Biorational control alternatives on Phytophthora infestans, phytopathogen causing gout in potatoes.

Alternativas de control biorracionales sobre Phytophthora infestans, fitopatógeno causante de la gota en papa.

The drop of the potato or late blight is one of the most aggressive diseases that attack the potato crops and in a short time destroys them, causing great economic losses, it is produced by the phytopathogen Phytophthora infestans, oomyceto that has taken great importance due to its devastating effects and difficulties in achieving its eradication. Fungicides of a chemical nature represent a problem due to the affected use, which makes it very difficult to eliminate the disease due to the appearance of new resistant species. There are new alternatives for its control, based on the use of substances of the plant nature, and the application of new specific tools to perform gene editing, reprogram or eliminate DNA / RNA sequences, thus favoring the obtaining of cultures free of toxic substances . In this review, specific biocontrol methods are presented, such as essential oils, microbial metabolites, molecular tools and the use of biodegradable substances that favor the management and prevention of pests, which help mitigate the environmental problems generated by the use of fungicides from chemical nature.

1. Reinhardt D, Sharma A. Methods in Rhizosphere Biology Research. Series ISSN 2523-8442. Singapore: Springer Singapore; 2019. Available from: https://www.springer.com/gp/book/9789811357664 [Accessed 06 June 2019]
2. Rezzonico F, Rupp O, Fahrentrapp J. Pathogen recognition in compatible plant-microbe interactions. Scientific Reports. 2017; 7, 6383. Available from: https://doi.org/10.1038/s41598-017-04792-5
3. Wang XW, Guo LY, Han M, Shan K. Diversity, evolution and expression profiles of histone acetyltransferases and deacetylases in oomycetes. BMC Genomics. 2016 ; 17(1): 927. Available from: https://doi.org/10.1186/s12864-016-3285-y
4. De Vrieze M, Germanier F, Vuille N, Weisskopf L. Combining Different Potato-Associated Pseudomonas Strains for Improved Biocontrol of Phytophthora infestans. Frontiers in Microbiology. 2018; 9: 2573. Available from: https://doi.org/10.3389/fmicb.2018.02573
5. Ortiz V, Phelan S, Mullins E. A temporal assessment of nematode community structure and diversity in the rhizosphere of cisgenic Phytophthora infestans-resistant potatoes. BMC Ecology. 2016 ; 16(1): 55. Available from: https://doi.org/10.1186/s12898-016-0109-5
6. Cai G, Fry WE, Hillman BI. PiRV-2 stimulates sporulation in Phytophthora infestans. Virus research. 2019 ; 271. Available from: https://doi.org/10.1016/j.virusres.2019.197674
7. Garcia PG, dos Santos FN, Zanotta S, Eberlin MN, Carazzone C. Metabolomics of Solanum lycopersicum Infected with Phytophthora infestans Leads to Early Detection of Late Blight in Asymptomatic Plants. Molecules. 2018; 23(12): 3330.Available from: https://doi.org/10.3390/molecules23123330
8. Leesutthiphonchai W, Vu AL, Ah-Fong AM v, Judelson HS. How Does Phytophthora infestans Evade Control Efforts? Modern Insight Into the Late Blight Disease. Phytopathology. 2018; 108(8): 916–924. Available from: https://doi:10.1094/PHYTO-04-18-0130-IA
9. Zhan F, Wang T, Iradukunda L, Zhan J. A gold nanoparticle-based lateral flow biosensor for sensitive visual detection of the potato late blight pathogen, Phytophthora infestans. Analytica Chimica Acta. 2018; 1036:153–161. Available from: https://doi.org/10.1016/j.aca.2018.06.083
10. Ostos Ortíz O, Rosas Arango S, González Devia J. Aplicaciones biotecnológicas de los microorganismos. NOVA. 2019 ;17(31):129-63. Available from: https://revistas.unicolmayor.edu.co/index.php/nova/article/view/950 [Accessed 12 sep.2020]
11. García-Bayona L, Garavito MF, Lozano GL, Vasquez JJ, Myers K, Fry WE, et al. De novo pyrimidine biosynthesis in the oomycete plant pathogen Phytophthora infestans. Gene. 2014; 537(2): 312–321. Available from: https://doi:10.1016/j.gene.2013.12.009
12. Chung I-M, Venkidasamy B, Upadhyaya CP, Packiaraj G, Rajakumar G, Thiruvengadam M. Alleviation of Phytophthora infestans Mediated Necrotic Stress in the Transgenic Potato (Solanum tuberosum L.) with Enhanced Ascorbic acid Accumulation. Plants. 2019; 8(10): 365. Available from: https://doi:10.3390/plants8100365
13. Garavito M, Narvaez H, Pulido D, Löffler M, Judelson H, Restrepo S et al. Phytophthora infestans Dihydroorotate Dehydrogenase Is a Potential Target for Chemical Control – A Comparison With the Enzyme From Solanum tuberosum. Frontiers in Microbiology. 2019; 10:1479. Available from: https://doi.org/10.3389/fmicb.2019.01479
14. Zhang S, Zheng X, Reiter RJ, Feng S, Wang Y, Liu S, et al. Melatonin attenuates potato late blight by disrupting cell growth, stress tolerance, fungicide susceptibility and homeostasis of gene expression in Phytophthora infestans. Frontiers in Plant Science. 2017 ; 8: 1993. Available from: https://doi:10.3389/fpls.2017.01993
15. Bedoya, O., Benavides, A., Daza, D. and Chazatar, L. Actividad inhibitoria del aceite esencial de Lippia origanoides H.B.K sobre el crecimiento de Phytophthora infestans. Acta Agronómica. 2014; 64 (2):116-124 . Available from: http://dx.doi.org/10.15446/acag.v64n2.42964.
16. Matusinsky P, Zouhar M, Pavela R, Novy P. Antifungal effect of five essential oils against important pathogenic fungi of cereals. Industrial Crops and Products. 2015; 1; 67:208–15. Available from: https://doi.org/10.1016/j.indcrop.2015.01.022
17. Carillo Y, Gomez M, Potes J, Ñustez C.Efecto de algunos aceites esenciales sobre el crecimiento de Phytophthora infestans (Mont.) de Bary en condiciones de laboratorio.Agronomía Colombiana. 2010; 38 (2):245-253 Available from: http://www.scielo.org.co/pdf/agc/v28n2/v28n2a14.pdf [cited 9 June 2019]
18. Portz D, Koch E, Slusarenko A. Effects of garlic (Allium sativum) juice containing allicin on Phytophthora infestans and downy mildew of cucumber caused by Pseudoperonospora cubensis. European Journal of Plant Pathology. 2008; 122 :197–206. Available from: https://doi.org/10.1007/s10658-008-9334-x
19. Alvarez S D, Salazar G C, Hurtado B A, Delgado B D, Arango B O. In vitro sensitivity of Phytophthora Infestans to fique extract (Furcraea gigantea vent.) and systemic fungicides. Biotecnología en el Sector Agropecuario y Agroindustrial. 2011; 9 (2) :96-104. Available from: http://www.scielo.org.co/scielo.php?script=sci_arttext&pid=S1692-35612011000200011&lng=en&nrm=iso [cited 11 June 2019]
20. Solarte RD, Osorio O. Evaluación de la concentración del jugo de fique (Furcraea spp) para el control in vitro de Phytophthora infestans en plantas de papa (Solanum tuberosum L). Información Tecnológica. 2014 ;25(5):47–54 Available from: http://dx.doi.org/10.4067/S0718-07642014000500008
21. Otero I, Hurtado A, Arango O, Fernández P, Martinez F, Parra Z. Bacterias aisladas del jugo de fique con actividad antagónica sobre Phytophthora infestans (mont.) de bary. Biotecnología en el Sector Agropecuario y Agroindustrial.2014; 12(1): 28-35. Available from: http://www.scielo.org.co/scielo.php?script=sci_arttext&pid=S1692-35612014000100004&lng=en&nrm=iso [Accessed 11June 2019]
22. Bacalla K. Actividad antimicrobiana in vitro de dos aceites esenciales contra Phytophthora infestans en Chachapoyas, Amazonas, 2018. Universidad Nacional Toribio Rodríguez de Mendoza - UNTRM [Internet]. 2019; Available from: http://repositorio.untrm.edu.pe/handle/UNTRM/1697 [Accessed 13 June 2019]
23. Andrade G, García A, Cervantes L, Aíl C, Borboa J, Rueda E. Estudio del potencial biocontrolador de las plantas autóctonas de la zona árida del noroeste de México: control de fitopatógenos. Revista de la Facultad de Ciencias Agrarias [Internet]. 2017;49(1):127–42. Available from: https://www.redalyc.org/articulo.oa?id=382852189011 [Accessed 15 June 2019]
24. Thanh V, Bui L, Bach L, Nguyen N, Le Thi H, Thi T. Origanum majorana L. essential oil-associated polymeric nano dendrimer for antifungal activity against Phytophthora infestans. Materials. 2019;12(9). Available from: https://doi:10.3390/ma12091446.
25. Andrango A, Espinoza S. Uso de extractos de penco azul (agave americana) y hongos de sombrero (estrobilurus tenacellus) como preventivos del tizón tardío (phytophthora infestans) en el cultivo de papa (solanum tuberosum) variedad chaucha amarilla. 2017; Available from: https://repositorio.uta.edu.ec:8443/jspui/handle/123456789/26385 [Accessed 15 June 2019]
26. Oshchepkova Y, Veshkurova O, Salikhov S, Zaitsev D, Smirnov A, Egorov T, et al. Comparative analysis of extracts of Nigella sativa exhibiting antifungal activity against the Oomycete Phytophthora infestans. Chemistry of Natural Compounds. 2013;49(5):985–987. Available from: https://doi.org/10.1007/s10600-013-0803-x
27. Quintanilla P, Rohloff J, Iversen T. Influence of essential oils on Phytophthora infestans. Potato Research. 2002;45(2–4):225–35. Available from: https://doi.org/10.1007/BF02736117
28. Soylu E, Soylu S, Kurt S. Antimicrobial Activities of the Essential Oils of Various Plants against Tomato Late Blight Disease Agent Phytophthora infestans. Mycopathologia. 2006;161(2):119-128. Available from: doi:10.1007/s11046-005-0206-z
29. De Vrieze M, Gloor R, Massana Codina J, Torriani S, Gindro K, L’Haridon F, et al. Biocontrol Activity of Three Pseudomonas in a Newly Assembled Collection of Phytophthora infestans Isolates. Phytopathology. 2019; 109(9):1555–1565. Available from: https://doi:10.1094/PHYTO-12-18-0487-R
30. Benítez S, Bentley J, Bustamante P, Sánchez L, Corrales L. Aislamiento de los microorganismos cultivables de la rizosfera de Ornithogalum umbellatum y evaluación del posible efecto biocontrolador en dos patógenos del suelo. NOVA.2007;5(8). Available from: https://revistas.unicolmayor.edu.co/index.php/nova/article/view/212. [Accessed 13 Sep 2020]
31. Morrison CK, Arseneault T, Novinscak A, Filion M. Phenazine-1-carboxylic acid production by Pseudomonas fluorescens LBUM636 alters Phytophthora infestans growth and late blight development. Phytopathology. 2017; 107(3):273-279. Available from: https://doi:10.1094/PHYTO-06-16-0247-R.
32. Hunziker L, Bönisch D, Groenhagen U, Bailly A, Schulz S, Weisskopf L. Pseudomonas Strains Naturally Associated with Potato Plants Produce Volatiles with High Potential for Inhibition of Phytophthora infestans. Applied and Environmental Microbiology. 2015 81(3):821-30. Available from: https://doi:10.1128/AEM.02999-14
33. Tomar S, Singh BP, Lal M, Ma K, Hussain T, Sharma S, et al. Screening of novel microorganisms for biosurfactant and biocontrol activity against Phytophthora infestans. Journal of environmental biology. 2014; 35(5):893–899. Available from: https://pubmed.ncbi.nlm.nih.gov/25204064/ [Accessed 4 July 2019]
34. De Vrieze M, Pandey P, Bucheli TD, Varadarajan AR, Ahrens CH, Weisskopf L, et al. Volatile organic compounds from native potato-associated Pseudomonas as potential anti-oomycete agents. Frontiers in Microbiology. 2015; 6: 1295.Available from: https://doi.org/10.3389/fmicb.2015.01295
35. Fonseca Y, Castellanos D, León T. Efecto Antagónico in vitro de Actinomicetos Aislados de Purines de Chipaca (Bidens pilosa L.) Frente a Phytophthora infestans (Mont) de Bary. Revista Facultad Nacional de Agronomía Medellín. 2011;64 (2):6111-6119. Available from: https://www.redalyc.org/pdf/1799/179922664008.pdf [Accessed 7 July 2019]
36. Bóka B, Manczinger L, Kocsubé S, Shine K, Alharbi NS, Khaled JM, et al. Genome analysis of a Bacillus subtilis strain reveals genetic mutations determining biocontrol properties. World Journal of Microbiology and Biotechnology. 2019; 35(3): 52. Available from: https://doi.org/10.1007/s11274-019-2625-x
37. Castañeda Alvarez E, Sánchez LC. Evaluación del crecimiento de cuatro especies del género Bacillus sp., primer paso para entender su efecto biocontrolador sobre Fusarium sp. NOVA. 2016;14(26):53-5. Available from: https://revistas.unicolmayor.edu.co/index.php/nova/article/view/517 [Accessed 12 sep 2020]
38. Layton et al. C. Bacillus spp.; perspectiva de su efecto biocontrolador mediante antibiosis en cultivos afectados por fitopatógenos. NOVA. 2011 ;9(16). Available from: https://revistas.unicolmayor.edu.co/index.php/nova/article/view/185 [Accessed 12 sep.2020]
39. Bailly A, Weisskopf L. Mining the volatilomes of plant-associated microbiota for new biocontrol solutions. Frontiers in Microbiology. 2017;8:1638. Available from: https://doi.org/10.3389/fmicb.2017.01638
40. Thomas C, Mabon R, Andrivon D, Val F. The Effectiveness of Induced Defense Responses in a Susceptible Potato Genotype Depends on the Growth Rate of Phytophthora infestans. Molecular plant-microbe interactions : 2019; 32(1): 76–85. Available from: https://doi:10.1094/MPMI-03-18-0064-R
41. Dahlin P, Müller MC, Ekengren S, McKee LS, Bulone V. The impact of steroidal glycoalkaloids on the physiology of Phytophthora infestans, the causative agent of potato late blight. Molecular Plant-Microbe Interactions. 2017 ; 30(7): 531–542. Available from: https://doi:10.1094/MPMI-09-16-0186-R
42. Wang Y, Zhang C, Wu L, Wang L, Gao W, Jiang J et al. Inhibitory effect of Bacillus subtilis WL-2 and its IturinA lipopeptides against Phytophthora infestans. bioRxiv. 2019. Available from: https://doi.org/10.1101/751131
43. Tomada S, Sonego P, Moretto M, Engelen K, Pertot I, Perazzolli M, et al. Dual RNA-Seq of Lysobacter capsici AZ78 – Phytophthora infestans interaction shows the implementation of attack strategies by the bacterium and unsuccessful Oomycete defense responses. Environmental Microbiology. 2017;19(10):4113–4125. Available from: doi:10.1111/1462-2920.13861
44. Lazazzara V, Perazzolli M, Pertot I, Biasioli F, Puopolo G, Cappellin L. Growth media affect the volatilome and antimicrobial activity against Phytophthora infestans in four Lysobacter type strains. Microbiological Research. 2017; 201:52–62. Available from: https://doi.org/10.1016/j.micres.2017.04.015
45. Van de Wouw A, Idnurm A. Biotechnological potential of engineering pathogen effector proteins for use in plant disease management. Microbial Engineering Biotechnologies. 2019; 37 (6) Available from: https://doi.org/10.1016/j.biotechadv.2019.04.009
46. Goulin E, Manzano D, Moreira L, Emy E, Durigan R, Machado M. RNA interference and CRISPR: Promising approaches to better understand and control citrus pathogens.Microbiological Research. 2019; 226:1-9. Available from: https://www.sciencedirect.com/science/article/pii/S0944501318311704 [Accessed 9 July 2019]
47. Hernández M. CRISPR/Cas: aplicaciones y perspectivas para el mejoramiento genético de plantas. Biotecnología Vegetal.2018;18 (3):135 - 149. Available from: https://revista.ibp.co.cu/index.php/BV/article/view/585 [Accessed 8 July 2019]
48. Van den Hoogen J, Govers F. Attempts to implement CRISPR/Cas9 for genome editing in the oomycete Phytophthora infestans. bioRxiv. 2019. Available from: https://doi.org/10.1101/274829
49. Jahan SN, Åsman AKM, Corcoran P, Fogelqvist J, Vetukuri RR, Dixelius C. Plant-mediated gene silencing restricts growth of the potato late blight pathogen Phytophthora infestans. Journal of Experimental Botany. 2015; 66(9): 2785–2794. Available from: doi:10.1093/jxb/erv094
50. Bhimanagoud Kumbar, Riaz Mahmood, S.N. Nagesha, M.S. Nagaraja, D.G. Prashant, Ondara Zablon Kerima, Arti Karosiya, Mohan Chavan. Field application of Bacillus subtilis isolates for controlling late blight disease of potato caused by Phytophthora infestans. Biocatalysis and Agricultural Biotechnology. 2019;22:101366 Available from: https://doi.org/10.1016/j.bcab.2019.101366
51. Schepers H, Kessel G, Lucca F, Förch M, van den Bosch v, Topper C et al. Reduced efficacy of fluazinam against Phytophthora infestans in the Netherlands. European Journal of Plant Pathology. 2018;151:947–960. Available from: https://doi.org/10.1007/s10658-018-1430-y
52. Nechwatal J, Zellner M. Potential suitability of various leaf treatment products as copper substitutes for the control of late blight (Phytophthora infestans) in organic potato farming.Potato Research. 2015;58 :261–276. Available from: https://doi.org/10.1007/s11540-015-9302-8
53. Fukamachi K, Konishi Y, Nomura T. Disease control of Phytophthora infestans using cyazofamid encapsulated in poly lactic-co-glycolic acid (PLGA) nanoparticles. Colloids and Surfaces A: Physicochemical and Engineering Aspects. 2019; 577:315-322. Available from: https://doi.org/10.1016/j.colsurfa.2019.05.077
54. Tomar S, Lal M, Khan M, Singh B, Sharma S. Characterization of glycolipid biosurfactant from Pseudomonas aeruginosa PA 1 and its efficacy against Phytophthora infestans].Journal of Environmental Biology. 2019;40(4): 725-730.Available from: http://doi.org/10.22438/jeb/40/4/MRN-910