Somatic deficiency causes reproductive parasitism in a fungus

TY - JOUR

T1 - Somatic deficiency causes reproductive parasitism in a fungus

AU - Grum-Grzhimaylo, Alexey A.

AU - Bastiaans, Eric

AU - van den Heuvel, Joost

AU - Berenguer Millanes, Cristina

AU - Debets, Alfons J.M.

AU - Aanen, Duur K.

N1 - 7179, ME

PY - 2021

Y1 - 2021

N2 - Some multicellular organisms can fuse because mergers potentially provide mutual benefits. However, experimental evolution in the fungus Neurospora crassa has demonstrated that free fusion of mycelia favours cheater lineages, but the mechanism and evolutionary dynamics of this exploitation are unknown. Here we show, paradoxically, that all convergently evolved cheater lineages have similar fusion deficiencies. These mutants are unable to initiate fusion but retain access to wild-type mycelia that fuse with them. This asymmetry reduces cheater-mutant contributions to somatic substrate-bound hyphal networks, but increases representation of their nuclei in the aerial reproductive hyphae. Cheaters only benefit when relatively rare and likely impose genetic load reminiscent of germline senescence. We show that the consequences of somatic fusion can be unequally distributed among fusion partners, with the passive non-fusing partner profiting more. We discuss how our findings may relate to the extensive variation in fusion frequency of fungi found in nature.

AB - Some multicellular organisms can fuse because mergers potentially provide mutual benefits. However, experimental evolution in the fungus Neurospora crassa has demonstrated that free fusion of mycelia favours cheater lineages, but the mechanism and evolutionary dynamics of this exploitation are unknown. Here we show, paradoxically, that all convergently evolved cheater lineages have similar fusion deficiencies. These mutants are unable to initiate fusion but retain access to wild-type mycelia that fuse with them. This asymmetry reduces cheater-mutant contributions to somatic substrate-bound hyphal networks, but increases representation of their nuclei in the aerial reproductive hyphae. Cheaters only benefit when relatively rare and likely impose genetic load reminiscent of germline senescence. We show that the consequences of somatic fusion can be unequally distributed among fusion partners, with the passive non-fusing partner profiting more. We discuss how our findings may relate to the extensive variation in fusion frequency of fungi found in nature.

KW - national

KW - Plan_S-Compliant_OA

KW - Cell Fusion

KW - Hyphae/physiology

KW - Fungal Proteins/genetics

KW - DNA Mutational Analysis

KW - Mutation

KW - Gene Knockout Techniques

KW - Genes, Fungal/genetics

KW - Neurospora crassa/physiology

KW - Evolution, Molecular

U2 - 10.1038/s41467-021-21050-5

DO - 10.1038/s41467-021-21050-5

M3 - Article

C2 - 33542245

AN - SCOPUS:85100459721

SN - 2041-1723

VL - 12

SP - 783

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 783

ER -