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Anatomy and Morphology |
2Viticulture and Enology Dept., University of California, Davis, California, 95616 USA; 3Food Science and Technology Dept., University of California, Davis, California, 95616 USA; 4Section of Plant Biology, University of California, Davis, California, 95616 USA; 5Plant Sciences Dept., University of California, Davis, California, 95616 USA
Received for publication December 1, 2005. Accepted for publication January 24, 2006.
ABSTRACT
Xylem-dwelling pathogens become systemic, suggesting that microorganisms move efficiently in the xylem. To better understand xylem pathways and how bacteria move within the xylem, vessel connectivity between stems and leaves of Vitis vinifera cv. Chardonnay and Muscadinia rotundifolia cv. Cowart was studied. Three methods were used: (1) the light-producing bacterium, Yersinia enterocolitica, (Ye) strain GY5232 was loaded into petioles and followed using X-ray film, (2) fluorescent beads were loaded and followed by microscopy, and (3) low-pressure air was pumped into leaves and extruded bubbles from cuts in submerged leaves were followed. Bacteria, beads, and air moved through long and branched xylem vessels from the petiole into the veins in leaves of both varieties. From the stem, bacteria and air traveled into primary and secondary veins of leaves one, two, and three nodes above the loading point of the bacteria or air. Particles and air could move unimpeded through single xylem vessels or multiple vessels (conduits) connected possibly through broken pit membranes from within the stem axis into leaf blades. Bacteria were also able to move long distances within minutes from stem to leaf passively without having to cross pit membranes. Such complex, open xylem conduits have not been well documented before; these findings will help elucidate mechanisms involved in the systemic spread of pathogens.
Key Words: grapevine • Muscadinia rotundifolia • particle movement • pit membrane • Vitis vinifera • xylem vessel connectivity
During the formation of vascular bundles in leaves, xylem development is discontinuous, with an auxin-regulated bidirectional differentiation such that xylem maturation occurs both basipetally and acropetally until neighboring longitudinal segments connect to form the xylem network (Esau, 1965a
, b
; Sachs, 1969
, 1981
; Aloni, 2005
). As xylem vessel members mature, secondary cell walls thicken according to some pattern. The vessel members making up a vessel have perforated end walls, but the vessel members at the ends of a vessel have an imperforate end wall (Esau, 1965a
). Thus, xylem vessels have a finite length and form discrete units hydraulically linked to adjacent vessels by pit membranes through which water and low molecular mass solutes can pass, but microorganisms (except for very small viruses) and gas bubbles cannot (Tarbah and Goodman, 1987
; Fosket, 1994
; Bové and Garnier, 2002
; Tyree and Zimmermann, 2002
; Zwieniecki et al., 2002
; Choat et al., 2005
). Perforation plates can also form on the unreinforced sections of lateral walls when vessels are in physical contact (Fosket, 1994
). Accordingly, a certain number of neighboring xylem vessel members may be connected by perforation plates to form branched xylem vessels.
Many pathogenic bacteria use the xylem to move throughout the plant to become systemic (Bové and Garnier, 2002
). Researchers examining the vascular interconnectedness of organs (e.g., stem to leaf) have described the hydraulic connections within a plant (Howard, 1974
; Ewers and Fisher, 1989a
, b) and focused nearly exclusively on the movement of water (Rouschal, 1940
; Zimmermann, 1983
; Tyree and Zimmermann, 2002
; Zwieniecki et al., 2002
; Choat et al., 2005
). However, the presence of pit membranes creates a distinct difference between where water flows and where particles or microorganisms are able to reach via the transpiration stream. In the few investigations into potential xylem pathways available to particles or bacteria between stems and leaves, only insignificant movement from one organ to another was observed (Canny, 1997
; Suhayda and Goodman, 1981
; Wiebe et al., 1984
). Within leaves, the majority of xylem vessels ended near junctions, specifically the petiole–lamina (Wiebe et al., 1984
; Canny, 1997
) and the petiole–stem junction (Wiebe et al., 1984
; Tyree and Zimmermann, 2002
). In this organization, microorganisms would have to pass across pit membranes to leave the stem and move into a leaf blade.
To gain a better understanding of how xylem-dwelling pathogens travel throughout the plant, our primary objective was to determine the xylem pathways through which such pathogens might move unimpeded. The movement of the bacterium Yersinia enterocolitica (strain GY5232, engineered to emit light), fluorescent beads, and low-pressure air was followed to determine the xylem pathways. We will show long, branched xylem conduits that facilitate the rapid and passive movement of particles from stems into leaves in grapevine shoots.
MATERIALS AND METHODS
Well-watered 3-year-old Vitis vinifera cv. Chardonnay and Muscadinia rotundifolia cv. Cowart grapevines were grown in greenhouses in 7.9 liter plastic pots; the leaves and stems assayed in this study were from the current year's growth. Leaf and stem segments were generally taken between the 6th and 14th leaves basal to the shoot meristem and leaf blades ranged from 6 to 12 cm in width and height. Chardonnay leaves from 8-yr-old vineyard-grown vines in Napa, California were harvested in May 2004. Leaf and stem sampling occurred at the same time of day (1000 to 1100 hours). During this time, the relative humidity in the vineyard ranged from 40–70%, and photosynthetically active radiation (PAR) ranged from 1300 to 1800 µmol · m–2 · s–1.
Shoots were held under water, and three or four leaves were severed from the vines at the basal end of the petiole (Fig. 1A). Likewise, shoot segments having three attached leaves were severed underwater for bacterial and air movement experiments (Fig. 1B). In transferring leaves or stems from the water to bacterial or bead suspensions, a drop of water was left on the cut end. Cutting the leaves and stems underwater and retaining a water droplet on the cut surface minimized cavitation and the introduction of air emboli. In the bacteria and bead experiments, cut ends were not exposed to air at any point during the experiments. In the air-movement experiments, cut ends were exposed to air only as air was introduced into the stem or petiole.
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Bacterial movement
The psycrotrophic bacterium Yersinia enterocolitica (Ye) strain GY5232 engineered to express the lux operon was introduced into leaves by submerging either the cut end of the petiole or the cut end of the stem in a test tube of Ye GY5232 bacterial suspension. Leaves or stems with leaves were allowed to take up bacterial suspension under transpiring conditions for 0.5, 1, 2, 3, or 5 h. The same results were obtained for all times, so 2 h was used for convenience.
At the end of the time period, bacterial movement was evaluated in leaves containing Ye GY5232 by either removing leaves from the suspension or cutting the leaves from stems in the suspension at the base of the petioles (as indicated by the double lines in Fig. 1B), then exposing the leaves (petiole and leaf blade) to photosensitive x-ray film. Bacteria were detected by the light they produced due to expression of the lux operon. The luxCDBAE operon contains genes that encode proteins needed for the enzyme luciferase, synthesis of the luciferase substrate, and other relevant elements required for the bacterium to emit light de novo (Winson et al., 1998
). The leaf tissue was sufficiently transparent that the light emitted by the bacteria was easily detected by the photosensitive x-ray film. This resulted in images of the locations of Ye GY5232 inside the xylem vessels of the leaves (Fig. 3). Varying exposure times (0.25–24 h) to photosensitive film of the same leaves showed that no bacterial movement occurred after removal of leaves from bacterial suspension; therefore, a 16-h exposure time was used for convenience and to obtain the most easily visualized bacterial pathways.
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). This formed a transciptional fusion of flhB with the luxCDBAE operon. The resulting plasmid, designated pGY377, was transferred by electroporation (BioRad Gene Pulser) into Yersinia enterocolitica. This strain was designated GY5232. Ye was routinely cultivated in tryptone (1% ) yeast extract (0.5% ) (TYE) at 26°C. Prior to the start of each experiment, Ye strain GY5232 was grown overnight in TYE at 26°C and then subcultured at a 1:30 dilution and incubated another 2 h at 26°C to ensure high expression of flhB-lux CDBAE.
Bead movement
Leaves were removed from stems as stated, then transferred to vials of fluorescent polystyrene beads suspended in TYE at a concentration of 1.0 x 108 microspheres/mL (FluoSpheres polystyrene microspheres, 1.0 µm, blue-green fluorescent [430/465 nm], Molecular Probes, Eugene, Oregon, USA). Leaves were allowed to transpire under lighted conditions from several hours to overnight. Petioles and leaf veins were then freehand sectioned in transverse view and observed under violet light wavelengths with an Olympus Vanox-AHBT compound microscope (Olympus America, Melville, New York, USA), and digital images were captured with a Pixera (Los Gatos, California, USA) 600ES digital camera.
Air movement
Leaves or stems with three leaves were removed as stated previously. Filtered (with glass wool), pressurized air at a maximum of 80 kPa, which was low enough to avoid inducing cavitation in xylem vessels (Skene and Balodis, 1968
; Cohen et al., 2003
), was applied to the cut ends of petioles or stems. Leaves were placed under water and, starting at the leaf margins, incisions were made at 1 to 2 mm intervals in the leaf blade. With each incision, newly cut vein endings were examined with a dissecting microscope for signs of bubbles emerging from the veins. The first appearance of a stream of bubbles was evidence of an open xylem vessel, starting at the cut end of a petiole or stem and ending at the location of the cut. When low-pressure air is forced through xylem vessels of fresh tissue, air will only pass through open vessels because wet pit membranes will block air flow (Skene and Balodis, 1968
; Tyree and Zimmermann, 2002
; Cohen et al., 2003
). If vessels are already embolized, air will also be able to flow through those vessels, which could compromise the accuracy of continuous vessel length measurements. However, bacteria and beads cannot flow through embolized vessels. Because results from the three methods were uniform and all plant parts were detached under water, embolisms in vessels were highly unlikely to contribute or detract from the lengths of open, continuous vessels determined in this study.
Leaf clearing
Leaves were cleared using a NaOH and chloral hydrate method (Ruzin, 1999
). Dissected leaf tissue was soaked in 70% ethanol to remove pigment, then placed in water, treated with 5% NaOH for several days to remove all cell contents, and finally treated with a saturated chloral hydrate solution overnight. Leaves were then rinsed several times in water, stained with 0.1% safranin O, and dehydrated and permanently mounted on microscope slides with Permount and a cover glass. All material was examined with an Olympus Vanox-AHBT compound light microscope (Olympus America, Melville, New York, USA) with bright-field optics, and photographed with a Pixera (Los Gatos, USA) 600ES digital camera.
Statistical analysis
Analysis of variance (ANOVA) was used to test the significance of the main effects and corresponding interactions (SAS, SAS Institute, Cary, North Carolina, USA). Three replications of 15 plants were used for each treatment. In all cases, there was no statistical difference between methods or between cultivars. Where appropriate, means were compared by Fisher's LSD (least significant difference) at the P = 0.05 level.
RESULTS
Analysis of leaf clearings of Chardonnay and Cowart showed vascular bundle branches between lower order veins (1°, 2°, 3°; Roth-Nebelsick et al., 2001
) consisting of simple divergence of vessels (Fig. 2). Junctions between higher order veins (3° and quaternary) appeared to be mediated by irregular tracheary elements, possibly tracheids (Fig. 2B) (Esau, 1977
). Chardonnay and Cowart showed equivalent branching patterns and vascular structure. The branching from lower to higher order veins suggested the potential for continuous vessels to exist within in the leaf blade. However, simple anatomical examination of leaf vasculature did not show which veins had open vessels that could allow particles, such as bacteria, to move freely from lower to higher order veins or from organ to organ. Therefore, potential xylem pathways for passive particle movement were identified using bead, bacterial, and air flow movement experiments.
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Bacteria moved rapidly throughout the leaf blade, reaching a maximum distance in 0.5 h, the shortest time interval evaluated. After 5 h, more bacteria had moved into the leaf (judging by a stronger signal on photosensitive film exposed for the same length of time), but the distances the bacteria traveled within the leaf from the 0.5 h time to the 5 h time did not differ. Identical results were obtained in these tests with light-producing Escherichia coli (E.coli) (data not shown). Further, there were no overall differences between Chardonnay and Cowart leaves in the distribution of bacteria or in the distances the bacteria moved.
Low-pressure air moved through open xylem vessels from the base of the petiole up to 3° veins in both Chardonnay and Cowart leaves as determined by the first appearance of a stream of bubbles. Air moved into all five 1° leaf blade veins, most 2° veins, and generally followed the same pattern as the Ye GY5232 bacteria. In addition, leaves of Chardonnay grown in the field were equivalent to Chardonnay leaves of greenhouse vines (Fig. 4 and Table 1).
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Continuous, open vessels existed from the base of the petiole to all five primary veins based on air, bacterial and bead movement. The average distances that bacteria, beads, and air traveled through open, continuous vessels were similar, and ranged from 60 to 80% of the total length of the potential vascular path from petiole base to individual leaf blade vein endings (Table 1). The maximum distances reached by Ye GY5232, the fluorescent beads, and air were identical, as indicated by the white dashed line in Fig. 4.
Stem to leaf blade
Low pressure air and Ye GY5232 were loaded at the cut end of a stem segment with three leaves still attached. Similar to the petiole-to-leaf-blade loading experiments, there were continuous open vessels from the point of loading on stems, which resulted in rapid particle movement from the stem into all three leaves, apparently without crossing any pit membranes. Bacteria and air traveled from the cut stem into 1° and 2° leaf blade veins of at least three leaves above the bacteria or air source (refer to Fig. 1B), moving passively between multiple organs. Cowart differed somewhat in that no bacteria were observed in the 2° veins of the third leaves, and only one 2° vein in the third leaf had any air movement (Table 2); other than this, Chardonnay and Cowart were indistinguishable. No Ye GY5232 or air flow was observed in 3° veins of any of the leaves (first, second, or third) when air or bacteria were introduced through the stem. As one would expect, the length of open vessels running from the stem into 2° veins was longest in the third leaves above the stem cut. Although fewer bacteria reached the third leaf than the first or second, the movement within leaf blades was strikingly similar in all three leaves. The distribution patterns were comparable to those seen when air, bacteria, or beads were administered from the petiole base (Fig. 3).
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DISCUSSION
In this study, we show for the first time, using three complementary methods, that xylem conduits are present that facilitate the movement of bacteria-sized particles long distances unimpeded and passively through xylem vessels from stems and petioles to higher order veins in the lamina, in some instances covering a distance of over 30 cm. The long pathways and their incorporation of stems, petioles, and lamina suggest that these conduits may be comprised of single branched vessels, but may also include more than one vessel joined via damaged pit membranes.
Long-distance bacterial movement within grapevine stems has been reported before, but no previous study investigating pathogen or particle movement within the xylem system has reported evidence of the open conduits shown in this study. In Jonathan apple trees (Malus pumila), Erwinia amylovora labeled with 32P moved a total of 35 mm along the stem but not into leaves (Suhayda and Goodman, 1981
). After a second treatment with 32P-labeled E. amylovora, some bacteria were detected in the first petiole from the inoculation site (a total of 9 mm), but most of the labeled bacteria remained in the stem (Suhayda and Goodman, 1981
). Tarbah and Goodman (1987)
reported that the bacterium Agrobacterium tumefaciens moved up to 30 cm in 24 h in grapevine (Vitis vinifera) stem, but they did not follow the bacteria into leaves. Weibe et al. (1984) showed that India ink moved as much as 3 mm into the petiole from the stem in alfalfa (Medicago sativa), but not into the leaf lamina. Similarly, Canny (1997)
introduced latex particles to petioles and found latex in only three of over 600 vessels in sunflower leaf lamina (Helianthus annuus), and no latex particles were found beyond a few millimeters into the leaf lamina. These particle movement studies have led to the conclusion that xylem vessels end in groupings at junctions, e.g., the petiole–lamina junction (Canny, 1997
; Wiebe et al., 1984
).
Compant et al (2005) inoculated agar with Burkholderia spp. strain PsJN and then planted small tissue-cultured grape seedlings (~6 cm tall) on the agar. Using GFP- or GUS-tagged bacteria, they followed the movement of the bacteria onto the root surface, into the root tissues via small cracks in the root surface, and then into the xylem vessels. They observed that Burkholderia spp. was able to secrete cell-wall-digesting enzymes, suggesting that this may assist the bacteria in its passage into the root xylem. Compant et al. (2005)
then observed that the bacteria were present inside the xylem vessels of the fifth leaf within 96 h of inoculation. This observation is consistent with that of the current study by showing the rapid movement of a bacterium through the xylem vessels into a leaf blade. Compant et al. (2005)
used small plantlets instead of fully grown grape plants, so we would expect the xylem network in a plantlet to be considerably smaller, the xylem to be mostly primary xylem, and obviously the vessels appeared to be interconnected.
The open continuous xylem conduits observed in the current study are unlikely to be an artifact. Rupture of pit membranes due to air flow can be discounted, because we used very low pressures, and Choat et al. (2004)
showed that in Fraxinus americana L., pit membranes stretched but did not tear at pressures as high as 6 MPa. Enzymatic degradation of pit membranes can also be discounted. Of the three methods used in this study (bacteria, beads, and air flow), only Ye GY5232 had the potential to synthesize wall-degrading enzymes (there is no evidence that it does), yet the distances traveled from stem to petiole to leaf blade were equivalent for all three methods. Scanning electron micrographs suggest that naturally occurring, degraded pit membranes are present in several species (Carlquist and Schneider, 2004
). Ruptured pit membranes have been observed in grapevine xylem vessels (J. Stevenson, T. Rost, M. Matthews, and Q. Sun, unpublished data). However, more work needs to be done to document that the observed ruptured pit membranes existed before sample preparation.
Bacteria, beads, and air moved the same distance from the petiole into the leaf blade, delineated by the white line in Fig. 4, suggesting that beyond this point anatomical limitations of the xylem prevented further movement. One explanation for this is that increasingly narrow vessels with proximity to leaf margins prevented bead and Ye GY5232 movement. However, air movement would not have been inhibited because air would have been able to move through narrower vessels than bacteria or beads unless pit membranes were present to prevent air passage by imposing greater pressure requirements. Thus, the movement of Ye GY5232, beads, and air was most likely stopped by vessel ends with intact pit membranes.
The facility of travel within grapevine that open, continuous conduits allow has implications for the systemic spread of xylem-dwelling bacteria. For example, the systemic spread of Xylella fastidiosa increases Pierce's disease development and eventually results in plant death (Goodwin and Purcell, 1992
; Purcell and Hopkins, 1996
). The insect vector of Xylella fastidiosa (Xf), the sharpshooter, feeds on petioles, leaf blades, and stems of grapevine (Purcell, 1975
; Feil et al., 2003
). If sharpshooters feed on open, continuous vessels and infest the vine with X f, the bacteria can be rapidly and passively moved into nearby leaves. The extent of the rapid, passive movement of Ye GY5232 through xylem vessels and conduits seen in this study suggests that passive movement of bacteria could be a contributing mechanism for systemic movement of xylem-borne bacteria, such as Xfin grapevine.
FOOTNOTES
1 The authors thank Dr. K. A. Shackel for helpful discussion; N.-M. Nguyen, J. Chang, and C. DeBen for technical assistance; Monticello Vineyards, Napa, California for their cooperation; and Cal-Western Nurseries, Visalia, California, for their gift of Chardonnay grapevines. This work was funded by the California Department of Food and Agriculture, Agreement no. 01-0712, No. 03-8500-0503-GR and no. 04-0527 and USDA-CREES no. 2003-34442-13148, subaward SA6783. 
6 Current address: Department of Plant and Animal Sciences, Brigham Young University, Provo, UT 84602 USA
7 Current address: Department of Biology and Chemistry, Texas A&M International University, Laredo, TX 78041 USA
8 Author for correspondence (tlrost{at}ucdavis.edu
)
LITERATURE CITED
Aloni R.. 2005. The induction of vascular tissue by auxin. In P. Davies [ed.] Plant hormones: biosynthesis, signal transduction, action! Springer, New York, New York, USA.
Bové J. M. Garnier M.. 2002. Phloem- and xylem-restricted plant pathogenic bacteria. Plant Science 163: 1083-1098.[CrossRef][Web of Science]
Canny M. J.. 1997. Vessel contents of leaves after excision: a test of Scholander's assumption. American Journal of Botany 84: 1217-1222.[Abstract]
Carlquist S. Schneider E. L.. 2004. Pit membrane remnants in perforation plates of Hydrangeales with comments on pit membrane remnant occurrence, physiological significance and phylogenetic distribution in dicotyledons. Botanical Journal of the Linnean Society 146: 41-51.[CrossRef]
Choat B. Jansen S. Zwieniecki M. A. Smets E. Holbrook N. M.. 2004. Changes in pit membrane porosity due to deflection and stretching: the role of vestured pits. Journal of Experimental Botany 55: 1569-1575.
Choat B. Lahr E. Melcher P. J. Zwieniecki M. A. Holbrook N. M.. 2005. The spatial pattern of air seeding thresholds in mature sugar maple trees. Plant, Cell & Environment 28: 1082-1089.[CrossRef]
Cohen S. Bennink J. Tyree M.. 2003. Air method measurements of apple vessel length distributions with improved apparatus and theory. Journal of Experimental Botany 54: 1889-1897.
Compant S. Reiter B. Sessitsch A. Nowak J. Clément C. Ait Barka E.. 2005. Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Applied and Environmental Microbiology 71: 1685-1693.
Esau K.. 1965a. Plant anatomy, 2nd ed Wiley, New York, New York, USA.
Esau K.. 1965b. Vascular differentiation in plants Holt, Rinehart and Winston, New York, New York, USA.
Esau K.. 1977. Anatomy of seed plants, 2nd ed Wiley, New York, New York, USA.
Ewers F. W. Fisher J. B.. 1989a. Techniques for measuring vessel lengths and diameters in stems of woody plants. American Journal of Botany 76: 645-656.[CrossRef][Web of Science]
Ewers F. W. Fisher J. B.. 1989b. Variation in vessel length and diameter in stems of six tropical and subtropical lianas. American Journal of Botany 76: 1452-1459.[CrossRef][Web of Science]
Feil H. Feil W. S. Purcell A. H.. 2003. Effects of date of inoculation on the within-plant movement of Xylella fastidiosa and persistence of Pierce's disease within field grapevines. Phytopathology 93: 244-251.[CrossRef][Web of Science][Medline]
Fosket D. E.. 1994. Plant growth and development: a molecular approach Academic Press, San Diego, California, USA.
Goodwin P. H. Purcell A. H.. 1992. Pierce's disease. In D. H. Flaherty, L.P. Christensen, W. T. Lanini, J. J. Marois, P. A. Phillips, L. T. Wilson [eds.] Grape pest management, 2nd ed 76-84 University of California, Division of Agriculture and Natural Resources, Oakland, California, USA.
Howard R. A.. 1974. The stem-node-leaf continuum of the Dicotyledonae. Journal of the Arnold Arboretum 55: 125-181.
Purcell A. H.. 1975. Role of the blue-green sharpshooter, Hordnia circellata, in the epidemiology of Pierce's disease of grapevines. Environmental Entomology 4: 745-752.[Web of Science]
Purcell A. H. Hopkins D. L.. 1996. Fastidious xylem-limited bacterial plant pathogens. Annual Review of Phytopathology 34: 131-151.[CrossRef][Web of Science][Medline]
Roth-Nebelsick A. Uhl D. Mosbrugger V. Kerp H.. 2001. Evolution and function of leaf venation architecture: a review. Annals of Botany 87: 553-566.
Rouschal E.. 1940. Fluoreszenzoptische Messungen der Geschwindigkeit des Transpirations-stromes an krautigen Pflanzen mit Berücksichtigung der Blattspurleitflächen. Flora 134: 229-256.
Ruzin S. E.. 1999. Plant microtechnique and microscopy Oxford University Press, New York, New York, USA.
Sachs T.. 1969. Polarity and the induction of organized vascular tissues. Annals of Botany 33: 263-275.
Sachs T.. 1981. The control of patterned differentiation of vascular tissue. Advances in Botanical Research 9: 151-262.[CrossRef]
Skene D. S. Balodis V.. 1968. A study of vessel length on Eucalyptus oblique L'herit. Journal of Experimental Botany 19: 825-830.
Suhayda C. G. Goodman R. N.. 1981. Infection courts and systemic movement of 32P-labeled Erwinia amylovora in apple petioles and stems. Phytopathology 71: 656-660.[Web of Science]
Tarbah F. Goodman R. N.. 1987. Systemic spread of Agrobacterium tumefaciens biovar 3 in the vascular system of grapes. Phytopathology 77: 915-920.[CrossRef][Web of Science]
Tyree M. T. Zimmermann M. H.. 2002. Xylem structure and the ascent of sap, 2nd ed. Springer-Verlag, New York, New York, USA.
Wiebe H. H. Greer R. L. Van Alfen N. K.. 1984. Frequency and grouping of vessel endings in alfalfa (Medicago sativa) shoots. New Phytologist 97: 583-590.[CrossRef][Web of Science]
Winson M. K. Swift S. Fish L. Throup J. P. Jørgensen F. Chhabra S. R. Bycroft B. W. Williams P. Stewart G. S. A. B.. 1998. Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiology Letters 163: 85-192.[CrossRef][Web of Science][Medline]
Zimmermann M. H.. 1983. Xylem structure and the ascent of sap Springer-Verlag, New York, New York USA.
Zwieniecki M. A. Melcher P. J. Boyce C. K. Sack L. Holbrook N. M.. 2002. Hydraulic architecture of leaf venation in Laurus nobilis L. Plant, Cell & Environment 25: 1445-1450.[CrossRef]
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