A Plastic Vegetative Growth Threshold Governs Reproductive Capacity inAspergillus nidulans

Abstract

Ontogenetic phases separating growth from reproduction are a common feature of cellular life. Long recognized for flowering plants and animals, early literature suggests this life-history component may also be prevalent among multicellular fungi. We establish the basis of developmental competence-the capacity to respond to induction of asexual development-in the filamentous saprotroph Aspergillus nidulans, describing environmental influences, including genotype-by-environment interactions among precocious mutants, gene expression associated with wild type and precocious competence acquisition, and the genetics of competence timing. Environmental effects are consistent with a threshold driven by metabolic rate and organism density, with pH playing a particularly strong role in determining competence timing. Gene expression diverges significantly over the competence window, despite a lack of overt morphological change, with differentiation in key metabolic, signaling, and cell trafficking processes. We identify five genes for which mutant alleles advance competence timing, including the conserved GTPase RasB (AN5832) and ambient pH sensor PalH (AN6886). In all cases examined, inheritance of competence timing is complex and non-Mendelian, with F 1 progeny showing highly variable transgressive timing and dominant parental effects with a weak contribution from progeny genotype. Competence provides a new model for nutrient-limited life-cycle phases, and their elaboration from unicellular origins. Further work is required to establish the hormonal and bioenergetic basis of the trait across fungi, and underlying mechanisms of variable inheritance.

The role of tradeoffs among life-history traits in a filamentous fungus

“…We would have expected, that the observed reduction in spore yield of the ASEX populations was due to mutations in core genes involved in asexual sporulation, such as brlA, abaA, and wetA (T. H. Adams et al, 1998;Martinelli & Clutterbuck, 1971;Mooney & Yager, 1990;Park & Yu, 2012;J.-H. Yu, 2010). Alternatively, selection could also have acted on other stages in the complex life cycle of A. nidulans, for example via (i) Changes in the timing of initiating sporulation/development (Noble et al, 2016), (ii) Changes in sensing environmental cues necessary for making decisions to fine-tune investments in growth, colony maintenance (via recycling of damaged mycelium) and reproduction (Heaton et al, 2016) and (iii) Changes in secondary metabolism, known to play a role in fungal development and both positive and negative social interactions (Bayram & Braus, 2012;Hibbing et al, 2010;Keller, 2019).…”

“…Asexual conidiation can be induced by environmental factors like the exposure of the colony to air interface and light, but not before a period of vegetative growth (Axelrod, 1972;Noble & Andrianopoulos, 2013). The timing of acquiring reproductive competence is directly correlated to organismal density and is presumably a response to resource colonization (Noble et al, 2016). The timing of sporulation is predicted to reflect life-history optimization to growth on patchy resources (Heaton et al, 2016).…”