| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
|
First published online August 21, 2009; 10.1104/pp.109.142067 Plant Physiology 151:820-829 (2009) © 2009 American Society of Plant Biologists OPEN ACCESS ARTICLE
Extracellular DNA Is Required for Root Tip Resistance to Fungal Infection1,[W],[OA]Department of Plant Sciences, Division of Plant Pathology and Microbiology, University of Arizona, Tucson, Arizona 85713
Plant defense involves a complex array of biochemical interactions, many of which occur in the extracellular environment. The apical 1- to 2-mm root tip housing apical and root cap meristems is resistant to infection by most pathogens, so growth and gravity sensing often proceed normally even when other sites on the root are invaded. The mechanism of this resistance is unknown but appears to involve a mucilaginous matrix or "slime" composed of proteins, polysaccharides, and detached living cells called "border cells." Here, we report that extracellular DNA (exDNA) is a component of root cap slime and that exDNA degradation during inoculation by a fungal pathogen results in loss of root tip resistance to infection. Most root tips (>95%) escape infection even when immersed in inoculum from the root-rotting pathogen Nectria haematococca. By contrast, 100% of inoculated root tips treated with DNase I developed necrosis. Treatment with BAL31, an exonuclease that digests DNA more slowly than DNase I, also resulted in increased root tip infection, but the onset of infection was delayed. Control root tips or fungal spores treated with nuclease alone exhibited normal morphology and growth. Pea (Pisum sativum) root tips incubated with [32P]dCTP during a 1-h period when no cell death occurs yielded root cap slime containing 32P-labeled exDNA. Our results suggest that exDNA is a previously unrecognized component of plant defense, an observation that is in accordance with the recent discovery that exDNA from white blood cells plays a key role in the vertebrate immune response against microbial pathogens.
Root diseases caused by soil-borne plant pathogens are a perennial source of crop loss worldwide (Bruehl, 1986  ; Curl and Truelove, 1986). These diseases are of increasing concern, as pesticides like methyl bromide are removed from the market due to environmental concerns (Gilreath et al., 2005). One possible alternative means of crop protection is to exploit natural mechanisms of root disease resistance (Nelson, 1990; Goswami and Punja, 2008; Shittu et al., 2009). Direct observation of root systems under diverse conditions has revealed that root tips, in general, are resistant to infection even when lesions are initiated elsewhere on the same plant root (Foster et al., 1983; Bruehl, 1986; Curl and Truelove, 1986; Smith et al., 1992; Gunawardena et al., 2005; Wen et al., 2007). This form of disease resistance is important for crop production because root growth and its directional movement in response to gravity, water, and other signals can proceed normally as long as the root tip is not invaded. The 1- to 2-mm apical region of roots houses the root meristems required for root growth and cap development, and when infection does occur, root development ceases irreversibly within a few hours even in the absence of severe necrosis (Gunawardena and Hawes, 2002). Mechanisms underlying root tip resistance to infection are unclear, but the phenomenon appears to involve root cap "slime," a mucilaginous matrix produced by the root cap (Morré et al., 1967; Rougier et al., 1979; Foster, 1982; Chaboud, 1983; Guinel and McCully, 1986; Moody et al., 1988; Knee et al., 2001; Barlow, 2003; Iijima et al., 2008). Within the root cap slime of cereals, legumes, and most other crop species are specialized populations of living cells called root "border cells" (Supplemental Fig. S1; Hawes et al., 2000). Border cell numbers increase in response to pathogens and toxins such as aluminum, and the cell populations maintain a high rate of metabolic activity even after detachment from the root cap periphery (Brigham et al., 1995; Miyasaka and Hawes, 2000).
As border cells detach from roots of cereals and legumes, a complex of more than 100 proteins, termed the root cap secretome, is synthesized and exported from living cells into the matrix ensheathing the root tip (Brigham et al., 1995
exDNA has long been known to be a component of slimy biological matrices ranging from purulent localized human infections to bacterial capsules, biofilms, and snail exudate (Sherry and Goeller, 1950
Loss of Root Tip Resistance to Infection in Response to in Situ DNase Treatment of Root Cap Slime
Deoxyribose previously was detected in root exudates of young monocot seedlings by chromatographic analysis (Vancura, 1964
Brinkmann et al. (2004) directly established evidence for a functional role of neutrophil exDNA by showing that the structural integrity of NETs is lost when the exDNA is degraded enzymatically. We used the same approach by proposing that, if presumptive exDNA visualized by histological staining (Fig. 1) plays a role in the defense response of plant roots, as it does in mammalian immunity, then degrades during the infection process, it would be predicted to result in increased susceptibility of root tips to fungal invasion. This hypothesis was tested directly by treating root tips with the endonuclease DNase I in the presence of spores of the pea root-rotting pathogen, Nectria haematococca (Fig. 2
). When roots are uniformly inoculated with spores, N. haematococca infects most roots (>90%) in the region of elongation behind the root tip, but the tip remains uninvaded and growth proceeds normally (Gunawardena and Hawes, 2002; Wen et al., 2007). The presence of the fungus does not trigger expression of defense responses within the root tip unless there is a visible necrosis, and lateral roots that emerge during the course of the infection assay resist infection as does the primary root tip, despite growing among fungal hyphae (Gunawardena et al., 2005). In approximately 3% of inoculated roots, fungal hyphae can be seen to invade the inoculated root tip, which then expresses defense genes, develops necrosis, and ceases growth within 24 h. In this study, the incidence of infection increased from 3% ± 3% in inoculated root tips without DNase I (Fig. 2A) to 100% in inoculated root tips treated with DNase I (Fig. 2B). These differences were statistically distinct at P < 0.0001. Infections that developed in the presence of DNase I were marked by severe necrosis, total cessation of growth, and proliferation of hyphal growth surrounding the root tip regions (Fig. 2B, arrowheads).
One explanation for these results is that nuclease activity and/or the degradation of exDNA somehow results in plant cell death, allowing increased tissue ingress for the fungus. However, control experiments using DNase I treatment alone did not support this explanation: treatment with DNase I caused no root tip necrosis among treated roots (Fig. 2C; n > 100). At 48 h after treatment, the mean increase in root length, with and without DNase treatment of root tips, was 36 ± 8 mm (n = 18) and 34 ± 9 mm (n = 18), respectively. Border cell viability in uninoculated control roots was 95% ± 5%, with or without DNase treatment. Similar results were obtained when salmon sperm DNA or pea genomic DNA was added to roots and incubated with DNase I. These data suggested that it is the loss of the root cap slime exDNA, per se, that is responsible for loss of root tip resistance to infection when root tips are treated with DNase I. An alternative explanation for increased fungal infection of root tips in the presence of DNase I is that breakdown of exDNA within the surrounding root cap slime provides an enhanced nutrient resource for the fungus, fostering more rapid growth and development during early stages of the interaction. However, control experiments in which root mucilage collected from nuclease-treated roots was added to spores did not support this explanation: no increase in the rate of spore germination or hyphal growth was detected. Within 3 h of culturing spores with root exudates with and without DNase I treatment, spore germination rates were 78% ± 7% (n = 792) and 80% ± 4% (n = 853), respectively. During the 16-h course of incubation of spores with DNase I, measurements for hyphal growth in root exudates with and without DNase I treatment were A620 = 0.027 ± 0.016 (n = 20) and A620 = 0.028 ± 0.012 (n = 20), respectively, and were not statistically distinct. The same results observed in growth pouch experiments (Fig. 2) occurred when the experiment was carried out under alternative conditions, with excised root tips immersed directly within the treatment solutions in wells of a microtiter plate (Fig. 3 ; Supplemental Fig. S2). A reporter strain of N. haematococca expressing GFP was used to visualize early stages of infection (Supplemental Fig. S2). At 24 h after inoculation of root tips with fungal spores alone, hyphal growth was minimal (Supplemental Fig. S2A). At 48 h, hyphal growth remained dispersed away from the root tip and no strands of GFP-expressing hyphae could be seen in contact with root tissues (Supplemental Fig. S2C). In root tips coinoculated with N. haematococca and DNase I (Supplemental Fig. S2, B and D), proliferation of GFP-expressing hyphae (black arrows) on the surface of and penetrating within root tissue was evident within 24 h. As in the growth pouch assay, the incidence of root tip infection, manifested as cessation of growth and development of root tip necrosis, increased within 72 h from 3% ± 4% in the absence of DNase I to 100% of roots inoculated in the presence of DNase I (P < 0.0001). As in the growth pouch assay, adding salmon sperm DNA or pea genomic DNA did not alter the frequency of root tip infection, and no necrosis occurred on control roots treated with DNase I alone. Confocal microscopy revealed that in inoculated roots without DNase I treatment, growth of individual hyphae within 36 h was unbranched and limited to less than 100 µm in length (Fig. 3A), whereas growth in DNase I-treated samples hyphae was branched and more than 200 µm long (Fig. 3B). In DNase I-treated root tips, direct contact between proliferating fungal hyphae and the plant cell surface was evident (Fig. 3B). A profusion of border cells (Fig. 3B, white arrow) was apparent, and some fungal strands were seen to have penetrated the root epidermis (Fig. 3B, black arrows).
Slower DNA Digestion Is Correlated with Delayed Onset of Infection
The process of pea root infection by N. haematococca is a time-dependent process (Gunawardena and Hawes, 2002 First, BAL31, an exonuclease, was shown to require a significantly longer period of time to degrade pea DNA polymers than is required for DNase I under the conditions of our pea pathogenicity assay (Fig. 4). When a sample of pea genomic DNA was treated with DNase I under the conditions used in the root tip infection assay, as described above, the entire sample was degraded to fragments smaller than 250 bp within 2 h. By contrast, after 24 h of treatment with BAL31, the size range of pea genomic DNA remained within 250 bp to 6 kb.
If exDNA is required for root tip resistance to infection and its degradation underlies the observed changes in DNase I-treated root tip infection (Figs. 2 and 3; Supplemental Fig. S2), then the reduced rate of exDNA digestion seen with BAL31 (Fig. 4) would be predicted to result in delayed and/or reduced infection. We tested this prediction by treating inoculated roots with BAL31 instead of DNase I and found that this change was correlated with a 24-h delay in onset of necrosis and root tip destruction, compared with the response to DNase I. Most roots inoculated with N. haematococca (97% ± 3%) escaped necrosis, and roots with uninvaded root tips continued to grow in a manner indistinguishable from that of uninoculated control roots (Fig. 5A ). Root tips treated with BAL31 developed a tan discoloration within 72 h (Fig. 5B) but growth continued, and the degree of infection in BAL31-treated root tips was noticeably less severe than in root tips treated with DNase I (Fig. 5C). Only after 96 h did infection in roots treated with BAL31 and N. haematococca progress to blackened necrosis and cessation of growth. This would be the predicted result if intact DNA polymers within root cap slime are required for its observed effect on the root tip resistance.
DNA in Root Cap Slime
The observation that DNase added to root tips eliminates resistance to infection lends support to the hypothesis that DNA is present in the extracellular matrix and that its presence and structural integrity are required for root tip defense. The possibility that exDNA is a component of root cap slime was confirmed by electrophoretic display of exDNA extracted from pea root cap slime (Fig. 6
). In this study, the presence of DNA in the cell-free supernatant was estimated based on A260 and then was confirmed by analyzing a sample obtained using a standard phenol-chloroform protocol for DNA isolation (Sambrook et al., 1989
One possible source of exDNA is dead, dying, or lysed border cells that are released into slime upon immersion of root tips into water but were not detected by the methods used to control for such events. We estimated the number of cells that would be required to account for our results. In pea (cv Little Marvel), approximately 150 to 175 (5%) of the 3,500 ± 500 cells produced per root tip daily are nonviable when the radicle is 25 to 35 mm in length (Brigham et al., 1995 ). Given a genome size of approximately 4,000 Mb per haploid genome, 100% of the total nuclear DNA for the 3,500 diploid pea border cells delivered into the extracellular matrix would yield approximately 28 ng of exDNA. The 150 to 175 dead cells, assuming 100% of nuclear DNA content for every cell was extruded from all the cells and successfully collected from a fraction of the supernatant (as described above), would yield 1.4 ng, approximately 14% of the actual yield obtained when root cap slime was harvested. Moreover, this yield would be the expected result only if killed cells release exDNA through their cell walls after death. This possibility was examined. In control samples of slime from border cells that were washed to remove existing exDNA and then killed by freezing at –80C, as described previously for secreted proteins (Wen et al., 2007), no additional exDNA could be collected from the supernatant.
Previously, we showed that proteins of the root cap secretome are synthesized and secreted by living cells (Brigham et al., 1995
A hallmark of root tip resistance to invasion by fungal pathogens is a phenomenon in which the pathogen appears to be prevented from forming intimate contact with the root surface (Hawes et al., 1998 ; Gunawardena and Hawes, 2002). Instead, there is formation of a "mantle" of germinating hyphae and border cells that detaches, leaving the root cap uninvaded. The mechanism underlying the surprising observation that a pathogenic fungus can germinate and grow within the immediate vicinity of newly emergent root tips without invading the cells or triggering a defense response has remained unclear (Gunawardena et al., 2005). Striking parallels appear to exist between the defense response in vertebrate white blood cells and in legume root tips. In response to microbial invasion in humans and other animal species, neutrophils enter the bloodstream and form NETs, extracellular structures that aggregate and kill pathogens by localizing them within a matrix of antimicrobial peptides and proteins (Brinkmann et al., 2004; Medina, 2009). These extracellular traps also are produced by mast cells, which are present at the surface of tissues exposed to the environment and microorganisms (von Köckritz-Blickwede et al., 2008). exDNA linked with extracellular histone is a structural component of NETs, and treatment with DNase destroys NET integrity and function (Wartha et al., 2007). Perhaps the most compelling information regarding the importance of NETs is the discovery that pathogens like group A Streptococcus require extracellular DNases for virulence (Sumby et al., 2005). In plants, a population of detached cells ensheathed within root cap slime is released into the environment to form a mantle that localizes and inhibits growth of pathogenic fungi (Gunawardena et al., 2005; Wen et al., 2007). When the root tip is treated with DNase, this NET-like mantle is destroyed and the normal resistance to infection is abolished. Like human pathogens that produce extracellular DNase activities now known to be involved in virulence (Sherry and Goeller, 1950; Sumby et al., 2005; Buchanan et al., 2006), root-associated bacteria and fungi also produce extracellular DNase activities (Klosterman et al., 2001; Tavares and Sellstedt, 2001; Balestrazzi et al., 2007). Klosterman et al. (2001) have proposed that such enzymes in pathogenic fungi function by entering the nuclei of plant cells and causing DNA damage that triggers defense responses in nonhost tissues. It will be of interest in future studies to examine the alternative hypothesis that, as with human pathogens, these enzymes play a role in plant cell exDNA degradation as part of the infection process.
How exDNA might be delivered to the extracellular matrix of plants is unknown. Root caps are secretory organs, actively exporting the component polymers that make up root cap slime (Morré et al., 1967 Our study indicates that, in plants as well as animals, DNA can serve in critical biological roles other than as the language of inheritance.
Plant Material
Sterilization and germination of seeds of pea (Pisum sativum ‘Little Marvel’; Meyer Seed), border cell collection, and viability measurement were as described (Brigham et al., 1995
Border cells or root tips of intact seedlings were stained by DNA stain DAPI (Invitrogen) or SYTOX Green (Invitrogen) according to the manufacturer's instructions. Each treatment was replicated at least 10 times. Samples were viewed using an Olympus fluorescence microscope equipped with U-MWU2 (for DAPI excitation). The images were captured with an Olympus digital camera using MicroFire software.
Nectria haematococca culture, collection of spores, root tip inoculation, and evaluation of infection using a growth pouch assay (Caetano-Anollés et al., 1992
Root exudates and border cells were collected separately from root tips incubated in water and in DNase I in microtiter plate wells. Root exudates were separated from border cells by a pulse spin of the mixture at the lowest speed in a microcentrifuge. Both exudate samples were heated at 75°C for 10 min to inactivate DNase I activity. Subsequently, fungal spores (104 spores mL–1) were added to replicate exudate samples (at 200 µL) in independent microtiter plate wells. Five independent experiments, each with at least three replicate samples per treatment, were performed to examine the frequency of spore germination and fungal growth. Spore germination assays were assessed by direct counts of germinating spores, and fungal growth was assessed by measuring A620 using a microtiter plate scanner as described previously (Gunawardena et al., 2005 For confocal microscopy analysis of interactions between root tips and N. haematococca fungal hyphae, root tips were incubated with fungal spores in microtiter plate wells with or without DNase I. Treated root tips were then observed with a confocal laser scanning microscope (Leica SP5). GFP green fungal hyphae and red root autofluorescence images were obtained by dual excitation at 490 and 568 nm, respectively. One optical section (5 µm) is shown in Figure 3.
Root tip mucilage was collected from the supernatant of washed border cells (Brigham et al., 1995
For sequence analysis, exDNA (200 ng) was subjected to A-tailing using RedMix Taq DNA polymerase (Sigma-Aldrich) at 72°C for 20 min and then cloned into pGEM-T Easy vector (Promega) through direct cloning as described (Janska et al., 1998
Protoplasts of N. haematococca were prepared as described by Miao et al. (1991)
Ten seedlings, with border cells attached, were arranged radially in a sterile petri dish as described in previous assays for in vivo labeling of newly synthesized proteins (Brigham et al., 1995
The following materials are available in the online version of this article.
We thank Dr. Ravishankar Palanivelu for expertise with confocal microscopy experiments. Received May 26, 2009; accepted August 12, 2009; published August 21, 2009.
1 This work was supported by the College of Agriculture and Life Sciences, University of Arizona, and by the U.S. Department of Energy and the U.S. Department of Agriculture (grants awarded to M.C.H. and H.D.V., respectively).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Martha C. Hawes (mhawes{at}u.arizona.edu).
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.109.142067 * Corresponding author; e-mail mhawes{at}u.arizona.edu.
Allesen-Holm M, Barken KB, Yang L, Klausen M, Webb JS, Kjelleberg S, Molin S, Givskov M, Tolker-Nielsen T (2006) A characterization of the DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 59: 1114–1128[CrossRef][Web of Science][Medline] Balestrazzi A, Bonadei M, Carbonepa D (2007) Nuclease-producing bacteria in soil cultivated with herbicide resistant transgenic white poplars. Ann Microbiol 57: 531–536 Barlow PW (2003) The root cap: cell dynamics, cell differentiation and cap function. J Plant Growth Regul 21: 261–286[CrossRef][Web of Science] Braun W, Whallon J (1954) The effects of DNA and enzyme-treated DNA on bacterial population changes. Proc Natl Acad Sci USA 40: 162–164 Brigham LA, Woo HH, Hawes MC (1995) Differential expression of proteins and mRNAs from border cells and root tips of pea. Plant Physiol 109: 457–460[Abstract] Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A (2004) Neutrophil extracellular traps kill bacteria. Science 303: 1532–1535 Brinkmann V, Zychlinsky A (2007) Beneficial suicide: why neutrophils die to make NETs. Nat Rev Microbiol 5: 577–582[CrossRef][Web of Science][Medline] Bruehl GW (1986) Soilborne Plant Pathogens. Macmillan Publishing, New York Buchanan JT, Simpson AJ, Aziz RK, Liu GY, Kristian SA, Kotb M, Feramisco J, Nizet V (2006) DNase expression allows the pathogen group A Streptococcus to escape killing in neutrophil extracellular traps. Curr Biol 16: 396–400[CrossRef][Web of Science][Medline] Caetano-Anollés G, Wrobel-Boerner E, Bauer WD (1992) Growth and movement of spot inoculated Rhizobium meliloti on the root surface of alfalfa. Plant Physiol 98: 1181–1189 Carrolla AD, Moyena C, Van Kesterenb P, Tookeb F, Battey NH, Brownlee C (1998) Ca2+, annexins, and GTP modulate exocytosis from maize root cap protoplasts. Plant Cell 10: 1267–1276 Catlin BW (1956) Extracellular deoxyribonucleic acid of bacteria and a deoxyribonuclease inhibitor. Science 124: 441–442 Chaboud A (1983) Isolation, purification and chemical composition of maize root cap slime. Plant Soil 73: 395–402[CrossRef][Web of Science] Clark JM (1988) Novel non-templated nucleotide addition reactions catalyzed by procaryotic and eucaryotic DNA polymerases. Nucleic Acids Res 16: 9677–9686 Cooper PC, Burgess AW (1985) Biosynthetic labeling with 32P: radiation damage to mammalian cells. Anal Biochem 144: 329–335[CrossRef][Web of Science][Medline] Curl EA, Truelove B (1986) The Rhizosphere. Springer-Verlag, Berlin De-la-Peña C, Lei Z, Watson BS, Sumner LW, Jorge M, Vivanco JM (2008) Root-microbe communication through protein secretion. J Biol Chem 283: 25247–25255 Fahy JV, Steiger DJ, Liu J, Basbaum CB, Finkbeiner WE, Boushey HA (1993) Markers of mucus secretion and DNA levels in induced sputum from asthmatic and from healthy subjects. Am Rev Respir Dis 147: 1132–1137[Web of Science][Medline] Foster RC (1982) The fine structure of epidermal cell mucilages of roots. New Phytol 91: 727–740[CrossRef][Web of Science] Foster RC, Rovira AD, Cock TW (1983) Ultrastructure of the Root-Soil Interface. American Phytopathological Society, St. Paul Gilreath JP, Noling JW, Bielinski M, Santos BM (2005) Methyl bromide alternatives for bell pepper (Capsicum annuum) and cucumber (Cucumis sativus) rotations. Crop Prot 23: 347–351[CrossRef][Web of Science] Goswami RS, Punja ZK (2008) Molecular and biochemical characterization of defense responses in ginseng (Panax quinquefolius) roots challenged with Fusarium equiseti. Physiol Mol Plant Pathol 72: 10–20[CrossRef] Guimaraes-Costa AB, Nascimento MTC, Froment GS, Soares RPP, Morgado FN, Conceicao-Silva F, Saraiva EM (2009) Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proc Natl Acad Sci USA 106: 6748–6753 Guinel FC, McCully ME (1986) Some water-related physical properties of maize root cap mucilage. Plant Cell Environ 9: 657–666[CrossRef] Gunawardena U, Hawes MC (2002) Role of border cells in localized root infection by pathogenic fungi. Mol Plant Microbe Interact 15: 1128–1136[Web of Science][Medline] Gunawardena U, Rodriguez M, Straney D, Romeo JT, VanEtten HD, Hawes MC (2005) Tissue-specific localization of pea root infection by Nectria haematococca: mechanisms and consequences. Plant Physiol 137: 1363–1374 Hawes MC, Brigham LA, Wen F, Woo HH, Zhu Y (1998) Function of root border cells in plant health: pioneers in the rhizosphere. Annu Rev Phytopathol 36: 311–327[CrossRef][Web of Science][Medline] Hawes MC, Gunawardena U, Miyasaka S, Zhao X (2000) The role of root border cells in plant defense. Trends Plant Sci 5: 128–133[CrossRef][Web of Science][Medline] Hawes MC, Wheeler HE (1982) Factors affecting victorin-induced root cap cell death: temperature and plasmolysis. Physiol Plant Pathol 20: 137–145[CrossRef] Iijima M, Morita S, Barlow PW (2008) Structure and function of root cap. Plant Prod Sci 11: 17–27[CrossRef][Web of Science] Izano EA, Amarante MA, Kher WB, Kaplan JB (2008) Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Appl Environ Microbiol 74: 470–476 Janska H, Sarria R, Woloszynska M, Arrieta-Montiel M, Mackenzie SA (1998) Stoichiometric shifts in the common bean mitochondrial genome leading to male fertility and spontaneous reversion to fertility. Plant Cell 10: 1163–1180 Jones JL, Singer LV (2001) Fluorescence microplate-based assay for tumor necrosis factor activity using SYTOX green stain. Anal Biochem 293: 8–11[CrossRef][Web of Science][Medline] Jones PA (1977) Development of the quiescent center in maturing embryonic radicles of pea. Planta 135: 233–240[CrossRef][Web of Science] Klosterman SJ, Chen J, Choi JJ, Chinn EE, Hadwiger LA (2001) Characterization of a 20 kD DNase elicitor from Fusarium salani f. sp. phaseoli and its expression at the onset of induced resistance in Pisum sativum. Mol Plant Pathol 2: 147–158[CrossRef] Knee EM, Gong FC, Gao M, Teplitski M, Jones AR, Foxworthy A, Mort AJ, Bauer WD (2001) Root mucilage from pea and its utilization by rhizosphere bacteria as a sole carbon source. Mol Plant Microbe Interact 14: 775–784[Web of Science][Medline] Kraszewska EK, Bjerknes CA, Lamm SS, Van't Hof J (1985) Extrachromosomal DNA of pea-root (Pisum sativum) has repeated sequences and ribosomal genes. Plant Mol Biol 5: 353–361[CrossRef][Web of Science] Krimer DB, Van't Hof J (1983) Extrachromosomal DNA of pea root-tip cells replicates by strand displacement. Proc Natl Acad Sci USA 80: 1933–1937 Kubista M, Akerman B, Norden B (1987) Characterization of interaction between DNA and 4',6-diamidino-2-phenylindole by optical spectroscopy. Biochemistry 26: 4545–4553[CrossRef][Web of Science][Medline] Kwon C, Bednarek P, Schulze-Lefert P (2008) Secretory pathways in plant immune responses. Plant Physiol 147: 1575–1583 Leuchtenberger C, Schrader F (1952) Variation in the amounts of desoxyribose nucleic acid (DNA) in cells of the same tissue and its correlation with secretory function. Proc Natl Acad Sci USA 38: 99–105 Lynch MA, Staehelin LA (1992) Domain-specific and cell type specific localization of 2 types of cell-wall matrix polysaccharides in the clover root tip. J Cell Biol 118: 467–479 Macas J, Neumann P, Navrátilová A (2007) Repetitive DNA in the pea (Pisum sativum L.) genome: comprehensive characterization using 454 sequencing and comparison to soybean and Medicago truncatula. BMC Genomics 8: 427[CrossRef][Medline] Medina E (2009) Neutrophil extracellular traps: a strategic tactic to defeat pathogens with potential consequences for the host. J Inn Immun 1: 176–180[CrossRef] Miao VPW, Matthews DE, VanEtten HD (1991) Identification and chromosomal locations of a family of cytochrome P-450 genes for pisatin detoxification in the fungus Nectria haematococca. Mol Gen Genet 226: 214–223[CrossRef][Web of Science][Medline] Miyasaka SC, Hawes MC (2000) Possible role of root border cells in detection and avoidance of aluminum toxicity. Plant Physiol 125: 1978–1987[CrossRef][Web of Science] Moody SF, Clarke AE, Bacic A (1988) Structural analysis of secreted slime from wheat and cowpea roots. Phytochemistry 27: 2857–2861[CrossRef][Web of Science] Morré DJ, Jones DD, Mollenhauer HH (1967) Golgi apparatus meditated polysaccharide secretion by outer root cap cells of Zea mays. I. Kinetics and secretory pathway. Planta 74: 286–301[CrossRef][Web of Science] Nelson EB (1990) Exudate molecules initiating fungal responses to seeds and roots. Plant Soil 129: 61–73[CrossRef][Web of Science] Pali Phillips HL, Torrey JG (1971) Deoxyribonucleic acid synthesis in root cap cells of cultured roots of Convolvulus. Plant Physiol 48: 213–218 Qin Z, Ou Y, Yang L, Zhu Y, Tolker-Nielsen T, Molin S, Qu D (2007) Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology 153: 2083–2092 Rougier M, Kieda C, Monsigny M (1979) Use of lectin to detect the sugar components of maize root cap slime. J Histochem Cytochem 27: 878–881[Web of Science][Medline] Roy S, Vian B (1991) Transmural exocytosis in maize root cap: visualization by simultaneous use of a cellulose-probe and a fucose-probe. Protoplasma 161: 181–191 Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual, Ed 2. Cold Spring Harbor Laboratory Press, Cold Spring Harbor , NY Sherry S, Goeller JP (1950) The extent of the enzymatic degradation of desoxyribonucleic acid (DNA) in purulent exudates by streptodornase. J Clin Invest 29: 1588–1594[CrossRef][Web of Science][Medline] Shittu HO, Castroverde DCM, Nazar RN, Robb J (2009) Plant-endophyte interplay protects tomato against a virulent Verticillium. Planta 229: 415–426[CrossRef][Web of Science][Medline] Smith S, Dickson S, Walker N (1992) Distribution of VA mycorrhizal entry points near the root apex: is there an uninfectible zone at the root-tip of leek or clover? New Phytol 122: 469–477[CrossRef][Web of Science] Smithies WR, Gibbons NE (1955) The deoxyribose nucleic acid slime layer of some halophilic bacteria. Can J Microbiol 1: 614–621[Web of Science][Medline] Spoering AL, Gilmore MS (2006) Quorum sensing and DNA release in bacterial biofilms. Curr Opin Microbiol 9: 133–137[CrossRef][Web of Science][Medline] Sumby P, Barbian KD, Gardner DJ, Whitney AR, Welty DM, Long RD, Bailey JR, Parnell MJ, Hoe NP, Adams GG, et al (2005) Extracellular DNase made by group A Streptococcus assists pathogenesis by enhancing evasion of the innate immune response. Proc Natl Acad Sci USA 102: 1679–1684 Sweigard JA, Chumley FG, Valent B (1992) Cloning and analysis of CUT1, a cutinase gene from Magnaporthe grisea. Mol Gen Genet 232: 174–182[Web of Science][Medline] Tavares F, Sellstedt A (2001) DNase-resistant DNA in the extracellular and cell wall-associated fractions of Frankia strains R43 and CcI3. Curr Microbiol 42: 168–172[CrossRef][Web of Science][Medline] Urban CF, Reichard U, Brinkmann V, Zychlinsky A (2006) Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell Microbiol 8: 668–676[CrossRef][Web of Science][Medline] Vancura V (1964) Root exudates of plants. I. Analysis of root exudates of barley and wheat in their initial phases of growth. Plant Soil 2: 231–245 Van't Hof J, Bjerknes CA (1982) Cells of pea (Pisum sativum) that differentiate from G2 phase have extrachromosomal DNA. Mol Cell Biol 2: 339–345 von Köckritz-Blickwede M, Rohde M, Oehmcke S, Miller LS, Cheung AL, Herwald H, Foster S, Medina E (2008) Immunological mechanisms underlying the genetic predisposition to severe Staphylococcus aureus infection in the mouse model. Am J Pathol 173: 1657–1668 Wartha F, Beiter K, Normark S, Henriques-Normark B (2007) Neutrophil extracellular traps: casting the NET over pathogenesis. Curr Opin Microbiol 10: 52–56[CrossRef][Web of Science][Medline] Wen F, VanEtten H, Tsaiprailis G, Hawes MC (2007) Extracellular proteins in Pisum sativum L. root tip and border cell exudates. Plant Physiol 143: 773–783 Yousefi S, Gold JA, Andina N, Lee JJ, Kelly AM, Kozlowski E, Schmid I, Straumann A, Reichenbach J, Gleich GJ, et al (2008) Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense. Nat Med 14: 949–953[CrossRef][Web of Science][Medline] Related articles in Plant Physiol.:
|
|||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| ASPB Publications | PLANT PHYSIOLOGY® | THE PLANT CELL | |
|---|---|---|---|
TOP
ABSTRACT
RESULTS
et al., 2007
