The Developmental Anatomy of Pierce's Disease Symptoms in Grapevines: Green Islands and Matchsticks
Stevenson, J. F., Matthews, M. A., and Rost, T. L.
Symptoms of Pierce's disease were studied in an anatomical context from infected vines collected from field sites within Napa Valley , CA . Two symptoms, green islands and matchsticks are reported in this study. Green islands formed as a result of incomplete initiation of the phellogen. In regions of the stem where a phellogen and subsequent periderm arose, immediately exterior tissue was cut off, causing it to brown. In regions of the stem where no periderm is formed, the exterior tissues remained green. Consequently, the stem is mottled with both green living epidermis and brown dying epidermis as determined by the presence or absence of an underlying periderm. Matchsticks formed when the leaf lamina separated from the petiole, and the petiole remained attached to the stem. Lamina broke off from the petioles consistently in a fracture zone where xylem from the petiole anastomoses into the five major veins of the leaf. No separation layer was found to explain this pseudoabscission.
Plant Disease (2005) 89: 543-548
Pierce’s Disease Symptoms: Comparison with Symptoms of Water Deficit and the Impact of Water Deficits
Thorne, E.T. Stevenson, J.F., Rost, T.L., Labavitch, J.M., Matthews, M.A.
The pathology of diseases such as Pierce’s disease (PD) of grapevine (Vitis vinifera L.) that are caused by the xylem-limited bacterium Xylella fastidiosa (Xf) is widely attributed to vessel occlusion and subsequent water deficits. Grapevines (Vitis vinifera L. ‘Chardonnay’) were exposed to water deficits, stem inoculation with Xf, and combinations of both to evaluate whether symptoms of PD were a consequence of water deficits. When vines were inoculated with Xf and exposed to water deficits, more extensive PD symptoms developed throughout the plant than when infected vines were well-watered. However, vines infected with Xf exhibited symptoms unique to PD that included inhibited periderm development in stems (green islands), leaf blade separation from the petiole (matchsticks), and irregular leaf scorch. Vines exposed to water deficits and not Xf, displayed accelerated periderm development, basal leaf abscission at the stem/petiole junction, and uniform leaf chlorosis. Water deficits induced the development of an abscission zone at the stem/petiole junction, but PD did not. Pierce’s disease symptoms could not be produced with any of several water deficit treatments, including severing all but one secondary vein near the leaf tip. The results indicate that factors other than water deficits are involved producing the symptoms of PD. We conclude that the widely accepted hypothesis that PD-infected plants develop water deficits that cause green islands, matchsticks, localized leaf scorch, and eventual death of vines should be reevaluated.
American Journal of Enology and Viticulture (In Press)
The structure of xylem vessels in grapevine (Vitaceae) and a possible passive mechanism for the systemic spread of bacterial disease
Thorne, E.T., Young, B.M., Young, G.M., Stevenson, J.F., Labavitch, J.M., Matthews, M.A.,and Rost, T.L..
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 were studied. Three methods were used: (1)light-producing
bacteria, Yersinia enterocolitica, (Ye) strain GY5232 were 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 the extrusion of 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.
American Journal of Botany (In Press)
Chatelet, D.S., Matthews, M.A., and Rost, T.L.
Background and Aims: Bacterial leaf scorch occurring in a number of economically important plants is caused by the xylem-limited bacterium Xylella fastidiosa (Xf). In grapevine, Xf infection causes Pierce’s disease (PD) and is lethal when the bacteria become systemic. Traditional dogma is that Xf movement between vessels requires the digestion of intervessel pit membranes. However, Yersinia enterocolitica (Ye) and fluorescent beads have been observed to move rapidly within grapevine xylem from stem into leaf lamina, suggesting open conduits consisting of long branched xylem vessels for passive movement.
Methods: Air, latex paint and GFP-Xf were loaded into leaves and followed to confirm such pathways. Leaf xylem anatomy was studied to determine the basis for the free and sometimes restricted movement of Ye, beads, air, paint and GFP-Xf into the lamina.
Key Results: Reverse loading experiments demonstrated that the long branched xylem vessels observed were an exclusive property of the primary xylem. They were observed in the stem for three internodes before diverging into mature leaves. However this stem-leaf connection was and age-dependent character and was absent for young leaves apical to internodes 10-12. Free movement in leaf blade xylem was cell type specific with vessels facilitating movement in the body of the blade and tracheids being found near the leaf margin. Air, latex paint and GFP-Xf all moved about 50-60% of the leaf length. GFP-Xf was never observed close to the leaf margin.
Conclusions: The open vessels of the primary xylem offered unimpeded long distance pathways bridging stem to leaves without interruption, possibly facilitating the spread of bacterial pathogen in planta. GFP-Xf never reached the leaf margins where scorching appeared, suggesting a signal targeting specific cells.
Annals of Botany (Submitted)
Pruning-induced tylose development in stems of current-year shoots of Vitis vinifera cv. Chardonnay (Vitaceae).
Sun, Q., Rost, T.L., and Matthews, M.A.
Tyloses form in xylem vessels in response to various environmental stimuli, but little is known of the kinetics or regulation of tylose development in any system. Preliminary investigations indicated that wounds sealed quickly with tyloses after pruning grapevine shoots. Therefore, xylem structure and pruning-induced tylose development was investigated in three stem regions (basal, middle and apical) of current-year shoots of grapevines. The three stem regions showed a similar xylem structure; however, the apical region, compared to the other regions, had a smaller value in vessel element length, fiber length and ratio of xylem width and stem diameter but a greater value in vessel density. Axial parenchyma cells contributed predominantly to tylose development through half-bordered pits with vessels in the three regions. Tylose development occurred simultaneously within a single vessel but much separated in time among vessels. Qualitative and quantitative analyses of tylose development in current-year shoots of grapevines were made at different depths and times from pruning cuts at three positions along current-year shoots. The fraction of vessels forming tyloses was greatest in basal (86 %) and least in apical (53 %) stem regions. The maximum density of tyloses was 4 mm in the basal stem region or 2 mm in the middle and apical stem region from the cut. Tylose development was faster in the basal and middle than in the apical stem region. The results show that pruning caused prodigious tylosis in vessels of grape stems that extended approximately 1 cm and 7 days from the wound, but that about half of the vessels did not become completely occluded. The pattern of tylose development suggests tylosis is too slow to prevent movement of mobile pathogens.
American Journal of Botany (Submitted)
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