Keywords
rust fungi
teliospores
ultrastructure
urediniospores
alteraciones histopatológicas
royas
teliosporas
ultrastructura
urediniosporas
How to Cite
Abstract
Introduction: Histopathological and histochemical aspects linked to the attack of fungal rusts to plants, as well as its relation with the different spore stages are topics rather scarce in the scientific literature. Objective: To describe and analyze the histopathological and histochemical aspects of Cymbopogon citratus and its relation with the different stages of the spores from the rust fungi Puccinia nakanishikii. Methods: During the months April and August 2013, leaves healthy and infected by Puccinia nakanishikii were collected in the Northwestern scarp of the Bucaramanga-Colombia plateau. The samples with injuries on diverse developmental stages were fixated and processed according to the standard protocols for embedding and sectioning in paraffin and resin. Sections obtained from paraffin (5-7 µm) were stained with Safranin-Alcian blue and Alcian blue-Hematoxylin. On the other hand, sections obtained from resin (0.5 µm) were stained with Toluidine blue. Further, freehand sections were obtained for an autofluorescence analysis. The observations and photographic record were done via photonic microscope and epifluorescence microscope. For the observations via scanning electron microscopy (SEM), the samples were fixated in Glutaraldehyde, dehydrated with 2,2 dimethoxypropane, then desiccated to critical point and finally coated with gold. Results: The leaves are generally hypostomatic, with long and short epidermic cell forming parallel rows and showing unicellular prickle trichomes and micro-trichomes. The abaxial surface is covered by epicuticular wax forming a dense layer. The adaxial epidermis is formed by groupings of bulliform cells and epidermal cells with rectangular or squared contour. In the mesophyll, there is no differentiation between palisade and spongy parenchyma, its anatomy reflects the C4 metabolism. The formation of uredosori and teliosori both hypophyllous was observed. Urediniospores are the reinfecting agents phase, they have 4-5 equatorial germ pores and echinulate wall. Teliospores have smooth wall and a persistent pedicel. The urediniospores form a germ tube, generally on the abaxial leaf surface, these tubes develop towards the stomata reaching the mesophyll interior. No appressorium were observed. The epidermis limiting the uredosorus detaches due the development and pressure that exert both the urediniospores and capitate paraphyses. As the infection progresses, autofluorescense of the chlorophyll is lost and the cells undergo necrotic processes. Afterwards, the phloem collapses and the xylem becomes slightly disorganized. At this moment, the infection is extended along the whole leaf blade, resulting in the leaf death and the plant defoliation. On advanced stages of the infection, the uredosori showed pycnidia, probably belonging to the hyperparasite Sphaerellopsis, these structures were closely associated to the rust infected tissues. Conclusions: Puccinia nakanishikii develops on the leaves of Cymbopogon citratus producing uredosori and teliosori. Urediniospores are the reinfective stage, teliospores were only observed at late stages of the infection. The epidermis and photosynthetic tissue are severely affected by cell necrosis. The vascular tissues are deeply affected on the advances stages of the infection.
References
Abdulbagiyeva, S., Zamanov, A., Talai, J., & Allahverdiyev, T. (2015). Effect of rust diseaseon photosynthetic rate of wheat plant. Journal of Agricultural Science andTechnology B, 5, 486-490.
Agrios, G. N. (2005). Plant pathology (5th Ed.). San Diego, USA: Academic Press Inc.
Aoun, M. (2017). Host defense mechanisms during fungal pathogenesis and how these are overcome in susceptible plants: A review. International Journal of Botany, 13, 82-102.
Aoun, M., Rioux, D., Simard, M., & Bernier, L. (2009). Fungal colonization and host defense reactions in Ulmus americana callus cultures inoculated with Ophiostoma novo-ulmi. Phytopathology, 99, 642-650.
Bender, C. M., Pretorius, Z. A., Kloppers, F. J., & Spies, J. J. (2000). Histopathology of leaf rust infection and development in wheat genotypes containing Lr12 and Lr13. Journal of Phytopathology, 148(2), 65-76.
Bertea, M. C., Tesio, M., D'agostino, G., Buffa, G., Camusso, W., Bossi, S., Mucciarelli, M., Scannerini, S., & Maffei, M. (2003). The C 4 biochemical pathway and the anatomy of lemongrass (Cymbopogon citratus (DC) Stapf.) cultivated in temperate climates. Plant Biosystems, 137(2), 175-184.
Bertea, M. C., & Maffei, M. E. (2010). The genus Cymbopogon botany, including anatomy, physiology, biochemistry, and molecular biology. In A. Akhila (Ed.), Essential Oil- Bearing Grasses: The genus Cymbopogon (pp. 1-24). Boca Raton, USA: CRC Press.
Bhattacharya, S. (2017). Wheat rust back in Europe. Nature, 542, 145-146.
Buckley, T. N., Sack, L., & Gilbert, M. E. (2011). The role of bundle sheath extension and life form in stomatal responses to leaf water status. Plant Physiology, 156, 962-973.
Buriticá, P. (1978). Los hongos de Colombia II: Nuevas especies de uredinales. Caldasia, 12(57), 165-170.
Buriticá, P. (1991). Familias del orden Uredinales con ciclo de vida completamente reducido. Revista de la Academia Colombiana de Ciencias Exactas Físicas y Naturales, 18(69), 131-148.
Buriticá, P. (2001). Descubriendo ancestros de uredinales. Revista de la Academia Colombiana de Ciencias Exactas Físicas y Naturales, 25(96), 395-401.
Buriticá, P. (2003). Estado del conocimiento universal sobre el orden Uredinales. (Fungi, royas). Revista Facultad Nacional de Agronomía Medellín, 56(1), 1813-1838.
Buriticá, P., & Pardo, V. M. (1996). Flora uredineana colombiana. Revista de la Academia Colombiana de Ciencias Exactas Físicas y Naturales, 20(77), 183-236.
Buriticá, P., & Salazar, M. A. (2007). Nuevos registros de royas (Uredinales) potencialmente importantes en Colombia. Revista Facultad Nacional de Agronomía Medellín, 60(1), 3645-3655.
Buriticá, C. P., Salazar, Y. M., & Pardo, C. V. M. (2014). Pucciniales (Fungi), royas de Colombia. Revista Facultad Nacional de Agronomía, Medellín, 67(Suplemento 1), 1-93.
Carris, L. M., & Littlefield, L. J. (2017). Rust and smut diseases. In B. H. Ownley & R. N. Trigiano (Eds.), Plant Pathology Concepts and Laboratory Exercises (3th Ed., pp. 221-236). Boca Raton, Florida: CRC Press Taylor & Francis Group.
Carver, T. L. W., & Gurr, S. J. (2006). Filamentous fungi on plant surfaces. Annual Plant Reviews, 23, 368- 397.
Chardón, C. E., & Toro, R. A. (1930). Mycological explorations of Colombia. Journal of the Department of Agriculture of Porto Rico, 14(4), 195-301.
Clement, J. A., Butt, T. M., & Beckett, A. (1993a). Characterization of the extracellular matrix produced in vitro by urediniospores and sporelings of Uromyces viciae-fabae. Mycological Research, 97, 594-602.
Clement, J. A., Martin, S. G., Porter, R., Butt, T. M., & Beckett, A. (1993b). Germination and the role of extracellular matrix in adhesion of urediniospores of Uromyces viciae-fabae to synthetic surfaces. Mycological Research, 97, 585-593.
Clement, J. A., Porter, R., Butt, T. M., & Beckett, A. (1994). The role of hydrophobicity in attachment of urediniospores and sporelings of Uromyces viciae-fabae. Mycological Research, 98, 1217-1228.
Clement, J. A., Porter, R., Butt, T. M., & Beckett, A. (1997). Characteristics of adhesion pads formed during imbibition and germination of urediniospores of Uromyces viciaefabae. Mycological Research, 101, 1445-1458.
Clement, J. A., Porter, R., & Beckett, A. (1998). The orientation of urediniospores of Uromyces viciae-fabae during fall and after landing. Mycological Research, 102, 907-913.
Cummins, G. (1971). The rust fungi of cereals, grasses and bamboos. Nueva York, USA: Springer-Verlag.
Cummins, G., & Hiratsuka, Y. (2003). Illustrated general of rust fungi (3rd Ed.). San Pablo, USA: The American Phytopathological Society.
Dai, G. H., Andary, C., Mondolot-Cosson, L., & Boubals, D. (1995). Histochemical studies on the interaction between three species of grapevine, Vitis vinifera, V. rupestris and V. rotundifolia and the downy mildew fungus, Plasmopara viticola. Physiological and Molecular Plant Pathology, 46, 177-188.
Dixon, L. J., Castlebury, L. A., Aime, M. C., Glynn, N. C., & Comstock, J. C. (2010). Phylogenetic relationships of sugarcane rust fungi. Mycological Progress, 9, 459-468.
Doohan, F., & Zhou, B. (2018). Fungal pathogens of plants. In K. Kavanagh (Ed.), Fungi biology and applications (3rd Ed., pp. 355-386). County Kildare, Ireland: John Wiley & Sons, Inc.
Eltahir, S. A., & Abuereish, I. B. (2010). Leaf and stem anatomy of Cymbopogon citratus and Cymbopogon schoenanthus in Sudan. Journal of Chemical and Pharmaceutical Research, 2(4), 766-771.
Epstein, A. H., Simons, M. D., Frey, K. J., & Rothman, P. (1998). Field resistance of oats to Puccinia graminis f. sp. avenae measured via yield and seed weight reduction. Plant Disease, 72, 154-156.
Eversmeyer, M. G., & Kramer, C. L. (2000). Epidemiology of wheat leaf and stem rust in the central great plains of the USA. Annual Review of Phytopathology, 38, 491-513.
García, G. D., Buriticá, P., & Henao, M. L. M. (2007). Elementos para la elaboración del libro rojo de hongos royas de Colombia. Revista de la Academia Colombiana de Ciencias Exactas Físicas y Naturales, 31(121), 449-468.
García, L. E., Leyva, M. S. G., Cárdenas, S. E., Huerta, E. J., Sandova, I. S., & Villaseñor, M. E. (2007). Proceso de infección de la roya de la hoja del trigo (Puccinia triticina erikson) en genotipos con resistencia parcial. Agrociencia, 41, 775-785.
García, P. J. I., Fernández, M. B., Duke, O. E., Hernández, A., López, A. F., & Becerril, J. M. (2015). Autofluorescence: biological functions and technical applications. Plant Science, 236, 136-145.
Gardner, E. D. (1985). Lemongrass Rust Caused by Puccinia nakanishikii in Hawaii. Plant Disease, 69, 1100.
Guerra, M., Rodríguez, M., García, G., & Rangel, C. (2004). Actividad antimicrobiana del aceite esencial y crema de Cymbopogon citratus (DC), Stapf. Revista Cubana de Plantas Medicinales, 9, 1-6.
Grass Phylogeny Working Group II (GPWG). (2012). New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytologist, 193, 304-312.
Haque, A. M. N. A., Remadevi, R., & Naebe, M. (2018). Lemongrass (Cymbopogon): a review on its structure, properties, applications and recent developments. Cellulose, 25(10), 5455-5477.
Hardham, A. R. (2007). Cell biology of fungal and Oomycete infection of plants. In K. Esser (Ed.), The Mycota. Biology of the fungal cell VIII (2nd Ed., pp. 251-289). Berlin, Germany: Springer-Verlag.
Hatfield, D. R., Rancour, M. D., & Marita, M. J. (2017). Grass cell walls: a story of cross linking. Frontiers in Plant Science, 7, 1-15.
Harris, P. J., & Hartley, R. D. (1976). Detection of bound ferulic acid in cell walls of the gramineae by ultraviolet fluorescence microscopy. Nature, 259, 508-510.
Hawksworth, D. L., & Lücking, R. (2017). Fungal diversity revisited: 2.2 to 3.8 million species. Microbiology Spectrum, 5(4), 1-17.
Hernandez, J. R., & Hennen, J. F. (2003). Rust fungi causing galls, witches' brooms, and other abnormal plant growths in northwestern Argentina. Mycologia, 95(4), 728-755.
Hiratsuka, Y., & Hiratsuka, N. (1980). Morphology of spermogonia and taxonomy of rust fungi. Reports of the Tottori Mycological Institute, 18, 257-268.
Jiang, X. L., & Kang, Z. S. (2010). Ultrastructural changes in the interaction between Puccinia striiformis and wheat cultivar with slow-rusting resistance. Agricultural Sciences in China, 9(1), 64-70.
Kang, Z., Tang, C., Zhao, J., Cheng, Y., Liu, Y., Guo, J., Wang, X., & Chen, X. (2017). Wheat- Puccinia striiformis interactions. In X. Chen & Z. Kang (Eds.), Stripe rust (pp. 155-183). Dordrecht, The Netherlands: Springer.
Kellogg, A. E. (2015). The families and genera of vascular plants. volume XIII. Flowering plants. Monocots. Poaceae. Heidelberg, Germany: Springer International Publishing.
Kloppers, F. J., & Pretorius, Z. A. (1995). Histology of the infection and development of Puccinia recondita f. sp. tritici in a wheat line with Lr37. Journal of Phytopathology, 143(5), 261-267.
Koike, S. T., & Molinar, R. H. (1999). Rust Disease on Lemongrass in California. Plant Disease, 83(3), 304.
Kolmer, J. A., Ordonez, M. E., & Groth, J. V. (2009). The rust fungi. In Encyclopedia of Life Sciences (ELS) (pp. 1-8). John Wiley & Sons, Ltd: Chichester.
Lattanzio, V., Lattanzio, M. T. V., & Cardinali, A. (2006). Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects. In F. Imperato (Ed.), Phytochemistry: advances in research (pp. 23-67). Trivandrum, India: Research Signpost.
Leyva, M. S. G., Espitia, R. E., Villaseñor, M. H. E., & Huerta, E. J. (2004). Pérdidas ocasionadas por Puccinia graminis f. sp. avenae Eriks. y Henn., Causante de la roya del tallo en seis cultivares de avena (Avena sativa L.) en los valles altos de México. Revista Mexicana de Fitopatología, 22(2), 166-171.
Lewinsohn, E., Dudai, N., Tadmor, Y., Katzir, I., Ravid, U., Putievsky, E., & Joel, M. D. (1998). Histochemical localization of Citral accumulation in lemongrass leaves (Cymbopogon citratus (DC.) Stapf. Poaceae). Annals of Botany, 81, 35-39.
Lichtenthaler, K. H., & Schweiger, J. (1997). Cell wall bound ferulic acid, the major substance of the blue-green fluorescence emission of Plants. Journal of Plant Physiology, 52, 272-282.
Li, Y. M., Windham, M. T., & Trigiano, R. N. (2007). Microscopic and macroscopic studies of the development of Puccinia hemerocallidis in resistant and susceptible daylily cultivars. Plant Disease, 91(6), 664-668.
Lin, C. H., Falk, R. H., & Stocking, C. R. (1977). Rapid chemical dehydration of plant material for light and electron microscopy with 2,2-dimethoxypropane and 2,2-diethoxypropane. American Journal of Botany, 64(5), 602-605.
Longo, N., Naldini, B., Paolillo, A., Drovandi, F., Tani, G., & Gonnelli, T. (1997). Morphological aspects of early host-parasite interactions in infections of Melampsora pinitorqua and Melampsora larici-tremulae on Pinus sylvestris: Implications in the taxonomical relationship of the two rust fungi. Caryologia, 50(1), 37-57.
Lundgren, R. M., Osborne, P. C., & Christin, A. P. (2014). Deconstructing Kranz anatomy to understand C4 evolution. Journal of Experimental Botany, 65(13), 3357-3369.
Ma, Q., & Shang, S. H. (2009). Ultrastructure of stripe rust (Puccinia striiformis f. sp. tritici) interacting with slow-rusting, highly resistant, and susceptible wheat cultivars. Journal of Plant Pathology, 91(3), 597-606.
Maheshwari, R. A. (2007). Scourge of mankind: From ancient times into the genomics era. Current Science, 93(9), 1249-1256.
Mahlein, K. A. (2016). Plant disease detection by imaging sensors-parallels and specific demands for precision agriculture and plant phenotyping. Plant disease, 100(2), 241-251.
Mahlein, K. A., Steiner, U., Hillnhütter, C., Dehne, W. H., & Oerke, C. E. (2012). Hyperspectral imaging for small-scale analysis of symptoms caused by different sugar beet diseases. Plant Methods, 8(3), 1-13.
Mahlein, K. A., Kuska, T. M., Behmann, J., Polder, G., & Walter, A. (2018). Hyperspectral sensors and imaging technologies in phytopathology: state of the art. The Annual Review of Phytopathology, 56, 535-558.
Maier, W., Begerow, D., Wei, M., & Oberwinkle, R. F. (2003). Phylogeny of the rust fungi: an approach using nuclear large subunit ribosomal DNA sequences. Canadian Journal of Botany, 81(1), 12-23.
Mayor, E. (1913). Contribution a l'etude de Uredinées de Colombie. Mémoires de la Société Neuchateloise de Sciences Naturelles, 5, 442-509.
Melo, P., Araújo, J., Carvalho, A., Tostes, G., & Areâs, M. (2010). Puccinia nakanishikii, nova ocorrência de ferrugem em capim-limão (Cymbopogon citratus) no Brasil. Tropical Plant Pathology, 35(2), 129-130.
Mendgen, K. (1996). Fungal attachment and penetration. In G. Kerstiens (Ed.), Plant cuticles (pp. 175-188). Oxford, England: Garland Science.
Mendgen, K., & Hahn, M. (2002). Plant infection and the establishment of fungal biotrophy. Trends in Plant Science, 7(8), 352-356.
Metcalfe, C. R. (1960). Anatomy of the Monocotyledons I: Gramineae (1St Ed.). New York, USA: Oxford Clarenden Press.
Moldenhauer, J., Moerschbacher, B. M., & Westhuizen, A. J. (2006). Histological investigation of stripe rust (Puccinia striiformis f.sp. tritici) development in resistant and susceptible wheat cultivars. Plant Pathology, 55(4), 469-474.
Morales, L. Á., & Salazar, Y. M. (2014). Caracterización morfológica de las royas (Pucciniales) que afectan el limoncillo (Cymbopogon citratus (dc.) stapf) en Colombia. Bioagro, 26(3), 171-176.
Nelson, S. (2008). Rust of lemongrass. Plant Disease, 57, 1-5.
Negrelle, R., & Gómez, E. (2007). Cymbopogon citratus (DC.) Stapf: Chemical composition and biological activities. Revista Brasileira de Plantas Medicinais, 9(1), 80-92.
O'brien, T. P., & Mccully, M. E. (1981). The study of plant structure principles and selected methods. Melbourne, Australia: Termarcarphy Pty. Ltd.
Omaraa, I. R., Khaled, A. A., & Abdelaal, A. A. K. (2018). Biochemical, histopathological and genetic analysis associated with leaf rust infection in wheat plants (Triticum aestivum L.). Physiological and Molecular Plant Pathology, 104, 48-57.
Pavgi, M. S. (1972). Morphology and taxonomy of the Puccinia species on corn and Sorghum. Mycopathologia et Mycologia Applicata, 47(3), 207-220.
Pardo, V. M. (1998). Registros nuevos para la flora de uredinales (royas) de Colombia. Revista de la Academia Colombiana de Ciencias Exactas Físicas y Naturales, 22(84), 347-354.
Pardo, V. M. (1999). La roya del limoncillo, una nueva enfermedad para Colombia y Sudamérica. Fitopatología Colombiana, 3(1), 43-44.
Pardo, V. M. (2003). Nuevas especies y registros de uredinales para Colombia y Sudamérica. Caldasia, 25(2), 283-296.
Pareek, S. K., & Gupta, R. (1985). On the status of agronomic research in Cymbopogon grasses in India with projections on future work. India, 29, 215-224.
Płachecka, A. (2005). Microscopical observations of Sphaerellopsis filum, a parasite of Puccinia recondita. Acta Agrobotanica, 58(1), 67-7.
Ploetz, C. R., Palmateer, J. A., Lopez, P., & Aime, C. M. (2013). First Report of Rust Caused by Puccinia nakanishikii on Lemongrass, Cymbopogon citratus, in Florida. Plant Disease, 98(1), 156.
Read, D. N., Kellock, J. L., Collins, J. T., & Gundlach, M. A. (1997). Role of topography sensing for infection-structure differentiation in cereal rust fungi. Planta, 202(2), 163-170.
Roshchina, V. V. (2012). Vital autofluorescence: application to the study of plant living cells. International Journal of Spectroscopy, 2012, 1-14.
Ruzin, S. E. (1999). Plant microtechnique and microscopy. Nueva York, USA: Oxford University.
Salazar, Y. M., & Buriticá, C. P. (2003). Uredobiota de la familia Poaceae en la zona cafetera colombiana. Revista Cenicafé, 5(4), 329-346.
Salazar, M. A., & Buriticá, C. P. (2004). Nuevos registros para la Uredobiota colombiana (Fungi, Uredinales). Caldasia, 26(1), 79-87.
Salazar, M. A., & Buriticá, C. P. (2008). Nuevas especies para la Uredobiota Neotropical. Revista Facultad Nacional de Agronomía Medellín, 6(1), 4291-4301.
Salazar, M. A., Buriticá, C. P., & Cadena, C. G. (2002). Implicaciones de los estudios sobre biodiversidad de los Uredinales (royas) en la región cafetera colombiana. Revista Cenicafé, 53(3), 219-238.
Savile, D. B. O. (1984). Taxonomy of the cereal rust fungi. In W. R. Bushnell & A. P. Roelfs (Eds.), The cereal rusts, Origins, specificity, structures, and physiology (pp. 79-112). Florida, USA: Academic Press.
Serrano, M., Coluccia, F., Torres, M., L’Haridon, F., & Métraux, P. J. (2014). The cuticle and plant defense to pathogens). Frontiers in Plant Science, 1(274), 1-8.
Schumann, G. L., & D'Arcy, C. J. (2009). Essential plant pathology (2nd Ed.). Minnesota, USA: American Phytopathological Society.
Scot, N. (2008). Rust of lemongrass. Hawaii, USA: College of Tropical Agriculture and Human Resources.
Scholes, D. J., & Rolfe, A. S. (2009). Chlorophyll fluorescence imaging as tool for understanding the impact of fungal diseases on plant performance: a phenomics perspective. Functional Plant Biology, 36, 880-892.
Serrato, C. A., & Moreno, B. A. M. (2003). Efecto del abono orgánico y de la edad del corte en la producción de biomasa y de aceite esencial de limoncillo. Revista Cenicafé, 54(4), 273-277.
Shah, G., Kaur, M., Dhabiliya, F., & Shri, R. (2012). Pharmacognostic standardization of Cymbopogon citratus (dc.) stapf leaves. Pharmacognosy Journal, 4(22), 19-25.
Singh, R. P., Hodson, D. P., Huerta-Espino, J., Jin, Y., Njau, P., Wanyera, R., … Ward, R. W. (2008). Will stem rust destroy the world’s wheat crop? In D. L. Sparks (Eds.), Advances in Agronomy (Vol. 98, pp. 271-309). Newark, USA: Academic Press.
Singh, R. P., Singh, P. K., Rutkoski, J., Hodson, D. P., He, X., Jørgensen, L. N., & Huerta-Espino, J. (2016). Disease impact on wheat yield potential and prospects of genetic control. The Annual Review of Phytopathology, 54, 303-322.
Soto, O. R., Vega, M. G., & Tamajón, N. A. L. (2002). Instructivo técnico del cultivo de Cymbopogon citratus (D.C) Stapf (caña santa). Revista Cubana de Plantas Medicinales, 7(2), 89-95.
Soto, E. A., Förster, H., DeMason, A. D., & Adaskaveg, E. J. (2005). Initial infection and colonization of leaves and stems of cling peach by Tranzschelia discolor. Phytopathology, 5(8), 942-950.
Srivastava, R. C., & Abraham, J. (1977). Anatomical studies on abnormal growth caused by Puccinia ruelliae Syd. on Ruellia prostrata. Mycopathologia, 62(2), 113-116.
Staples, R. C. (2000). Research on the rust fungi during the twentieth century. Annual Review of Phytopathology, 38, 49-69.
Talamond, P., Verdeil, J. L., & Conéjéro, G. (2015). Secondary metabolite localization by autofluorescence in living plant cells. Molecules, 20(3), 5024-5037.
Torres, B. M. R., Silva, M. M., Nogueira, G., Alvarenga, A., & Silva, P. S. (2016). Occurrence of homobaric and heterobaric leaves in two forest types of southern Brazil. Acta Botanica Brasilica, 30(2), 304-312.
Trakunyingcharoen, T., Lombard, L., Groenewald, Z. J., Cheewangkoon, R., Toanun, C., Alfenas, C. A., & Crous, W. P. (2014). Mycoparasitic species of Sphaerellopsis, and allied lichenicolous and other genera. IMA Fungus, 5(2), 391-414.
Vida, J., Carvalho, J. A. A., & Verzignassi, J. R. (2006). Primeira ocorrência de ferrugem em capim-limão causada por Puccinia cymbopogonis no Brasil. Summa Phytopathologica, 32(1), 89-91.
Voegele, R. T., Hahn, M., & Mendgen, K. (2009). The Uredinales: cytology, biochemistryand molecular biology. In K. Esser & H. B Deising (Eds.), The Mycota. A Comprehensive Treatise on Fungi as Experimental Systems for Basic and Applied Research (pp. 69-98). Berlin, Alemania: Springer-Verlag.
Voegele, R. T., & Mendgen, K. W. (2011). Nutrient uptake in rust fungi: how sweet is parasitic life? Euphytica, 179, 41-55.
Wahyuno, D., & Kakishima, M. (2015). Aecidium cinnamomi (Uredinales) has an endocyclic life cycle on Cinnamomum spp. (Lauraceae) in Indonesia. Australasian Plant Disease Notes, 10(154), 1-4.
Walters, R. D. (2015). Physiological responses of plants to attack. Oxford, England: John Wiley & Sons, Ltd.
Watkinson, C. S., Boddy, L., & Money, P. N. (2016). The fungi. Oxford, London: Academic Press.
Webster, J., & Weber, W. S. (2007). Introduction to Fungi (3rd Ed.). Cambridge, England: Cambridge University Press.
Wesp, G. C., Martinelli, J. A., Graichen, S. F. A., & Soares, C. M. (2013). Histopathology of durable adult plant resistance to leaf rust in the Brazilian wheat variety Toropi. The European Journal of Plant Pathology, 137(1), 181-196.
Yeung, E. C. T., Stasolla, C., Sumner, M. J., & Huang, B. Q. (2015). Plant microtechniques and protocols. New York, USA: Springer.
Yuan, W. Z., Pei, H. M., Hunter, T., & Royle, J. (1998). Eudarluca caricis, the teleomorph of the mycoparasite Sphaerellopsis filum, on blackberry rust Phragmidium violaceum. Mycological Research, 102(7), 866-868.
Zhao, D., Glynn, C. N., Glaz, B., Comstock, C. J., & Sood, S. (2011). Orange rust effects on leaf photosynthesis and related characters of sugarcane. Plant Disease, 95(6), 880-892.
Zuluaga, M. C., Buriticá, C. P., & Marín, M. M. (2009). Generalidades de los Uredinales (Fungi: Basidiomycota) y de sus relaciones filogenéticas. Acta Biológica Colombiana, 14(1), 39-54.
Zuluaga, C., Buriticá, P., & Marín, M. (2011). Filogenia de los hongos roya (Uredinales) en la zona andina colombiana mediante el uso de secuencias del ADN ribosomal 28S. Revista de Biología Tropical, 59(2), 517-540.
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