Structures That Enable Internalization

Naturally occurring surface apertures and wounds are keys to the internalization of microbes. Two apertures, stomata and lenticels, function in gas exchange, whereas hydathodes provide relief of excessive internal water pressures. Stomata occur in the epidermis of all above-ground parts of plants. Specialized stomata function as nectaries (secrete nectar) in certain types of flowers [1]. Stomata are apertures in the plant's epidermis that are created by two specialized cells called guard cells. The turgor of the guard cells changes with exposure to sunlight, darkness, or moisture stress [21]. The guard cells swell during daylight opening the pore, and shrink during darkness or with water stress, closing the pore. Epidermal cells adjacent to the guard cells may grow under the stoma forming a substomatal chamber [18]. Schonherr and Bukovac [22] suggested that stomata be viewed as narrow capillaries having inclined walls.

Lenticels are specialized portions of a periderm, which is an impervious secondary surface layer that replaces the epidermis or forms on the surfaces of wounds [18]. The periderm is composed of a phellogen (cambium), phellum (corky cells), and phelloderm (resembles parenchyma cells formed inside the phellogen). A lenticel is similar in organization to the surrounding periderm, except that the lenticel phellogen is more active and contains intercellular spaces [1,18]. It produces a phellum that is loosely organized with many intercellular spaces. Thus, gases readily diffuse through lenticels into the underlying tissues of the plant organ. Phellum cells in lenticels may or may not be suberized (cell walls infiltrated with and coated by a polymeric organic chemical complex that is a barrier to moisture diffusion) [15], whereas the phellum of the regular periderm is nearly always suberized.

Lenticel-like structures may form on certain types of fruit [18]. In certain types of apple fruit, a periderm-like structure forms under stomata but a phellogen is usually absent. Certain types of melons crack as they approach maturity. Living cells beneath the crack develop into a phellogen that produces the characteristic net common to cantaloupes and certain other fruit. The net resembles a lenticel in structure. Certain lenticels respond to changes in the environment around them. For example, cells in lenticels on potato tubers proliferate when the soil becomes moist [23,24]. These proliferated cells are thin-walled, surrounded by large intercellular spaces, and highly susceptible to microbial attack.

Hydathodes, apparently designed to release excessive water pressure in the plant, vary in complexity among different plant species but all provide a connection between the water-conducting elements and the external environment [18]. Certain ones resemble stomata except for not closing during darkness. Others are specialized for water release and may be better termed "water glands.'' Gas exchange could occur through hydathodes that are not water congested. Water congestion develops in above-ground tissues of plants when the roots absorb water more rapidly than above-ground parts lose it to evapotranspiration [25]. The excess water can pool under the epidermis causing edemas or, more often, water moves from the ends of the vascular strands through the leaf mesophyll and then into and out of hyda-thodes in a process called guttation [21]. Guttation droplets, which are derived from xylem sap, appear on the edges of leaves and are often confused with dew. However, guttation may occur at any time of the day, particularly if the soil is moist, plants are growing rapidly, and evapotranspiration is low [26]. Lawn grasses and corn have been observed to excrete water in bright sunlight. Guttation may be part of a natural detoxification method in certain plants, particularly when rainfall, fog, or dew cause the droplets to fall from the plant surface [17].

Fruit attachment structures on certain plants contain natural openings involved with gas exchange. Most of the gas exchange required by the internal cells of tomato fruit occurs through the stem scar [27]. If the stem scar is covered with wax, the carbon dioxide levels in the intercellular spaces increase two to four times above normal, evidence that the wax layer blocks equilibration of respiratory CO2 with the external environment. If the rest of the fruit is waxed and the stem scar is not, the CO2 level in the fruit remains similar to that in nonwaxed fruit. Air injected into a tomato fruit submerged in water bubbles from cracks in the edges of the stem scar [28]. Only rarely are any bubbles observed at the blossom end of the fruit. If the stem is still attached, the air bubbles from the area between the stem and fruit.

Wounds also connect a plant's intercellular air-space network with the surrounding environment. Wounds can arise from various biotic and abiotic factors including insects, storms, wind-blown particles, harvest crews, etc. Excessive water uptake or even normal growth may produce cracks in the surface of plant organs. Trichomes, defined as outgrowths of the epidermis [18], are easily damaged and are a frequent site for infection by plant pathogenic bacteria and growth of epiphytes [9]. Whether broken trichomes enable the internalization of resident or casual microbes is unclear. The porosity of wounds to gases and moisture often changes over time due to healing processes involving the formation of closing layers such as a periderm, or suberization and lignification of cell layers [15]. These changes usually quickly restore the wound to an imperviousness to water loss and penetration by particulate matter similar that of the intact surface layers [18].

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