1 Oomycete Interactions with Plants: Infection Strategies and Resistance Principles
Total Page：16
File Type：pdf, Size：1020Kb
View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Apollo 1 Oomycete Interactions with Plants: Infection Strategies and Resistance Principles 2 3 Stuart Fawke1, Mehdi Doumane1*, Sebastian Schornack1# 4 5 1Sainsbury Laboratory (SLCU), University of Cambridge, United Kingdom 6 *Current address: Department of Biology, École Normale Supérieure de Lyon, Lyon, France 7 8 #Address correspondence to Sebastian Schornack, [email protected] 9 10 Running head: Plant pathogenic oomycetes 1 11 Table of Contents 12 13 Summary ................................................................................................................................. 3 14 Introduction ............................................................................................................................ 3 15 16 Main Text 17 . Phylogeny .......................................................................................................................... 4 18 . Early life cycle stages: asexual reproduction and infection structures ..................... 4 19 . Plants recognise oomycete-derived molecules ............................................................ 5 20 . Effectors suppress host immunity .................................................................................. 7 21 . How are effectors deployed in the host? ....................................................................... 9 22 . Plant innate immunity ..................................................................................................... 11 23 . R gene-mediated resistance ......................................................................................... 12 24 . S gene-mediated resistance ......................................................................................... 13 25 . Future directions for developing oomycete resistant plants ..................................... 15 26 . Potential for comparative pathogen-mutualist studies .............................................. 17 27 . Summary .......................................................................................................................... 18 28 29 Acknowledgements ............................................................................................................ 18 30 31 Tables 32 . Table 1. Plant pathogenic oomycete genome sequence resources ....................... 19 33 . Table 2. Lifestyle, host range and infection structures of important plant-infecting 34 oomycete species ........................................................................................................... 20 35 . Table 3. Examples of known oomycete elicitors ........................................................ 21 36 . Table 4. Examples of effectors that suppress host immunity during interactions 37 with oomycetes, together with their host targets and virulence effects .................. 21 38 . Table 5. Cloned resistance (R) and susceptibility (S) genes affecting oomycete- 39 plant interactions ............................................................................................................. 22 40 41 42 Figure Legends .................................................................................................................... 24 43 References ............................................................................................................................ 25 44 Biographical Text ................................................................................................................ 37 45 2 46 Summary 47 The Oomycota include many economically significant microbial pathogens of crop species. 48 Understanding the mechanisms by which oomycetes infect plants and identifying methods 49 to provide durable resistance are major research goals. Over the last few years, many 50 elicitors that trigger plant immunity have been identified, as well as host genes that mediate 51 susceptibility to oomycete pathogens. The mechanisms behind these processes have 52 subsequently been investigated and many new discoveries made, marking a period of 53 exciting research in the oomycete pathology field. This review provides an introduction to our 54 current knowledge of the pathogenic mechanisms used by oomycetes, including elicitors and 55 effectors, plus an overview of the major principles of host resistance: the established R gene 56 hypothesis and the more recently defined susceptibility (S) gene model. Future directions for 57 development of oomycete-resistant plants are discussed, along with ways that recent 58 discoveries in the field of oomycete-plant interactions are generating novel means of 59 studying how pathogen and symbiont colonizations overlap. 60 Abstract 61 The Oomycota include many economically significant microbial pathogens of crop species. 62 Understanding the mechanisms by which oomycetes infect and identifying methods to 63 provide durable resistance is a major research goal. Over the last few years many elicitors 64 that trigger plant immunity have been identified as well as host genes that mediate 65 susceptibility to oomycete pathogens. The mechanisms behind these processes have 66 subsequently been investigated and many new discoveries made, marking a period of 67 exciting research in the oomycete pathology field. This review provides an introduction to our 68 current knowledge of the pathogenic mechanisms used by oomycetes, including elicitors and 69 effectors, plus an overview of the major principles of host resistance: the established R gene 70 hypothesis and the more recently defined susceptibility (S) gene model. Future directions for 71 developing oomycete-resistant plants will be discussed, alongside how recent discoveries in 72 the oomycete-plant interactions field are generating novel ways of studying how pathogen 73 and symbiont colonisations overlap. 74 75 Introduction 76 The Oomycota are a distinct class of fungal-like eukaryotic microbes, many of which are 77 highly destructive plant or animal pathogens. They share a range of morphological features 78 with fungi, but possess various unique characteristics which set them apart (1). Cellulose is 79 a major component of oomycete cell walls. By contrast, chitin, but not cellulose, is a major 3 80 cell wall component of true fungi. However, oomycetes also possess chitin synthases that 81 are activated during tip morphogenesis (2, 3). Oomycetes are diploid during their vegetative 82 mycelial stage, whereas fungi predominantly produce haploid thalli, although exceptions do 83 exist (2, 4). Cells of oomycetes can be distinguished morphologically from true fungi by their 84 mitochondria, possessing tubular cristae as opposed to the flattened cristae of fungi (5) or 85 their hyphae which are always non-septate (6). 86 Typical structural features guided identification of oomycetes in the fossil record. The oldest 87 existing evidence for oomycete-like structures dates back to the Devonian period, c. ~400- 88 360 Ma (7) and there is evidence of oomycete parasitism occurring during the Carboniferous 89 period, c. ~300 Ma (8). Molecular clock estimates position the origin of oomycetes as early 90 as the Silurian period, c. ~430-400 Ma (9). 91 This review provides an overview of our current knowledge of oomycete plant pathogens. 92 We introduce the elicitors, effector proteins and disease resistance and susceptibility 93 principles involved in our current understanding of how oomycetes interact with their plant 94 hosts. We also present strategies for developing oomycete-resistant crop plants and 95 highlight the potential of oomycetes as tools to investigate common and contrasting 96 mechanisms of pathogenic and mutualistic filamentous microbes. 97 98 Phylogeny 99 Analysis of conserved DNA sequences such as mitochondrial COX2 (10-12), LSU rDNA (13) 100 and SSU rDNA (14) have confirmed that oomycetes belong outside the fungal kingdom, 101 within the Chromalveolata. The Chromalveolata kingdom contains mainly photosynthetic 102 species, a result of ancestral ‘enslavement’ of red algae (15), but oomycetes have since lost 103 their chloroplasts (16). Availability of several sequenced genomes for some genera (see 104 Table 1), in particular Phytophthora, has greatly facilitated multilocus assessment of 105 oomycete taxonomic relationships (17). The Oomycota are broadly divided into two 106 subclasses. The Saprolegniomycetidae, referred to as the ‘water moulds’, include the orders 107 Eurychasmales, Leptomitales and Saprolegniales, whilst the Peronosporomycetidae are 108 mostly plant pathogen orders and consist of the Rhipidiales, Pythiales and Peronosporales. 109 The existence of early diverging genera of marine parasites within the mainly terrestrial 110 Saprolegniales and Peronosporales orders has led evolutionary biologists to suggest that 111 oomycetes made their migration onto the land and into the soil via parasitism of nematode 112 hosts or by switching from colonisation of estuarine seaweed to the roots or shoots of early 113 coastal vegetation (18) . 4 114 115 Early life cycle stages: asexual reproduction and infection structures 116 Dispersal of oomycetes by wind or water is achieved through asexual sporangia. 117 Germination of sporangia can either occur directly, forming invasive hyphae or indirectly, 118 releasing motile zoospores, which are chemotactically and electrotactically attracted to the 119 surfaces of host plants (19). Zoospores swim until reaching the plant surface at which point 120 they shed their flagella