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plants Review Fantastic Downy Mildew Pathogens and How to Find Them: Advances in Detection and Diagnostics Andres F. Salcedo 1 , Savithri Purayannur 1 , Jeffrey R. Standish 1 , Timothy Miles 2, Lindsey Thiessen 1 and Lina M. Quesada-Ocampo 1,* 1 Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC 27695-7613, USA; [email protected] (A.F.S.); [email protected] (S.P.); [email protected] (J.R.S.); [email protected] (L.T.) 2 Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, MI 48824, USA; [email protected] * Correspondence: [email protected] Abstract: Downy mildews affect important crops and cause severe losses in production worldwide. Accurate identification and monitoring of these plant pathogens, especially at early stages of the disease, is fundamental in achieving effective disease control. The rapid development of molecular methods for diagnosis has provided more specific, fast, reliable, sensitive, and portable alternatives for plant pathogen detection and quantification than traditional approaches. In this review, we provide information on the use of molecular markers, serological techniques, and nucleic acid amplification technologies for downy mildew diagnosis, highlighting the benefits and disadvantages of the technologies and target selection. We emphasize the importance of incorporating information on pathogen variability in virulence and fungicide resistance for disease management and how the Citation: Salcedo, A.F.; Purayannur, development and application of diagnostic assays based on standard and promising technologies, S.; Standish, J.R.; Miles, T.; Thiessen, including high-throughput sequencing and genomics, are revolutionizing the development of species- L.; Quesada-Ocampo, L.M. Fantastic specific assays suitable for in-field diagnosis. Our review provides an overview of molecular detection Downy Mildew Pathogens and How technologies and a practical guide for selecting the best approaches for diagnosis. to Find Them: Advances in Detection and Diagnostics. Plants 2021, 10, 435. Keywords: downy mildews; molecular diagnostics; plant pathogens https://doi.org/10.3390/plants100 30435 Academic Editor: Anna Aksmann 1. Downy Mildew Pathogens and How to Find Them Downy mildew (DM) pathogens include several species of obligate oomycetes that Received: 30 November 2020 can cause devastating damage to commercial [1], landscape [2], and natural ecosystem Accepted: 15 February 2021 plants [3–5]. Species such as Plasmopara viticola [6], Pseudoperonospora cubensis [7], Pseu- Published: 25 February 2021 doperonospora humuli [8,9], Peronospora belbahrii [10], Plasmopara obducens [11], Peronospora tabacina [12] Peronospora effusa [13], Peronosclerospora philippinensis, and Sclerophthora rayssiae Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in var. zeae [14] have resulted in significant losses due to downy mildew epidemics around published maps and institutional affil- the world. In some instances, the epidemics have been so severe that they have prompted iations. historical shifts in crop production [15–18]. In addition to the aggressiveness of these pathogens, fungicide insensitivity further compounds losses attributed to disease [19–22]. Thus, research to improve diagnostics and management of downy mildew pathogens has become a priority for the scientific community in recent years [23–26]. The diagnostics of downy mildew diseases has mainly relied upon direct observation Copyright: © 2021 by the authors. of symptoms and signs using the naked eye or hand lenses and microscopes [27]. This is Licensee MDPI, Basel, Switzerland. This article is an open access article possible after observing their sexual (e.g., antheridia and oogonia) and asexual structures distributed under the terms and (e.g., sporangiophores, sporangia, and zoospores) (Figure1) involved in survival and conditions of the Creative Commons dispersion, and because many downy mildew pathogens produce distinctive foliar signs Attribution (CC BY) license (https:// and symptoms when colonizing a host plant [2,28,29]. However, such methods fall short creativecommons.org/licenses/by/ when detection in seed or planting material is needed [8,23], when symptoms and/or signs 4.0/). are not characteristic enough, resulting in misdiagnosis [30], or when the pathogen identity Plants 2021, 10, 435. https://doi.org/10.3390/plants10030435 https://www.mdpi.com/journal/plants Plants 2021, 10, x FOR PEER REVIEW 2 of 25 Plants 2021, 10, x FOR PEER REVIEW 2 of 25 Plants 2021, 10, 435 2 of 24 not characteristic enough, resulting in misdiagnosis [30], or when the pathogen identity not characteristic enough, resulting in misdiagnosis [30], or when the pathogen identity to species, pathotype, or clade level has disease management implications [31] (Figures 2– to species, pathotype, or clade level has disease management implications [31] (Figures 2– to5). species, For example, pathotype, Ps. humuli or clade, the level downy has disease mildew management pathogen of implications hop, causes [systemic31] (Figures infec-2– 5). For example, Ps. humuli, the downy mildew pathogen of hop, causes systemic infec- 5tions). For including example, thePs. humulirhizomes, the used downy as planting mildew pathogen material ofto hop,start causesnew hop systemic yards infections [8]. Simi- tions including the rhizomes used as planting material to start new hop yards [8]. Simi- includinglarly, the identification the rhizomes of used basil as downy planting mildew material caused to start by Pe. new belbahrii hop yards can be [8 complicated]. Similarly, larly, the identification of basil downy mildew caused by Pe. belbahrii can be complicated thebecause identification foliar lesions of basilcan be downy confused mildew with causednutritional by Pe.disorders belbahrii in thecan absence be complicated of patho- because foliar lesions can be confused with nutritional disorders in the absence of patho- becausegen sporulation foliar lesions [30]. canFurthermore, be confused isolates with nutritional of Ps. cubensis disorders causing in the downy absence mildew of pathogen in cu- gen sporulation [30]. Furthermore, isolates of Ps. cubensis causing downy mildew in cu- sporulationcurbits belong [30 ].to Furthermore,two host-adapted isolates clades of Ps. [31], cubensis with cladecausing 1 isolates downy mainly mildew infecting in cucurbits wa- curbits belong to two host-adapted clades [31], with clade 1 isolates mainly infecting wa- belongtermelon, to twosquash, host-adapted and pumpkin, clades and [31 ],clade with 2 clade isolates 1 isolates mainly mainly infecting infecting cucumber watermelon, and can- termelon, squash, and pumpkin, and clade 2 isolates mainly infecting cucumber and can- squash,taloupe, andthus pumpkin, initiation of and fungicide clade 2 isolatesapplicatio mainlyns in a infecting particular cucumber cucurbit crop and cantaloupe,depends on taloupe, thus initiation of fungicide applications in a particular cucurbit crop depends on thusthe clade initiation present of fungicide in a given applications area and time in a du particularring the cucurbitgrowing crop season depends [31,32]. on Molecular the clade the clade present in a given area and time during the growing season [31,32]. Molecular presenttechniques in a can given assist area with and early time duringdetection the of growing the pathogen season and [31, 32provide]. Molecular more accurate techniques di- techniques can assist with early detection of the pathogen and provide more accurate di- canagnostics assist withfor timely early detectiondeployment of the of pathogendisease management and provide morestrategies accurate for downy diagnostics mildew for agnostics for timely deployment of disease management strategies for downy mildew timely[33,34]. deployment of disease management strategies for downy mildew [33,34]. [33,34]. FigureFigure 1.1. SporangiophoresSporangiophores andand sporangiasporangia of of downy downy mildew mildew pathogens pathogens observed observed under under a compounda com- Figure 1. Sporangiophores and sporangia of downy mildew pathogens observed under a com- microscope.pound microscope.Bremia lactucaeBremia (lactucaeA); Peronospora (A); Peronospora belbahrii ( belbahriiB); Pseudoperonospora (B); Pseudoperonospora cubensis ( Ccubensis); Peronospora (C); pound microscope. Bremia lactucae (A); Peronospora belbahrii (B); Pseudoperonospora cubensis (C); chenopodii-ambrosioidisPeronospora chenopodii-ambrosioidis(D). (D). Peronospora chenopodii-ambrosioidis (D). Figure 2. Cucurbit downy mildew caused by Pseudoperonospora cubensis in cucumber and canta- Figureloupe.Figure Cucumber 2. 2.Cucurbit Cucurbit symptoms downy downy mildew mildew (A) and caused caused signs by by(BPseudoperonospora) Pseudoperonospora are very distinct, cubensis whilecubensis cantaloupein in cucumber cucumber symptoms and and cantaloupe. canta- (C) loupe. Cucumber symptoms (A) and signs (B) are very distinct, while cantaloupe symptoms (C) Cucumber symptoms (A) and signs (B) are very distinct, while cantaloupe symptoms (C) are often confused with other leaf spots or injury due to little sporulation on the underside of the leaf (D). Plants 2021, 10, x FOR PEER REVIEW 3 of 25 Plants 2021, 10, 435 3 of 24 are often confused with other leaf spots or injury due to little sporulation on the underside of the leaf (D). FigureFigure 3. 3.Hop Hop downy downy mildew mildew caused caused by byPseudoperonospora Pseudoperonospora humuli humulisporulates sporulates
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