The Touch Of Phytophthora

July 14, 1998

Researchers at the Max Planck Institute for Plant Breeding Research (MPIZ), Cologne, report on the role of physical pressure exerted by an invading fungus. This pressure serves as a signal to trigger plant defense responses (PNAS Vol. 95, No 14, 7 July 1998).

Plants serve as food not only for animals and insects, but also for a variety of microbes. That's why microbes, such as bacteria, nematodes, and fungi constantly attack plants. To protect themselves from being devour plants have developed broad-acting defense mechanisms. To identify such threats, plants must be able to perceive signals from a large variety of potential pathogens to trigger this general "nonhost" resistance. In recent years, a set of biological signal molecules (referred to as elicitors) from different pathogens, have been identified and characterized with respect to the defense responses induced in plant cells. Basic knowledge of plant-defense mechanisms can help to improve crop plants so that they will be better protected against pathogens.

Scientists in the MPIZ Department of Biochemistry, headed by Klaus Hahlbrock, use cell-suspension cultures of parsley (Petroselinum crispum) as a system for studying the nonhost resistance responses to Phytophthora sojae and Phytophthora infestans, two important fungal pathogens. Recently, coworkers of this department purified a glycoprotein from the mycelium cell wall of P. sojae that was shown to act as an elicitor in this nonhost system. Incubation of parsley cells with the elicitor resulted in dramatic biochemical changes in the affected plant cells, e.g., the generation of reactive oxygen intermediates (ROI), increased ion fluxes across the plasma membrane, and changes in gene activity. Researchers observed the same processes upon infecting parsley cells with P. infestans.

However, these changes to the physiological status of the cells do not reflect the entirety of defense responses induced by fungal infection. Morphological changes in infected cells can also be observed. At very early stages of the infection process, before the fungal hypha (a thin tube formed by the fungus to grow and to invade plant material) has completely penetrated the cell wall and formed intracellular structures, increased motion of cell contents (cytoplasm) towards the penetration site can be detected in plant cells, with the nucleus moving towards this site. The cell deposits cell-wall material beneath the penetration site as a physical barrier against penetration. If all these defense reactions are not sufficient to prevent further penetration of the fungus, the plant cell commits suicide, a process known as hypersensitive cell death. This can be observed under the microscope as a rapid and sudden collapse of the cell contents around the intracellular fungal structure. Furthermore, the plant cell releases toxic compounds that possibly kill both the plant cell and the fungus. However, in the parsley/P. infestans system, morphological changes have never been observed when the cells are treated with the elicitor molecule alone.

The question therefore arises as to whether additional signals other than the elicitor are required to induce of the complete defense response. The scientists speculated that attempted penetration by the pathogen generates not only chemical signals represented by the elicitor, but also mechanical signals resulting from the contact of the fungal hypha to the plant cell wall and that a combination of both these signals must be perceived by the plant cell for it to display the full complement of defense reactions.

Dr. Sabine Gus-Mayer, a postdoctoral fellow of the Deutsche Forschungsgemeinschaft at the MPIZ, tested this hypothesis. In her study, she replaced the penetrating fungus with gentle local mechanical stimulation of the cells using a tungsten needle of the same diameter as a fungal hypha (2-5 μm). As with the fungal infection hypha, by itself this local mechanical stimulus induced the translocation of cytoplasm and nucleus to the site of stimulation. Interestingly, some of the biochemical defense responses were also observed. Only a few minutes of local mechanical stimulation were required to induce the intracellular generation of ROI (see figure), in the same way as was previously demonstrated to occur by fungal infection or elicitor treatment. Surprisingly, some, but not all, elicitor-responsive plant genes were expressed upon mechanical stimulation.

These results provide evidence, that a fungal hypha need not necessarily penetrate a cell to trigger the plant's defense machinery. The physical touch exerted by an invading fungus is already sufficient to be sensed by the plant cell as a signal to instigate its own defense response. Concerning the signaling involved in the nonhost resistance response of parsley to P. sojae or P. infestans , these results lead to the following conclusions. At an initial stage of attempted fungal colonization, probably prior to penetration of the plant cell wall, the perception of a local mechanical signal from the emerging infection tube is sufficient to induce the generation of ROI, cytoplasmic rearrangements, and the expression of some infection-related genes. To trigger local cell-wall thickening, the fungal infection tube may have to penetrate the plant cell wall. As soon as the fungal infection tube is in contact the plasma membrane of the plant cell, the elicitor binds to its specific plant cell receptor, thereby activating additional biochemical defense reactions.

Thus, the combination of physical and chemical stimuli are likely to be responsible for triggering intracellular rearrangements as well as the various biochemical changes involved in gene activation and product accumulation. However, other signals are apparently required for induction of cell-wall thickening and the hypersensitive cell death.

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Max-Planck-Gesellschaft

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