Multiple separate cases of pseudogenized meiosis genes Msh4 and Msh5 in Eurotiomycete fungi: associations with Zip3 sequence evolution and homothallism, but not Pch2 losses

Abstract

The overall process of meiosis is conserved in many species, including some lineages that have lost various ancestrally present meiosis genes. The extent to which individual meiosis gene losses are independent from or dependent on one another is largely unknown. Various Eurotiomycete fungi were investigated as a case system of recent meiosis gene losses after BLAST and synteny comparisons found Msh4, Msh5, Pch2, and Zip3 to be either pseudogenized or undetected in Aspergillus nidulans yet intact in congeners such as A. fumigatus. Flanking gene-targeted degenerate PCR primers applied to 9 additional Aspergillus species found (i) Msh4, Msh5, and Zip3 pseudogenized in A. rugulosus (sister taxon to A. nidulans) but intact in all other amplified sequences; and (ii) Pch2 not present at the syntenic locus in most of the 9 species. Topology tests suggested two independent Pch2 losses in genus Aspergillus, neither directly coinciding with pseudogenization of the other three genes. The A. nidulans-A. conjunctus clade Pch2 loss was not associated with significant Ka/Ks changes for Msh4, Msh5, or Zip3; this suggests against prior Pch2 loss directly altering sequence evolution constraints on these three genes. By contrast, Zip3 Ka/Ks tended to be elevated in several other Eurotiomycete fungi with independently pseudogenized Msh4 and Msh5 (Talaromyces stipitatus, Eurotium herbariorum). The coinciding Ka/Ks elevation and/or clear pseudogenization of Zip3 in taxa with pseudogenized Msh4 and Msh5 is consistent with some degree of molecular coevolution. Possible molecular, environmental, and life history variables (e.g., homothallism) that may be associated with these numerous independent meiosis gene losses (Msh4: 3, Msh5: 3, Zip3: ≥ 1, Pch2: 4) are discussed.

Obligate sexual reproduction of a homothallic fungus closely related to the Cryptococcus pathogenic species complex

“…If confirmed, such scenario may be analogous to the loss of Msh4 and Msh5 in the fission yeast Schizosaccharomyces pombe, along with class I crossover formation and crossover interference losses (Hollingsworth and Brill 2004;Malik et al 2007), or parallel the loss of class I crossovers via loss-of-function mutations in Msh4 and/or Msh5 in model species as diverse as S. cerevisiae, Caenorhabditis elegans, and Arabidopsis thaliana, where such events result in fewer crossovers, and those that remain are interference-independent (i.e., produced by a pathway involving instead the Mus81-Mms4/Eme1 protein complex) (Zalevsky et al 1999;Kelly et al 2000;Higgins et al 2004;Hollingsworth and Brill 2004). While in C. depauperatus the effects of Msh4 and Msh5 losses are presently elusive, a recent comparative study in several Aspergillus species suggest an association between the absence of crossover interferencerelated genes and changes in chromosome number and size, with species lacking those genes having in general fewer and more uniform chromosome sizes (Savelkoul 2013;Savelkoul et al 2019) -a trend we interestingly observe between C. depauperatus (with 8 chromosomes) and other Cryptococcus species (with 14 chromosomes) that merits analysis in future studies.…”