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Advance View Proofs M&E Papers in Press. Published online on February 17, 2009 doi:10.1264/jsme2.ME09101 1 Minireview 2 Revised ME09101 3 4 Snow Molds: A Group of Fungi that Prevail under Snow 5 6 Naoyuki MATSUMOTO1* 7 8 1 Department of Planning and Administration, National Agricultural 9 Research Center for Hokkaido Region, 1 Hitsujigaoka, Toyohira-ku, Sapporo 10 062-8555, Japan 11 12 (Received January 5, 2009–Accepted January 30, 2009) 13 14 Running headline: Snow Molds Prevailing under Snow 15 16 Key words: snow mold, snow cover, low temperature, Typhula spp., Sclerotinia 17 borealis. Proofs 18 19 *Corresponding author. E-mail: [email protected]; Tel: +81-11-857-9257; 20 Fax: +81-11-859-2178. 21 View 22 23 24 25 26 27 Advance 28 29 30 31 32 33 34 35 36 1 Copyright 2009 by The Japanese Society of Microbial Ecology 37 Snow molds are a group of fungi that attack dormant plants under snow. In this paper, 38 their survival strategies are illustrated with regard to adaptation to the unique 39 environment under snow. Snow molds consist of diverse taxonomic groups and are 40 divided into obligate and facultative fungi. Obligate snow molds exclusively prevail 41 during winter with or without snow, whereas facultative snow molds can thrive even in 42 the growing season of plants. Snow molds grow at low temperatures in habitats where 43 antagonists are practically absent, and host plants deteriorate due to inhibited 44 photosynthesis under snow. These features characterize snow molds as opportunistic 45 parasites. The environment under snow represents a habitat where resources available 46 are limited. There are two contrasting strategies for resource utilization, i.e., 47 individualisms and collectivism. Freeze tolerance is also critical for them to survive 48 freezing temperatures, and several mechanisms are illustrated. Finally, strategies to cope 49 with annual fluctuations in snow cover are discussed in terms of predictability of the 50 habitat. 51 52 Proofs View Advance 2 Copyright 2009 by The Japanese Society of Microbial Ecology 53 Introduction 54 In northern regions with prolonged snow cover, plants often suffer from damage due 55 to overwintering problems. However, the process itself cannot be observed because it 56 occurs under snow and, consequently, realize the damage only by the death and poor 57 regrowth of plants after snowmelt. The phenomenon is referred to as winterkill (in 58 Japanese, “toson” for winter cereals and “fuyugare” for forage crops) which does not 59 define the cause and is ambiguous. Such damage is mostly ascribed to diseases caused 60 by fungi, i.e., snow molds. Field and laboratory experiments using 12 cultivars of 61 orchardgrass, Dactylis glomerata, in Sapporo, Hokkaido revealed that survival was 62 most strongly correlated to resistance to Typhula spp. (1). Direct evidence comes from 63 experiments with turfgrass sprayed with fungicides in late fall to control snow molds; 64 plants were green just after snowmelt in plots treated with chemicals, while untreated 65 control plots remained brown. 66 Snow mold fungi are taxonomically diverse and vary ecologically. Not all snow 67 molds prevail exclusively under snow, and several species can thrive even on plants 68 during the growing season in summer. Matsumoto (43) divided them into obligate and 69 facultative snow molds (Table 1). Obligate snow molds growProofs exclusively in winter with 70 or without snow, whereas facultative snow molds can damage growing plants. 71 Facultative snow molds tend to have higher optimum growth temperatures than obligate 72 snow molds, which explains their relativeView ubiquity in time and space. Cook (11) showed 73 that the pink snow mold fungus Microdochium nivale was associated with every growth 74 stage of winter cereals. 75 Typical snow molds have a distinct life cycle, i.e., an active phase under snow and a 76 dormant phase from spring to fall. This life cycle is as follows; 1) spring to fall: 77 Dormancy mostly in the form of sclerotia. Sclerotia are attacked by mycoparasites (48) 78 and arthropodsAdvance (25); 2) late fall: Sclero tia germinate to resume growth by producing 79 sporocarps. Ascospores of the Sclerotinia snow mold fungus, Sclerotinia borealis and 80 basidiospores of the gray snow mold fungus, T. incarnata are effective as propagules, 81 whereas those of the speckled snow mold fungus, T. ishikariensis are not infective. The 82 former two pathogens are epidemic as compared to T. ishikariensis since they have 83 airborne propagules; 3) early winter: Infection occurs normally under snow (59), but T. 84 incarnata monokaryons derived from basidiospores are obtained from plants before 85 snow cover develops (45). Mycelia developed from overmature sporocarps after 86 sporulation can infect host plants when plants are pressed against them by snow (13); 87 and 4) winter: Snow molds attack dormant plants under snow to propagate. Plants resist 88 fungal invasion using reserve material accumulated before winter. Sclerotia are 89 produced before snowmelt. 3 Copyright 2009 by The Japanese Society of Microbial Ecology 90 Snow molds are, as a whole, endemic, but unusual winter climates often result in 91 outbreaks. S. borealis badly affected orchardgrass in eastern Hokkaido in 1975, 92 resulting in a serious shortage of cattle feed (4). Of 15,000ha of damaged grasslands, 93 62% were reseeded, 28% renovated, and 10% planted with other crops. The 1974-75 94 winter favored an outbreak because of the following unusual climatic conditions: 1) 95 persistent snow cover started much later than usual, and plants were predisposed to the 96 disease, and 2) snow cover was deeper, and snowfall in late March prolonged thawing 97 of persistent snow cover and extended the active phase of S. borealis. The outbreak 98 motivated farmers to grow cold-tolerant (resistant to S. borealis) timothy, Phleum 99 pretense, instead of productive orchardgrass. T. ishikariensis is a typical endemic 100 pathogen, and its occurrence does not usually fluctuate. However, in 1988, the early 101 onset of persistent snow cover in mid-November in the Abashiri area hindered the 102 spraying of fungicides on winter wheat. Surveys made the following spring revealed 103 that 30% of the fields were abandoned (55). 104 Several reviews on snow molds have been published with regard to the evolutionary 105 ecology of Typhula spp. (42), Typhula snow molds on turfgrass (32), and biological 106 control (44). The present article overlaps to some extent withProofs a previous paper (43), 107 which also referred to mechanisms of adaptation by snow molds, but the emphasis here 108 is on recent findings, including roles in natural ecosystems, the freeze tolerance of snow 109 molds, and adaptations to the predictabilityView of the habitat under snow. 110 111 The habitat under snow 112 Snow molds as opportunistic parasites. Snow cover insulates against freezing 113 temperatures and protects plants from freezing damage (Fig. 1A and B). The 114 under-snow environment is characterized by constant low temperatures, darkness, and 115 high moisture.Advance The psychrophily of snow molds is used to monopolize plant resources 116 in a habitat where antagonists are practically absent. Matsumoto and Tajimi (49) 117 demonstrated stress tolerance of T. ishikariensis using plate cultures covered with 118 unsterile field soil at 0˚C, the ambient temperature under snow, and at 10˚C, the optimal 119 growth temperature. The mycelial growth rate of the fungus at 0˚C was ca. half that at 120 10˚C; however, the fungus failed to grow at 10˚C when cultures were covered with 121 unsterile soil to introduce microbial antagonism despite that growth was not affected at 122 0˚C. Thus, snow molds are thought to avoid antagonism by escaping to the 123 under-snow habitat. They are stress-tolerant strategists that prevail under snow with 124 high stress and low disturbance (17). 125 Since the low temperature under snow restricts species diversity, the mycoflora is 126 poor. For example, Bruehl et al. (9) found 55 fungi, including unidentified species from 4 Copyright 2009 by The Japanese Society of Microbial Ecology 127 winter wheat in winter and early spring. Årsvoll (6) described 33 fungi from forage 128 grasses just after snowmelt. These fungi were, however, mosophiles and unlikely to 129 have been actively growing under snow. Inventories of plant diseases indicate that the 130 low temperature under snow does restrict diversity; 40 fungi are described as pathogenic 131 to wheat, but only five species are recognized as snow mold pathogens (71). 132 Orchardgrass has 29 fungal pathogens, and four kinds of snow molds are incited by 133 seven fungi (3). In Hokkaido, winter crops are grown even in areas where persistent 134 snow cover lasts for 140 days or more. The habitat of snow molds is also characterized 135 by the fact that only a few fungal species monopolize host plants for such a long time. 136 Darkness under snow inhibits photosynthesis. Reserve materials are depleted by 137 respiration, and plants are predisposed to attack by snow molds. Nakajima and Abe (56) 138 demonstrated the decrease in resistance of winter wheat varieties to M. nivale coupled 139 with depletion of reserve materials under controlled conditions. Varietal difference in 140 disease resistance coincided with the rate of nutrient depletion. 141 Their growth in the absence of antagonists and with physiologic decline of host plants 142 under snow characterizes snow mold fungi as opportunistic parasites, allowing them to 143 monopolize plant resources for a long period of time. Proofs 144 145 Snow molds in the ecosystem. Like ordinary plant parasites, snow molds are 146 involved in succession in the ecosystem Viewas decomposers. However, their significance is 147 little studied. Examples may be found in snow molds of forest trees such as Racodium 148 therryanum and Phacidium abietis ( = Ph.
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