Abstract
In order to produce multicellular structures filamentous fungi combine various morphogenetic programs that are fundamentally different from those used by plants and animals. The perithecium, the female sexual fruitbody of Neurospora crassa, differentiates from the vegetative mycelium in distinct morphological stages, and represents one of the more complex multicellular structures produced by fungi. In this study we defined the stages of protoperithecial morphogenesis in the N. crassa wild type in greater detail than has previously been described; compared protoperithecial morphogenesis in gene-deletion mutants of all nine mitogen-activated protein (MAP) kinases conserved in N. crassa; confirmed that all three MAP kinase cascades are required for sexual development; and showed that the three different cascades each have distinctly different functions during this process. However, only MAP kinases equivalent to the budding yeast pheromone response and cell wall integrity pathways, but not the osmoregulatory pathway, were essential for vegetative cell fusion. Evidence was obtained for MAP kinase signaling cascades performing roles in extracellular matrix deposition, hyphal adhesion, and envelopment during the construction of fertilizable protoperithecia.
Highlights
The perithecium is the female sexual reproductive organ, or fruitbody, of Neurospora crassa within which ascospores, the products of meiosis, are generated [1,2]
Notable key aspects highlighted by our analyses include: (1) the initial stage being the ascogonial coil, a tight-helical branch with outer dimensions not exceeding 15 mm in diameter, that forms the ascogonium in the center of the developing protoperithecium; (2) septation of the ascogonial coil is a precursor to the emergence of enveloping hyphae; (3) enveloping hyphae, which differentiate as branches of either the ascogonium or one of its neighboring compartments, enlarge the structure; (4) additional enwrapping by enveloping hyphae that may originate from the surrounding vegetative mycelium determine shape, and (5) regulated deposition of extracellular matrix involved in the tight adhesion of ascogonial coil and enveloping hyphae seals the subspherical encasing of the developing fruitbody
Our analysis indicates that mitogen-activated protein (MAP) kinase gene deletions did not lead to the disruption of protoperithecial development at a conserved stage, but that blockage occurred at distinct stages dependent on the affected MAP kinase cascade
Summary
The perithecium is the female sexual reproductive organ, or fruitbody, of Neurospora crassa within which ascospores, the products of meiosis, are generated [1,2]. The fertilizing agent (spermatium) may be: an asexual spore, the conidium, of which there are three types in N. crassa (macroconidia, microconidia and arthroconidia [3]); a germinated ascospore (meiospore); or any vegetative cell or hypha of the mating partner [10,11]. In heterothallic species, such as N. crassa, fertilization by an opposite mating-type ‘male’ partner provides the necessary signal for the transition from the protoperithecial to the perithecial stage of fruitbody development [12].
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