The role of morphogenetic cell death in the histogenesis of the mycelial cord of Agaricus bisporus and in the development of macrofungi

Abstract

Hyphal growth of the white button mushroom Agaricus bisporus on spawn grains and compost is typically vegetative. Hyphae are loosely arranged, in contrast to the organized texture in tissues, and needle-like calcium oxalate crystals are frequently present on the surface of vegetative hyphae. The mycelial cord is the first well-organized tissue of the fruiting mycelium; it is surrounded by fluffy white hyphae that grow vegetatively. The hyphae of the cord are held together through a semi-fluid medium, the extracellular matrix, which aids in creating a three-dimensional pseudoparenchymatous structure. The matrix material seems to be secreted into the extracellular environment by specifically differentiated cells, but the vegetatively growing hyphae of A. bisporus initially exploit a different mechanism in the production of matrix which involves a type of cell death different from cell necrosis. This primary matrix production leads to the formation of minute cord tissues in which oxalate crystals are no longer present. Once the hyphal cells of A. bisporus pass the threshold from a vegetative form into organized structures, they become differentiated and self-maintaining in the production of the extracellular matrix material. Morphogenetic cell death has been observed before in A. bisporus development and here we show that it occurs in various species of macrofungi: a mucoid zone of the pileipellis typically found in developing fruit bodies of Psilocybe and Panaeolus spp. contains numerous, dying or dead hyphal cells which show ultrastructural features comparable to those observed during the mycelial cord formation of A. bisporus. Studies performed using specimens of Stropharia rugoso-annulata, Coprinus domesticus, Psathyrella candolleana, Tremella mesenterica, Otidea onotica and Peziza ostracoderma in representative growth stages revealed supporting evidence for the view that morphogenetic cell death plays a key role at different stages during the development of fungal fruit bodies. This phenomenon may be related to the programmed cell death occurring in developing plants and animals.