Water Channels and Water Congestion

Free water in surface apertures such as stomata constitutes a "water channel'' that connects a plant's apoplast with its external environment. Microorganisms can internalize through water channels in various ways. Additionally, persistent congestion of the apoplast by water may restrict oxygen availability, which could compromise the resistance of the cells to microbial attack [1,13,14]. Burton [20] noted that cells in respiring plant tissues become anaerobic if water congestion blocked them from direct contact with air in intercellular spaces. Tissues in a potato tuber covered with a film of water and stored at 20°C become anaerobic within 2.5 hours [39]. Wet tubers are susceptible to bacterial soft rot [40]. The loss of natural resistance to the disease associated with tissue anaerobiosis occurs relatively quickly. Bartz and Kelman [41] reported that freshly harvested and then washed tubers developed soft rot during subsequent storage at 20°C if their surfaces remained wet for 20 hours, whereas if the tuber surfaces dried within 16 hours the disease did not develop.

Water channels in leaf tissues have been associated with a large-scale internalization of plant pathogenic bacteria. Massive wildfire and blackfire lesions developed on field-grown tobacco only if leaf tissues were water congested at the time the plants were exposed to inoculum [36,42]. In the absence of water congestion, lesions tended to be small and of little consequence. By contrast, in the absence of inoculum (disease absent from the field), water-congested leaves recovered from a water-soaked appearance without evidence of necrosis or other damage.

Experimentally, water-soaked areas on leaf surfaces were correlated with rapid internalization of bacteria [36,42,43-46]. Leaves of various plant species were water-soaked by applying water under pressure to the root system or cut surface of petioles [42,43] or as a water stream from a syringe or sprayer [36,45,46]. Bacteria misted or poured on such surfaces were rapidly internalized as were the carbon particles in India ink, solutions of water-soluble dye, and suspensions of plant viruses. In the absence of water congestion, a similar application of aqueous cell suspensions or India ink led to little or no evidence of internalization. Cocci of Staphylococcus aureus penetrated rapidly into water-congested leaf tissues providing clear evidence that internalized bacteria need not be motile [46] or from a plant-associated ecological niche. Johnson [43] concluded that bacterial suspensions were pulled into water-congested tissues by capillary forces, which is inconsistent with the concept that intercellular spaces are bounded with hydrophobic surfaces [17]. Even with established water channels, however, water does not totally flood intercellular spaces on submerged or partially submerged leaves. Partially flooded intercellular spaces should function like closed capillary tubes. Water would enter until pressure on trapped air balanced the capillary forces. Thus, aqueous suspensions or solutions could penetrate quickly through water channels but would move only a few cell layers due to a developing back pressure.

The guttation of water through hydathodes creates water channels where bacteria and similarly sized microbes can passively internalize in plant leaves [26]. Under normal conditions, guttation disappears when leaves begin to transpire. Curtis [26] concluded that most guttation droplets are sucked back into the leaf at this time. The drying of guttation moisture may concentrate solutes such that certain ones may damage the leaf surface. Mechanical movement of guttation moisture back into hydathodes could passively internalize bacteria and any other particulates that are small enough to pass through the pore.

Mild water congestion of leaf tissues, which would not be visible as water soaking also appears to enhance microbial internalisation [25]. For example, preinoculation incubation of plants under high humidity leads to more disease than postinoculation incubation [45,47]. Citrus leaves become infected by Xanthomonas citri only if the substomatal chambers are filled with water [48]. This level of water congestion would not be visible to the unaided eye. A bacterial disease of cucumber, angular leaf spot, progressed most rapidly when the soil was warm and contained high moisture despite daytime air temperatures that inhibited pathogen development [50]. It is precisely this type of environment that favors guttation.

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