Pythium Oligandrum : an Example of Opportunistic Success
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Microbiology (2012) DOI……. ______________________________________________________________________________ 1 Pythium oligandrum : an example of opportunistic success 1 2 3 3 2 Nicole Benhamou, Gaêtan le Floch, Jessica Vallance , Jonathan Gerbore, 4 3 3 Damien Grizard, and Patrice Rey 4 1Centre de recherche en horticulture, Pavillon de l'ENVIROTRON, 2480 Boulevard Hochelaga, 5 Université Laval, Québec, Québec, CANADA, G1V 0A6 6 2Université Européenne de Bretagne / Université de Brest, Laboratoire Universitaire de 7 Biodiversité et Ecologie Microbienne, ESMISAB, 29 820 Plouzané, France 8 3Université de Bordeaux, ISVV, UMR1065 Santé et Agroécologie du Vignoble (SAVE), 9 Bordeaux Sciences Agro, F-33140, Villenave d’Ornon, France et INRA, ISVV, UMR1065 10 SAVE, F-33140, Villenave d’Ornon, France 11 4BIOVITIS, Saint Etienne de Chomeil, 15 400, France 12 13 14 15 16 Correspondence 17 18 Nicole Benhamou 19 [email protected] 20 21 22 23 24 Summary: 250 words 25 Text: 8 679 Words 26 Figure number: 6 27 28 29 30 31 32 33 34 Abbreviations: CWP, cell wall protein; EST, expressed sequence tag; ET, ethylene; FORL, 35 Fusarium oxysporum f.sp. radicis-lycopersici; HR, hypersensitive reaction; IAA, indole-3-acetic 36 acid; IVET, in vivo expression technology; JA, jasmonic acid; MAMP, microbe-associated 37 molecular pattern; MAPK, mitogen-activated protein kinase; PAMP, pathogen-associated 38 molecular pattern; PR, pathogenesis-related; ROS, reactive oxygen species; SA, salicylic acid; 39 RT-PCR, real-time polymerase chain reaction; SSCP, single-strand conformational 40 polymorphism; Trp, tryptophan. 41 N. Benhamou and others __________________________________________________________________________________________________________ 42 43 Summary 44 45 Pythium oligandrum, a non-pathogenic soil-inhabiting oomycete, colonizes the root ecosystem 46 of many crop species. Whereas most members in the Pythium genus are plant pathogens, P. 47 oligandrum distinguishes itself from the pathogenic species by its ability to protect plants from 48 biotic stresses in addition to promote plant growth. The success of P. oligandrum at controlling 49 soilborne pathogens is partly associated with direct antagonism mediated by mycoparasitism and 50 antibiosis. Interestingly, P. oligandrum has evolved with several sophisticated molecular 51 mechanisms to specifically attack its preys even when these belong to closely related species, Of 52 particular relevance is the question of how P. oligandrum distinguishes between self- and non- 53 self cell wall degradation during the mycoparasitic process of pathogenic oomycete species. The 54 ability of P. oligandrum to enter and colonize the root system through an unusual lifestyle is one 55 of the most striking features that differentiate it from all other known biocontrol fungal agents. In 56 spite of this atypical behaviour, P. oligandrum sensitizes the plant to defend itself through the 57 production of at least two types of microbe-associated molecular patterns (MAMPs), including 58 oligandrin and cell wall protein fractions (CWP), which appear to be closely involved in the 59 early events preceding activation of the JA- and ET-dependent signalling pathways and 60 subsequent localized and systemic induced resistance. The aim of this review is to highlight the 61 expanding knowledge of the mechanisms by which P. oligandrum provides beneficial effects to 62 plants and to explore the potential use of this oomycete or its metabolites as new disease 63 management strategies. 64 65 66 67 68 69 70 71 72 73 74 75 76 2 N. Benhamou and others __________________________________________________________________________________________________________ 77 Introduction 78 In a large number of agricultural ecosystems, crop productions are severely hampered by 79 soilborne pathogen-incited diseases that cause heavy economic losses (van West et al., 2003). In 80 spite of significant advances in crop protection (i.e. crop rotation, use of chemical pesticides and 81 breeding of resistant crop varieties), soilborne plant pathogens still significantly reduce yield and 82 quality in diverse economically important crops. These pathogens are particularly challenging 83 because they often survive in soil through resilient survival structures. In the past few decades, 84 the expanding movement toward more environmentally friendly agricultural practices has 85 accelerated the search for alternative strategies that could provide safe and reliable means to 86 combat root diseases (Alabouvette et al., 2006). Among the proposed approaches, the exploration 87 of the mechanisms by which naturally occurring beneficial microorganisms can suppress disease 88 incidence or severity has attracted much attention in relation to their potential at fighting root 89 pathogens and modulating the plant immunity (Benhamou et al., 1997, 1999; Harman et al., 90 2010; Validov et al., 2010; Yedidia et al., 1999). 91 While the beneficial effects of rhizobacteria and true fungi such as Trichoderma spp. have been 92 abundantly explored (Berg, 2009; Lorito et al., 2010), the possibility that selected members of 93 the oomycetes may contribute to protect plants from infection has often been occulted by plant 94 pathologists who long considered that oomycetes were essentially virulent pathogens (Blair et 95 al., 2008; Latijnhouwers et al., 2003). In the past few years, however, the field of beneficial 96 plant-oomycete interactions has started to be the focus of interest and it is anticipated that 97 scientists from both fields will work together to provide an integrated view of the molecular 98 mechanisms that evolved in pathogenic and beneficial plant–oomycete interactions. Within the 99 oomycetes, the Pythium genus (about 130 species) occupies a large variety of terrestrial and 100 aquatic ecological niches (Lévesque & de Cook, 2004). Some members of this genus are active 101 saprophytes, others are pathogens on an array of organisms including algae, fishes and insects 102 (van der Plaats-Niterink et al., 1981) while the most economically important members are plant 103 pathogens with a broad host range (Thines & Kamoun, 2010). That beneficial relationships 104 between plants and some Pythium spp. may occur in nature has long been mentioned (Drechsler, 105 1943), but it is only in the last two decades that the intimate relationships established between 106 plants and beneficial Pythium spp. has been deeply explored (Mohamed et al., 2007; Picard et 107 al., 2000b; Takenaka et al., 2008). Among the few mycoparasitic Pythium spp. so far identified, 108 Pythium oligandrum Drechsler, a soil inhabitant with a worldwide distribution, is undoubtedly 109 considered as the most promising biocontrol oomycete for use in agriculture (Rey et al., 2008). 110 The beneficial effects of P. oligandrum on plants are the result of the synergistic action of 111 several mechanisms including antagonism against an array of soilborne pathogens, plant growth 112 promotion through the production of auxin precursors and plant-induced resistance mediated by 113 at least two Microbe-Associated Molecular Patterns (MAMPs). A critical feature of the 114 relationships established between P. oligandrum and the plant relies in its remarkable ability to 115 rapidly colonize all root tissues in a way similar to pathogenic oomycetes and to subsequently 3 N. Benhamou and others __________________________________________________________________________________________________________ 116 degenerate without causing host tissue damage. This unusual behaviour, leading to net fitness 117 benefits for the plant, suggests that P. oligandrum, unlike other beneficial microorganisms 118 (Lorito et al., 2010), does not have the ability to cope with the host immune response that is 119 triggered at the onset of MAMP perception. 120 In this review, we provide an overview of the complex though coordinated mechanisms by 121 which P. oligandrum protects plants from diseases and interacts with the soil ecosystem. It is 122 also our purpose to discuss on the biological principles that drive the action of P. oligandrum 123 during its interaction with either plant pathogenic oomycetes or plant root tissues. How P. 124 oligandrum differentiates between self and non-self cell wall degradation during mycoparasitism 125 and why it degenerates in the root tissues are two crucial questions that are addressed in this 126 review. Finally, we discuss future directions of research that would contribute to enhance the 127 performance of P. oligandrum prior to its use as a powerful biocontrol agent. 128 Pythium oligandrum: an intruder in the Pythium genus 129 Drechsler (1943) was the first to describe that some Pythium species, characterized by their spiny 130 oogonia, were parasites of other pathogenic Pythium species. These non-pathogenic plant 131 Pythium species were reported as being P. periplocum, P. acanthicum and P. oligandrum. 132 Several years later, Lifshitz et al., (1984) found that another Pythium species, identified as P. 133 nunn and isolated from a soil in Colorado, suppressed preemergence damping-off of cucumber 134 seedlings caused by P. ultimum in greenhouse trials. At the same time, Foley and Deacon (1985) 135 reported that a new Pythium species, referred to as P. mycoparasiticum, was able to parasitize a 136 number of fungal pathogens. Two other spiny oogonial Pythium species with mycoparasitic 137 activity, P. acantophoron, discovered by Lodha and Webster (1990), and P. lycopersicum, 138 isolated in Turkey