The Plot Thickens: Haploid and Triploid-Like Thalli, Hybridization, and Biased Mating Type Ratios in Letharia.

Sandra Lorena Ament-Velásquez,Toby Spribille,Linnea Bergström,Göran Thor,Dan Vanderpool,Yoshikazu Yamamoto,Juri Nascimbene,Veera Tuovinen,Hanna Johannesson

doi:10.3389/ffunb.2021.656386

Abstract

The study of the reproductive biology of lichen fungal symbionts has been traditionally challenging due to their complex lifestyles. Against the common belief of haploidy, a recent genomic study found a triploid-like signal in Letharia. Here, we infer the genome organization and reproduction in Letharia by analyzing genomic data from a pure culture and from thalli, and performing a PCR survey of the MAT locus in natural populations. We found that the read count variation in the four Letharia specimens, including the pure culture derived from a single sexual spore of L. lupina, is consistent with haploidy. By contrast, the L. lupina read counts from a thallus' metagenome are triploid-like. Characterization of the mating-type locus revealed a conserved heterothallic configuration across the genus, along with auxiliary genes that we identified. We found that the mating-type distributions are balanced in North America for L. vulpina and L. lupina, suggesting widespread sexual reproduction, but highly skewed in Europe for L. vulpina, consistent with predominant asexuality. Taken together, we propose that Letharia fungi are heterothallic and typically haploid, and provide evidence that triploid-like individuals are hybrids between L. lupina and an unknown Letharia lineage, reconciling classic systematic and genetic studies with recent genomic observations.

Highlights

The way an organism reproduces is one of its most important traits, since patterns of inheritance drastically affect a species ability to adapt and survive over evolutionary time (Bell, 1982; Whittle et al, 2011)
Contig 1 is composed of 87% repetitive elements, in stark contrast with most other contigs that harbor around 30% repetitive elements (Supplementary Figure 5)
Future research should aim at clarifying if this contig is a core feature of the Letharia genome, or if it represents some form of accessory or B chromosome, FIGURE 8 | How is a triploid-like hybrid of Letharia formed? (A) We present four main models that can explain a triploid-like pattern where only two out of threegenomes belong to the same species

Summary

Introduction

The way an organism reproduces is one of its most important traits, since patterns of inheritance drastically affect a species ability to adapt and survive over evolutionary time (Bell, 1982; Whittle et al, 2011). Researchers can use the structure of the mating-type (MAT) locus, and the frequency of mating types in natural populations to shed light on the reproductive biology of a species. Successful mating is only possible between haploid individuals of opposite mating types (Glass et al, 1988). The relative frequency of allelic variants at the MAT-locus in natural populations can be used to investigate the reproductive mode of the species (e.g., Mandel et al, 2007), as an even distribution indicates frequent sexual reproduction while an uneven distribution points toward a relatively high frequency of asexual propagation. Homothallic Lecanoromycetes do exist, such as some members of the genus Xanthoria s. lat. (Honegger et al, 2004; Scherrer et al, 2005), emphasizing that taxa must be investigated in a case-by-case manner

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