Academic journal article Genetics

A Plastic Vegetative Growth Threshold Governs Reproductive Capacity in Aspergillus Nidulans

Academic journal article Genetics

A Plastic Vegetative Growth Threshold Governs Reproductive Capacity in Aspergillus Nidulans

Article excerpt

ORGANISMS must grow before they can reproduce. Discrete states oriented toward growth or reproduction are fundamental to ontogenesis, and important components of fitness (Istock 1967; Stearns 1976, 1992; Wilbur 1980; Roff 1993; Moran 1994). In unicellular microbes, the decision to grow or differentiate may be tightly integrated or even synonymous with the cell cycle (Johnston et al. 1977; Turner et al. 2012); while in multicellular organisms, intercellular signaling reflecting nutritional state coordinates development. Plants pass through one or more vegetative phase changes before acquiring the capacity to flower (Poethig 2003, 2010), many invertebrates attain the adult form through an intermediate juvenile stage (or stages) (Truman and Riddiford 1999; Bishop et al. 2006), and mammals reach sexual maturity (Zacharias and Wurtman 1969; Young 1976; Gluckman and Hanson 2006; Ahmed et al. 2009). All such examples involve interaction between the unfolding developmental program and nutrient accumulation, mediated by hormones.

Several genera of fungi, sister kingdom to animals within the Opistokhont supergroup, also require a minimum period of growth before acquisition of reproductive competence (Axelrod 1972; Noble and Andrianopoulos 2013). While development of dormant, stress-resistant spores via asexual conidiation can be rapidly induced by exposure of a mature colony to an air interface and light, induction is without effect before a critical period of vegetative growth.

In contrast to plants and animals, competence in filamentous fungi is not associated with obvious morphological differentiation and, perhaps consequently, has received little attention since description in Trichoderma (Gressel and Galun 1967), Pénicillium (Hadley and Harrold 1958; Morton et al. 1958), and Aspergillus (Axelrod et al. 1973) species (exceptions include Adams et al. 1998; Roncal and Ugalde 2003; Sheppard 2005; Gravelat et al. 2008; Nahlik et al. 2010; Ruger-Herreros et al. 2011). Early work in Aspergillus nidulans showed competence acquisition is not simply a consequence of external nutrient limitation (Pastushok and Axelrod 1976), unlike analogous transitions in Dictyostelid amoebae and bacteria (Marin 1976; Bonner 2003). Rapid, concerted changes in metabolic enzyme inducibility (Gealt and Axelrod 1974), intracellular iron availability (Hall and Axelrod 1978), and nutrient uptake rate were found; suggesting competence represents a transition between somewhat discrete organismal states (Kurtz and Champe 1979; Kurtz 1980). More recently, competence for one species, Penicillium cyclopium, was shown to be under control of a diterpenoid hormone constitutively produced via the highly conserved mevalonate pathway (Roncal et al. 2002), which produces diverse signaling compounds, such as steroids and insect juvenile hormones, through hydroxymethylglutarylCoA (Keller et al. 2005)

While the genetic basis for synthesis and sensing of this cue is unknown, regulation of growth and development by extracellular signals is known to be common in fungi, controlling processes such as spore germination inhibition, mating type recognition, negative autotropism, and metabolic influence on alternative reproductive strategies (Vining 1990; Yu and Keller 2005; Fox and Howlett 2008). In the Aspergilli, much is also known of the molecular genetics of development, and of metabolism, hyphal extension, and mitosis during growth, but relatively little of integration between these areas, which may be most relevant to competence.

For A. nidulans, reproduction involves some combination of rapid vegetative growth, producing clonal nuclei distributed throughout the mycelium; asexual development, producing spores by the millions through iterated mitosis of stem cell-like phialides in conidiophores; parasexual development, resulting in chromosomal reassortment with rare recombination; and, given sufficient nutrients, sexual development producing durable fruiting bodies (Figure 1A) (Pontecorvo et al. …

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