® Dynamic Biochemistry, Process Biotechnology and Molecular Biology ©2012 Global Science Books Penicillium restrictum as an Antagonist of Plant Pathogenic Fungi Rosario Nicoletti1* • Mario De Stefano2 1 Council for Research and Experimentation in Agriculture, CAT Research Unit, 84018 Scafati, Italy 2 Department of Environmental Sciences, the Second University of Naples, 81100 Caserta, Italy Corresponding author: * rosario.nicoletti@entecra.it ABSTRACT The genus Penicillium includes many ubiquitous species which are able to colonize very diverse natural and anthropic contexts as a result of their capacity to adapt to extreme environmental conditions and utilize almost any kind of organic substrate. A number of species are reported to assume agricultural relevance at some extent based on their interactions with cultivated plants and/or other organisms which may sort an effect on the crop outcome. The monoverticillate species Penicillium restrictum is cosmopolitan and mostly regarded as a soil saprotroph. Such a widespread occurrence is reflected in an extensive literature introducing its ecological role and biological properties which are considered and exploited in several biotechnological fields. This review particularly focuses on the antagonistic activity which has been documented against soil-borne plant pathogenic fungi, with special consideration for its recently discovered aptitude to exert mycoparasitism, in view of possible implications for use as an effective biocontrol agent in crop protection. _____________________________________________________________________________________________________________ Keywords: biocontrol, crop protection, mycoparasitism, rhizosphere, soil fungi CONTENTS INTRODUCTION........................................................................................................................................................................................ 61 TAXONOMY AND OCCURRENCE ......................................................................................................................................................... 61 IMPLICATIONS IN BIOTECHNOLOGY AND SOIL ECOLOGY ........................................................................................................... 63 ANTAGONISTIC PROPERTIES ................................................................................................................................................................ 64 CONCLUSIONS.......................................................................................................................................................................................... 65 REFERENCES............................................................................................................................................................................................. 65 _____________________________________________________________________________________________________________ INTRODUCTION TAXONOMY AND OCCURRENCE The cosmopolitan genus Penicillium includes many ubiquitous species which are considered for various aspects related to human activities. A particular field is represented by the agricultural application in plant protection, especially against soil-borne fungal pathogens, based on an adaptation to the soil environment which has stimulated consistent competitive abilities toward other microorganisms. Even not considering the former subgenus Biverticillium including well known mycoparasites such as P. dangeardii (syn. P. vermiculatum) and P. pinophilum, whose more pertinent classification in the teleomorphic genus Talaromyces has been recently agreed after the results of a phylogenetic study (Samson et al. 2011), a number of Penicillium species have been reported as antagonists of plant pathogens with a mechanism of action based on the induction of resistance (Madi and Katan 1998; Hossain et al. 2007), the production of antibiotic compounds (Nicoletti et al. 2004; Yang et al. 2008), and the establishment of mycoparasitic interactions (Sempere and Santamarina 2008). Recent data gathered by several research groups indicate that Penicillium restrictum is another species to be considered with reference to its properties as a fungal antagonist, which are reviewed in the present paper. Occasionally referred to as an interfaces between the genera Penicillium and Aspergillus (Raper and Thom 1949; Pitt and Hocking 1985), the species Penicillium restrictum Gilman et Abbott is classified in the section Exilicaulis of the subgenus Aspergilloides (Pitt 2000; Houbraken and Samson 2011) based on its monoverticillate conidiophores which are non-vesciculate, smooth, quite short (10-30 μm), and bear few ampulliform phialides producing conspicuously roughened conidia with a globose to ellipsoid shape. These conidial structures are the smallest in the genus Penicillium, recalling the species name which also reflects a quite restricted colony development on agar media. Mycelial growth can be appreciated at 37°C, while no conidial germination is generally observed at 5°C. However, intraspecies variation is far from being occasional, and many strains have been found to show some deviation (Pitt 2000). No teleomorph has been observed so far. To this regard, it must be considered that a number of studies have pointed out phylogenetic relationships between monoverticillate Penicillium species and the genus Eupenicillium (Eurotiales), which have now been combined and included in the new family Aspergillaceae (Houbraken and Samson 2011); however, the case is reported of a Talaromyces species, T. purpureus, presenting a conidial stage to be ascribed to the P. restrictum series (Stolk and Samson 1972). Recognized synonyms of P. restrictum are Penicillium gilmanii Thom and Penicillium kazachstanicum Novobr. (CBS database on Received: 10 September, 2012. Accepted: 12 October, 2012. Review Dynamic Biochemistry, Process Biotechnology and Molecular Biology 6 (Special Issue 2), 61-69 ©2012 Global Science Books Table 1 Checklist of isolations of Penicillium restrictum from substrates other than soil. Source Location Butter Manitoba (Canada) Living moss Pullman, Washington (USA) Flowers of Cucumis sativus Ayden, North Carolina (USA) Airborne Manhattan, Kansas (USA) Cucumber salt-stock brines Ontario (Canada) Frozen fruit-filled pastry New Jersey (USA) Fresh, brackish and sea water Hercegovina (Bosnia) Mattress dust France Human toeweb San Francisco, California (USA) Rhizoplane of Oryza sativa Dacca (Bangladesh) Human lung Tokyo (Japan) Horse dung Viña del Mar (Chile) Starch Spain Coral (Goniastrea australensis) Lizard Island (Australia) Coral (Porites australensis) Heron Island (Australia) Phylloplane of Capsicum annuum India Seeds of Cedrus deodara Nainital (India) Cinnamon Mayagüez (Puerto Rico) Gut of larva of Vespula pensylvanica Tilden Park, California (USA) Roots of Triticum aestivum and Lolium rigidum Western Australia Soybean and wheat crop residues Columbia, Missouri (USA) Wheat grains Iran Floor dust in school Palestine Leaves of Citrus sinensis Riverside, California (USA) Wall of mycological laboratory Singapore Cured Burley tobacco England Airborne and leaf surface in greenhouse Sardinia (Italy) Hive, pollen Las Marías and Mayagüez (Puerto Rico) Corn grains Bulgaria Seeds of Glycine max Thailand Corn grains Argentina Paper of historic documents Paris (France) Wall paintings Florence (Italy) and Ikaruga (Japan) Dry-cured ham Spain Leaves of Guarea guidonia and Manilkara bidentata El Verde (Puerto Rico) Leaves of Solanum tuberosum Hermiston, Oregon (USA) Babassu (Orbignya oleifera) cake Brazil Sorghum grains Pergamino (Argentina) Cheese Southern Spain Poultry feed Rio Cuarto, Cordoba (Argentine) Airborne in food warehouses Bursa (Turkey) Hay Lanco and Rio Bueno la Union (Chile) Airborne in rural areas Banyapara, west Bengal (India) Airborne in Sistine Chapel Rome (Italy) Cherries of Coffea arabica Sul de Minas (Brazil) Library shelf Rome (Italy) Wall of church Okoliné (Slovakia) Airborne in cheese factory Franche-Comté (France) Arzúa, Galicia (Spain) Airborne in houses Upper Silesia (Poland) Airborne in rural areas Edirne (Turkey) Airborne in wine cellars Arbois (France) House dust Wallaceburg, Ontario (Canada) Library Paris (France) Salt lake water Dead Sea (Israel) Leaf pack of Phragmites australis Lake Vico (Italy) Needles of Chamaecyparis obtusa Lake Biwa (Japan) Airborne Istanbul (Turkey) House dust Ohio (USA) Roots of Betula pendula East of Vilnius (Lithuania) Roots of Hypericum perforatum Fajsawice (Poland) Seeds of Phaseolus vulgaris Salta province (Argentina) Compost and vermicompost Piedmont (Italy) House dust England Naked pumpkin seeds Serbia San José de la Mariquina (Chile) Rhizoplane of Dactylis glomerata, Lolium perenne and Trifolium repens Airborne in peat moss processing plant Quebéc (Canada) Cherries (Prunus cerasus), onions (Allium cepa) Lithuania Cork Ponte de Sôr (Portugal) Tap water Norway Wheat grains Lithuania 62 Reference Bisby et al. 1933 Bridge Cooke 1955 Etchells et al. 1958 Kramer et al. 1960 Hamilton and Johnston 1961 Kuehn and Gunderson 1962 Ristanovi and Miller 1969 Mallea 1974 McGinnis et al. 1975 Jalaluddin 1975 Okudaira et al. 1977 Piontelli et al. 1981 Suarez et al. 1981 Kendrick et al. 1982 Kendrick et al. 1982 Tyagi and Chauhan 1982 Mittal 1983 Ramirez et al. 1988 Gambino and Thomas 1988 Dewan and Sivasithamparam 1988 Broder and Wagner 1988 Lacey 1988 Ali-Shtayeh and Arda 1989 Fenn et al. 1989 Lim et al. 1989 Mutasa et al. 1990 Cosentino and Palmas 1991 Seguí-Crespo et al. 1991 Mantle and McHugh 1993 Pitt et al. 1994 Gonzalez et al. 1995 Dartois 1995 Garg et al. 1995 Núñez et al. 1996 Polishook et al. 1996 Donegan et al. 1996 Freire et al. 1997 Gonzalez et al. 1997 Barrios et al. 1998 Dalcero et al. 1998 Simsekli et al. 1999 Zaror et al. 1999 Adhikari et al. 2000 Montacutelli et al. 2000 Silva et al. 2000 Maggi et al. 2000 Šimonoviová et al. 2000 Chaumont et al. 2001 Vazquez et al. 2001 Zyska 2001; Górny and Dutkiewicz 2002 Sen 2001 Simeray et al. 2001 Scott 2001 Roquebert et al. 2001 Kis-Papo et al. 2001 Mancinelli et al. 2002 Osono et al. 2002 Çolakolu 2004 Meklin et al. 2004 Lygis et al. 2004 Zimowska 2004 Castillo et al. 2004 Anastasi et al. 2005 Vesper et al. 2005 Dimi et al. 2005 Quitral Villanueva 2005 Mériaux et al. 2006 Lugauskas et al. 2006 Basilio et al. 2006 Hageskal et al. 2006 Lugauskas et al. 2006 Fungal antagonism in P. restrictum. Nicoletti and De Stefano Table 1 (Cont.) Source Grains of Pennisetum typhoides Plants micropropagated in vitro Rice grains Airborne in child day care centres Cattle feed Fresh water Marine sponge (Suberites zetekii) Paper of historic documents Sand and marine water Airborne in cave Endophyte in Dactylis glomerata Iron mine Oilseed cake Rhizoplane of Vitis vinifera Surface water Airborne Airborne in rabbit farm Dry-fermented sausage Endophyte in root of Myriophyllum spicatum Grapes (Vitis vinifera) Sea floor Gardens of Tachymyrmex septentrionalis Paper of historic documents Rhizoplane of Myristica fatua var. magnifica, Myristica malabarica and Gymnacranthera farquhariana Wood core of Pseudotsuga menziesii Apple of Malus sylvestris Location Andhra Pradesh (India) Poland Central Vietnam Edirne (Turkey) Rio de Janeiro state (Brazil) Žitava river (Slovakia) Hawaii Genoa (Italy) Olinda, Pernambuco (Brazil) Domica Cave (Slovakia) Spain Orissa (India) Calvados (France) Kiedrich (Germany) Portugal Thrace (Turkey) Qingdao (China) Tandil (Argentina) Lewisville, Texas (USA) Loire Valley (France) Amur river plume (Russia) Smithville, Texas (USA) Tanta City (Egypt) Kathalkan, Karnataka (India) Reference Raghavender et al. 2007 Kowalik 2007 Minh Tri 2007 Aydogdu et al. 2008 Rosa et al. 2008 Javorekova and Felšociova 2008 Gao et al. 2008 Zotti et al. 2008 Gomes et al. 2008 Novakova 2009 Sánchez Márquez 2009 Sabat and Gupta 2009 Lanier et al. 2009 Neuhauser et al. 2009 Pereira et al. 2009 Asan et al. 2010 Miao et al. 2010 Castellari et al. 2010 Shearer 2010 Guérin et al. 2010 Slinkina et al. 2010 Rodrigues et al. 2011 Abdel-Maksoud 2011 Rama Bhat and Kaveriappa 2011 McDonald-Dunn Forest, Oregon (USA) Alma Ata region (Kazakhstan) Kiser et al. 2011 CBS Database 2012 in the pre-treatment of biomasses to be used for the production of biofuels (Muthukkaruppan 2002; Palaniswamy et al. 2008). P. restrictum strains have been also considered for soil bioremediation in consequence of contamination by metals (Kendrick 1962; Schoenlein et al. 2008), hydrocarbons (Cabello and Arambarri 1993; Châneau et al. 1999; Garon et al. 2000; Belviso et al. 2005) and nonylphenol (Girlanda et al. 2009). Other strains have showed to be able to degrade bioplastic (polyhydroxyalkanoate) films (LopezLlorca et al. 1993; Mergaert et al. 1993). Finally, an effectiveness has been also demonstrated for the removal of dyes from aqueous solutions (Iscen et al. 2007; Ilhan et al. 2008). Bioremediation properties may be also exploited in cropped soils based on the capacity of P. restrictum to degrade pesticides. In fact, the species proved to be able to defluorinate sodium monofluoroacetate (1080), even by using this molecule as the sole carbon source in vitro (Wong et al. 1992). Moreover, it has showed to resist or promptly recover after fumigations with D-D (dichloropropene-dichloropropane) and vapam (Martin et al. 1956), or herbicide treatments (Wacha and Tiffany 1979; Mekwatanakarn and Sivasithamparam 1987), and exhibited tolerance to the bioherbicide phosphinothricin (Ahmad and Malloch 1995) and the fungicide dithane (Mittal 1983). A beneficial outcome on crops may also derive from an increased availability of phosphorous and microelements for root uptake. In fact, the ability to solubilize phosphates with ensuing benefits on plant growth has been experimentally demonstrated on wheat in India, where the use of rock phosphate coupled with the inoculation of P. restrictum resulted in a notable increase in the grain yield (Gupta and Baig 2001). The same effects on phosphorous mobilization resulted for strains recovered in southern Chile (Quitral Villanueva 2005; Morales et al. 2011). Besides degradation of rock phosphate, other isolates from India have proved to be able to leach iron from low grade ores (Sabat and Gupta 2009; Sharma 2011), a property which again may establish more favourable nutritional conditions for crop plants in certain soils. Besides influencing plant nutrition, P. restrictum may be directly involved in the food pyramide of soil. In fact, the species has been found to sustain typical fungal feeders filamentous fungi, 2012), while other taxa formerly reported in synonymy, such as Penicillium striatisporum Stolk, Penicillium kurssanovii Chalab., Penicillium griseolum G.Sm. and Penicillium malacaense C.Ramírez et A.T.Martínez, are now regarded as separated species (Peterson and Horn 2009; Houbraken and Samson 2011). Finally, validity of synonymy with Penicillium griseum Sopp (Asan 2004) is questionable, since this species was never satisfactorily identified (Raper and Thom 1949), and a possible mismatch with the valid name P. griseolum cannot be excluded. P. restrictum presents a worldwide geographical distribution, and is commonly regarded as a typical soil species. Nevertheless, it has been recovered from very diverse natural contexts (Table 1), including any kind of plant organs and products, farms, and even a few sea organisms. It also displays an aptitude to colonize the ‘anthropic’ environment, as attested by its finding in air, water, food processing plants, buildings, libraries, etc. Particularly, the occurrence in houses may have some implications on human health considering that this species proved to be capable to produce hemolysins when growing at 37°C, and that these substances have been reported to play a role in the sick building syndrome (Vesper and Vesper 2004). IMPLICATIONS IN BIOTECHNOLOGY AND SOIL ECOLOGY Such a widespread occurrence has stimulated the study and the employment of P. restrictum strains for several biotechnological purposes, starting from the exploitation of enzyme activities. To this regard, the use of a strain recovered from babassu (Orbignya oleifera) cakes in Brazil (Freire et al. 1997) as a source of lipases (Jesus et al. 1999; Palma et al. 2000; de Azeredo et al. 2007) has been particularly considered for the treatment of wastewaters with a high oily content, such as dairy (Cammarota et al. 2001; Rodrigues Rosa et al. 2006) and poultry slaughterhouse effluents (Valladão et al. 2007, 2011). Other investigated enzyme complexes include amylases (Xie and Zhang 1994; Palma et al. 2000), proteases (Rodríguez et al. 1998; Palma et al. 2000; Nathiya et al. 2011), inulinases (de Souza-Motta et al. 2003), and tannases (Batra and Saxena 2005), while cellulolytic and hemicellulolytic functions find an application 63 Dynamic Biochemistry, Process Biotechnology and Molecular Biology 6 (Special Issue 2), 61-69 ©2012 Global Science Books such as collembolans (Tiunov and Scheu 2005), while an in vitro investigation showed it to support growth of the fungivorous nematodes Aphelenchus avenae and Aphelenchoides bicaudatus (Ikonen 2001). More recently, a natural trophic association resulted in a survey on microfungal communities developing in gardens of fungus-growing ants, where P. restrictum was found to be the dominant fungal species in anthills of Tachymyrmex septentrionalis during winter (Rodrigues et al. 2011). ANTAGONISTIC PROPERTIES The occurrence of P. restrictum in rhizosphere and rhizoplane in both natural and agricultural contexts (Jalaluddin 1975; Arora and Dwivedi 1976; Požárová et al. 2001; de Souza-Motta et al. 2003; Lygis et al. 2004; Jamiokowska and Wagner 2005; Quitral Villanueva 2005; Neuhauser et al. 2009; Das and Dkhar 2010; Hindumathi and Reddy 2011; Rama Bhat and Kaveriappa 2011) represents a clue for a possible involvement in antagonism against fungal pathogens. Circumstantial evidence in this sense has resulted on St. John's wort (Hypericum perforatum) affected by a complex of soil-borne pathogens including Rhizoctonia solani, Botrytis cinerea, Phoma exigua var. exigua and a number of Fusarium species (F. avenaceum, F. culmorum, F. equiseti, F. oxysporum and F. solani), where P. restrictum was isolated from roots and basal stem with rot symptoms (Zimowska et al. 2004). In a lupin (Lupinus albus) field heavily infested with a similar pathogen complex, including Pythium ultimum, R. solani AG-2-1 and AG-4, F. culmorum, F. oxysporum and F. solani, the occurrence of P. restrictum was particularly notable in the rhizosphere of plants growing in patches which had escaped the disease (Nicoletti et al. 2008a). P. restrictum was also found amidst saprotrophs occurring in the rhizosphere of potato plants, but it was reported not to be able to exert a protective effect against R. solani and Helminthosporium solani (Kurzawiska 2006). Nevertheless, this conclusion is somehow questionable since it is not clear how the author numerically quantifies the ‘individual biotic effect’ and the ‘general biotic effect’ on which her judgement on the outcome of the interaction with the above pathogens is based. It is quite reasonable to assume that the occurrence of P. restrictum in soil is largely influenced by its competitiveness toward the other microbial components, as at least in part regulated by the bioactivity of the extrolites it may produce. To this regard, indications of an ability to possibly overcome fungistasis and antibiosis promoted by other microorganisms was inferred based on the tolerance toward the staling products released by fungi inhabiting lentil rhizosphere (Arora and Dwivedi 1976, 1979), while assays in dual cultures against Sporotrichum schenckii and Scopulariopsis brevicaulis (Blunt and Baker 1968) first documented its ability to exert antibiosis toward soil fungi. Consistent inhibitory capacities were later showed against Gaeumannomyces graminis var. tritici (Mekwatanakarn and Sivasithamparam 1987), although in a following assay car- Fig. 1 Inhibition of mycelial growth of R. solani AG-2-1 by isolate XLT3S of P. restrictum in dual culture. ried out at the same laboratory isolates from ryegrass (Lolium rigidum) and wheat roots were reported not to be able to inhibit the same pathogen in dual cultures in vitro (Dewan and Sivasithamparam 1988), introducing a possible diversity in the range of fungitoxic extrolites produced by isolates within the species. Again and independently, in vitro effectiveness against the agent of the take-all disease was pointed out in Poland (Tashein 1988). Finally, antifungal properties resulting in dual cultures have been reported against other soil saprotrophs, namely Paecilomyces lilacinus and Humicola fuscoatra (Stahl and Christensen 1992), and more recently against widespread polyphagous pathogens, such as Pythium aphanidermatum and P. ultimum (Gravel et al. 2005), P. ultimum and R. solani AG-2-1 and AG-4 (Nicoletti et al. 2008a) (Fig. 1), and Verticillium dahliae (Arriagada et al. 2012). Besides these indirect evidences, antifungal products have been actually extracted and characterized by soil strains of P. restrictum which may account for its antagonistic properties at some extent. The first secondary metabolites reported from this species were dehydrocarolic acid and gliotoxin (Sankhala 1968). Both compounds had been previously found in culture filtrates of another species belonging in the section Exilicaulis, Penicillium cinerascens (Bracken and Raistrick 1947). While the former has never been reported to possess significant antibiotic properties, the latter is a potent mycotoxin (Gardiner et al. 2005) which has been shown to play an effective role in fungal antagonism (Lumsden et al. 1996). Afterwards, two more extrolites, namely 2,3-dihydro-3,6-dihydroxy-2-methyl-4pyrone and curvularin, were evidenced in cultures of a strain mentioned as P. gilmanii (Raistrick and Rice 1971), and the production of a derivative of the latter compound, dihydrocurvularin, was documented at the same laboratory (Rice and Chen 1984). Compounds of this macrolide series are produced by a number of Penicillium species (Houbraken et al. 2011), and are known for some extent of antifun- Fig. 2 Parasitic interactions of P. restrictum with P. ultimum (A), and R. solani AG-2-1 (B) and AG-4 (C). 64 Fungal antagonism in P. restrictum. Nicoletti and De Stefano equivocally demonstrate the capacity of P. restrictum to develop mycoparasitically (Fig. 3). Considering that the above plant pathogens are not taxonomically related, a more comprehensive study was carried out to evaluate if mycoparasitism could actually be exerted against other plant pathogens. Within a group of strains belonging to the species Fusarium culmorum, F. solani, Cladosporium oxysporum, Macrophomina phaseolina, Sclerotinia sclerotiorum, Sclerotium rolfsii, Thielaviopsis basicola and Colletotrichum gloeosporioides, the latter was the only one to disclose susceptibility (Sinapi 2009). These results indicated that the range of mycoparasitism by the tested strains of P. restrictum may not be broad, and that P. restrictum itself may be affected by competitive capacities of soil fungal pathogens, as particularly evident in the case of S. sclerotiorum which consistently inhibited its hyphal growth in dual cultures. CONCLUSIONS The widespread occurrence of P. restrictum has incited a notable amount of studies considering its ecology and biological properties which are occasionally exploited in biotechnology. Particularly, the available literature underlines its competitive ability in the rhizosphere of plants in both natural and agricultural contexts, introducing it as a plausible and effective antagonist of plant pathogenic fungi. The establishment of a favourable balance among microbial species in the rhizosphere is more and more considered as a fundamental factor in crop development and protection against biological adversities, and fungal antagonists are recognized to play a key role to this regard, even by inducing soil suppressiveness (Whipps 2001; Weller et al. 2002; Mazzola 2004). Therefore the finding of new species able to ultimately improve soil fertility by interacting in a multiple mode with cultivated plants and their pathogens deserves to be highlighted and exploited. The available data are oriented to qualify P. restrictum as a species exerting such a biocenotic role, not only based on the production and possible effects of antifungal extrolites, but also on the capacity to more directly affect the subsistence of a number of fungal pathogens which may be susceptible to its mycoparasitic aptitude. Indeed these properties stimulate further investigations concerning the possible application of P. restrictum strains as biocontrol agents in crop protection. Fig. 3 Images at SEM of mycoparasitism by P. restrictum. Hyphae wrapping those of P. ultimum (A; bar = 20 μm) and R. solani AG-2-1 (B; bar = 10 μm). Magnification of hyphal interactions with R. solani AG-4 (C-F; bars: C and E = 5 μm, D and F = 2 μm) and C. gloeosporioides (G-H, bars: G = 10 μm, H = 1 μm). gal activity (Dai et al. 2010). Later on, a new class of antifungal compounds including restricticin and its dimethyl derivative was characterized from culture extracts of an Indian isolate; these extrolites, whose molecule presents triene, pyran and glycine ester functionalities, are active against a broad range of yeasts and filamentous fungi (Hensens et al. 1991; Schwartz et al. 1991). Furthermore, the calbistrin complex, whose denomination is derived by the inhibitory properties against Candida albicans, was extracted by liquid cultures of a Brazilian isolate (Jackson et al. 1993). The structure of such compounds is based on a carboxylic acid conjugated tetraene which is attached to a hexahydronaphthalene system (Brill et al. 1993). More recently, the production of patulin and penicillic acid has been reported in a strain isolated from dry-cured ham (Martín et al. 2004). Both compounds are well-known mycotoxins of a number of Penicillium species, which have been also found to be implicated in the expression of antagonism against other fungi (Steiman et al. 1989; Frisvad et al. 2004; Kang and Kim 2004; Nicoletti et al. 2004). Although the described inhibitory effects may prevent hyphal contacts in dual cultures with fungal pathogens, our investigations concerning P. restrictum isolates from lupin rhizosphere showed them to be able to slowly overgrow the inhibition zone in pairings with R. solani and P. ultimum, creating an opportunity for a direct hyphal interaction (Nicoletti et al. 2008b). In the above conditions, hyphae of P. restrictum grew adpressed to those of the challenged strains with occasional sketches of coiling, establishing hyphal penetration through haustorium-like structures produced at quite regular intervals, as shown in Fig. 2. 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