Abstract
Late wilt (causal agent Harpophora maydis), with initial symptoms appearing around flowering, has become frequent in maize fields of the Iberian Peninsula. The geographical distribution of the pathogen in the main maize - growing areas in the South of Portugal and Spain was determined by prospecting 59 fields from 2009 to 2013. Among all the isolates of H. maydis identified, 14 isolates were molecularly confirmed by ITS amplification, and their pathogenic traits (i.e. aggressiveness) were analyzed by inoculation of the maize susceptible cultivar PR32W86 grown in pots under shade-house conditions for the whole growing season. One of the isolates was highly aggressive, causing intense symptoms as well as significant reductions in weight of both aboveground parts and roots. Moderately aggressive isolates caused significantly high disease values but not all of them were related to reductions in plant weight. The infection by H. maydis was monitored by measurements of canopy temperature and crop water stress index of maize. Canopy temperature was assessed in potted control plants and in plants inoculated with the most aggressive isolate in two experiments conducted outdoors in 2012 and 2013. Both indices responded to the presence of fungal infection in both years, which was detected up to 17 days before development of symptoms in the plants. This study shows the wide distribution of H. maydis in the Iberian Peninsula and highlights the importance of genetic resistance for controlling the pathogen in southern Europe. In addition, the thermal detection of the infection prior to symptom development might lead to useful applications of non-destructive pre-symptomatic disease diagnosis in controlling late wilt disease in maize.
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Abd El-Rahim, M. F., Fahmy, G. M., & Fahmy, Z. M. (1998). Alterations in transpiration and stem vascular tissues of two maize cultivars under conditions of water stress and late wilt disease. Plant Pathology, 47, 216–223.
Allen, R. G., Pereira, J. S., Raes, D., & Smith, M. (1998). Crop evapotranspiration: guidelines for computing crop water requirements. Rome: Food and Agriculture Organization of the United Nations.
Bergstrom, G., Leslie, J., Huber, D., Lipps, P., Warren, H., Esker, P., Grau, C., Botratynski, T., Bulluck, R., Floyd, J., Bennett, R., Bonde, M., Dunkle, L., Smith, K., Zeller, K., Cardwell, K., Daberkow, S., Bell, D., & Chandgoyal, T. (2008). Recovery plan for late wilt of corn caused by Harpophora maydis syn. Cephalosporium maydis. Washington, DC: National Plant Disease Recovery System.
Bowden, R. L., & Rouse, D. I. (1991). Effects of Verticillium dahliae on gas exchange of potato. Phytopathology, 81, 293–301.
Calderón, R., Navas-Cortés, J. A., Lucena, C., & Zarco-Tejada, P. J. (2013). High-resolution airborne hyperspectral and thermal imagery for early detection of verticillium wilt of olive using fluorescence, temperature and narrow-band spectral indices. Remote Sensing of Environment, 139, 231–245.
Campbell, C. L., & Madden, L. V. (1990). Introduction to plant disease epidemiology. New York: John Wiley & Sons, Inc..
Degani, O., & Cernica, G. (2014). Diagnosis and control of Harpophora maydis, the cause of late wilt in maize. Advances in Microbiology, 4, 94–105.
Dimond, A. E. (1970). Biophysics and biochemistry of the vascular wilt syndrome. Annual Review of Phytopathology, 8, 301–322.
Drori, R., Sharon, A., Goldberg, D., Rabinovitz, O., Levy, M., & Degani, O. (2013). Molecular diagnosis for Harpophora maydis, the cause of maize late wilt in Israel. Phytopathologia Mediterranea, 52, 16–29.
Eaton, F. M., & Belden, G. O. (1929). Leaf temperatures of cotton and their relation to transpiration, varietal differences, and yields. U.S.D.A Technical Bulletin, 91, 1–39.
Ehrler, W. L. (1973). Cotton leaf temperatures as related to soil-water depletion and meteorological factors. Agronomy Journal, 65, 404–409.
El-Shafey, H. A., & Claflin, L. E. (1999). Late wilt. In D. G. White (Ed.), Compendium of corn diseases (pp. 43–44). St. Paul: APS Press.
El-Shafey, H. A., El-Shorbagy, F. A., Khalil, I. I., & El-Assiuty, E. M. (1988). Additional sources of resistance to the late-wilt disease of maize caused by Cephalosporium maydis. Agricultural Research Review, 66, 221–230.
Eyal, Z., & Blum, A. (1989). Canopy temperature as a correlative measure for assessing host response to Septoria tritici blotch of wheat. Plant Disease, 73, 468–471.
Gams, W. (2000). Phialophora and some similar morphologically little-differentiated anamorphs of divergent ascomycetes. Studies in Mycology, 45, 187–199.
García-Carneros, A. B., Girón, I., & Molinero-Ruiz, L. (2012). Aggressiveness of Cephalosporium maydis causing late wilt of maize in Spain. Communications in Agricultural and Applied Biological Sciences, 77, 173–179.
Idso, S. B., Jackson, R. D., Pinter, P. J., Reginato, R. J., & Hatfield, J. L. (1981). Normalizing the stress-degree-day parameter for environmental variability. Agricultural Meteorology, 24, 45–55.
Idso, S. B. (1982). Non-water-stressed baselines - a key to measuring and interpreting plant water-stress. Agricultural Meteorology, 27, 59–70.
Jackson, R. D., Reginato, R. J., & Idso, S. B. (1977). Wheat canopy temperature: a practical tool for evaluating water requirements. Water Resources Research, 13, 651–656.
Jones, H. G. (1999). Use of infrared thermometry for estimation of stomatal conductance as a possible aid to irrigation scheduling. Agricultural and Forest Meteorology, 95, 139–149.
Lindenthal, M., Steiner, U., Dehne, H. W., & Oerke, E. C. (2005). Effect of downy mildew development on transpiration of cucumber leaves visualized by digital infrared thermography. Phytopathology, 95, 233–240.
Lorenzini, G., Guidi, L., Nali, C., Ciompi, S., & Soldatini, G. F. (1997). Photosynthetic response of tomato plants to vascular wilt diseases. Plant Science, 124, 143–152.
Molinero-Ruiz, M. L., Melero-Vara, J. M., & Mateos, A. (2010). Cephalosporium maydis, the cause of late wilt in maize, a pathogen new to Portugal and Spain. Plant Disease, 94, 379.
Oerke, E. C., Steiner, U., Dehne, H. W., & Lindenthal, M. (2006). Thermal imaging of cucumber leaves affected by downy mildew and environmental conditions. Journal of Experimental Botany, 57, 2121–2132.
Parke, J. L., Oh, E., Voelker, S., Hansen, E. M., Buckles, G., & Lachenbruch, B. (2007). Phytophthora ramorum colonizes tanoak xylem and is associated with reduced stem water transport. Phytopathology, 97, 1558–1567.
Passioura, J. B. (2006). The perils of pot experiments. Functional Plant Biology, 33, 1075–1079.
Payak, M. M., Lal, S., Lilaramani, J., & Renfro, B. L. (1970). Cephalosporium maydis a new threat to maize in India. Indian Phytopathology, 23, 562–569.
Pecsi, S., & Nemeth, L. (1998). Appearance of Cephalosporium maydis samra, sabet and hingorani in Hungary. Faculteit Landbouwkundige en Toegepaste Biologische Wetenschappen, Universiteit Gent, 63, 873–877.
Sabet, K. A., Zaher, A. M., Samra, A. S., & Mansour, I. M. (1970). Pathogenic behavior of Cephalosporium maydis and C. acremonium. Annals of Applied Biology, 66, 257–263.
Saleh, A. A., Zeller, K. A., Ismael, A. M., Fahmy, Z. M., El-Assiuty, E. M., & Leslie, J. F. (2003). Amplified fragment length polymorphism diversity in Cephalosporium maydis from Egypt. Phytopathology, 93, 853–859.
Saleh, A. A., & Leslie, J. F. (2004). Cephalosporium maydis is a distinct species in the gaeumannomyces-harpophora species complex. Mycologia, 96, 1294–1305.
Samra, A. S., Sabet, K. A., & Hingorani, M. K. (1963). Late wilt disease of maize caused by Cephalosporium maydis. Phytopathology, 53, 402–406.
Singh, S. D., & Siradhana, B. S. (1987). Influence of some environmental conditions on the development of late wilt of maize induced by Cephalosporium maydis. Indian Journal of Mycology and Plant Pathology, 17, 1–5.
Soliman, F. H. S., & Sadek, S. E. (1998). Combining ability of new maize inbred lines and its utilization in the Egyptian hybrid program. Bulletin of the Faculty of Agriculture of the University of Cairo Egypt, 50, 1–20.
Testi, L., Goldhamer, D. A., Iniesta, F., & Salinas, M. (2008). Crop water stress index is a sensitive water stress indicator in pistachio trees. Irrigation Science, 26, 395–405.
Waggoner, P. E., & Dimond, A. E. (1954). Reduction in water flow by mycelium in vessels. American Journal of Botany, 41, 637–640.
Wang, M., Ling, N., Dong, X., Zhu, Y., Shen, Q., & Guo, S. (2012). Thermographic visualization of leaf response in cucumber plants infected with the soil-borne pathogen Fusarium oxysporum f. sp. cucumerinum. Plant Physiology and Biochemistry, 61, 153–161.
White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR protocols: a guide to methods and applications (pp. 315–322). New York: Academic Press.
Zeller, K. A., Jurgenson, J. E., El-Assiuty, Z. M., & Leslie, J. F. (2000). Isozyme and amplified fragment length polymorphisms from Cephalosporium maydis in Egypt. Phytoparasitica, 28, 121–130.
Zeller, K. A., Ismael, A. M., El-Assiuty, E. M., Fahmy, Z. M., & Bekheet, F. M. (2002). Relative competitiveness and virulence of four clonal lineages of Cephalosporium maydis from Egypt toward greenhouse-grown maize. Plant Disease, 86, 373–378.
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Research partially supported by the Spanish National Research Council (CSIC) (PIE200940I120). The authors are grateful to Monsanto Agricultura España SL, Pioneer Hi-Bred Agro Servicios Spain SL and Semillas Fitó for providing some of the samples of diseased maize plants.
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Ortiz-Bustos, C.M., Testi, L., García-Carneros, A.B. et al. Geographic distribution and aggressiveness of Harpophora maydis in the Iberian peninsula, and thermal detection of maize late wilt. Eur J Plant Pathol 144, 383–397 (2016). https://doi.org/10.1007/s10658-015-0775-8
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DOI: https://doi.org/10.1007/s10658-015-0775-8