Fungal Morphogenesis Tracking of Blumeria graminis f. sp. tritici on Leaf Freed of Epicuticular Wax Using Scanning Electron Microscopy
International Journal of Microbiology and Biotechnology
Volume 2, Issue 4, November 2017, Pages: 181-188
Received: Oct. 4, 2017; Accepted: Nov. 6, 2017; Published: Nov. 30, 2017
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Authors
Samar Mohamed Esmail, Wheat Disease Research Department, Plant Pathology Research Institute, Agricultural Research Centre, Giza, Egypt
Ibrahim Sobhy Draz, Wheat Disease Research Department, Plant Pathology Research Institute, Agricultural Research Centre, Giza, Egypt
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Abstract
Fungal morphogenesis development of Blumeria graminis f. sp. tritici was tracked on leaves freed of epicuticular wax using the scanning electron microscopy during successive times, 1 day post inoculation (dpi), 2 dpi, 3 dpi, 4 dpi, 5 dpi and 7 dpi. A conidium seen 1 dpi landing on a leaf showed spore germination and the presence of primary germ tube and the appressria formation revealing their dimensions. Appressorial germ tube has elongated and swollen to form an infection structure, the appressorium has a hooked apical lobe. At 2 dpi, the network of tubular cells forms the mycelial hyphae growing over the leaf surface being fed by a haustorium hidden inside the cell under the appresorium. By 3 dpi, colony consisted of mycelial hyphae with rare hyphal lobes. Appressorial lobes tightly adhered to the surface of epidermal cells. At 4 dpi, extensive hyphal growth and repeated penetration from hyphal appressoria resulted in the formation of further haustoria and bulbous conidiophores. On 5 dpi, bulbous conidiophores have started generating conidia. By 7 dpi, well-developed fungal colony were formed with many chains of conidia sticking up into the air and can be wind spread to initiate new infection cycles. We cannot be sure that removing of the waxes did not affect the pathogen's ability to produce conidial exudates or extracellular material from its germ tubes, appressoria, or hyphae. However, we believe this is unlikely, since removing of leaf waxes prior to inoculation has very little effect on many different aspects of fungal development.
Keywords
Wheat Powdery Mildew, Blumeria graminis, Fungal Morphogenesis, Removal Epicuticular Wax, SEM Examination
To cite this article
Samar Mohamed Esmail, Ibrahim Sobhy Draz, Fungal Morphogenesis Tracking of Blumeria graminis f. sp. tritici on Leaf Freed of Epicuticular Wax Using Scanning Electron Microscopy, International Journal of Microbiology and Biotechnology. Vol. 2, No. 4, 2017, pp. 181-188. doi: 10.11648/j.ijmb.20170204.16
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Copyright © 2017 Authors retain the copyright of this article.
This article is an open access article distributed under the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
References
[1]
J. R. Green, T. L. W. Carver, and S. J. Gurr, “The formation and function of infection and feeding structures,” in: The Powdery Mildews-A Comprehensive Treatise. R. R. Bélanger, W. Bushnell, A. J. Dik, and T. L. W. Carver, eds. American Phytopathological Society Press, St. Paul, MN, U.S.A., 2002, pp. 66-82.
[2]
Z. Zhang, C. Henderson, E. Perfect, T. L. W. Carver, B. J. P. Thomas, and S. J. Gurr, “Of genes and genomes, needles and haystacks: Blumeria graminis and functionality,” Mol. Plant Pathol., vol. 6, pp. 561-575, 2005.
[3]
T. L. W. Carver, S. M. Ingerson, and B. J. Thomas, “Influences of host surface features on development of Erysiphe graminis and Erysiphe pisi,” in: Plant Cuticles: An Integrated Functional Approach. G. Kerstiens, ed. BIOS Scientific Publishers Ltd., vol. 22, no. 12, 2009/1609, Oxford, 1996, pp. 255-256.
[4]
T. L. W. Carver, H. Kunoh, B. J. Thomas, and R. L. Nicholson, “Release and visualization of the extracellular matrix of conidia of Blumeria graminis,” Mycol. Res., vol. 103, pp. 547-560, 1999.
[5]
A. J. Wright, B. J. Thomas, and T. L. W. Carver, “Early adhesion of Blumeria graminis to plant and artificial surfaces demonstrated by centrifugation,” Physiol. Mol. Plant Pathol., vol. 61, pp. 217-226, 2002.
[6]
I. Staub, H. Dahmen, and F. J. Schwinn “Light and scanning electron microscopy of cucumber and barley powdery mildew on host and non-host plants,” Phytopathology, vol. 64, pp. 364-37, 1974.
[7]
H. Kunoh, N. Yamaoka, H. Yoshioka, R. L. Nicholson, “Preparation of the infection court by Erysiphe graminis. 11. Contact-mediated changes in morphology of the conidium surface,” Exp. Mycol., vol. 12, pp. 325-335, 1988.
[8]
R. L. Nicholson, H. Kunoh, T. Shiraishi, and T. Yamada “Initiation of the infection process by Erysiphe graminis: Conversion of the conidial surface from hydrophobicity to hydrophilicity and influence of the conidial exudate on the hydrophobicity of the barley leaf surface,” Physiol. Mol. Plant Pathol., vol. 43, pp. 307-318, 1993.
[9]
H. Kunoh, R. L. Nicholson, H. Yoshioka, N. Yamaoka, I. Kobayashi, “Preparation of the infection court by Erysiphe graminis: degradation of the host cuticle,” Physiol. Plant Pathol., vol. 36, pp. 397-407, 1990.
[10]
P. Whitehouse, P. J. Holloway, and J. C. Casely, “The epicuticular wax of wild oats in relation to foliar entry of the herbicides diclofop-methyl and difenzoquat,” in: The Plant Cuticle. Edited by D. F. Butler, K. L. Alvin, and C. E. Price. Academic Press, London. 1982, pp. 315-330.
[11]
P. J. Holloway, “The structure and histochemistry of plant cuticular membranes: an overview” in: The Plant Cuticle. Edited by D. F. Butler, K. L. Alvin, and C. E. Price. Academic Press, London, 1982, pp. 1-32.
[12]
T. L. W. Carver, and B. J. Thoma, “Normal germling development by Erysiphe graminis on cereal leaves freed of epicuticular wax,” Plant Pathol., vol. 39, pp. 367-375, 1990.
[13]
H. Kunoh, R. L. Nicholson, and I. Kobayashi, “Extracellular materials of fungal structures: their significance at penetration stages of infection,” It1 Electron Microscopy of Plant Pathogens. Edited by K. Mendgen and D.-E. Lesemann. Springer-Verlag, Berlin. 1991, pp. 223-234.
[14]
R. L. Nicholson, and L. Epstein, “Adhesion of fungi to the plant surface: prerequisite for pathogenesis,” in: The Fungal Spore and Disease Initiation In Plants and Animals. Edited by G. T. Cole and H. C. Hoch. Plenum Press, New York, 1991, pp. 3-24.
[15]
K. Mendgen, and H. Deising, “Tansley review no. 48: Infection structures of fungal plant pathogens-a cytological and physiological evaluation,” New Phytol., vol. 124, pp. 193-213, 1993.
[16]
R. L. Nicholson, H. Yoshioka, N. Yamaoka, and H Kunoh, “Preparation of the infection court by Erysiphe graminis. 11. Release of esterase enzyme from conidia in response to a contact stimulus,” Exp. Mycol., vol. 12, pp. 336-349, 1988.
[17]
S. F. Pascholati, H. Yoshioka, H. Kunoh, and R. L. Nicholson, “Preparation of the infection court by E. graminis f. sp. hordei: cutinase is a component of the conidial exudate,” Physiol. Mol. Plant Pathol., vol. 41, pp. 53-59, 1992.
[18]
I. El-Salamony, “Pathological studies on wheat powdery mildew disease in Egypt,” Ph.D. Thesis, Fac. Agric., Zagazig Univ., 2002, pp. 120.
[19]
K. S. Opalski, S. Tresch, K-H. Kogel, K. Grossmann, H. Köhle, and R. Hückelhoven, “Metrafenone: studies on the mode of action of a novel cereal powdery mildew fungicide,” Pest Manag. Sci., vol. 62, pp. 393–401, 2006.
[20]
M. M. Harley, and L. K. Fergusen, “Thee of SEM in poleen morphology and plant systemic,” in: Scanning Electron Microscopy Studies In Taxonomy And Functional Morphology. ED by Clangher D., systems association special vol. 41, clarendon press. Express. Oxford, 1990, pp. 45-68.
[21]
T. L. W. Carver, “Histology of infection by Erysiphe graminis f. sp. hordei in spring barley lines with various levels of partial resistance,” Plant Pathol., vol. 35, pp. 232–240, 1986.
[22]
H. Thordal-Christensen, P. L. Gregersen, and D. B. Collinge, “The barley/Blumeria (syn. Erysiphe) graminis interaction,” in: Mechanism of Resistance to Plant Diseases. Ed. by Slusarenko A, Fraser R. and van Loon K. Kluwer Academic, Dordrecht, 1999, pp. 77–100.
[23]
R. T. A. Cook, and U. Braun, “Conidial germination patterns in powdery mildews,” Mycol. Res., vol. 113, pp. 616-636, 2009.
[24]
L. Kiss, A. Pintye, G. Zséli, T. Jankovics, O. Szentivanyi, Y. M. Hafez, and R. T. A. Cook, “Microcyclic conidiogenesis in powdery mildews and its association with intracellular parasitism by Ampelomyces,” Eur. J. Plant Pathol., vol. 126, pp. 445-451, 2010.
[25]
A. Pintye, S. E. Legler, L. Kiss, “New records of microcyclic conidiogenesis in some powdery mildew fungi,” Mycoscience, vol. 52, pp. 213-216, 2011.
[26]
Samar M. Esmail, and I. S. Draz, “An active role of systemic fungicides to curb wheat powdery mildew caused by Blumeria graminis f. sp. tritici,” In Press.
[27]
T. L. W. Carver, B. J. Thomas, and S. M. Ingerson-Morris, “The surface of Erysiphe graminis and the production of extracellular material at the fungus-host interface during germling and colony development,” Can. I. Bot., vol. 73, pp. 272-287, 1995.
[28]
T. L. W. Carver, R. J. Zeyen, G. G. Ahlstrand, “The relationship between insoluble silicon and success or failure of attempted primary penetration by powdery mildew (Erysiphe graminis) germlings on barley,” Physiol. Mol. Plant Pathol., vol. 31, pp. 133-148, 1987.
[29]
R. T. Plumb, and R. H. Turner, “Scanning electron microscopy of Erysiphe graminis.,” Trans. Br. Mycol. Soc., vol. 59, pp. 149-153, 1972.
[30]
G. T. Cole, and R. A. Samson, “Patterns Of Development In Conidial Fungi,” Pitman Publishing Ltd., London, 1979.
[31]
E. B. G. Jones, “Fungal Adhesion,” Mycol. Res., vol. 98, pp. 961-981, 1994.
[32]
T. L. W. Carver, and S. J. Gurr, “Filamentous fungi on plant surfaces,” in: Biology of the Plant Cuticle. M. Riederer and M. Müller, eds. Blackwell Publishing Ltd., Oxford, 2006, pp. 368-397.
[33]
S. A. Francis, F. M. Dewey, and S. J. Gurr, “The role of cutinase in germling development and infection by Erysiphe graminis f. sp. hordei,” Physiol. Mol. Plant Pathol., vol. 49, pp. 201-211, 1996.
[34]
Y. Hegde, and P. E. Kolattukudy, “Cuticular waxes relieve self-inhibition of germination and appressorium formation by the conidia of Magnaporthe grisea,” Physiol. Mol. Plant Pathol., vol. 51, pp. 75-84, 1997.
[35]
Skamnioti P, and S. J. Gurr, “Magnaporthe grisea cutinase mediates appressorium differentiation and host penetration and is required for full virulence,” Plant Cell, vol. 19, pp. 2674-2689, 2007.
[36]
T. M. Bourett, and R. J. Howard, “In vitro development of penetration structures in the rice blast fungus Magnaporthe grisea,” Can. J. Bot., vol. 68, pp. 329-342, 1990.
[37]
E. W. Mercure, B. Leite, and R. L. Nicholson, “Adhesion of ungerminated conidia of Colletotrichum graminicola to artificial hydrophobic surfaces,” Physiol. Mol. Plant Pathol., vol. 45, pp, 421-440, 1994.
[38]
E. W. Mercure, H. Kunoh, and R. L. Nicholson, “Visualization of materials released from adhered ungerminated conidia of Colletotrichum graminicola,” Physiol. Mol. Plant Pathol., vol. 46, pp. 121-135, 1995.
[39]
R. Chaubal, V. A. Wilmot, and W. K. Wynn, “Visualization, adhesiveness and cytochemistry of the extracellular matrix produced by urediniospore germ tubes of Puccinia sorghi,” Can. J. Bot., vol. 69, pp. 2044-2054, 1991.
[40]
C. W. Mims, K. A. Liljebjelke, and E. A. Richardson, “Surface morphology wall structure and initial adhesion of conidia of the powdery mildew fungus Uncinuliella australiana,” Phytopathology, vol. 85, pp. 352-358, 1995.
[41]
L. Samuels, L. Kunst, and R. Jetter, “Sealing plant surfaces: Cuticular wax formation by epidermal cells,” Annu. Rev. Plant Biol., vol. 59:683-707, 2008.
[42]
H. Deising, R. L. Nicholson, M. Haug, R. J. Howard, and K. Mengden, “Adhesion pad formation and the involvement of cutinase and esterases in the attachment of uredospores to the host cuticle,” Plant Cell, vol. 4, pp. 1101-1111, 1992.
[43]
J. D. Walton, “Deconstructing the cell wall,” Plant Physiol., vol. 104, pp. 1113-1118, 1994.
[44]
H. Chahinian, L. Nini, E. Boitard, J. P. Dubes, L. C. Comeau, and L. Sarda, “Distinction between esterases and lipases: A kinetic study with vinyl esters and TAG,” Lipids, vol. 37, pp. 653-662, 2002.
[45]
P. E. Kolattukudy, “Cutinases from fungi and pollen,” Pages 471-504 in: Lipases. B. Borgstrom and H. L. Brockman, eds. Elsevier, New York, 1984, pp. 471-504.
[46]
S. Longhi, and C. Cambillau, “Structure-activity of cutinase, a small lipolytic enzyme,” Biochim. Biophys Acta, vol. 1141, pp. 185-196, 1999.
[47]
R. Verger, “Interfacial activation of lipases: Facts and artifacts,” Trends Biotechnol., vol. 15, pp. 32-38, 1997.
[48]
C. Martinez, A. Nicolas, H. van Tilbeurgh, M. P. Egloff, C. Cudrey, R. Verger, and C. Cambillau, “Cutinase, a lipolytic enzyme with a preformed oxyanion hole,” Biochemistry, vol. 33, pp. 83-89, 1994.
[49]
J. Feng, F. Wang, G. Liu, D. Greenshields, W. Shen, S. Kaminskyj, R. Hughes Geoff., Y. Peng, G. Selvaraj, J. Zou, and Y. Wei, “Analysis of a Blumeria graminis-secreted lipase reveals the importance of host epicuticular wax components for fungal adhesion and development,” Mol. Plant-Microbe. Interact., vol. 22, no. 12, pp. 1601–1610, 2009.
[50]
A. L. Kidger, and T. L. W. Carver, “Autofluorescence in oats infected by powdery mildew,” Trans. Br. Mycol. Soc., vol. 76: pp. 405-409, 1981.
[51]
H. Kunoh, “Primary germ tubes of Erysiphe graminis conidia,” in: Plant Infection: the physiological and biochemical basis. Edited by Y. Asada, W. R. Bushnell, S. Ouchi, and C. P. Vance. Springer-Verlag, Berlin. 1982, pp. 45-59.
[52]
T. L. W. Carver, M. P. Robbins, R. J. Zeyen, “Effects of two PAL inhibitors on the susceptibility and localized autofluorescent host cell responses of oat leaves attacked by Erysiphe graminis DC,” Physiol. Mol. Plant Pathol., vol. 39, pp. 269-287, 1991.
[53]
W. R. Bushnell, “The haustorium of E. graminis. An experimental study by light microscopy,” in: Morphological and Biochemical Events In Plant-Parasite Interaction. Edited by S. Akai and S. Ouchi. Phytopathological Society of Japan, Tokyo, 1971, pp. 229-254.
[54]
J. R. Aist, and W. R. Bushnell, “Invasion of plants by powdery mildew fungi, and cellular mechanisms of resistance,” in: The Fungal Spore and Disease Initiation In Plants and Animals. Edited by G. T. Cole and H. C. Hoch. Plenum Press, New York, 1991, pp. 321-345.
[55]
T. A. Clark, R. J. Zeyen, A. G. Smith, W. R. Bushnell, L. J. Szabo, and C. P. Vance, “Host response gene transcript accumulation in relation to visible cytological events during Erysiphe graminis attack in isogenic barley lines differing at the M1-a locus,” Physiol. Mol. Plant Pathol., vol., 43, pp. 283-298, 1993.
[56]
T. A. Clark, R. J. Zeyen, A. G. Smith, T. L. W. Carver, and C. P. Vance, “Phenylalanine ammonia lyase mRNA accumulation, enzyme activity, and cytoplasmic responses in barley isolines differing at the M1-a and M1-o loci, attacked by Erysiphe graminis f. sp. hordei,” Physiol. Mol. Plant Pathol., vol. 44, pp. 171–185, 1994.
[57]
T. Shiraishi, N. Yamaoka, and H. Kunoh, “Association between increased phenylalanine ammonia-lyase activity and cinnamic acid synthesis and the induction of temporary inaccessibility caused by Erysiphe graminis primary germ tube penetration of the barley leaf,” Physiol. Mol. Plant Pathol., vol. 34: 75-83, 1989.
[58]
A. S. Ryabchenko, G. V. Serezhkina, G. N. Mishina, and L. N. Andreev, “Morphological variability of wheat powdery mildew in the context of its parasitic adaptation to wheat–Aegilops lines with different resistance,” Biology Bulletin, vol. 30, no. 3, pp. 255–261, 2003.
[59]
G. Mustafa, N. G. Khong, B. Tisserant, B. Randoux, J. Fontaine, M. Magnin-Robert, P. Reignault and L-H. Sahraoui Anissa, “Defence mechanisms associated with mycorrhiza-induced resistance in wheat against powdery mildew,” Functional Plant Biology, 2017, doi: 10.1071/FP16206.
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