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Phytophthora capsici: the diseases it causes and management strategies to produce healthier vegetable crops

Phytophthora capsici: as doenças que causa e estratégias de manejo para produzir hortaliças mais saudáveis

ABSTRACT

Vegetable crops are exposed to constant infection by numerous diseases, including those caused by the oomycete Phytophthora capsici. This microorganism is a polyphagous plant pathogen, capable of infecting dozens of plant species, including cultivated plants and weeds. The aim of this review is to address topics related to etiology and symptoms of the diseases caused by this oomycete (leaf blight, root rot, crown rot and fruit rot), as well as the integration and application of different control alternatives, such as genetics, cultural, physical, biological, and chemical. Crops such as sweet pepper (Capsicum annuum), chili pepper (Capsicum spp.), tomato (Solanum lycopersicum), eggplant (S. melongena), cucurbits (Cucumis sativus, Cucurbita spp.), among others, are subject to considerable economic losses induced by this pathogen. High soil humidity, high temperatures, resistance structures of the pathogen (oospores), scarce availability of resistant cultivars and a reduced range of effective fungicides are conditions that difficult the management of diseases caused by P. capsici in the field. Despite the irrefutable importance of this pathogen, the existing information regarding its integrated management is limited. Therefore, a successful management will depend to a great extent on its knowledge and its control. Thus, the joint application of different control strategies seeks to maintain the pathogen at low population levels and also keeping the epidemics under the threshold of economic loss. At the end, an integrated pest management approach for P. capsici could result in higher economic returns, long-term sustainable harvests, reduction of the environment impact and better quality products for consumers.

Keywords:
Solanaceae; Cucurbitaceae; integrated disease management; oomycete; soil borne pathogen

RESUMO

As hortaliças estão expostas a constantes infecções por inúmeras doenças, incluindo as causadas pelo oomiceto Phytophthora capsici. Este microrganismo é um patógeno vegetal polífago, capaz de infectar dezenas de espécies de plantas cultivadas ou invasoras. O objetivo desta revisão é abordar tópicos relacionados à etiologia e sintomas das doenças causadas por este oomiceto (queima de folhas, podridão da raiz, podridão da coroa e podridão dos frutos), bem como também a integração e aplicação de diferentes alternativas de controle como genética, cultural, física, biológica e química. É assim que, culturas como pimentão (Capsicum annuum), pimenta (Capsicum spp.), tomate (Solanum lycopersicum), berinjela (S. melongena), cucurbitáceas (Cucumis sativus, Cucurbita spp.), entre outras, estão sujeitas a perdas econômicas consideráveis. Elevada umidade do solo, altas temperaturas, estruturas de resistência do patógeno (oósporos), baixa disponibilidade de cultivares resistentes e reduzida disponibilidade de fungicidas eficazes são condições que dificultam o manejo de doenças causadas por P. capsici no campo. Apesar da importância irrefutável deste patógeno, as informações existentes sobre seu manejo integrado são limitadas. Portanto, uma gestão bem sucedida das lavouras dependerá em grande parte de seu conhecimento e controle. Assim, a aplicação conjunta de diferentes estratégias de controle visa manter o patógeno em níveis populacionais baixos e também manter a epidemia sob o limiar de danos econômicos. No final, um manejo integrado para P. capsici poderá gerar maiores retornos econômicos, colheitas sustentáveis de longo prazo, redução do impacto ambiental e produtos de melhor qualidade para os consumidores.

Palavras-chave:
Solanaceae; Cucurbitaceae; manejo integrado de doenças; oomiceto; patógeno transmitido pelo solo

The plant pathogen Phytophthora capsici is a highly destructive oomycete, causing various symptoms such as root, stem, fruit and crown rot in vegetables, mainly in the Solanaceae and Cucurbitaceae families (Dunn et al., 2014DUNN, AR; LANGE, HW; SMART, CD. 2014. Evaluation of commercial bell pepper cultivars for resistance to Phytophthora blight (Phytophthora capsici). Plant Health Progress15: 19-24. https://doi.org/10.1094/PHP-RS-13-0114
https://doi.org/10.1094/PHP-RS-13-0114...
). It was isolated and first reported in New Mexico by Leonian (1922LEONIAN, LH. 1922. Stem and fruit blight of peppers caused by Phytophthora capsici. Phytopathology12: 401-408.) from pepper plants (Capsicum annuum). For several years this pathogen was associated with species of the genus Capsicum as the sole hosts. However, current reports indicate that there are several plant species that can be infected by this oomycete, including tomato, eggplant, cucurbits (cucumber, watermelon, melon and squash), as well as some legumes such as broad beans, common beans, runner beans and strawberry, totaling 49 botanical families (Reis et al., 2007REIS, A; CAFÉ-FILHO, A; HENZ, GP. 2007. Phytophthora capsici: Patógeno agressivo e comum às solanáceas e cucurbitáceas. Available at: Available at: https://ainfo.cnptia.embrapa.br/digital/bitstream/CNPH-2009/33435/1/ct_55.pdf . AccessedJanuary 10, 2021.
https://ainfo.cnptia.embrapa.br/digital/...
; Lamour et al., 2012LAMOUR, KH; STAM, R; JUPE, J; HUITEMA, E. 2012. The oomycete broadhost- range pathogen Phytophthora capsici. Molecular Plant Pathology, 13: 329-337. https://doi.org/10.1111/j.1364-3703.2011.00754.x
https://doi.org/10.1111/j.1364-3703.2011...
; Barboza et al., 2017BARBOZA, EA; FONSECA, MEN; BOITEUX, LS; REIS, A. 2017. First worldwide report of a strawberry fruit rot disease caused by Phytophthora capsici isolates. Plant Disease 101: 259-259. https://doi.org/10.1094/PDIS-06-16-0864-PDN
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; Petry et al., 2017aPETRY, R; FONSECA, MEN; BOITEUX, LS; REIS, A. 2017a. First report of Phytophthora capsici as causal agent of snap-bean (Phaseolus vulgaris) pod decay in Brazil. Plant Disease 101: 800-800. https://doi.org/10.1094/PDIS-11-16-1602-PDN
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; Abeysekara et al., 2019ABEYSEKARA, NS; HICKMAN, H; WESTHAFER, S; JOHNSON, GC; EVANS, TA; GREGORY, NF; DONOFRIO, NM. 2019. Characterization of Phytophthora capsici isolates from lima bean grown in Delaware, United States of America. Phytopathologia Mediterranea 58: 535-546. https://doi.org/10.14601/Phyto-10823
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; Parada-Rojas & Quesada-Ocampo, 2019PARADA-ROJAS, CH; QUESADA-OCAMPO, LM. 2019. Characterizing sources of resistance to Phytopthora blight of pepper caused by Phytophthora capsici in North Carolina. Plant Health Progress 20: 112-119. https://doi.org/10.1094/PHP-09-18-0054-RS
https://doi.org/10.1094/PHP-09-18-0054-R...
; Farr & Rossman, 2020FARR, DF; ROSSMAN, AY. 2020. Fungal databases, U.S. National Fungus Collections, ARS, USDA. Available at:Available at:https://nt.ars-grin.gov/fungaldatabases/ . AccessedJanuary 05, 2021.
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). This makes P. capsici one of the most destructive and widespread soil-borne pathogens, limiting the production of many species of agricultural importance worldwide, especially in host plants within the Solanaceae and Cucurbitaceae families (Castro et al., 2014CASTRO, A; FLORES, J; AGUIRRE, M; FERNÁNDEZ, SP; RODRÍGUEZ, G; OSUMA, P. 2014. Traditional and molecular studies of the plant pathogen Phytophthora capsici: a review. Journal of Plant Pathology & Microbiology 5: 245-253. https://doi.org/10.4172/2157-7471.1000245
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; Reis et al., 2018REIS, A; PAZ-LIMA, ML; MOITA, AW; AGUIAR, FM; FONSECA, ME; CAFÉ FILHO, AC; BOITEUX, LS. 2018. A reappraisal of the natural and experimental host range of neotropical Phytophthora capsici isolates from Solanaceae, Cucurbitaceae, Rosaceae, and Fabaceae. Journal of Plant Pathology100: 215-223. https://doi.org/10.1007/s42161-018-0069-z
https://doi.org/10.1007/s42161-018-0069-...
).

Diseases caused by P. capsici can reduce productivity up to 100% when the infection occurs early in the season and conditions favor the disease (Liu et al., 2014LIU, WT; KANG, JH; JEONG, HS; CHOI, HJ; YANG, HB; KIM, KT; CHOI, D; CHOI, GJ; JAHN, M; KANG, BC. 2014. Combined use of bulked segregant analysis and microarrays reveals SNP markers pinpointing a major QTL for resistance to Phytophthora capsici in pepper. Theoretical and Applied Genetics 127: 2503-2513. https://doi.org/10.1007/s00122-014-2394-8
https://doi.org/10.1007/s00122-014-2394-...
). This pathogen can survive for many years (>24 months) in the absence of a host through resistant structures called oospores, a condition that makes its management very challenging (Gandariasbeitia et al., 2019GANDARIASBEITIA, M; OJINAGA, M; ORBEGOZO, E; ORTIZ-BARREDO1, A; NÚÑEZ-ZOFÍO, M; MENDARTE, S; LARREGLA, S. 2019. Winter biodisinfestation with Brassica green manure is a promising management strategy for Phytophthora capsici control of protected pepper crops in humid temperate climate regions of northern Spain. Spanish Journal of Agricultural Research 17: 1-11. https://doi.org/10.5424/sjar/2019171-13808
https://doi.org/10.5424/sjar/2019171-138...
). Temperatures between 25 and 28°C and high humidity (>80%) favor fungal infection and disease spread promoting large epidemics (Granke et al., 2009GRANKE, LL; WINDSTAM, ST; HOCH, HC; SMART, CD; HAUSBECK, MK. 2009. Dispersal and movement mechanisms of Phytophthora capsici sporangia. Phytopathology 99: 1258-1264. https://doi.org/10.1094/PHYTO-99-11-1258
https://doi.org/10.1094/PHYTO-99-11-1258...
). Soils with high humidity are ideal for the primary inoculum (oospores) to initiate infection on susceptible plants (Gandariasbeitia et al., 2019GANDARIASBEITIA, M; OJINAGA, M; ORBEGOZO, E; ORTIZ-BARREDO1, A; NÚÑEZ-ZOFÍO, M; MENDARTE, S; LARREGLA, S. 2019. Winter biodisinfestation with Brassica green manure is a promising management strategy for Phytophthora capsici control of protected pepper crops in humid temperate climate regions of northern Spain. Spanish Journal of Agricultural Research 17: 1-11. https://doi.org/10.5424/sjar/2019171-13808
https://doi.org/10.5424/sjar/2019171-138...
).

The management of diseases caused by P. capsici is expensive and difficult (Granke et al., 2012aGRANKE, LL; QUESADA‐OCAMPO, LM; LAMOUR, K; HAUSBECK, MK. 2012a. Advances in research on Phytophthora capsici on vegetable crops in the United States. Plant Disease 95: 1588‐1600. https://doi.org/10.1094/PDIS-02-12-0211-FE
https://doi.org/10.1094/PDIS-02-12-0211-...
). Chemical control still plays a prominent role in controlling crop pests in spite of its innumerable problems such as changes in physical-chemical properties of soils, accumulation of toxic compounds in fruits and fungicide resistance on pathogen populations (Dunn et al., 2010DUNN, AR; MILGROOM, MG; MEITZ, JC; MCLEOD, A; FRY, WE; MCGRATH, MT; DILLARD, HR; SMART, CD. 2010. Population structure and resistance to mefenoxam of Phytophthora capsici in New York State. Plant Disease 94: 1461-1468. https://doi.org/10.1094/PDIS-03-10-0221
https://doi.org/10.1094/PDIS-03-10-0221...
; Hung-Wan & Liew, 2020HUNG-WAN, JS; LIEW, EC. 2020. Efficacy of chemical and biological agents against pepper blight (Phytophthora capsici Leonion) in East Asia: a meta-analysis of laboratory and field trial data. Journal of Plant Pathology 102: 835-842. https://doi.org/10.1007/s42161-020-00519-0
https://doi.org/10.1007/s42161-020-00519...
). This is why the combined application of control methods, such as genetic, physical, cultural, biological and chemical (use of fungicides / oomiceticides of synthetic origin) from an integrated management approach constitutes the best option to reduce economic losses in any crop, besides being more environmental friendly (Majid et al., 2016MAJID, MU; AWAN, MF; FATIMA, K; TAHIR, MS; ALI, Q; RASHID, B; RAO, AQ; NASIR, IA; HUSNAIN, T. 2016. Phytophthora capsici on chilli pepper (Capsicum annuum L.) and its management through genetic and bio-control: a review. Zemdirbyste103: 419-430. https://doi.org/10.13080/z-a.2016.103.054
https://doi.org/10.13080/z-a.2016.103.05...
).

The use of diversified and integrated disease management practices minimizes the disturbance of the natural dynamics of an agro-ecosystem (ecological niches, microbiome), with a positive effect for sustainable agricultural production (Abrol & Shankar, 2012ABROL, DP; SHANKAR, U. 2012. History, overview and principles of ecologically-based pest management. In: ABROL, DP; SHANKAR U(eds). Integrated Pest Management: Principles and practice. London, UK: CABI International. p. 1-26.). Therefore, this review into each of the topics related to the integrated management of P. capsici, aimed to provide the reader with current technical information, in order to avoid and / or reduce damage to horticultural production systems associated with it.

Symptoms associated with Phytophthora capsici

Regardless their species, plants may be affected during any phenological stage and symptoms can appear in various organs (Hung-Wan & Liew, 2020LI, Y; FENG, X; WANG, X; ZHENG, L; LIU, B. 2020. Inhibitory effects of Bacillus licheniformis BL06 on Phytophthora capsici in pepper by multiple modes of action. Biological Control 144: 104210. https://doi.org/10.1016/j.biocontrol.2020.104210
https://doi.org/10.1016/j.biocontrol.202...
) (Figure 1), these being dependent on environmental conditions, pathogen’s virulence and host resistance levels (Reis et al., 2007REIS, A; CAFÉ-FILHO, A; HENZ, GP. 2007. Phytophthora capsici: Patógeno agressivo e comum às solanáceas e cucurbitáceas. Available at: Available at: https://ainfo.cnptia.embrapa.br/digital/bitstream/CNPH-2009/33435/1/ct_55.pdf . AccessedJanuary 10, 2021.
https://ainfo.cnptia.embrapa.br/digital/...
; Granke et al., 2012bGRANKE, LL; QUESADA-OCAMPO, LM; HAUSBECK, MK. 2012b. Differences in virulence of Phytophthora capsici isolates from a worldwide collection on host fruits. European Journal of Plant Pathology 132: 281-296. https://doi.org/10.1007/s10658-011-9873-4
https://doi.org/10.1007/s10658-011-9873-...
; Barchenger et al., 2018BARCHENGER, DW; LAMOUR, KH; BOSLAND, PW. 2018. Challenges and strategies for breeding resistance in Capsicum annuum to the multivarious pathogen. Phytophthora capsici. Frontiers in Plant Science 9: 628. https://doi.org/10.3389/fpls.2018.00628
https://doi.org/10.3389/fpls.2018.00628...
; Saltos et al., 2021SALTOS, LA; COROZO-QUIÑONES, L; PACHECO-COELLO, R; SANTOS-ORDÓÑEZ, E; MONTEROS-ALTAMIRANO, A; GARCÉS-FIALLOS, FR. 2021. Tissue specific colonization of Phytophthora capsici in Capsicum spp.: molecular insights over plant-pathogen interaction. Phytoparasitica. https://doi.org/10.1007/s12600-020-00864-x
https://doi.org/10.1007/s12600-020-00864...
). Young and immature tissues are often more susceptible to infection (Roberts et al., 1999ROBERTS, PD; MCGOVERN, RJ; HERT, A; VAVRINA, CS; URS, RR. 1999. Phytophthora capsici on tomato: Survival, severity, age, variety, and insensitivity to mefenoxam. In: Florida Tomato Institute Proceedings. CS VAVRINA, ed. University of Florida and Citrus & Vegetable Magazine. PRO41-43.).

Figure 1
Symptoms caused by Phytophthora capsici in cucurbits and solanaceous plants: (A) wilt, (B) root rot, (C) crown and stem rot, and (D) leaf blight on sweet pepper (Capsicum annuum); (E) damping-off on zucchini plants (Cucurbita pepo); Fruit rot on (F) chili and (G) sweet pepper (Capsicum spp.), (H) eggplant (Solanum melongena), (I) cucumber (Cucumis sativus) and (J) pumpkin (C. maxima) plants. Source: Unpublished photographs from the authors. Ecuador, Technical University of Manabí, 2018-2020.

Symptoms of P. capsici on adult plants begin with sudden yellowing and wilting of the leaves as a consequence of the collapse of the water-conducting tissues of the roots and stems (Figure 1A) (Ristaino & Johnston, 1999RISTAINO, JB; JOHNSTON, SA. 1999. Ecologically based approaches to management of Phytophthora blight on bell pepper. Plant Disease 83: 1080-1089. https://doi.org/10.1094/PDIS.1999.83.12.1080
https://doi.org/10.1094/PDIS.1999.83.12....
; Barchenger et al., 2018BARCHENGER, DW; LAMOUR, KH; BOSLAND, PW. 2018. Challenges and strategies for breeding resistance in Capsicum annuum to the multivarious pathogen. Phytophthora capsici. Frontiers in Plant Science 9: 628. https://doi.org/10.3389/fpls.2018.00628
https://doi.org/10.3389/fpls.2018.00628...
). Roots present small, dark-colored lesions that expand rapidly until complete rotting (Figure 1B) (Ristaino & Johnston, 1999RISTAINO, JB; JOHNSTON, SA. 1999. Ecologically based approaches to management of Phytophthora blight on bell pepper. Plant Disease 83: 1080-1089. https://doi.org/10.1094/PDIS.1999.83.12.1080
https://doi.org/10.1094/PDIS.1999.83.12....
; Reis et al., 2007REIS, A; CAFÉ-FILHO, A; HENZ, GP. 2007. Phytophthora capsici: Patógeno agressivo e comum às solanáceas e cucurbitáceas. Available at: Available at: https://ainfo.cnptia.embrapa.br/digital/bitstream/CNPH-2009/33435/1/ct_55.pdf . AccessedJanuary 10, 2021.
https://ainfo.cnptia.embrapa.br/digital/...
; Lamour et al., 2012LAMOUR, KH; STAM, R; JUPE, J; HUITEMA, E. 2012. The oomycete broadhost- range pathogen Phytophthora capsici. Molecular Plant Pathology, 13: 329-337. https://doi.org/10.1111/j.1364-3703.2011.00754.x
https://doi.org/10.1111/j.1364-3703.2011...
). In advanced stages of the disease, dry, dark brown or black lesions are developed on the cortical tissue of the crown near the soil line (Figure 1C). Symptoms of leaf blight include dark, watery spots that rapidly increase in size and become necrotic in appearance (Figure 1D) (Ristaino & Johnston, 1999RISTAINO, JB; JOHNSTON, SA. 1999. Ecologically based approaches to management of Phytophthora blight on bell pepper. Plant Disease 83: 1080-1089. https://doi.org/10.1094/PDIS.1999.83.12.1080
https://doi.org/10.1094/PDIS.1999.83.12....
; Walker & Bosland, 1999WALKER, SJ; BOSLAND, PW. 1999. Inheritance of Phytophthora root rot and foliar blight resistance in pepper. Journal of the American Society for Horticultural Science 124: 14-18. https://doi.org/10.21273/JASHS.124.1.14
https://doi.org/10.21273/JASHS.124.1.14...
). The fruits first show water-soaked lesions with clear centers, which expand rapidly, usually covered with white structures of the pathogen, and completely rot the fruit in a few days (Figures 1F to 1J) (Ristaino & Johnston, 1999RISTAINO, JB; JOHNSTON, SA. 1999. Ecologically based approaches to management of Phytophthora blight on bell pepper. Plant Disease 83: 1080-1089. https://doi.org/10.1094/PDIS.1999.83.12.1080
https://doi.org/10.1094/PDIS.1999.83.12....
; Reis et al., 2007REIS, A; CAFÉ-FILHO, A; HENZ, GP. 2007. Phytophthora capsici: Patógeno agressivo e comum às solanáceas e cucurbitáceas. Available at: Available at: https://ainfo.cnptia.embrapa.br/digital/bitstream/CNPH-2009/33435/1/ct_55.pdf . AccessedJanuary 10, 2021.
https://ainfo.cnptia.embrapa.br/digital/...
). Symptom development is not uniform, depending, among other factors, on the degree of resistance of the host (Drenth & Sendall, 2001DRENTH, A; SENDALL, B. 2001. Practical guide to detection and identification of Phytophthora. Brisbane, AUS: CRC for Tropical Plant Protection. 42p.).

Description of the pathogen

Phytophthora capsici belongs to the Kingdom Chromist (Stramenopile), Phylum Oomycota, Class Peronosporea, Order Peronosporales and Family Peronosporaceae (Roskov et al., 2016ROSKOV, Y; ABUCAY, L; ORRELL, T; NICOLSON, D; FLANN, C; BAILLY, N; KIRK, P; BOURGOIN, T; DEWALT, RE; DECOCK, W; DE WEVER, A. 2016. Species 2000 & ITIS Catalogue of Life, 2016 Annual Checklist.). It has coenocytic mycelium and produces ovoid, ellipsoid and papillate zoosporangia which contains reniform and biflagellate zoospores (Vélez-Olmedo et al., 2020VÉLEZ-OLMEDO, JB; SALTOS, L; COROZO, L; BONFIM, BS; VÉLEZ-ZAMBRANO, S; ARTEAGA, F; GARCÍA, M; PINHO, D. 2020. First report of Phytophthora capsici causing wilting and root and crown rot on Capsicum annuum (Bell pepper) in Ecuador. Plant Disease 104: 2032-2032. https://doi.org/10.1094/PDIS-11-19-2432-PDN
https://doi.org/10.1094/PDIS-11-19-2432-...
) which are released quickly, isolated or grouped, and are chemotactically and electrostatically attracted to the surfaces of host plants (Fawke et al., 2015FAWKE, S; DOUMANE, M; SCHORNACK, S. 2015. Oomycete interactions with plants: infection strategies and resistance principles. Microbiology and Molecular Biology Reviews 79: 263-280. https://doi.org/10.1128/MMBR.00010-15
https://doi.org/10.1128/MMBR.00010-15...
).

The pathogen is a heterothallic species, with isolates having one of two mating types (designated A1 and A2). Both mating types are required in close proximity for mating to occur (Lamour et al., 2012LAMOUR, KH; STAM, R; JUPE, J; HUITEMA, E. 2012. The oomycete broadhost- range pathogen Phytophthora capsici. Molecular Plant Pathology, 13: 329-337. https://doi.org/10.1111/j.1364-3703.2011.00754.x
https://doi.org/10.1111/j.1364-3703.2011...
). It produces a male gametangium (antheridium), and a female gametangium (oogonium). The antheridium is amphigynous in P. capsici. Following by the formation of the antheridium and oogonium, meiosis occurs within the gametangia, and plasmogamy and karyogamy result in the formation of oospores (sexual spores). Oospore usually go through a rest period, and it serves also as an overwintering structure (Ristaino & Johnston, 1999RISTAINO, JB; JOHNSTON, SA. 1999. Ecologically based approaches to management of Phytophthora blight on bell pepper. Plant Disease 83: 1080-1089. https://doi.org/10.1094/PDIS.1999.83.12.1080
https://doi.org/10.1094/PDIS.1999.83.12....
). The oospores diameter ranges between 15 µm and 40 µm. They germinate after a period of rest (Erwin & Ribeiro, 1996ERWIN, D; RIBERO, O. 1996. Phytophthora Diseases Worldwide. Minnesota, USA: APS PRESS. 592p.). Under favorable environmental conditions, P. capsici will often produce massive numbers of sporangia on the surface of infected tissue (Lamour et al., 2012LAMOUR, KH; STAM, R; JUPE, J; HUITEMA, E. 2012. The oomycete broadhost- range pathogen Phytophthora capsici. Molecular Plant Pathology, 13: 329-337. https://doi.org/10.1111/j.1364-3703.2011.00754.x
https://doi.org/10.1111/j.1364-3703.2011...
). They also may be produced in vitro in V8-agar culture medium. Sporangia can have ovoid, elliptical, papillate or semi-papillate shapes (with sizes in a length:diameter ratio of 2.1:1.3). This oomycete rarely produces chlamydospores (resistance structures), but when these are produced they may be of different types: intercalary (formed between hyphae); terminal (at the end of the hypha) with a size ranging from 20.0 µm to 27.5 µm in diameter (Islam et al., 2004ISLAM, SZ; BABADOST, M; LAMBERT, K; NDEME, A. 2004. Characterization of Phytophthora capsici isolates from processing pumpkin in Illinois. Plant Disease 89: 191-197. https://doi.org/10.1094/PD-89-0191
https://doi.org/10.1094/PD-89-0191...
); and globose with long pedicels (Vélez-Olmedo et al., 2020VÉLEZ-OLMEDO, JB; SALTOS, L; COROZO, L; BONFIM, BS; VÉLEZ-ZAMBRANO, S; ARTEAGA, F; GARCÍA, M; PINHO, D. 2020. First report of Phytophthora capsici causing wilting and root and crown rot on Capsicum annuum (Bell pepper) in Ecuador. Plant Disease 104: 2032-2032. https://doi.org/10.1094/PDIS-11-19-2432-PDN
https://doi.org/10.1094/PDIS-11-19-2432-...
).

Like other Phytophthora species, under favorable conditions, P. capsici can spread rapidly between plants throughout the field due to multiple sporangium production and infection cycles. It has the potential for rapid polycyclic disease development from a limited amount of inoculum (Majid et al., 2016MAJID, MU; AWAN, MF; FATIMA, K; TAHIR, MS; ALI, Q; RASHID, B; RAO, AQ; NASIR, IA; HUSNAIN, T. 2016. Phytophthora capsici on chilli pepper (Capsicum annuum L.) and its management through genetic and bio-control: a review. Zemdirbyste103: 419-430. https://doi.org/10.13080/z-a.2016.103.054
https://doi.org/10.13080/z-a.2016.103.05...
). Rainfall plays an important role for the release and dispersal of sporangia, therefore, the rapid increase of the epidemic in the field (Sanogo & Ji, 2013SANOGO, S; JI, P. 2013. Water management in relation to control of Phytophthora capsici in vegetable crops. Agricultural Water Management 129: 113-119. https://doi.org/10.1016/j.agwat.2013.07.018
https://doi.org/10.1016/j.agwat.2013.07....
).

Plant-pathogen relation

Phytophthora capsici is a hemi-biotrophic pathogen, initially displaying a biotrophic lifestyle, followed by a change to a necrotrophic phase (Jupe et al., 2013JUPE, J; STAM, R; HOWDEN, A; MORRIS, JA; ZHANG, R; HEDLEY, PH; HUITEMA, E. 2013. Phytophthora capsici-tomato interaction features dramatic shifts in gene expression associated with a hemi-biotrophic lifestyle. Genome Biology 14: R63. https://doi.org/10.1186/gb-2013-14-6-r63
https://doi.org/10.1186/gb-2013-14-6-r63...
). High humidity in the soil favors the germination of oospores producing germination tube or sporangium (Hausbeck & Lamour, 2004HAUSBECK, MK; LAMOUR, KH. 2004. Phytophthora capsici on vegetable crops: Research progress and management challenges. Plant Disease 88: 1292-1303. https://doi.org/10.1094/PDIS.2004.88.12.1292
https://doi.org/10.1094/PDIS.2004.88.12....
). Through the germination tube, the pathogen can penetrate directly through the tissues of the susceptible host or by zoospores produced from sporangia (Waterhouse et al., 1983WATERHOUSE, GM; NEWHOOK, F; STAMPS, DJ. 1983. Present criteria for classification of Phytophthora. In: DONALD, E (ed). Phytophthora: its biology, taxonomy, ecology and pathology. Minnesota, USA: American Phytopathological Society. p. 139-147.). Biflagellate mobile zoospores move to the surface of the host and initiate the infection process (Fawke et al., 2015FAWKE, S; DOUMANE, M; SCHORNACK, S. 2015. Oomycete interactions with plants: infection strategies and resistance principles. Microbiology and Molecular Biology Reviews 79: 263-280. https://doi.org/10.1128/MMBR.00010-15
https://doi.org/10.1128/MMBR.00010-15...
). However, all plants present preformed structural and biochemical barriers that represent a limitation for the penetration of the pathogen (Kale & Tyler, 2011KALE, SD; TYLER, BM. 2011. Entry of oomycete and fungal effectors into plant and animal host cells. Cellular Microbiology 13: 1839-1848. https://doi.org/10.1111/j.1462-5822.2011.01659.x
https://doi.org/10.1111/j.1462-5822.2011...
).

During the initial events of the plant-pathogen interaction, the oomycete releases an array of biological weapons, called elicitors (Elicitins, NLPs, CRNs, SCRs) and pathogen-associated molecular patterns (PAMPs) (Hein et al., 2009HEIN, I; GILROY, EM; ARMSTRONG, MR; BIRCH, PR. 2009. The zig-zag-zig in oomycete-plant interactions. Molecular Plant Pathology 10: 547-562. https://doi.org/10.1111/J.1364-3703.2009.00547.X
https://doi.org/10.1111/J.1364-3703.2009...
). These are recognized by specific receptors located in the plant cell membranes, giving rise to an immunity triggered by PAMP (PTI). PTI constitutes the first line of defense that must be overcome by the pathogen for a successful colonization of the tissues. This is achieved through virulence determinants, called effectors, which suppress the plant innate immunity (Jupe et al., 2013JUPE, J; STAM, R; HOWDEN, A; MORRIS, JA; ZHANG, R; HEDLEY, PH; HUITEMA, E. 2013. Phytophthora capsici-tomato interaction features dramatic shifts in gene expression associated with a hemi-biotrophic lifestyle. Genome Biology 14: R63. https://doi.org/10.1186/gb-2013-14-6-r63
https://doi.org/10.1186/gb-2013-14-6-r63...
). Effector-triggered susceptibility (ETS) includes the suppression of PTI, which represents the first phase of events at the molecular level in the plant-pathogens interaction (Hein et al., 2009). Resistance proteins (PR) represent the second molecular barrier that detects effectors (avirulence proteins, AVRs), conferring immunity to the pathogen that may be successful in suppressing PTI. The effector-triggered immunity (ETI) constitutes the second line of defense at the molecular level between the plant and oomycete (Hein et al., 2009HEIN, I; GILROY, EM; ARMSTRONG, MR; BIRCH, PR. 2009. The zig-zag-zig in oomycete-plant interactions. Molecular Plant Pathology 10: 547-562. https://doi.org/10.1111/J.1364-3703.2009.00547.X
https://doi.org/10.1111/J.1364-3703.2009...
). Once all these restrictions have been overcome, the penetration of tissues by the oomycete is inevitable, thus initiating the infectious process.

Subsequently, the hyphae invade and colonize the tissues intercellularly and haustorium is emitted, which can infect the cells of the cortical and vascular tissue of different plant organs (Fawke et al., 2015FAWKE, S; DOUMANE, M; SCHORNACK, S. 2015. Oomycete interactions with plants: infection strategies and resistance principles. Microbiology and Molecular Biology Reviews 79: 263-280. https://doi.org/10.1128/MMBR.00010-15
https://doi.org/10.1128/MMBR.00010-15...
). Finally, under optimal conditions (25-30°C and high relative humidity) the sporulation phase (production of sporangia) occurs outside the tissues, ≈90 hours after infection (Lamour et al., 2012LAMOUR, KH; STAM, R; JUPE, J; HUITEMA, E. 2012. The oomycete broadhost- range pathogen Phytophthora capsici. Molecular Plant Pathology, 13: 329-337. https://doi.org/10.1111/j.1364-3703.2011.00754.x
https://doi.org/10.1111/j.1364-3703.2011...
).

Phytophthora capsici diseases methods of control

The integrated management strategy to control any plant disease, not differently from those caused by P. capsici, is fundamentally based on the selection and implementation of genetic, cultural, physical, biological and chemical measures, aiming to avoid, reduce and / or maintain disease severity below the economic threshold of damage to crops (Abrol & Shankar, 2012ABROL, DP; SHANKAR, U. 2012. History, overview and principles of ecologically-based pest management. In: ABROL, DP; SHANKAR U(eds). Integrated Pest Management: Principles and practice. London, UK: CABI International. p. 1-26.).

Genetic control

Genetic resistance of the host constitutes the main approach of any integrated program for P. capsici management, although it usually cannot be considered as the sole control measure (Hausbeck & Lamour, 2004HAUSBECK, MK; LAMOUR, KH. 2004. Phytophthora capsici on vegetable crops: Research progress and management challenges. Plant Disease 88: 1292-1303. https://doi.org/10.1094/PDIS.2004.88.12.1292
https://doi.org/10.1094/PDIS.2004.88.12....
; Granke et al., 2012aGRANKE, LL; QUESADA‐OCAMPO, LM; LAMOUR, K; HAUSBECK, MK. 2012a. Advances in research on Phytophthora capsici on vegetable crops in the United States. Plant Disease 95: 1588‐1600. https://doi.org/10.1094/PDIS-02-12-0211-FE
https://doi.org/10.1094/PDIS-02-12-0211-...
).

Some sources of resistance to P. capsici have been found in tomato, sweet and chili pepper, muskmelon and squash (Padley et al., 2009PADLEY, LD; KABELKA, EA; ROBERTS, PD. 2009. Inheritance of resistance to crown rot caused by Phytopthora capsici in Cucurbita. HortScience44: 211-213. https://doi.org/10.21273/HORTSCI.44.1.211
https://doi.org/10.21273/HORTSCI.44.1.21...
; Foster & Hausbeck, 2010FOSTER, JM; HAUSBECK, MK. 2010. Resistance of pepper to Phytophthora crown, root, and fruit rot is affected by isolate virulence. Plant Disease 94: 24-30. https://doi.org/10.1094/PDIS-94-1-0024
https://doi.org/10.1094/PDIS-94-1-0024...
; Quesada-Ocampo & Hausbeck, 2010QUESADA-OCAMPO, LM; HAUSBECK, MK. 2010. Resistance in tomato and wild relatives to crown and root rot caused by Phytophthora capsici. Phytopathology100: 619-627. https://doi.org/10.1094/PHYTO-100-6-0619
https://doi.org/10.1094/PHYTO-100-6-0619...
; Dunn et al., 2014DUNN, AR; LANGE, HW; SMART, CD. 2014. Evaluation of commercial bell pepper cultivars for resistance to Phytophthora blight (Phytophthora capsici). Plant Health Progress15: 19-24. https://doi.org/10.1094/PHP-RS-13-0114
https://doi.org/10.1094/PHP-RS-13-0114...
; Pontes et al., 2014PONTES, NC; AGUIAR, FM; BOITEUX, LS; PAZ-LIMA, ML; OLIVEIRA, VR; CAFÉ FILHO, AC; REIS, A. 2014. Identification of sources of seedling resistance to Phytophthora capsici in Cucumis melo. Tropical Plant Pathology39: 74-81. https://doi.org/10.1590/S1982-56762014000100009
https://doi.org/10.1590/S1982-5676201400...
; Petry et al., 2017bPETRY, R; PAZ-LIMA, ML; BOITEUX, LS. 2017b. Reaction of Solanum (section Lycopersicon) germplasm to Phytophthora capsici. European Journal of Plant Pathology 148: 481-489. https://doi.org/10.1007/s10658-016-1106-4
https://doi.org/10.1007/s10658-016-1106-...
). However, the majority of commercial varieties currently available, independent on the host species, lack resistance (Ando et al., 2009ANDO, K; HAMMAR, S; GRUMET, R. 2009. Age-related resistance of diverse cucurbit fruit to infection by Phytophthora capsici. Journal of the American Society for Horticulture Science 134: 176-182. https://doi.org/10.21273/JASHS.134.2.176
https://doi.org/10.21273/JASHS.134.2.176...
; Lamour et al., 2012LAMOUR, KH; STAM, R; JUPE, J; HUITEMA, E. 2012. The oomycete broadhost- range pathogen Phytophthora capsici. Molecular Plant Pathology, 13: 329-337. https://doi.org/10.1111/j.1364-3703.2011.00754.x
https://doi.org/10.1111/j.1364-3703.2011...
; Krasnow et al., 2017KRASNOW, CS; WYENANDDT, AA; KLINE, W; CAREY, JB; HAUSBECK, MK. 2017. Evaluation of pepper root rot resistance in an integrated Phytophthora blight management program. HortTecnology27: 409-415. https://doi.org/10.21273/HORTTECH03697-17
https://doi.org/10.21273/HORTTECH03697-1...
), because introgression of resistance genes from wild species onto commercial genotypes is usually complex. Examples of resistant commercial pepper genotypes to P. capsici are: Nathalie (Figure 2), Criollo de Morelos 334 and Paladín (Dunn et al., 2014DUNN, AR; LANGE, HW; SMART, CD. 2014. Evaluation of commercial bell pepper cultivars for resistance to Phytophthora blight (Phytophthora capsici). Plant Health Progress15: 19-24. https://doi.org/10.1094/PHP-RS-13-0114
https://doi.org/10.1094/PHP-RS-13-0114...
; Dunn & Smart, 2015DUNN, A; SMART, C. 2015. Interactions of Phytophthora capsici with resistant and susceptible pepper roots and stems. Phytopathology105: 1355-1361. https://doi.org/10.1094/PHYTO-02-15-0045-R
https://doi.org/10.1094/PHYTO-02-15-0045...
; Saltos et al., 2021SALTOS, LA; COROZO-QUIÑONES, L; PACHECO-COELLO, R; SANTOS-ORDÓÑEZ, E; MONTEROS-ALTAMIRANO, A; GARCÉS-FIALLOS, FR. 2021. Tissue specific colonization of Phytophthora capsici in Capsicum spp.: molecular insights over plant-pathogen interaction. Phytoparasitica. https://doi.org/10.1007/s12600-020-00864-x
https://doi.org/10.1007/s12600-020-00864...
). In a recent work carried out in Ecuador by Saltos et al. (2021)SALTOS, LA; COROZO-QUIÑONES, L; PACHECO-COELLO, R; SANTOS-ORDÓÑEZ, E; MONTEROS-ALTAMIRANO, A; GARCÉS-FIALLOS, FR. 2021. Tissue specific colonization of Phytophthora capsici in Capsicum spp.: molecular insights over plant-pathogen interaction. Phytoparasitica. https://doi.org/10.1007/s12600-020-00864-x
https://doi.org/10.1007/s12600-020-00864...
, Capsicum genotypes Nathalie, ECU-12831, ECU-9129, Código 5, and ECU-1296 were found to be resistant to root and crown rot.

Figure 2
Commercial hybrids of sweet pepper (Capsicum annuum) Nathalie (resistant), Quetzal and Marcato (susceptible) showing a differentiated response to Phytophthora capsici.

There are great challenges in the plant breeding of vegetable crops to confer resistance to P. capsici; among them, different inheritance models have been reported in different sources of resistance (Barchenger et al., 2018BARCHENGER, DW; LAMOUR, KH; BOSLAND, PW. 2018. Challenges and strategies for breeding resistance in Capsicum annuum to the multivarious pathogen. Phytophthora capsici. Frontiers in Plant Science 9: 628. https://doi.org/10.3389/fpls.2018.00628
https://doi.org/10.3389/fpls.2018.00628...
). Resistance to P. capsici is expressed in different ways in Capsicum spp., for instance, the resistance of the cultivar Criollo de Morelos 334, was associated with the expression of two genes (Sy et al., 2005SY, O; BOSLAND, PW; STEINER, R. 2005. Inheritance of Phytophthora stem blight resistance as compared to Phytophthora root rot and Phytophthora foliar blight resistance in Capsicum annuum L. Journal of the American Society for Horticultural Science 130: 75-78. https://doi.org/10.21273/JASHS.130.1.75
https://doi.org/10.21273/JASHS.130.1.75...
), whilst other studies related resistance to only one dominant gene, as well as resistance of multiple genes with additive or epistatic effects (Barchenger et al., 2018BARCHENGER, DW; LAMOUR, KH; BOSLAND, PW. 2018. Challenges and strategies for breeding resistance in Capsicum annuum to the multivarious pathogen. Phytophthora capsici. Frontiers in Plant Science 9: 628. https://doi.org/10.3389/fpls.2018.00628
https://doi.org/10.3389/fpls.2018.00628...
).

Some genes confer resistance to root rot, crown rot or leaf blight, while others provide resistance to fruit rot (syndrome-specific resistance), as has been demonstrated for Capsicum spp. (Sy et al., 2005SY, O; BOSLAND, PW; STEINER, R. 2005. Inheritance of Phytophthora stem blight resistance as compared to Phytophthora root rot and Phytophthora foliar blight resistance in Capsicum annuum L. Journal of the American Society for Horticultural Science 130: 75-78. https://doi.org/10.21273/JASHS.130.1.75
https://doi.org/10.21273/JASHS.130.1.75...
). On the other hand, the resistance of a genotype varies according to the virulence of the P. capsici isolate (race-specific resistance, associated with a qualitative gene model); a cultivar may be resistant to one strain but susceptible to another genetically different (Glosier et al., 2008GLOSIER, BR; OGUNDIWIN, EA; SIDHU, GS; SISCHO, DR; PRINCE, JP. 2008. A differential series of pepper (Capsicum annuum) lines delineates fourteen physiological races of Phytophthora capsici. Euphytica 162: 23-30. https://doi.org/10.1007/s10681-007-9532-1
https://doi.org/10.1007/s10681-007-9532-...
; Ribeiro & Bosland, 2012RIBEIRO, CSC; BOSLAND, PW. 2012. Physiological race characterization of Phytophthora capsici isolates from several host plant species in Brazil using New Mexico recombinant inbred lines of Capsicum annuum at two inoculum levels. Journal of the American Society for Horticultural Science 137: 421-426. https://doi.org/10.21273/JASHS.137.6.421
https://doi.org/10.21273/JASHS.137.6.421...
). Ontogenetic, developmental, or age-related resistance has also been highlighted, wherein plants or plant organs change their state of susceptibility to one of resistance as a result of changes in development (Mansfeld et al., 2020MANSFELD, BN; COLLE, M; ZHANG, C; LIN, YC, GRUMET, R. 2020. Developmentally regulated activation of defense allows for rapid inhibition of infection in age-related resistance to Phytophthora capsici in cucumber fruit. BMC Genomics 21: 628. https://doi.org/10.1186/s12864-020-07040-9
https://doi.org/10.1186/s12864-020-07040...
). Plants develop PTI to detect nonspecific MAMPs and ETI which is resistance specific and accompanied by a hypersensitive response (Du et al., 2021DU, JS; HANG, LL; HAO, Q; YANG, HT; ALI, S; EZAAT, RS; XU, XY; TAN, HQ; SU, LH; LI, HX; ZOU, KX; LI, Y; SUN, B; LIN, LJ; LAI, YS. 2021. The dissection of R genes and locus Pc5.1 in Phytophthora capsici infection provides a novel view of disease resistance in peppers. BMC Genomics 22:372. https://doi.org/10.1186/s12864-021-07705-z
https://doi.org/10.1186/s12864-021-07705...
).

Grafting is another control strategy within genetic resistance (Gisbert et al., 2010GISBERT, C; SÁNCHEZ-TORRES, P; RAIGON, MD; NUEZ, F. 2010. Phytophthora capsici resistance evaluation in pepper hybrids: agronomic performance and fruit quality of pepper grafted plants. Journal of Food, Agriculture & Environment 8: 116-121.; Sanogo & Ji, 2012SANOGO, S; JI, P. 2012. Integrated management of Phytophthora capsici on solanaceous and cucurbitaceous crops: current status, gaps in knowledge and research needs. Canadian Journal of Plant Pathology 34: 479-492. https://doi.org/10.1080/07060661.2012.732117
https://doi.org/10.1080/07060661.2012.73...
). In this technique, the scion of a genotype with high productive potential is grafted onto rootstocks from another line or resistant cultivar. Grafting is a technique that has gained remarkable momentum and is used as important practice to reduce the incidence of many diseases caused by soilborne pathogens, such as P. capsici. For example, Jang et al. (2012JANG, Y; YANG, E; CHO, M; UM, Y; KO, K; CHUN, CH. 2012. Effect of grafting on growth and incidence of phytophthora blight and bacterial wilt of pepper (Capsicum annuum L.). Horticulture, Environment, and Biotechnology 53: 9-19. https://doi.org/10.1007/s13580-012-0074-7
https://doi.org/10.1007/s13580-012-0074-...
) found that grafted pepper plants showed greater resistance to both P. capsici and Ralstonia solanacearum, without a reduction in yield and fruit quality. These highest levels of resistance to P. capsici were obtained with the combination of peppers “Nokkwang”, “Saengsaeng Matkkwari”, and “Shinhong”, grafted onto breeding lines “PR 920”, “PR 921”, and “PR 922”.

Other source of resistance has been discovered in the wild relative of tomato Solanum habrochaites (accession LA407), which showed resistance to a variety of P. capsici isolates, while other genotypes (Ha7998, Fla7600, Jolly Elf and Talladega) exhibited moderate resistance (Quesada-Ocampo & Hausbeck, 2010). Black pepper has also displayed resistance in its wild species Piper colubrinum (Suraby et al., 2020SURABY, EJ; PRASATH, D; BABU, KN; ANANDARAJ, M. 2020. Identification of resistance gene analogs involved in Phytophthora capsici recognition in black pepper (Piper nigrum L.). Journal of Plant Pathology103: 1-11. https://doi.org/10.1007/s42161-020-00586-3
https://doi.org/10.1007/s42161-020-00586...
). In cucurbits, there are few wild species such as C. pepo (accessions PI 169417, PI 181761, PI 512709 and Table Ace) with resistance to P. capsici (Krasnow et al., 2014KRASNOW, CS; NAEGELE, RP; HAUSBECK, MK. 2014. Evaluation of fruit rot resistance in cucurbita germplasm resistant to Phytophthora capsici crown rot. HortsCience49: 285-288. https://doi.org/10.21273/HORTSCI.49.3.285
https://doi.org/10.21273/HORTSCI.49.3.28...
). On the contrary, species under the genus Solanum (Petry et al., 2017bPETRY, R; PAZ-LIMA, ML; BOITEUX, LS. 2017b. Reaction of Solanum (section Lycopersicon) germplasm to Phytophthora capsici. European Journal of Plant Pathology 148: 481-489. https://doi.org/10.1007/s10658-016-1106-4
https://doi.org/10.1007/s10658-016-1106-...
) or Capsicum (Glosier et al., 2008GLOSIER, BR; OGUNDIWIN, EA; SIDHU, GS; SISCHO, DR; PRINCE, JP. 2008. A differential series of pepper (Capsicum annuum) lines delineates fourteen physiological races of Phytophthora capsici. Euphytica 162: 23-30. https://doi.org/10.1007/s10681-007-9532-1
https://doi.org/10.1007/s10681-007-9532-...
), wild genotypes with complete resistance have been identified, although with unfavorable horticultural characteristics (Granke et al., 2012aGRANKE, LL; QUESADA‐OCAMPO, LM; LAMOUR, K; HAUSBECK, MK. 2012a. Advances in research on Phytophthora capsici on vegetable crops in the United States. Plant Disease 95: 1588‐1600. https://doi.org/10.1094/PDIS-02-12-0211-FE
https://doi.org/10.1094/PDIS-02-12-0211-...
). Partial resistance to P. capsici was also found in habanero (C. chinense) pepper accessions (Soares et al., 2019SOARES, RS; RIBEIRO, CSC; RAGASSI, CF; LOPES, CA; CARVALHO, SIC; REIS, A; BRAZ, LT; REIFSCHNEIDER, FJB. 2019. Reaction of advanced inbred lines of Habanero pepper to Ralstonia pseudosolanacearum and Phytophthora capsici. Horticultura Brasileira 37: 95-401. https://doi.org/10.1590/S0102-053620190406
https://doi.org/10.1590/S0102-0536201904...
). In muskmelon, wild accesses with good resistance sources to root and stem rot were identified in Brazil (Pontes et al., 2014PONTES, NC; AGUIAR, FM; BOITEUX, LS; PAZ-LIMA, ML; OLIVEIRA, VR; CAFÉ FILHO, AC; REIS, A. 2014. Identification of sources of seedling resistance to Phytophthora capsici in Cucumis melo. Tropical Plant Pathology39: 74-81. https://doi.org/10.1590/S1982-56762014000100009
https://doi.org/10.1590/S1982-5676201400...
). Sources of resistance to crown rot caused by P. capsici have also been identified in Cucurbita germplasm (Brune & Lopes, 1994BRUNE, S; LOPES, JF. 1994. Resistência de Cucurbita maxima a Phytophthora capsici. Pesquisa Agropecuria Brasileira. 29: 341-344.).

Despite the high number of genebank accessions evaluated for resistance, mostly wild species, they do not present satisfactory agronomic characteristics, such as high yields and fruit quality. However, they represent important genetic resources to be explored and considered in plant breeding to improve resistance to P. capsici, especially in species of Solanaceae and Cucurbitaceae. On the other hand, the scarce sources of resistance encountered so far, in few resistant cultivars (or none in the case of tomato, melon and pumpkins) available on the market, is probably due to complex genetic control, governed by few or several genes.

Cultural control

The use of adequate cultural practices that favor the plant and disfavor the pathogen contributes substantially to the reduction of plants affected by P. capsici (Narayanasamy, 2013NARAYANASAMY, P. 2013. Biological disease management systems for agricultural crops. In Biological Management of Diseases of Crops. NARAYANASAMY, P. COIMBATORE, ID (eds): Springer. p.189-236. https://doi.org/10.1007/978-94-007-6377-7_6
https://doi.org/10.1007/978-94-007-6377-...
). Continuous cropping of susceptible cultivars in the same field favors the increase of inoculum levels in the soil over time (Bowers & Mitchell, 1991BOWERS, JH; MITCHELL, DJ. 1991. Relationship between inoculum level of Phytophthora capsici and mortality pepper. Phytopathology81: 178-184. https://doi.org/10.1094/Phyto-81-178
https://doi.org/10.1094/Phyto-81-178...
). Crop rotation with non-host species is recommended for the reduction of plant pathogens. However, the survival of P. capsici oospores for more than 36 months makes rotation not completely effective and viable when both pathogen mating types are present in the field (Babadoost & Pavon, 2013BABADOOST, M; PAVON, C. 2013. Survival of oospores of Phytophthora capsici in soil. Plant Disease 97: 1478-1483. https://doi.org/10.1094/PDIS-12-12-1123-RE
https://doi.org/10.1094/PDIS-12-12-1123-...
). However, the natural presence of both mating types in a field and on an infected plant is rare (Ristaino, 1991RISTAINO, JB. 1991. Influence of rainfall, drip irrigation, and inoculum density on the development of Phytophthora root and crown rot epidemics and yield in bell pepper. Phytopathology81: 922-929.; Erwin & Ribeiro, 1996ERWIN, D; RIBERO, O. 1996. Phytophthora Diseases Worldwide. Minnesota, USA: APS PRESS. 592p.). Kim (1989KIM, CH. 1989. Phytophthora blight and other diseases of red pepper in Korea: disease and pest problems from continuous cropping. Research in Plant Disease 302: 10-17. https://doi.org/10.5423/RPD.2002.8.3.131
https://doi.org/10.5423/RPD.2002.8.3.131...
) observed a reduction in the incidence of leaf blight in chili peppers in rotations with peanuts (Arachis hypogaea) and sesame (Sesamum indicum). It was shown that a four-year crop rotation program with non-host species and effective weed control are recommended for management of Phytophthora blight of peppers, for significantly reducing the level of inoculum (oospores) in the field (Babadoost et al., 2015BABADOOST, M; PAVON, C; ISLAM, SZ; TIAN, D. 2015. Phytophthora blight (Phytophthora capsici) of pepper and its management. Acta Horticulturae, 1105: 61-66. https://doi.org/10.17660/ActaHortic.2015.1105.9
https://doi.org/10.17660/ActaHortic.2015...
).

Intense rains or excess moisture in the soil due to excess irrigation water (ponding), provide ideal conditions for the pathogen (Café Filho et al., 2019CAFÉ-FILHO, A; DUNIWAY, JM; DAVIS, RM. 1995. Effects of the frequency of furrow irrigation on root and fruits rots of squash caused by Phytophthora capsici. Plant Disease 79: 44-48. https://doi.org/10.1094/PD-79-0044
https://doi.org/10.1094/PD-79-0044...
) (Figure 3). Thus, irrigation should limit to soil saturation because accumulation and movement of water within the field contribute to the spread of P. capsici (Ristaino, 1991RISTAINO, JB. 1991. Influence of rainfall, drip irrigation, and inoculum density on the development of Phytophthora root and crown rot epidemics and yield in bell pepper. Phytopathology81: 922-929.; Granke et al., 2012aGRANKE, LL; QUESADA‐OCAMPO, LM; LAMOUR, K; HAUSBECK, MK. 2012a. Advances in research on Phytophthora capsici on vegetable crops in the United States. Plant Disease 95: 1588‐1600. https://doi.org/10.1094/PDIS-02-12-0211-FE
https://doi.org/10.1094/PDIS-02-12-0211-...
).

Figure 3
Sweet pepper plants (Capsicum annuum) affected by Phytophthora capsici under field conditions: (A) plant affected in a plantation with a drip irrigation system, (B) high incidence of wilt in pepper plants due to improper use of gravity (furrow) irrigation, and (C) excessive application of water in a gravity irrigation system. Source: Unpublished photographs from the authors. Ecuador, Technical University of Manabí, 2018-2020.

In zucchini (Cucurbita pepo var. melopepo cv. Early) the effect of a 7-day interval irrigation resulted in more incidence of P. capsici than a 14 or 21 interval (Café Filho et al., 1995CAFÉ-FILHO, A; LOPES, CA; ROSSATO, M. 2019. Management of plant disease epidemics with irrigation practices. In: ONDRAŠEK, G (ed). Irrigation in Agroecosystems. London, UK: IntechOpen. p. 123-141. https://doi.org/10.5772/intechopen.7825
https://doi.org/10.5772/intechopen.7825...
). Xie et al. (1999XIE, J; CARDENAS, ES; SAMMIS, TW; WALL, MM; LINDSEY, DL; MURRAY, LW. 1999. Effects of irrigation method on chile pepper yield and Phytophthora root rot incidence. Agricultural Water Management 42: 127-142. https://doi.org/10.1016/S0378-3774(99)00038-4
https://doi.org/10.1016/S0378-3774(99)00...
) observed less damage by P. capsici in peppers when drip irrigation was used than of gravity irrigation. Usually, irrigation in high-frequency increases fruit yield in crops such as chili pepper (Ristaino, 1991RISTAINO, JB. 1991. Influence of rainfall, drip irrigation, and inoculum density on the development of Phytophthora root and crown rot epidemics and yield in bell pepper. Phytopathology81: 922-929.). In addition, it creates unfavorable conditions for spreading the pathogen in the field (Xie et al., 1999CAFÉ-FILHO, A; DUNIWAY, JM; DAVIS, RM. 1995. Effects of the frequency of furrow irrigation on root and fruits rots of squash caused by Phytophthora capsici. Plant Disease 79: 44-48. https://doi.org/10.1094/PD-79-0044
https://doi.org/10.1094/PD-79-0044...
).

Damage caused by P. capsici may be reduced with the establishment of crops in soils with good drainage, low compaction and adequate irrigation system (Ristaino & Johnston, 1999RISTAINO, JB; JOHNSTON, SA. 1999. Ecologically based approaches to management of Phytophthora blight on bell pepper. Plant Disease 83: 1080-1089. https://doi.org/10.1094/PDIS.1999.83.12.1080
https://doi.org/10.1094/PDIS.1999.83.12....
; Café Filho et al., 2019CAFÉ-FILHO, A; LOPES, CA; ROSSATO, M. 2019. Management of plant disease epidemics with irrigation practices. In: ONDRAŠEK, G (ed). Irrigation in Agroecosystems. London, UK: IntechOpen. p. 123-141. https://doi.org/10.5772/intechopen.7825
https://doi.org/10.5772/intechopen.7825...
). Raised beds also minimize the probabilities of moisture accumulation at the base of the plants. During the rainy season, it is advisable to remodel the planting beds with a slight angle of inclination to promote the displacement of excess water towards leakage areas (Granke et al., 2012aGRANKE, LL; QUESADA‐OCAMPO, LM; LAMOUR, K; HAUSBECK, MK. 2012a. Advances in research on Phytophthora capsici on vegetable crops in the United States. Plant Disease 95: 1588‐1600. https://doi.org/10.1094/PDIS-02-12-0211-FE
https://doi.org/10.1094/PDIS-02-12-0211-...
; Ristaino & Johnston, 1999RISTAINO, JB; JOHNSTON, SA. 1999. Ecologically based approaches to management of Phytophthora blight on bell pepper. Plant Disease 83: 1080-1089. https://doi.org/10.1094/PDIS.1999.83.12.1080
https://doi.org/10.1094/PDIS.1999.83.12....
). In this sense, the use of natural (wheat, rice or other leftovers) or synthetic (plastic) mulch, is also a good strategy for the management of P. capsici (Hausbeck & Lamour, 2004HAUSBECK, MK; LAMOUR, KH. 2004. Phytophthora capsici on vegetable crops: Research progress and management challenges. Plant Disease 88: 1292-1303. https://doi.org/10.1094/PDIS.2004.88.12.1292
https://doi.org/10.1094/PDIS.2004.88.12....
).

Plant covers can significantly reduce epidemics caused by soilborne Phytophthora spp. avoiding water splashes (an important factor of dispersal of the pathogen) on infested soils. For example, the use of wheat stubble on bell peppers established under a zero-tillage cultivation system avoided splash generated by water and reduced both the spread and incidence of the Phytophthora blight (Ristaino et al., 1997RISTAINO, JB; PARRA, G; CAMBELL, L. 1997. Suppression of Phytophthora blight in bell pepper by a no-till wheat cover crop. Phytopathology 87: 242-249. https://doi.org/10.1094/PHYTO.1997.87.3.242
https://doi.org/10.1094/PHYTO.1997.87.3....
). Madden & Ellis (1990MADDEN, LV; ELLIS, MA. 1990. Effect of ground cover on splash dispersal of Phytophthora cactorum from strawberry. Journal of Phytopathology 129: 170-174. https://doi.org/10.1111/j.1439-0434.1990.tb04301.x
https://doi.org/10.1111/j.1439-0434.1990...
) also observed a reduction in the incidence of leather rot caused by P. cactorum on strawberries. The use of cover affects the physical, chemical and biological dynamics of the soil, with a positive impact on the spatial and temporal progress of epidemics caused by P. capsici (Liu et al., 2007LIU, B; GUMPERTZ, ML; HU, S; RISTAINO, JB. 2007. Effect of prior tillage and soil fertility amendments on dispersal of Phytophthora capsici and infection of pepper. European Journal Plant Pathology 120: 273-287. https://doi.org/10.1007/s10658-007-9216-7
https://doi.org/10.1007/s10658-007-9216-...
).

The black polyethylene plastic cover is a variant of the vegetal cover (Figure 4), but it works under the same principle; reduce the dispersion of inoculum by water splashes on bare soils and also prevents the growth of weeds that serve as hosts of the pathogen within rows or seed beds (Ploetz & Haynes, 2000PLOETZ, RC; HAYNES, JL. 2000. How does Phytophthora capsici survive in squash fields in Southeastern Florida during the off-season? Proceedings of the Annual Meeting of the Florida State Horticultural Society 113: 211-215.). A notable decrease in leaf blight epidemics, high yields and higher quality fruits have been obtained in pepper by using this system (Roe et al., 1994ROE, NE; STOFFELLA, PJ; BRYAN, HH. 1994. Growth and yields of bell pepper and winter squash grown with organic and living mulches. Journal of the American Society for Horticultural Science 119: 193-1999. https://doi.org/10.21273/JASHS.119.6.1193
https://doi.org/10.21273/JASHS.119.6.119...
; Ristaino & Johnston, 1999RISTAINO, JB; JOHNSTON, SA. 1999. Ecologically based approaches to management of Phytophthora blight on bell pepper. Plant Disease 83: 1080-1089. https://doi.org/10.1094/PDIS.1999.83.12.1080
https://doi.org/10.1094/PDIS.1999.83.12....
).

Figure 4
(A and B) Preparation of raised beds with plastic mulch for the establishment of pepper (Capsicum annuum), (C) tomato (Solanum lycopersicum) and (D) watermelon (Citrullus sp.) crops with plasticulture system. Source: Unpublished photographs from the authors. Ecuador, Technical University of Manabí, 2018-2020.

Organic amendments can also contribute to the maintenance of low levels of diseases caused by soil-associated pathogens by providing a natural biocontrol through increasing the diversity of microorganisms in the soil (Bonanomi et al., 2007BONANOMI, G; ANTIGNANI, V; PANE, C; SCALA, F. 2007. Suppression of soilborne fungal diseases with organic amendments. Journal of Plant Pathology 89: 311-324.). This practice has been effective in the cultivation of bell pepper by the addition of compost (obtained from solid urban and biodegradable waste) to the soil, reducing neck rot caused by P. capsici (Gilardi et al., 2013GILARDI, G; BAUDINO, M; MOIZIO, M; PUGLIESE, M; GARIBALDI, A; GULLINO, ML. 2013. Integrated management of Phytophthora capsici on bell pepper by combining grafting and compost treatment. Crop Protection 53: 13-19. https://doi.org/10.1016/j.cropro.2013.06.008
https://doi.org/10.1016/j.cropro.2013.06...
). This practice is low-cost and contributes to the improvement of soil fertility, to be considered an alternative for organic farming.

Physical control

Plant pathogens cause disease within an ideal temperature range and are sensitive to extreme modifications compromising their survival status (Kanaan et al., 2017KANAAN, H; FRENK, S; RAVIV, M; MEDINAB, S; MINZC, D. 2017. Long and short term effects of solarization on soil microbiome and agricultural production. Applied Soil Ecology 124: 54-61. https://doi.org/10.1016/j.apsoil.2017.10.026
https://doi.org/10.1016/j.apsoil.2017.10...
). This is the principle of soil solarization, which may be used in the management of pathogens such as Phytophthora spp. and Pythium ultimum (Gamliel & Stapleton, 1993GAMLIEL, A; STAPLETON, JJ. 1993. Effect of chicken compost or ammonium phosphate and solarization on pathogen control, rhizosphere microorganisms, and lettuce growth. Plant Disease 77: 886-891. https://doi.org/10.1094/PD-77-0886
https://doi.org/10.1094/PD-77-0886...
; Hartz et al., 1993HARTZ, TK; DEVAY, JE; ELMORE, CL. 1993. Solarization is an effective soil disinfestation technique for strawberry production. HortScience 28: 104-106. https://doi.org/10.21273/HORTSCI.28.2.104
https://doi.org/10.21273/HORTSCI.28.2.10...
). Soil solarization is a special mulching process that causes hydrothermal disinfection and changes in the biological composition of soils with benefits for the health and growth of plants (Kanaan et al., 2017). This effective strategy used in pre- and post-sowing is compatible with chemical treatments and biological amendments (Gandariasbeitia et al., 2019GANDARIASBEITIA, M; OJINAGA, M; ORBEGOZO, E; ORTIZ-BARREDO1, A; NÚÑEZ-ZOFÍO, M; MENDARTE, S; LARREGLA, S. 2019. Winter biodisinfestation with Brassica green manure is a promising management strategy for Phytophthora capsici control of protected pepper crops in humid temperate climate regions of northern Spain. Spanish Journal of Agricultural Research 17: 1-11. https://doi.org/10.5424/sjar/2019171-13808
https://doi.org/10.5424/sjar/2019171-138...
). The effectiveness of solarization is directly related to the availability and duration of direct sun exposure and to the thickness of the plastic sheet, with better results being observed with low thickness plastics (25 µm), compared to those with greater thickness (between 50 µm and 100 µm) (Souza, 1994SOUZA, NL. 1994. Solarização do solo. Summa Phytopathologica 20: 3-15.).

Solar collectors to disinfest substrates or transparent plastic polyethylene film can be found in the market (Ghini et al., 2000GHINI, R; MARQUES, JF; TOKUNAGA, T; BUENO, SCS. 2000. Controle de Phytophthora sp. e avaliação econômica do coletor solar para desinfestação de substratos. Fitopatologia Venezolana 13: 11-14.; May-de-Mio et al., 2002MAY-DE-MIO, LL; GHINI, R; KIMATI, H. 2002. Solarização para controle de Phytophthora parasitica em mudas de citros. Fitopatologia Brasileira 27: 254-258. https://doi.org/10.1590/S0100-41582002000300003
https://doi.org/10.1590/S0100-4158200200...
). The latter is based on covering the soil surface (in a state of high humidity; saturation) with a plastic film for 6 weeks. In this period, solar radiation increases the temperature of the soil to levels where most pathogens are unable to survive, thus reducing the inoculum density (oospores) and the potential danger of a disease (Gandariasbeitia et al., 2019GANDARIASBEITIA, M; OJINAGA, M; ORBEGOZO, E; ORTIZ-BARREDO1, A; NÚÑEZ-ZOFÍO, M; MENDARTE, S; LARREGLA, S. 2019. Winter biodisinfestation with Brassica green manure is a promising management strategy for Phytophthora capsici control of protected pepper crops in humid temperate climate regions of northern Spain. Spanish Journal of Agricultural Research 17: 1-11. https://doi.org/10.5424/sjar/2019171-13808
https://doi.org/10.5424/sjar/2019171-138...
). Most oomycetes may be eliminated in soil at temperatures above 40°C. In contrast, several beneficial microorganisms survive and occupy the soil niche more quickly than the pathogens (Etxeberria et al., 2011ETXEBERRIA, A; MENDARTE, S; LARREGLA, S. 2011. Thermal inactivation of Phytophthora capsici oospores. Revista Iberoamericana de Micología 28: 83-90. https://doi.org/10.1016/j.riam.2011.01.004
https://doi.org/10.1016/j.riam.2011.01.0...
), thus providing a natural biological control.

Soil solarization may be complemented with the application of organic amendments (Gamliel et al., 2000GAMLIEL, A; AUSTERWEIL, M; KRITZMAN, G. 2000. Non-chemical approach to soilborne pest management: organic amendment. Crop Protection19: 847-853. https://doi.org/10.1016/S0261-2194(00)00112-5
https://doi.org/10.1016/S0261-2194(00)00...
; Núñez-Zofío et al., 2010NÚÑEZ-ZOFÍO, M; GARBISU, C; LARREGLA, S. 2010. Application of organic amendments followed by plastic mulching for the control of Phytophthora root rot of pepper in Northern Spain. ISHS Acta Horticulturae 883: 353-360. https://doi.org/10.17660/ActaHortic.2010.883.44
https://doi.org/10.17660/ActaHortic.2010...
). The combination of both practices controls pathogens in several ways: (i) accumulation of volatile toxic compounds resulting from the decomposition of organic matter; (ii) creation of anaerobic soil conditions; and (iii) increased suppression of soil pathogens due to high levels of microbial activity (Gamliel et al., 2000GAMLIEL, A; AUSTERWEIL, M; KRITZMAN, G. 2000. Non-chemical approach to soilborne pest management: organic amendment. Crop Protection19: 847-853. https://doi.org/10.1016/S0261-2194(00)00112-5
https://doi.org/10.1016/S0261-2194(00)00...
). According to Núñez-Zofío et al. (2011)NÚÑEZ-ZOFÍO, M; LARREGLA, S; GARBISU, C. 2011. Application of organic amendments followed by soil plastic mulching reduces the incidence of Phytophthora capsici in pepper crops under temperate climate. Crop protection 30: 1563-1572. https://doi.org/10.1016/j.cropro.2011.08.020
https://doi.org/10.1016/j.cropro.2011.08...
, the incorporation of semi or non-decomposed compost mixtures followed by the use of transparent plastic reduces the incidence of root and crown rot up to 86% in pepper by partially reducing the viability of oospores in the soil. Cabbage cropping amendments plus solarization produce a significant control of Phytophthora nicotianae and P. capsici up to a depth of 10 cm (Coelho et al., 1999COELHO, L; CHELLEMI, DO; MITCHELL, DJ. 1999. Efficacy of solarization and cabbage amendment for the control of Phytophthora spp. in North Florida. Plant Disease 83: 293-299. https://doi.org/10.1094/PDIS.1999.83.3.293
https://doi.org/10.1094/PDIS.1999.83.3.2...
). Soil solarization is a significant advance in the non-chemical management of many soil-related pathogens, but it is limited to areas where climatic conditions are favorable.

Biologic control

Biological control agents (BCAs) can be viable alternative strategies to manage diseases caused by soil-associated pathogens (Diánez et al., 2015DIÁNEZ, F; SANTOS, M;CARRETERO MARÍN, F. 2015. Trichoderma saturnisporum, a new biological control agent. Science of Food and Agriculture 96: 1934-1944. https://doi.org/10.1002/jsfa.7301
https://doi.org/10.1002/jsfa.7301...
). These act through different modes of action, such as hyperparasitism, antibiosis, competition or induced resistance and priming in plants (Köhl et al., 2019KÖHL, J; KOLNAAR, R; RAVENSBERG, WJ. 2019. Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy. Frontiers in Plant Science 10: 845. https://doi.org/10.3389/fpls.2019.00845
https://doi.org/10.3389/fpls.2019.00845...
). The most widespread and used BCAs in the biological control of pathogens include fungi (Trichoderma spp.) and bacteria (Bacillus spp., Streptomyces spp. and Pseudomonas spp.), isolated from the rhizosphere or endosphere (Zohaib et al., 2019ZOHAIB, M, USMAN, M; HUSSAIN, I. 2019. Bio-efficacy of trichoderma isolates and Bacillus subtilis against root rot of muskmelon Cucumis melo L. Caused by Phytophthora drechsleri under controlled and field conditions. Pakistan Journal of Botany 51: 1877-1882. http://dx.doi.org/10.30848/PJB2019-5(13)
https://doi.org/10.30848/PJB2019-5(13)...
). The range of commercial biological products registered for diseases control caused by Phytophthora sp. is reduced. Currently, there is increasing research where the biological action of many strains of fungi and bacteria has been demonstrated against P. capsici (Das et al., 2019DAS, MM; HARIDAS, M; SABU, A. 2019. Biological control of black pepper and ginger pathogens, Fusarium oxysporum, Rhizoctonia solani and Phytophthora capsici, using Trichoderma spp. Biocatalysis and Agricultural Biotechnology 17: 177-183. https://doi.org/10.1016/j.bcab.2018.11.021
https://doi.org/10.1016/j.bcab.2018.11.0...
; Santos et al., 2019SANTOS, M; DIÁNEZ, F; MORENO-GAVÍRA, A; SÁNCHEZ-MONTESINOS, B; GEA, FJ. 2019. Cladobotryum mycophilum as potential biocontrol agent. Agronomy9: 891. https://doi.org/10.3390/agronomy9120891
https://doi.org/10.3390/agronomy9120891...
; Syed-Ab-Rahman et al., 2019SYED-AB-RAHMAN, SF; XIAO, Y; CARVALHAIS, LC; FERGUSONC, BJ; SCHENKA, PM. 2019. Suppression of Phytophthora capsici infection and promotion of tomato growth by soil bacteria. Rhizosphere9: 72-75. https://doi.org/10.1016/j.rhisph.2018.11.007
https://doi.org/10.1016/j.rhisph.2018.11...
; Abbasi et al., 2020ABBASI, S; SAFAIE, N; SADEGHI, A; SHAMSBAKHSH, M. 2020. Tissue-specific synergistic bio-priming of pepper by two Streptomyces species against Phytophthora capsici. PloS one, 15: e0230531. https://doi.org/10.1371/journal.pone.0230531
https://doi.org/10.1371/journal.pone.023...
; Bhusal & Mmbaga, 2020BHUSAL, B; MMBAGA, MT. 2020. Biological control of Phytophthora blight and growth promotion in sweet pepper by Bacillus species. Biological Control 150: 104373. https://doi.org/10.1016/j.biocontrol.2020.104373
https://doi.org/10.1016/j.biocontrol.202...
; Li et al., 2020LI, Y; FENG, X; WANG, X; ZHENG, L; LIU, B. 2020. Inhibitory effects of Bacillus licheniformis BL06 on Phytophthora capsici in pepper by multiple modes of action. Biological Control 144: 104210. https://doi.org/10.1016/j.biocontrol.2020.104210
https://doi.org/10.1016/j.biocontrol.202...
; Tomah et al., 2020TOMAH, AA; ALAMER, IS; LI, B; ZHANG, JZ. 2020. A new species of Trichoderma and gliotoxin role: A new observation in enhancing biocontrol potential of T. virens against Phytophthora capsici on chili pepper. Biological Control 145: 104261. https://doi.org/10.1016/j.biocontrol.2020.104261
https://doi.org/10.1016/j.biocontrol.202...
). Sometimes, certain BCAs can be used in a compatible way with some oomiceticides, expanding the control spectrum (Widmer, 2019WIDMER, TL. 2019. Compatibility of Trichoderma asperellum isolates to selected soil fungicides. Crop Protection 120: 91-96. https://doi.org/10.1016/j.cropro.2019.02.017
https://doi.org/10.1016/j.cropro.2019.02...
).

The aqueous extracts obtained from compost is another option for plant diseases control. These extracts are constituted by diverse microbial populations to control Phytophthora spp. as alternative to the use of synthetic oomycitecides (Koné et al., 2010KONÉ, SB; DIONNE, A; TWEDDELL, RJ; ANTOUN, H; AVIS, TJ. 2010. Suppressive effect of non-aerated compost teas on foliar fungal pathogens of tomato. Biological Control 52: 167-173. https://doi.org/10.1016/j.biocontrol.2009.10.018
https://doi.org/10.1016/j.biocontrol.200...
). These substances have suppressive properties and antagonistic activity against plant pathogens (Noble & Coventry, 2005NOBLE, R; COVENTRY, E. 2005. Suppression of soil-borne plant diseases with composts: a review. Biocontrol Science and Technology 15: 3-20. https://doi.org/10.1080/09583150400015904
https://doi.org/10.1080/0958315040001590...
). For instance, Marín et al. (2014MARÍN, F; DIÁNEZ, F; SANTOS, M; CARRETERO, F; GEA, FJ; CASTAÑEDA, C; YAU, JA. 2014. Control of Phytophthora capsici and Phytophthora parasitica on pepper (Capsicum annuum L.) with compost teas from different sources, and their effects on plant growth promotion. Phytopathologia Mediterranea 53: 216-228. https://doi.org/10.14601/Phytopathol_Mediterr-12173
https://doi.org/10.14601/Phytopathol_Med...
) observed positive effect on the development of chili and pepper plants infected by P. capsici and P. parasitica, when non-aerated compost tea extract was applied. This practice can also be used as an alternative to the use of synthetic fertilizers and oomycitecides, due to the stimulation of plant growth, sanitary protection and increased fruit yield in Capsicum spp.

Beneficial microorganisms in compost extracts include bacteria, fungi, and protozoa, which form a physical barrier against disease-causing agents, creating a suppressive environment where pathogenic organisms reduce their activity, furthermore, they can induce growth and resistance (González-Hernández et al., 2021GONZÁLEZ-HERNÁNDEZ, AI; SUÁREZ-FERNÁNDEZ, MB; PÉREZ-SÁNCHEZ, R; GÓMEZ-SÁNCHEZ, MA; MORALES-CORTS, MR. 2021. Compost tea induces growth and resistance against Rhizoctonia solani and Phytophthora capsici in pepper. Agronomy11: 781. https://doi.org/10.3390/agronomy11040781
https://doi.org/10.3390/agronomy11040781...
). Such microorganisms have been suggested to suppress plant pathogens through various mechanisms, including induction of resistance against pathogens (Hoitink et al., 1977HOITINK, HA; DOREN, DM; SCHMITTHENNER, AF. 1977. Suppression of Phytophthora cinnamomi in a composted hardwood bark potting medium. Phytopathology67: 561-565. https://doi.org/10.1094/Phyto-67-561
https://doi.org/10.1094/Phyto-67-561...
), inhibition of spore germination and antagonism and competition by nutrients (Whipps, 2001WHIPPS, JM. 2001. Microbial interactions and biocontrol in the rhizosphere. Journal of Experimental Botany 52: 487-511. https://doi.org/10.1093/jexbot/52.suppl_1.487
https://doi.org/10.1093/jexbot/52.suppl_...
). Aqueous extracts of compost have suppressed the infection caused by P. capsici in pepper by inducing systemic resistance in plants, promoting, for example, the expression of genes related to pathogenesis (CABPR1, CABGLU, CAChi2, CaPR-4, CAPO1, or CaPR-10), as well as the enzymatic activity of β-1,3-glucanase, chitinase and peroxidase, improving the defense response of plants against the attack of the pathogen (Sang et al., 2010SANG, MK; KIM, JG; KIM, KD. 2010. Biocontrol activity and induction of systemic resistance in pepper by compost water extracts against Phytophthora capsici. Phytopathology 100: 774-783. https://doi.org/10.1094/PHYTO-100-8-0774
https://doi.org/10.1094/PHYTO-100-8-0774...
). Although several studies have generated optimal results in the control of P. capsici as alternative methods, most of them were not adequately tested on large scale or under field conditions. However, the methods developed in such studies could in the future become successful or complementary tools in the control of P. capsici.

Chemical control

The chemical molecules (synthetic origin) are key components in the successful management of diseases caused by P. capsici under field conditions (Matheron & Porchas, 2014MATHERON, ME; PORCHAS, M. 2014. Effectiveness of 14 fungicides for suppressing lesions caused by Phytophthora capsici on inoculated stems of chile pepper seedlings. Plant Health Progress 15: 166-171. https://doi.org/10.1094/PHP-RS-14-0017
https://doi.org/10.1094/PHP-RS-14-0017...
). However, when environmental conditions favor the development of the disease, no currently available fungicide has shown to fully control the pathogen (Granke et al., 2012aGRANKE, LL; QUESADA‐OCAMPO, LM; LAMOUR, K; HAUSBECK, MK. 2012a. Advances in research on Phytophthora capsici on vegetable crops in the United States. Plant Disease 95: 1588‐1600. https://doi.org/10.1094/PDIS-02-12-0211-FE
https://doi.org/10.1094/PDIS-02-12-0211-...
). Despite the limited efficacy of fungicides, they exert an extra degree of protection when combined with other management practices such as crop rotation, raised beds, and irrigation water management (Hausbeck & Lamour, 2004HAUSBECK, MK; LAMOUR, KH. 2004. Phytophthora capsici on vegetable crops: Research progress and management challenges. Plant Disease 88: 1292-1303. https://doi.org/10.1094/PDIS.2004.88.12.1292
https://doi.org/10.1094/PDIS.2004.88.12....
). Currently, the range of active ingredients available in the market for the control of P. capsici is scarce and with inadequate control efficacy (Table 1), with specific formulations for application to the soil and foliage. The different molecules for the control of oomycetes are applied in a preventive way, both to the soil and to aerial organs (Gisi & Sierotzki, 2015GISI, U; SIEROTZKI, H. 2015. Oomycete fungicides: phenylamides, quinone outside inhibitors, and carboxylic acid amides. In: ISHI, H; HOLLOMON, DW (eds). Fungicides Resistance in Plant Pathogens. Tokyo, JP: Springer. p. 145-174. https://doi.org/10.1007/978-4-431-55642-8_10
https://doi.org/10.1007/978-4-431-55642-...
), because the applications of a curative type, after infection by P. capsici, are in most cases ineffective.

Table 1
Registered fungicides for use in the management of diseases caused by P. capsici. Ecuador, Technical University of Manabí, 2018-2020.

Fungicide application methods should be chosen based on the affected organ, for example, root or aerial infection. In this way, the control of root and crown rot caused by P. capsici is carried out with targeted applications through drip irrigation or drenching, while foliar applications include spraying the aerial organs with equipment such as hydraulic function, centrifuge, etc. (Granke et al., 2012aGRANKE, LL; QUESADA‐OCAMPO, LM; LAMOUR, K; HAUSBECK, MK. 2012a. Advances in research on Phytophthora capsici on vegetable crops in the United States. Plant Disease 95: 1588‐1600. https://doi.org/10.1094/PDIS-02-12-0211-FE
https://doi.org/10.1094/PDIS-02-12-0211-...
).

The inappropriate use of fungicides can increase resistance of P. capsici which is an organism with high genetic plasticity and have developed insensitivity to molecules such as metalaxyl (Parra & Ristaino, 2001PARRA, G; RISTAINO, JB. 2001. Resistance to mefenoxam and metalaxyl among field isolates of Phytophthora capsici causing Phytophthora blight of pepper. Plant Disease 85: 1069-1075. https://doi.org/10.1094/PDIS.2001.85.10.1069
https://doi.org/10.1094/PDIS.2001.85.10....
; Dunn et al., 2010DUNN, AR; MILGROOM, MG; MEITZ, JC; MCLEOD, A; FRY, WE; MCGRATH, MT; DILLARD, HR; SMART, CD. 2010. Population structure and resistance to mefenoxam of Phytophthora capsici in New York State. Plant Disease 94: 1461-1468. https://doi.org/10.1094/PDIS-03-10-0221
https://doi.org/10.1094/PDIS-03-10-0221...
; Wang et al., 2021WANG, W; LIU, D; ZHUO, X; WANG, Y; SONG, Z; CHEN, F; PANA, Y; GAO, Z. 2021. The RPA190-pc gene participates in the regulation of metalaxyl sensitivity, pathogenicity and growth in Phytophthora capsici. Gene764: 145081. https://doi.org/10.1016/j.gene.2020.145081
https://doi.org/10.1016/j.gene.2020.1450...
). In fact, resistance of P. capsici to metalaxyl has been caused by the long-term intense use of this fungicide (Wang et al., 2001WANG, W; LIU, D; ZHUO, X; WANG, Y; SONG, Z; CHEN, F; PANA, Y; GAO, Z. 2021. The RPA190-pc gene participates in the regulation of metalaxyl sensitivity, pathogenicity and growth in Phytophthora capsici. Gene764: 145081. https://doi.org/10.1016/j.gene.2020.145081
https://doi.org/10.1016/j.gene.2020.1450...
). A solution to dissipate this problem is the use of other active principles such as mandipropamid and dimethomorph, which act on the synthesis of lipids and membranes, as well as on the synthesis of cellulose and cell wall of oomycetes, and are considered as fungicides of low to medium risk of resistance (FRAC, 2020FRAC. 2020. Fungal control agents sorted by cross resistance pattern and mode of action. Available at: Available at: https://www.frac.info/ . AccessedJuly 02, 2021.
https://www.frac.info/...
; Siegenthaler & Hansen, 2021SIEGENTHALER, TB; HANSEN, Z. 2021. Sensitivity of Phytophthora capsici from Tennessee to mefenoxam, fluopicolide, oxathiapiprolin, dimethomorph, mandipropamid, and cyazofamid. Plant Disease https://doi.org/10.1094/PDIS-08-20-1805-RE
https://doi.org/10.1094/PDIS-08-20-1805-...
). Another aspect to consider in the management of resistance to fungicides is to have a wide range of molecules applied in periodic and programmed rotation at the maximum amount of application per crop cycle (Castro et al., 2014CASTRO, A; FLORES, J; AGUIRRE, M; FERNÁNDEZ, SP; RODRÍGUEZ, G; OSUMA, P. 2014. Traditional and molecular studies of the plant pathogen Phytophthora capsici: a review. Journal of Plant Pathology & Microbiology 5: 245-253. https://doi.org/10.4172/2157-7471.1000245
https://doi.org/10.4172/2157-7471.100024...
). Other approach used to reduce the selection pressure of resistant phytopathogenic fungi populations is the mixture of systemic and protective fungicides. This practice is important due to the several reports of resistance outbreaks in populations of P. capsici to cyazofamid, fluopicolide, mefenoxam, metalaxyl, and oxathiapiprolin fungicides (Parra & Ristaino, 2001RISTAINO, JB; JOHNSTON, SA. 1999. Ecologically based approaches to management of Phytophthora blight on bell pepper. Plant Disease 83: 1080-1089. https://doi.org/10.1094/PDIS.1999.83.12.1080
https://doi.org/10.1094/PDIS.1999.83.12....
; Wang et al., 2020WANG, W; LIU, X; HAN, T; LI, K; QU, Y; GAO, Z. 2020. Differential potential of Phytophthora capsici resistance mechanisms to the fungicide metalaxyl in peppers. Microorganisms8: 278. https://doi.org/10.3390/microorganisms8020278
https://doi.org/10.3390/microorganisms80...
; Siegenthaler & Hansen, 2021SIEGENTHALER, TB; HANSEN, Z. 2021. Sensitivity of Phytophthora capsici from Tennessee to mefenoxam, fluopicolide, oxathiapiprolin, dimethomorph, mandipropamid, and cyazofamid. Plant Disease https://doi.org/10.1094/PDIS-08-20-1805-RE
https://doi.org/10.1094/PDIS-08-20-1805-...
; Wang et al., 2021WANG, L; JI, P. 2021. Fitness and competitive ability of field isolates of Phytophthora capsici resistant or sensitive to fluopicolide. Plant Disease https://doi.org/10.1094/PDIS-08-20-1729-RE
https://doi.org/10.1094/PDIS-08-20-1729-...
; Wang & Ji, 2021WANG, W; LIU, X; HAN, T; LI, K; QU, Y; GAO, Z. 2020. Differential potential of Phytophthora capsici resistance mechanisms to the fungicide metalaxyl in peppers. Microorganisms8: 278. https://doi.org/10.3390/microorganisms8020278
https://doi.org/10.3390/microorganisms80...
).

Integrated management

The long-term risk of P. capsici infection in infested fields decreases when a disease management plan is applied using various tools in an integrated way from a sustainable approach, ranging from the use of resistant cultivars to proper soil operation, (Hausbeck & Lamour, 2004HAUSBECK, MK; LAMOUR, KH. 2004. Phytophthora capsici on vegetable crops: Research progress and management challenges. Plant Disease 88: 1292-1303. https://doi.org/10.1094/PDIS.2004.88.12.1292
https://doi.org/10.1094/PDIS.2004.88.12....
) (Figure 5).

Figure 5
Management methods to reduce epidemics associated with Phytophthora capsici and to increment the fruit yield and the economic return in horticultural crops. Source: Unpublished figure from the authors. Ecuador, Technical University of Manabí, 2018-2020.

The aim of integrated disease management is to minimize the activity of a causative agent and increase the yield of a given crop. The holistic and combined study of the soil and plant (Figure 5), which, within a conceptual framework operated as a whole, allows the development of strategies that help minimize the damage caused by pathogens such as P. capsici in vegetables (Sanogo & Ji, 2012SANOGO, S; JI, P. 2012. Integrated management of Phytophthora capsici on solanaceous and cucurbitaceous crops: current status, gaps in knowledge and research needs. Canadian Journal of Plant Pathology 34: 479-492. https://doi.org/10.1080/07060661.2012.732117
https://doi.org/10.1080/07060661.2012.73...
). The principles of integrated disease management are based on the integration of the basic concepts of immunization, exclusion, eradication and protection of plants against pathogens in order to prevent the potential economic, environmental and health risks that can occur (Razdan & Gupta, 2009RAZDAN, VK; GUPTA, S. 2009. Integrated disease management: concepts and practices. In: PESHIN, R; DHAWAN, AK (eds). Integrated pest management: innovation-development process. JAMMU, IN; Springer. p. 369-389. https://doi.org/10.1007/978-1-4020-8992-3_15
https://doi.org/10.1007/978-1-4020-8992-...
).

Usually, the adoption of only a single control practice is ineffective for the management of the diseases caused by P. capsici, regardless the host. Then farmers must be aware of the epidemiology of the disease and employ different strategies from early stages (pre-sowing) to the development and reproduction of the crop (Table 2).

Table 2
Strategies for managing Phytophthora capsici infection in vegetables in addition to the chemical control. Ecuador, Technical University of Manabí, 2018-2020.

Conclusions

The important economic losses that may be caused by P. capsici must be considered before establishing any horticultural production system. The selection and combined application of the different disease management practices will guarantee the avoidance and the reduction of losses caused by this oomycete plant pathogen. Thus, the integrated management of P. capsici seeks to create unfavorable conditions for the development of epidemics in the field. Starting from the principle of exclusion, which aims to prevent the entry of the pathogen into the agricultural exploitation area, followed by cultural operations and protection (chemical or biological) in order to maintain pathogen populations at non-harmful levels, with crops in optimal health, so they can express their maximum yield potential. The benefits of integrated disease management include reducing the use of chemical molecules, obtaining high fruit yields, and reducing costs associated with the control of other plant pathogenic agents. Finally, the results obtained from a successful P. capsici management program are: high economic return, long-term sustainable harvests, reduced environmental impact, and high-quality products that are safe for consumer health.

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Publication Dates

  • Publication in this collection
    22 Apr 2022
  • Date of issue
    Jan-Mar 2022

History

  • Received
    04 Mar 2021
  • Accepted
    13 Dec 2021
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