ORIGINAL ARTICLE
Histological changes induced during the biotrophic phase of infection of three potato varieties by Phytophthora infestans (Mont.) de Bary
Astrid Elena Gaviria 1, A-D,F
,  
Luis Fernando Patiño 2, A-C,E-F
,  
Juan Gonzalo Morales 1, A,C-F  
 
 
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1
Departamento de Ciencias Agronómicas, Facultad de Ciencias Agrarias Universidad Nacional de Colombia Sede Medellín, Medellin, Colombia
2
Ciencias Agrarias, Politécnico Colombano Jaime Isaza Cadavid, Medellin, Colombia
A - Research concept and design; B - Collection and/or assembly of data; C - Data analysis and interpretation; D - Writing the article; E - Critical revision of the article; F - Final approval of article
CORRESPONDING AUTHOR
Juan Gonzalo Morales   

Departamento de Ciencias Agronómicas, Facultad de Ciencias Agrarias Universidad Nacional de Colombia Sede Medellín, Medellin, Colombia
Online publication date: 2020-01-22
Submission date: 2019-04-24
Acceptance date: 2019-06-03
 
Journal of Plant Protection Research 2019;59(4):465–478
KEYWORDS
TOPICS
ABSTRACT
In this study defense responses in three potato varieties with different levels of reaction to the late blight disease caused by Phytophthora infestans were analyzed after inoculation with the pathogen. In the resistant cv. Pastusa Suprema, increased intensity of H2O2 and callose deposit accumulation was observed beginning at 24 hours after inoculation, followed by a hypersensitive response at the inoculation points. In the moderately resistant cv. Diacol-Monserrate, the same responses were observed as in the resistant variety, but with less intensity over time. For the susceptible cv. Diacol-Capiro, the responses observed occurred later than in the other two varieties, subsequent to the advance of the pathogen over extensive necrotic areas. These results suggest that early, intense peroxide and callose accumulation and a hypersensitive response are associated with the observed resistance of the cv. Pastusa Suprema and cv. Diacol-Monserrate to P. infestans.
CONFLICT OF INTEREST
The authors have declared that no conflict of interests exist.
FUNDING
This research was funded by Universidad Nacional de Colombia sede Medellín and Politécnico Colombiano Jaime Isaza Cadavid project code 2061080206. The experiments complied with the current laws of Colombia where they were performed.
 
REFERENCES (60)
1.
Andreu A.B., Guevara M.G., Wolski E.A., Daleo G.R., Caldiz D.O. 2006. Enhancement of natural disease resistance in potatoes by chemicals. Pest Management Science 62 (2): 162−170. DOI: https://doi.org/10.1002/ps.114....
 
2.
Avrova A.O., Boevink P.C., Young V., Grenville-Briggs L., Van West P., Birch P.J.R., Whisson S. 2008. A novel Phytophthora infestans haustorium-pecific membrane protein is required for infection of potato. Cellular Microbiology 10 (11): 2271−2284. DOI: https://doi.org/10.1111/j.1462....
 
3.
Balmer D., Flors V., Glauser G., Mauch-Mani B. 2013. Metabolomics of cereals under biotic stress: current knowledge and techniques. Frontiers in Plant Science 4 (82): 1−12. DOI: https://doi.org/10.3389/fpls.2....
 
4.
Basavaraju P., Shetty N., Shetty H., De Neergaard E., Jørgensen H. 2009. Infection biology and defence responses in sorghum against Colletotrichum sublineolum. Journal of Applied Microbiology 107 (2): 404−415. DOI: https://doi.org/10.1111/j.1365....
 
5.
Bhadauria V., Miraz P., Kennedy R., Banniza S., Wei Y. 2010. Dual trypan-aniline blue fluorescence staining methods for studying fungus-plant interactions. Biotechnology & Histochemistry 85 (2): 99−105. DOI: 10.1080/10520290903132196.
 
6.
Boller T., Felix G. 2009. A Renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annual Review in Plant Biology 60 (1): 379−406. DOI: https://doi.org/10.1146/annure....
 
7.
Bolton M.D. 2009. Primary metabolism and plant defense-fuel for the fire. Molecular Plant-Microbe Interactions 22 (5): 487−497. DOI: https://doi.org/10.1094/MPMI-2....
 
8.
Boyd L.A., Ridout C., O’Sullivan D.M., Leach J.E., Leung H. 2013. Plant–pathogen interactions: disease resistance in modern agriculture. Trends in Genetics 29 (4): 233−240. DOI: https://doi.org/10.1016/j.tig.....
 
9.
Buchanan B.B., Gruissem W., Jones R. 2000. Biochemistry and Molecular Biology of Plants. Wiley, Blackwell, American Society of Plant Physiologists, Rockville, USA, 1280 pp.
 
10.
Camire M.E., Kubow S., Donnelly D. 2009. Potatoes and human health. Food Science and Nutrition 49 (10): 823−840. DOI: https://doi.org/10.1080/104083....
 
11.
Cardenas M., Grajales A., Sierra R., Rojas A., Gonzalez-Almario A., Vargas A., Marin M., Fermin G., Lagos L., Grunwald N., Bernal A., Salazar C., Restrepo S. 2011. Genetic diversity of Phytophthora infestans in the Northern Andean region. BMC Genetics 12 (1): 23. DOI: https://doi.org/10.1186/1471-2....
 
12.
Cavalcante M., Escoute J., Madeira J., Romero R., Nicole M., Oliveira L., Hamelin C., Lartaud M., Verdeil J. 2011. Reactive oxygen species and cellular interactions between Mycosphaerella fijiensis and banana. Tropical Plant Biology 4 (2): 134−143. DOI: https://doi.org/10.1007/s12042....
 
13.
Chapman A. 2012. The Changing Phytophthora Infestans population: Implications for late blight epidemics and control. Doctoral thesis. College of Life Sciences, University of Dundee, Dundee, Scotland, United Kingdom.
 
14.
Chen Y., Halterman D. 2010. Phenotypic characterization of potato late blight resistance mediated by the broad-spectrum resistance gene RB. Phytopathology 101 (2): 263−270. DOI: https://doi.org/10.1094/PHYTO-....
 
15.
Coffey M., Gees R. 1991. Phytophthora infestans, the cause late blight of potato: the cytology of development. Advances in Plant Pathology 7: 31−51.
 
16.
Coffey M.D., Gees R. 1991. The cytology of development. p. 31−51. In: “Phytophthora infestans, the Cause of Late Blight of Potato. Advances in Plant Pathology”. Vol. 7 (D. Ingram, P. Williams, eds.). Academic Press, London, UK, 284 pp.
 
17.
De Vleesschauwer D., Van Buyten E., Satoh K., Balidion J., Mauleon R., Choi I., Vera-Cruz C., Kikuchi S., Höfte M. 2012. Brassinosteroids antagonize gibberellin- and salicylate-mediated root immunity in rice. Plant Physiology 158 (4): 1833−1846. DOI: https://doi.org/10.1104/pp.112....
 
18.
Doke N. 2005. A strategy to enhance disease resistance of potato using the mechanism of the hypersensitive reaction against potato late blight. Journal of General Plant Pathology 71 (6): 444−447. DOI: https://doi.org/10.1007/s10327....
 
19.
Estrada-Ramos N., Pérez-Montenegro E., Heidrick L. 1959. Diacol monserrate: a new potato variety. Bogotá: República de Colombia, Ministerio de Agricultura, Oficina de Investigaciones Especiales. D.I.A. boletín divulgativo 6: 9–20 (in Spanish).
 
20.
Friend J. 1991. The biochemistry and cell biology of interaction. p. 85−129. In: "Phytophthora infestans, the Cause of Late Blight of Potato. Advances in Plant Pathology”. Vol. 7 (D. Ingram, P. Williams, eds.). Academic Press, London, UK, 284 pp.
 
21.
García-Brugger A., Lamotte O., Vandelle E., Bourque S., Lecourieux D., Poinssot B., Wendehenne D., Pugin A. 2006. Early signaling events induced by elicitors of plant defenses. Molecular Plant-Microbe Interactions 19 (7): 711−724. DOI: https://doi.org/10.1094/MPMI-1....
 
22.
Ge Y., Bi Y., Guest D. 2013. Defence responses in leaves of resistant and susceptible melon (Cucumis melo L.) cultivars infected with Colletotrichum lagenarium. Physiological and Molecular Plant Pathology 81: 13−21. DOI: https://doi.org/10.1016/j.pmpp....
 
23.
Gees R., Hohl H. 1988. Cytological comparison of specific (R3) and general resistance to late blight in potato leaf tissue. Phytopathology 78 (3): 350−357.
 
24.
Govers F., Drenth A., Pieterse C. 1997. The potato late blight pathogen Phytophthora infestans and other pathogenic oomycota. In: “Plant Relationships. Part B, 5B. The Mycota” (G. Carroll, P. Tudzynski P., eds.). Springer-Verlag, Berlin, Germany. DOI: https://doi.org/10.1007/978-3-....
 
25.
Gómez S., Castañeda S., Morales J. 2019. Media preferences, micro-morphometric analysis, and cardinal growth temperature determination for Phytophthora infestans sensu lato isolated from different hosts in Colombia. Brazilian Journal of Biology. Ahead of print. 1−13. DOI: https://doi.org/10.1590/1519-6....
 
26.
Guzmán N. 1964. Nature of partial resistance of certain clones of three Solanum species to Phytophthora infestans. Phytopathology 54: 1398–1404.
 
27.
Guzmán J., Thurston H., Heidrick L. 1960. Results on the nature of the partial resistance of three clones of potato to Phytophthora infestans (Mont.) de Bary. (Mont) De Bary. Agricultura Tropical 16 (2): 89−99.
 
28.
Hao X., Yu K., Ma Q., Song X., Li H., Wang M. 2011. Histochemical studies on the accumulation of H2O2 and hypersensitive cell death in the nonhost resistance of pepper against Blumeria graminis f. sp. tritici. Physiological and Molecular Plant Pathology 76 (2): 104−111. DOI: https://doi.org/10.1016/j.pmpp....
 
29.
Hohl H., Stössel P. 1976. Host-parasite interfaces in a resistant and a susceptible cultivar of Solanum tuberosum inoculated with Phytophthora infestans: tuber tissue. Canadian Journal of Botany 54 (9): 900−912. DOI: https://doi.org/10.1139/b76-09....
 
30.
Hohl H., Suter E. 1976. Host–parasite interfaces in a resistant and a susceptible cultivar of Solanum tuberosum inoculated with Phytophthora infestans: leaf tissue. Canadian Journal of Botany 54 (16): 1956−1970. DOI: https://doi.org/10.1139/b76-20....
 
31.
Jindřichová B., Fodor J., Šindelářová M., Burketová L., Valentová O. 2011. Role of hydrogen peroxide and antioxidant enzymes in the interaction between a hemibiotrophic fungal pathogen, Leptosphaeria maculans, and oilseed rape. Environmental and Experimental Botany 72 (2): 149−156. DOI: https://doi.org/10.1016/j.enve....
 
32.
Kamoun S., Smart C. 2005. Late blight of potato and tomato in the genomics era. Plant Disease 89 (7): 692−699. DOI: http://dx.doi.org/10.1094/PD-8....
 
33.
Korgan S., Wolski E., Cicore P., Suarez P., Capezio S., Huarte M., Andreu A. 2011. Solanum tarijense reaction to Phytophthora infestans and the role of plant defence molecules. Plant Breeding 130 (2): 231−236. DOI: https://doi.org/10.1111/j.1439....
 
34.
Kotchoni S., Gachomo E. 2006. The reactive oxygen species network pathways: an essential prerequisite for perception of pathogen attack and the acquired disease resistance in plants. Journal of Bioscience 31 (3): 389−404. DOI: https://doi.org/10.1007/BF0270....
 
35.
Lambert C., Khiook I., Lucas S., Télef-Micouleau N., Mérillon J., Cluzet S. 2013. A faster and a stronger defense response: one of the key elements in grapevine explaining its lower level of susceptibility to esca? Phytopathology 103 (10): 1028−1034. DOI: https://doi.org/10.1094/PHYTO-....
 
36.
Luna E., Pastor V., Robert J., Flors V., Mauch-Mani V., Ton J. 2010. Callose deposition: a multifaceted plant defense response. Molecular Plant-Microbe Interactions 24 (2): 183−193. DOI: https://doi.org/10.1094/MPMI-0....
 
37.
Marone D., Russo M., Laidò G., De Leonardis A., Mastrangelo A. 2013. Plant nucleotide binding site-leucine-rich repeat (NBS-LRR) genes: active guardians in host defense responses. International Journal of Molecular Science 14 (4): 7302−7326. DOI: https://doi.org/10.3390/ijms14....
 
38.
McCann H., Nahal H., Thakur S., Guttman D. 2012. Identification of innate immunity elicitors using molecular signatures of natural selection. Proceedings of the National Academy of Sciences USA, PNAS 109 (11): 4215−4220. DOI: https://doi.org/10.1073/pnas.1....
 
39.
Michelmore R., Christopoulou M., Caldwell K. 2013. Impacts of resistance gene genetics, function, and evolution on a durable future. Annual Review of Phytopathology 51: 291−319. DOI: https://doi.org/10.1146/annure....
 
40.
Morel J., Dangl J. 1997. The hypersensitive response and the induction of cell death in plants. Cell Death Differentiation 4 (8): 671−683. DOI: https://doi.org/10.1038/sj.cdd....
 
41.
Ñústez C. 2011. Colombian varieties of potato. Facultad de Agronomía, Universidad Nacional de Colombia, Bogotá, D.C., Colombia, 46 pp. (in Spanish).
 
42.
Oyarzún P., Yánez J., Forbes G. 2004. Evidence for host mediation of preinfection stages of Phytophthora infestans on the leaf surface of Solanum phureja. Journal of Phytopathology 152: 651−657. DOI: https://doi.org/10.1111/j.1439....
 
43.
Palavan-Unsal N., Buyuktuncer E., Tufekci M. 2005. Programmed cell death in plants. Journal of Cell and Molecular Biology 4: 9−23.
 
44.
Pieterse C., Derksen A., Folders J., Govers F. 1994. Expression of the Phytophthora infestans ipiB and ipi0 genes in planta and in vitro. Molecular and General Genetics MGG 244 (3): 269−277. DOI: https://doi.org/10.1007/BF0028....
 
45.
Piršelová B., Matušíková I. 2013. Callose: the plant cell wall polysaccharide with multiple biological functions. Acta Physiologiae Plantarum 35 (3): 635−644. DOI: https://doi.org/10.1007/s11738....
 
46.
Pristou R., Gallegly M. 1956. Differential reaction of potato hosts to foreign and domestic potato physiologic races of Phytophthora infestans. American Potato Journal 33 (10): 287−295. DOI: https://doi.org/10.1007/BF0287....
 
47.
Ramos N. 2000. Biodiversity on the Genetic Potato Breeding. La Paz, Bolivia, 372 pp.
 
48.
Rodríguez H., Rodríguez-Arango E., Morales J., Kema G., Arango R. 2016. Defense gene expression associated with the biotrophic phase of Mycosphaerella fijiensis M. Morelet infection in banana. Plant Disease 100: 1170−1175. DOI: https://doi.org/10.1094/PDIS-0....
 
49.
Segura M., Marcela S., Ñústez C. 2006. Phenological development of four potato varieties (Solanum tuberosum L.) in the municipality of Zipaquira (Cundinamarca). Fitotecnia Colombiana 6 (2): 33−43. (in Spanish).
 
50.
Shimony C., Friend J. 1975. Ultrastructure of the interaction between Phytophthora infestans and leaves of two cultivars of potato (Solanum tuberosum L.) Orion and Majestic. New Phytologist 74 (1): 59−65. DOI: https://doi.org/10.1111/j.1469....
 
51.
Thurston D., Heidrick L., Guzmán J. 1962. Partial resistance to Phytophthora infestans (Mont.) de Bary within the Coleccion Central Colombiana. American Potato Journal 39 (2): 63−69. DOI: https://doi.org/10.1007/BF0286....
 
52.
Torres J., Calderón H., Rodríguez-Arango E., Morales J., Arango R. 2012. Differential induction of pathogenesis-related proteins in banana in response to Mycosphaerella fijiensis infection. European Journal of Plant Pathology 133 (4): 887−898. DOI: https://doi.org/10.1007/s10658....
 
53.
Vleeshouwers V., van Dooijeweert W., Govers F., Kamoun S., Colon L. 2000. The hypersensitive response is associated with host and nonhost resistance to Phytophthora infestans. Planta 210 (6): 853−864. DOI: https://doi.org/10.1007/s00425....
 
54.
Voigt C., Somerville S. 2009. Callose in biotic stress (pathogenesis) biology, biochemistry and molecular biology of callose in plant defence: callose deposition and turnover in plant-pathogen interactions. p. 525−562. In: "Chemistry, Biochemistry, and Biology of 1–3 Beta Glucans and Related Polysaccharides" (A. Bacic, G. Fincher, B. Stone, eds.). Elsevier, Oxford, UK, 350 pp. DOI: https://doi.org/10.1016/B978-0....
 
55.
Wang B., Liu J., Tian Z., Song B., Xie C. 2005. Monitoring the expression patterns of potato genes associated with quantitative resistance to late blight during Phytophthora infestans infection using cDNA microarrays. Plant Science 169 (6): 1155−1167. DOI: https://doi.org/10.1016/j.plan....
 
56.
Weigel D., Glazebrook J. 2002. Arabidopsis. A Laboratory Manual. CSHL Press, New York, USA, 354 pp.
 
57.
Wu G., Shortt B., Lawrence E., Levine E., Fitzsimmons K., Shah D. 1995. Disease resistance conferred by expression of a gene encoding H2O2-enerating glucose oxidase in transgenic potato plants. Plant Cell 7 (9): 1357−1368. DOI: https://doi.org/10.1105/tpc.7.....
 
58.
Xiao C., Gao J., Zhang Y., Wang Z., Zhang D., Chen Q., Ye X., Xu Y., Yang G., Yan L., Cheng Q., Chen J., Shen Y. 2019. Quantitative proteomics of potato leaves infected with Phytophthora infestans provides insights into coordinated and altered protein expression during early and late disease stages. International Journal of Molecular Science 20: 136. DOI: https://doi.org/10.3390/ijms20....
 
59.
Yakimova E., Yordanova Z., Slavov S., Kapchina-Toteva M., Woltering E. 2009. Alternaria alternata AT toxin induces programmed cell death in tobacco. Journal of Phytopathology 157 (10): 592−601. DOI: https://doi.org/10.1111/j.1439....
 
60.
Zhang L., Yang J., Li T., Yao Y., Zhang H. 2001. Late blight resistant transgenic potato expressing glucose oxidase gene. Journal of Agricultural University Hebei 2: 59−64.
 
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