Interactive signal transfer between host and pathogen during successful infection of barley leaves by Blumeria graminis and Bipolaris sorokiniana

• Published in: Journal of plant physiology 2008-01, Vol.165 (1), p.52-59
• Main Authors: Felle, Hubert H., Herrmann, Almut, Schäfer, Patrick, Hückelhoven, Ralph, Kogel, Karl-Heinz
• Format: Article
• Language: English
• Subjects: apoplastic fluids; Apoplastic pH; apoplasts; Barley; biochemical pathways; Bipolaris sorokiniana; Blumeria graminis; Cell Membrane - microbiology; Cell Membrane - physiology; Cell Membrane - radiation effects; cell membranes; Cochliobolus sativus; Compatibility; cytoplasm; disease resistance; electrolytes; Electrolytes - metabolism; electrophysiology; Erysiphe graminis; Erysiphe graminis f. sp. hordei; extracellular fluids; fungal diseases of plants; Fungi - physiology; Hordeum - microbiology; Hordeum vulgare; host plants; Host-Pathogen Interactions; host-pathogen relationships; Hydrogen-Ion Concentration; hyphae; infection; ion transport; Kinetics; Light; membrane potential; Membrane Potentials - radiation effects; Plant Diseases - microbiology; Plant Leaves - cytology; Plant Leaves - microbiology; Plant Leaves - physiology; plant pathogenic fungi; powdery mildew; Resistance; resistance mechanisms; signal transduction; Signal Transduction - physiology; stomata; Surface pH
• ISSN: 0176-1617; 1618-1328
• DOI: 10.1016/j.jplph.2007.08.006

Using ion-selective microprobes, interactive signalling between barley and Blumeria graminis or Bipolaris sorokiniana has been investigated. The question was raised whether a biotrophically growing fungus manipulates the electrical driving forces (membrane potential, transmembrane pH), required for H + cotransport of energy-rich compounds. Electrodes were positioned in the substomatal cavity of open stomata or on the leaf surface, and pH was measured continuously up to several days during fungal development. We demonstrate that surface and apoplastic fluids are electrically coupled and respond in a similar manner to stimuli. Apoplastic pH, monitored from the moment of inoculation with conidia, reveals several phases: 2–4 h after inoculation of the barley leaf with either fungus, the host displays rapid transient responses after its first contact with the fungal cell wall; apoplastic pH and pCa increases, cytoplasmic pH and pCa decreases. About 1 day after inoculation, the apoplastic pH increases by up to 2 pH units, which is thought to reflect a resistance response against the intruder. Whereas barley leaf cells possess a membrane potential of −152±5 mV, hyphae of B. graminis yield −251±8 mV, indicative of a substantial driving force advantage for the fungus. Although the resting membrane potential of barley remains constant during the first days after inoculation, leaves infected with B. sorokiniana get confronted with an energy problem, indicated by a retarded repolarization following a “light-off” stimulus. Five days after inoculation, apoplastic pH has increased to 5.97±0.47 ( n=11) and does no longer respond to “light-off” when measured within lesions. In contrast, it stays at near normal values outside the lesions and responds to “light-off”. It is concluded that biotrophically growing fungi do not manipulate the cotransport driving forces since (i) any change in apoplastic pH would be experienced by both partners; (ii) the resting membrane potential is not changed. It is suggested that measured pH changes reflect defence responses of the host against the fungus rather than fungal action to increase compatibility.