Effect of downy mildew development on transpiration of cucumber leaves visualized by digital infrared thermography.

ABSTRACT Disease progress of downy mildew on cucumber leaves, caused by the obligate biotrophic pathogen Pseudoperonospora cubensis, was shown to be associated with various changes in transpiration depending on the stage of pathogenesis. Spatial and temporal changes in the transpiration rate of infected and noninfected cucumber leaves were visualized by digital infrared thermography in combination with measurements of gas exchange as well as microscopic observations of pathogen growth within plant tissue and stomatal aperture during pathogenesis. Transpiration of cucumber leaf tissue was correlated to leaf temperature in a negative linear manner (r = -0.762, P < 0.001, n = 18). Leaf areas colonized by Pseudoperonospora cubensis exhibited a presymptomatic decrease in leaf tem perature up to 0.8 degrees C lower than noninfected tissue due to abnormal stomata opening. The appearance of chlorosis was associated with a cooling effect caused by the loss of integrity of cell membranes leading to a larger amount of apoplastic water in infected tissue. Increased water loss from damaged cells and the inability of infected plant tissue to regulate stomatal opening promoted cell death and desiccation of dying tissue. Ultimately, the lack of natural cooling from necrotic tissue was associated with an increase in leaf temperature. These changes in leaf temperature during downy mildew development resulted in a considerable heterogeneity in temperature distribution of infected leaves. The maximum temperature difference within a thermogram of cucumber leaves allowed the discrimination between healthy and infected leaves before visible symptoms appeared.

[1]  P. Ayres,et al.  Increased transpiration and the accumulation of root absorbed 86Rb in barley leaves infected by Rhynchosporium secalis (leaf blotch) , 1975 .

[2]  O. Majerník A Physiological Study of the Effects of SO2 Pollution, Phenylmercuric Acetate Sprays, and Parasitic Infection on Stomatal Behaviour and Ageing in Barley , 1971 .

[3]  R. Hückelhoven,et al.  Apoplastic pH signaling in barley leaves attacked by the powdery mildew fungus Blumeria graminis f. sp. hordei. , 2004, Molecular plant-microbe interactions : MPMI.

[4]  R D Jackson,et al.  Remote Detection of Biological Stresses in Plants with Infrared Thermometry , 1979, Science.

[5]  M. Karnovsky,et al.  A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron-microscopy , 1965 .

[6]  A. Ellingboe,et al.  Reduction of transpiration from wheat caused by germinating conidia of Erysiphe graminis f. sp. tritici , 1975 .

[7]  M. Wren,et al.  Effects of infection by Phytophthora injestans (Mont.) de Bary on the stomata of potato leaves , 1969 .

[8]  D. Straeten,et al.  Seeing is believing: imaging techniques to monitor plant health. , 2001, Biochimica et biophysica acta.

[9]  E Marre,et al.  Fusicoccin: A Tool in Plant Physiology , 1979 .

[10]  P. Ayres Patterns of Stomatal Behaviour, Transpiration, and CO2 Exchange in Pea Following Infection by Powdery Mildew (Erysiphe pisi) , 1976 .

[11]  S. Merlot,et al.  Use of infrared thermal imaging to isolate Arabidopsis mutants defective in stomatal regulation. , 2002, The Plant journal : for cell and molecular biology.

[12]  Donald L. Hopkins,et al.  Compendium of Cucurbit Diseases , 1996 .

[13]  J. M. Duniway Detrimental effect of rust infection on the water relations of bean. , 1971, Plant physiology.

[14]  Lilian Amorim,et al.  Gas Exchange and Emission of Chlorophyll Fluorescence during the Monocycle of Rust, Angular Leaf Spot and Anthracnose on Bean Leaves as a Function of their Trophic Characteristics , 2002 .

[15]  I. Cruickshank,et al.  Peronospora Tabacina In Tobacco: Transpiration, Growth, and Related Energy Considerations , 1961 .

[16]  K. McDonald,et al.  Evidence for a transmissible factor that causes rapid stomatal closure in soybean at sites adjacent to and remote from hypersensitive cell death induced by Phytophthora sojae , 1999 .

[17]  D. Straeten,et al.  Imaging techniques and the early detection of plant stress. , 2000, Trends in plant science.

[18]  Richard W. Michelmore,et al.  The Downy Mildews , 1988 .

[19]  M. Montagu,et al.  Presymptomatic visualization of plant–virus interactions by thermography , 1999, Nature Biotechnology.

[20]  D. Spencer,et al.  The Downy mildews , 1982 .

[21]  A. Boccara,et al.  Infra-red thermography revealed a role for mitochondria in pre-symptomatic cooling during harpin-induced hypersensitive response. , 2002, The Plant journal : for cell and molecular biology.

[22]  R. Jackson Remote sensing of biotic and abiotic plant stress , 1986 .

[23]  F. J. Schwinn,et al.  The downy mildews - an overview of recent research progress. , 1994 .

[24]  Yoshio Inoue,et al.  Remote estimation of leaf transpiration rate and stomatal resistance based on infrared thermometry , 1990 .

[25]  Z. Kiraly,et al.  The Biochemistry and Physiology of Plant Disease , 1986 .

[26]  Y. Cohen The Effect of Darkness and Moisture on Sporulation of Pseudoperonospora cubensis in Cucumbers , 1971 .

[27]  D. D. Giorgio,et al.  Syringopeptins, Pseudomonas syringae pv. syringae phytotoxins, resemble syringomycin in closing stomata , 1996 .

[28]  R. G. Smith,et al.  Effect of stripe rust (puccinia striiformis west.) and irrigation on the yield and foliage temperature of wheat , 1986 .

[29]  C. B. Tanner,et al.  Infrared Thermometry of Vegetation1 , 1966 .

[30]  J. Lucas,et al.  Plant pathology and plant pathogens , 1986 .

[31]  Manfred Stoll,et al.  Use of infrared thermography for monitoring stomatal closure in the field: application to grapevine. , 2002, Journal of experimental botany.

[32]  D. Knoppik,et al.  Effects of the cherry leaf spot pathogenBlumeriella jaapiion gas exchange before and after expression of symptoms on cherry leaves , 1997 .

[33]  Y. Cohen,et al.  The effect of humidity during darkness on the transfer of assimilates from cucumber leaves to sporangia of Pseudoperonospora cubensis , 1972 .

[34]  S. Lindow,et al.  Observations of Ice Nucleation and Propagation in Plants Using Infrared Video Thermography , 1997, Plant physiology.

[35]  D. Van Der Straeten,et al.  Thermographic visualization of cell death in tobacco and Arabidopsis , 2001 .

[36]  Y. Cohen The combined effects of temperature, leaf wetness, and inoculum concentration on infection of cucumbers with Pseudoperonospora cubensis. , 1977 .

[37]  H. Nilsson Remote sensing and image analysis in plant pathology. , 1995, Annual review of phytopathology.

[38]  Hamlyn G. Jones,et al.  Use of thermography for quantitative studies of spatial and temporal variation of stomatal conductance over leaf surfaces , 1999 .