The Top 10 Oomycete Pathogens in Molecular Plant Pathology 12 Albugo Laibachii Later, Breeding Efforts Have Yet to Provide a Durable Solution
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bs_bs_banner 2 S. KAMOUN et al. Top 10 oomycete plant pathogens 3 4 S. KAMOUN et al. The Top 10 MOLECULAR PLANT PATHOLOGY DOI: 10.1111/mpp.12190 introduction to these 10 taxa and a snapshot of current research. the umbrella of the ‘Oomycete Molecular Genetics Network’. This Table 2 Other oomycete species that received votes. which AVR3a stabilizes to prevent programmed cell death in response to elicitors such as INF1 (Bos et al., 2010). Review We hope that the list will serve as a benchmark for future trends community has moved the field beyond the gloomy view of the Rank Species Breeding for late blight resistance was initiated by James Torbitt of Belfast in oomycete research. 1980s that oomycetes are a ‘fungal geneticist’s nightmare’ (Shaw, in the 1870s, inspired by the theories of Charles Darwin, with whom he 1983; discussed in Schornack et al., 2009). It has produced novel 11 Aphanomyces euteiches shared considerable correspondence (DeArce, 2008). More than 130 years The Top 10 oomycete pathogens in molecular plant pathology 12 Albugo laibachii later, breeding efforts have yet to provide a durable solution. Occasionally, oomycete Keywords: oomycetes plant pathology, microbiology, diversity, paradigms in understanding host–microbe interactions, effector 13 Bremia lactucae local successes are reported; for example, variety C88, widely cultivated in 14 Phytophthora palmivora China for over a decade, retains its resistance (Li et al., 2011). Many resist- 1, 1 1 2 genomics. biology and genome evolution (Bozkurt et al., 2012; Govers and SOPHIEN KAMOUN *, OLIVER FURZER , JONATHAN D. G. JONES , HOWARD S. JUDELSON , Gijzen, 2006; Jiang and Tyler, 2012; Schornack et al., 2009; 15 Pseudoperonospora cubensis ance (R) genes effective against races of P. infestans have been identified 3 4 5 6 16 Plasmopara halstedii (Rodewald and Trognitz, 2013). Only with the recent identification of GUL SHAD ALI , RONALDO J. D. DALIO , SANJOY GUHA ROY , LEONARDO SCHENA , Vleeshouwers et al., 2011). The oomycete community was one of 7 8 9 10 17 Peronophythora litchi avirulence genes, all of which encode RXLR effectors, can breeders incorpo- ANTONIOS ZAMBOUNIS , FRANCK PANABIÈRES , DAVID CAHILL , MICHELINA RUOCCO , the first in plant pathology to initiate coordinated transcriptome 18 Peronosclerospora sorghi rate knowledge on how P. infestans evades detection into their breeding pathogens ANDREIA FIGUEIREDO11, XIAO-REN CHEN12, JON HULVEY13, REMCO STAM14, KURT LAMOUR15, and genome sequencing projects, and subsequently to exploit the 19 Peronospora belbahrii strategies (Vleeshouwers et al., 2011). Such information is critical for the 16 17 18 19,20 INTRODUCTION 20 Phytophthora alni prediction of the durability of R genes.The use of effectors as tools to rapidly MARK GIJZEN , BRETT M. TYLER , NIKLAUS J. GRÜNWALD , M. SHAHID MUKHTAR , resulting resources to drive conceptual advances (Govers and 21 Phytophthora brassicae identify R genes is a powerful step towards rational selection and combina- DANIEL F. A. TOMÉ21, MAHMUT TÖR22, GUIDO VAN DEN ACKERVEKEN23, JOHN MCDOWELL24, Oomycetes are eukaryotic organisms that superficially resemble Gijzen, 2006; Pais et al., 2013; Schornack et al., 2009).These days, 22 Phytophthora cactorum tion of lasting resistance (Vleeshouwers et al., 2008). We still know relatively little about how P. infestans effectors manipulate 25 26 27 28 filamentous fungi, but are phylogenetically related to diatoms and with the genomes serving as unique resources for basic and 23 Phytophthora meadii FOUAD DAAYF , WILLIAM E. FRY , HANNELE LINDQVIST-KREUZE , HAROLD J. G. MEIJER , 24 Phytophthora phaseoli host plants to establish disease. How do they translocate into host cells? Do 1,29 30 1 14 brown algae in the stramenopiles (Gunderson et al., 1987; Jiang applied research, oomycetes are best portrayed as a ‘genomicist’s BENJAMIN PETRE , JEAN RISTAINO , KENTARO YOSHIDA , PAUL R. J. BIRCH AND 25 Phytophthora plurivora (formerly P. citricola) they define host range? How do they work in concert to modulate complex in molecular 28 and Tyler, 2012; Lamour and Kamoun, 2009; Thines, 2014; Thines dream’ (Govers and Gijzen, 2006; Jiang and Tyler, 2012; Pais et al., 26 Plasmopara obducens networks of regulatory processes occurring in the host? Only recently FRANCINE GOVERS and Kamoun, 2010). Fossil evidence indicates that a number of 2013; Schornack et al., 2009). 27 Pythium aphanidermatum Fig. 1 Potato plants with typical late blight lesions. Infection starts when a have researchers started to adopt structural biology to fully investigate 1The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, UK 28 Pythium oligandrum spore lands on the leaf and germinates. The germ tube forms an functional relationships between interacting pathogen and plant proteins oomycetes emerged as endophytes of land plants at least by the It is therefore particularly fitting that the oomycetes are at last (Wirthmueller et al., 2013). Could such research catalyse the modification of 2Department of Plant Pathology and Microbiology, University of California, Riverside, CA 92521, USA 29 Sclerophthora rayssiae appressorium and an emerging penetration peg pushes into an epidermal Carboniferous period, approximately 300–350 million years ago covered by the Top 10 review series of Molecular Plant Pathology. 30 Hyaloperonospora brassicae molecular interactions in favour of the plant immune system through syn- 3Department of Plant Pathology and MREC, IFAS, University of Florida, Apopka, FL 32703, USA cell. Then the inner cell layers are colonized. During the biotrophic phase, NR Saprolegnia parasitica (fish parasite) thetic biology approaches? 4 (Krings et al., 2011). One species, Combresomyces williamsonii, The process to generate the list and the aim of this article are hyphae grow in the intercellular space, whereas haustoria enter plant cell Biotechnology Laboratory, Centro de Citricultura Sylvio Moreira/Instituto Agronomico, Cordeirópolis-Sao Paulo 13490-970, Brazil NR Lagenidium giganteum (mosquito parasite) The basic knowledge gained on P. infestans in the last decade is starting plant pathology 5 described from ∼320-million-year-old petrified stem cortex and similar to those of previous contributions on plant-pathogenic cavities and invaginate host cell plasma membrane. Later, Phytophthora Department of Botany, West Bengal State University, Barasat, Kolkata-700126, India NR Pythium insidiosum (mammalian parasite) to have an impact on the management of late blight disease. For the control 6Dipartimento di Gestione dei Sistemi Agrari e Forestali, Università degli Studi Mediterranea, 89122 Reggio Calabria, Italy rootlets of a seed fern, may have even been parasitic viruses (Scholthof et al., 2011), fungi (Dean et al., 2012), bacteria infestans switches to necrotrophic growth, resulting in the death of plant of late blight, farmers largely rely on agrochemicals, many with unknown modes of action. The emergence of insensitive strains is possibly a result of 7UMR1290 BIOGER-CPP, INRA-AgroParisTech, 78850 Thiverval-Grignon, France (Strullu-Derrien et al., 2011).Phylogenetic analyses of modern taxa (Mansfield et al., 2012) and nematodes (Jones et al., 2013). We NR, not ranked because the species is not associated with plants. cells and the appearance of necrotic lesions on the infected tissues. In this high mutation rates in the pathogen (Randall et al., 2014). The phenylamide 8 phase, hyphae escape through the stomata and produce numerous asexual INRA, UMR1355, Université Nice Sophia Antipolis, CNRS, UMR7254, ISA, F-06903 Sophia Antipolis, France have revealed that plant parasitism has evolved independently in undertook a survey to query the community for their ranking of This article is based on contributions from the voters to provide metalaxyl was one of the first chemicals to exhibit specificity to oomycetes. 9Deakin University, Geelong, Vic. 3217, Australia spores, named sporangia, that easily detach and disperse by wind or water. A three lineages of oomycetes (Thines and Kamoun, 2010). plant-pathogenic oomycete taxa based on scientific and economic an introduction to the 10 taxa and a snapshot of current research. Fig. 2 One of the many Great Famine memorials around the world. These Soon after its introduction and widespread use, fully insensitive strains 10Portici Division of the Italian National Research Council (CNR), Institute for Sustainable Plant Protection (IPSP), Via Università 133, 80055 Portici (NA), Italy sporangium that finds a new host can either germinate directly and initiate a emerged, but only 35 years later was the molecular basis of this insensitivity Well-known plant pathogens, namely downy mildews, importance. In total, we received 263 votes from 62 scientists in 15 sculptures on Customs House Quays in Dublin, by artist Rowan Gillespie, 11Centre for Biodiversity, Functional and Integrative Genomics, Faculty of Sciences, University of Lisboa, 1749-016 Lisbon, Portugal Each section starts with a brief overview of the selected species, new cycle or, at lower temperatures, undergo cleavage resulting in a uncovered (Randall et al., 2014). Mining of the P. infestans genome has stand as if walking towards the emigration ships on the Dublin Quayside Sophien Kamoun 12 Phytophthora and Pythium, appear to have radiated from a countries that yielded the Top 10 species (Table 1). To some revealed many novel proteins with domain combinations that are unique to College of Horticulture and Plant Protection, Yangzhou University, Yangzhou, 225009, China e.g. its importance,