N C N A D V A Root Border Cells and Their Role in Plant Defense Martha Hawes,1,∗ Caitilyn Allen,2 B. Gillian Turgeon,3 Gilberto Curlango-Rivera,1 Tuan Minh Tran,2 David A. Huskey,1 and Zhongguo Xiong4 1Department of Soil, Water and Environmental Sciences, Bio5 Institute, University of Arizona, Tucson, AZ 85721; email: [email protected], [email protected], [email protected] 2Department of Plant Pathology, University of Wisconsin, Madison, Wisconsin 53706; email: [email protected], [email protected] 3School of Integrative Plant Science, Plant Pathology & Plant-Microbe Biology Section, Cornell University, Ithaca, New York 14853; email: [email protected] 4School of Plant Science, Bio5 Institute, University of Arizona, Tucson, AZ 85721; email: [email protected] Annu. Rev. Phytopathol. 2016. 54:5.1–5.19 Keywords The Annual Review of Phytopathology is online at rhizosphere, extracellular traps, root cap slime, exDNA, exDNase phyto.annualreviews.org This article’s doi: Abstract 10.1146/annurev-phyto-080615-100140 Root border cells separate from plant root tips and disperse into the soil en- Copyright c 2016 by Annual Reviews. Annu. Rev. Phytopathol. 2016.54. Downloaded from www.annualreviews.org vironment. In most species, each root tip can produce thousands of metabol- All rights reserved ically active cells daily, with specialized patterns of gene expression. Their function has been an enduring mystery. Recent studies suggest that bor- der cells operate in a manner similar to mammalian neutrophils: Both cell types export a complex of extracellular DNA (exDNA) and antimicrobial proteins that neutralize threats by trapping pathogens and thereby prevent- ing invasion of host tissues. Extracellular DNases (exDNases) of pathogens promote virulence and systemic spread of the microbes. In plants, adding Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 05/25/16. For personal use only. DNase I to root tips eliminates border cell extracellular traps and abolishes root tip resistance to infection. Mutation of genes encoding exDNase activity in plant-pathogenic bacteria (Ralstonia solanacearum) and fungi (Cochliobolus heterostrophus) results in reduced virulence. The study of exDNase activities in plant pathogens may yield new targets for disease control. 5.1 Changes may still occur before final publication online and in print PY54CH05-Hawes ARI 13 May 2016 11:31 INTRODUCTION The story of root border cells and their role in plant defense begins with a conundrum: If carbon balance is important to life on earth, why do plants waste energy producing cells destined to be sloughed into the soil every day? Daily carbon release from roots of some species has been measured at 40 to 90 percent of the total carbon fixed by leaves (70, 77). Up to 98 percent of such root exudates are made up of the sloughed root cap cells and associated extracellular material (35). In plants, including legumes, cereals, cucurbits, cotton (Gossypium hirsutum), and gymnosperms, this carbon dump includes thousands of cells produced in a single day (Figure 1) (23, 53). Upon dispersal of the cells in response to water or mechanical forces, mitosis in the root cap meristem is activated, root cap turnover is initiated, and within minutes a new population of cells begins to emerge from the cap periphery to replace the departed population (7). The apparent illogic in such extravagance may have contributed to the long-standing presumption that the detached cells are moribund even before dispersal, as the waste that would be involved in the release of so many metabolically active cells would be hard to accept (41). Thus, the scientific community (e.g., 31, 81) did not assimilate the discovery by Knudson (67, 68) nearly 100 years ago that pea (Pisum sativum)andcorn(Zea mays) root cap cell populations can remain 100% viable and capable of active enzyme secretion for months after dispersal. In the 1980s, interest in sloughed root cap cells stemmed from the discovery that the cells from oats (Avena sativa) and corn expressed the same sensitivity as whole plants to host-specific toxins from Cochliobolus victoriae and Cochliobolus heterostrophus, the causal agents of Victoria blight of oats and Southern corn leaf blight, respectively (46, 56, 57). The potential to use root bor- der cells as a convenient model system to define cellular responses to virulence factors as they Annu. Rev. Phytopathol. 2016.54. Downloaded from www.annualreviews.org 1 mm Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 05/25/16. For personal use only. Figure 1 Border cell dispersal from root tips is initiated instantly upon exposure to water and is complete within minutes, leaving the root tip surface free of cells. Mitosis within the root cap meristem is evident within 5–10 minutes, and a new set of border cells is produced within 20 hours (7). Reproduced with permission from http://www.plantphysiol.org, Copyright American Society of Plant Biologists. 5.2 Hawes et al. Changes may still occur before final publication online and in print PY54CH05-Hawes ARI 13 May 2016 11:31 occur has therefore been explored (47, 54). This review summarizes the ensuing chronology of discoveries about border cell properties whose significance in plant defense finally came to light with the coincidental recognition of a similar property in human immune systems: In mammals as well as plants, extracellular DNA (exDNA)-based extracellular traps are previously unrecognized components of early immune responses (8–10, 13, 17, 23, 30, 50, 51, 72). BORDER CELLS AND PLANT PATHOGENS The complex developmental dynamics of pathogen invasion of intact plant tissue make it difficult to observe the sequence of events in situ and define the steps needed for infection to occur (88). Studies therefore were designed to exploit developmentally uniform, viable populations of border cells as a model system to track infection at the cellular level (49). Host-microbe–specific recognition of border cells observed with bacteria, nematodes, zoospores, and fungi were consistent with a logical model for the effect of root exudates on soilborne pathogens: Contents released from the sloughed cells provide nutrition needed to stimulate growth and thereby facilitate infection of the host. Host-specific chemotaxis and binding yielded promising evidence that the cell populations would facilitate tracking experiments that allow direct observation of the cellular invasion as it happens and thereby yield new insights into the infection process (48, 52, 54). Thus, for example, Agrobacterium tumefaciens populations were chemotactically attracted to host border cells, where they accumulated in large numbers within minutes (Figure 2). No attraction or binding occurred on border cells of nonhost species. Despite thousands of replicates, however, in no case was infection of a single border cell observed. Root-infecting fungi also responded rapidly and in a host-specific manner to border cells, as predicted if the detached cells, like intact root tissue, were susceptible to infection. Spores of Nectria haematococca (Fusarium solani f. sp. pisi ) were stimulated to undergo rapid germination in response to border cells of host species, but in no case was penetration of individual border cells observed (38). The predicted stimulation of growth in response to nutrients from the border cells also did not occur. Instead, fungal growth ceased and remained static (39). Similar results occurred with nematodes (116): Rapid chemotaxis to border cells resulted in masses of aggregated nematodes within minutes, suggesting that an invasion was in progress Annu. Rev. Phytopathol. 2016.54. Downloaded from www.annualreviews.org Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 05/25/16. For personal use only. 15 μm! Figure 2 Agrobacterium tumefaciens binding to pea border cells (54). Chemotaxis of bacteria toward the plant cells (black arrow) is initiated instantaneously, and most cells are aggregated with bacteria into masses over time (white arrows). www.annualreviews.org • Root Border Cells and Their Role in Plant Defense 5.3 Changes may still occur before final publication online and in print PY54CH05-Hawes ARI 13 May 2016 11:31 50 μm Figure 3 Nematode (white arrow) chemotaxis to border cells (blue arrow). Within 5 min of adding Meloidogyne incognita to pea roots, all the nematodes aggregate within the mass of border cells (116). No chemotaxis to root tips occurs if border cells are removed (59). (Figure 3). However, this was followed by an induced state of quiescence lasting for days (59). No border cell penetration was observed. Zoospores of Pythium dissotocum and Pythium catenulatum were chemotactically attracted to border cells of their hosts, cotton (Gossypium barbadense and G. hirsutum) and cucumber (Cucumus sativus), respectively, but were not responsive to nonhost species (34). Invasion of the single border cells did occur (Figure 4). However, growth of the pathogen ceased after penetration and did not resume. Most surprising was the observation that chemotaxis was specific to border cells: When border cells were removed prior to adding bacteria, zoospores, or nematodes, no attraction to the root tip occurred. These findings did
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