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Routes of fungal colonization of cereal grains and malt

Colonization of cereal grain used for malt production by fungi can basically occur via several different routes. Unspecific superficial colonization occurs by fungal and yeast propagules that are transported through air movement or are washed out from the atmosphere with rainfall. Such propagules are deposited directly on any part of the plant, including the ears. Fungi in that category mostly have small dry and mostly pigmented spores enabling them to survive long periods of dryness and irradiation by sunlight without suffering any physiological or genetic damage. Typically the propagules are unable to germinate and grow under the conditions in the field. During harvesting, threshing and transport manipulations, propagules resting on parts of the plant other than the grain are homogeneously distributed to the harvested grains. Under the conditions of storage they can survive for longer periods of time and will germinate and grow as the water content of barley exceeds 14-15% and CO2 accumulates at elevated temperatures (Magan and Lacey, 1984). Hence the name storage fungi.

Fungal species collectively summarized as the field fungi have evolved mechanisms enabling them to colonize the cereal plant by growing on its surface or even by penetrating its tissues. Deposition by airflow over greater distances is rather rare in such species since they are mostly unfit for survival in dryness and under sunlight irradiation. Species of field fungi are rather distributed by short-range deposition of ascospores by wind flow (Osborne and Stein, 2007; Xu and Nicholson, 2009), by rain splash (Ooka and Kommedahl, 1977; Madden, 1997) or by using insect vectors (Hajek and St. Leger, 1994) with a distribution radius of viable inoculum within a short distance ranging between centimetres and a few metres. Cereal grains are colonized by field species either by propagules deposited directly on the ear or indirectly by mycelia that have penetrated tissues remote from the ear and grow towards it subcutaneously (Kang and Buchenauer, 2000). True plant pathogens such as Septoria tritici or Septoria nodorum can actively penetrate tissues (Cohen and Eyal, 1993; Eyal, 1999) and infect cereal grains and other parts of the plant. Other species such as Fusarium culmorum and F. graminearum can only enter through injuries (mechanical damage, insect bite), preformed entrances (stomata) or very soft tissues (stamina, pistil and stigma of the gynoecium) and use production of mycotoxins such as DON and nivalenol (NIV) as virulence factors to undergo cellular defence mechanisms (Bai et al., 2002; Wagacha and Muthomi, 2007). Several pathogenic species of field fungi such as F. culmorum, Microdochium nivale or Bipolaris sorokiniana penetrate the plant during seedling germination either from inoculum present in the surrounding soil or from inoculum present as a seed borne infection (Knudsen et al., 1995; Bonde et al., 1997; Al-Sadi and Deadman, 2010). For some species symptomless growth within infected plants has been demonstrated where infection eventually may reach the developing grain.

Once the malting process has started by steeping the cereal grains in water, fungal propagules present on the surface or within the grain tissue will be activated and start growing and multiplying according to their ecological and physiological preferences. Initial inoculum of r-selected species will be distributed very quickly and evenly over the complete batch to grow and multiply immediately. An inoculum of s-selected species will be distributed quite evenly over the batch but since conditions will not be optimal for them, they will be unable to compete. Inoculum of c-selected species such as Fusarium spp., Alternaria spp., Epicoccum nigrum or Bipolaris sorokiniana will further develop on grains in which the species are present with some superficial spread first to neighbouring grains and later to be wider distributed as the malting process proceeds with mechanical turning of the green malt.

 
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