How the mushroom lost its gills: phylogenomics and population genetics of a morphological innovation in the fungal genus Lentinus

Clark University, Worcester MA

Investigators

Abstract

Fungi represent one of the few branches in the tree of life in which complex multicellular forms (i.e., mushrooms) have evolved. Mushrooms come in a dazzling array of shapes, from the classic “toadstool,” with a cap and stalk, to coral- and candelabra-shaped mushrooms, bird’s nest fungi, bracket fungi, puffballs, and others. Fungal biologists have learned a great deal about the historical patterns of changes in the shapes of mushrooms, but the genetic mechanisms that underlie changes in morphology (form) are obscure. This research will use genomic methods to understand patterns and mechanisms of morphological evolution in mushrooms in the genus Lentinus, which includes a mix of gilled mushrooms and polypores—mushrooms that form pores instead of gills. A particular focus will be the species Lentinus tigrinus (the “tiger sawgill”), which contains both gilled mushrooms and puffball-like “secotioid” forms, in which the gills are covered by a persistent layer of tissue. These two forms are so dissimilar that they were once thought to be different species, but they are capable of mating and they occur side-by-side in populations throughout North America. Lentinus tigrinus presents a case of “evolution caught in the act.” By studying the genetic basis of the switch from a gilled mushroom to the secotioid form in L. tigrinus, this project will shed light on the molecular mechanisms that contribute to the present diversity of mushrooms. This project will provide training for a graduate student and a Postdoctoral Fellow, and it has a significant outreach component, involving workshops on fungal biology for youths in the public schools of Worcester, Massachusetts, and mushroom forays for the general public. Undergraduates will be engaged through course activities that bring research into the classroom. This research will involve four main components: (1) Higher-level relationships of the genus Lentinus will be resolved, using phylogenomic approaches. Genome data will be collected from living cultures as well as herbarium specimens representing exemplars of previously recognized sections of Lentinus. (2) A detailed analysis of the section Tigrini (which contains L. tigrinus) will be conducted, with the aim of resolving species limits. Genomic data will be obtained from all species in section Tigrini, emphasizing populations of L. tigrinus in North America, Europe, and Asia. (3) Two approaches will be taken to identify the genetic region(s) responsible for the secotioid form: (a) a cross-population population-genomic analysis of secotioid and agaricoid (gilled) individuals will be conducted, using specimens collected from populations in Illiniois and Massachusetts, and (b) a genome-wide association study will be performed, using progeny of a cross between secotioid and agaricoid individuals from the Massachusetts population. (4) Population-genetic analyses will be conducted to assess whether the genetic region(s) responsible for the secotioid form is(are) under positive selection. Analyses of genotype frequencies will also be performed to determine if there is assortative mating among the secotioid and agaricoid forms. Collectively, the results of this research will reconstruct higher-level relationships in Lentinus and resolve the genetic bases and population-level dynamics of a morphological innovation in L. tigrinus. This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.