An Interspecific Fungal Hybrid Reveals Cross-Kingdom Rules for Allopolyploid Gene Expression Patterns

Abstract

Polyploidy, a state in which the chromosome complement has undergone an increase, is a major force in evolution. Understanding the consequences of polyploidy has received much attention, and allopolyploids, which result from the union of two different parental genomes, are of particular interest because they must overcome a suite of biological responses to this merger, known as “genome shock.” A key question is what happens to gene expression of the two gene copies following allopolyploidization, but until recently the tools to answer this question on a genome-wide basis were lacking. Here we utilize high throughput transcriptome sequencing to produce the first genome-wide picture of gene expression response to allopolyploidy in fungi. A novel pipeline for assigning sequence reads to the gene copies was used to quantify their expression in a fungal allopolyploid. We find that the transcriptional response to allopolyploidy is predominantly conservative: both copies of most genes are retained; over half the genes inherit parental gene expression patterns; and parental differential expression is often lost in the allopolyploid. Strikingly, the patterns of gene expression change are highly concordant with the genome-wide expression results of a cotton allopolyploid. The very different nature of these two allopolyploids implies a conserved, eukaryote-wide transcriptional response to genome merger. We provide evidence that the transcriptional responses we observe are mostly driven by intrinsic differences between the regulatory systems in the parent species, and from this propose a mechanistic model in which the cross-kingdom conservation in transcriptional response reflects conservation of the mutational processes underlying eukaryotic gene regulatory evolution. This work provides a platform to develop a universal understanding of gene expression response to allopolyploidy and suggests that allopolyploids are an exceptional system to investigate gene regulatory changes that have evolved in the parental species prior to allopolyploidization.

Epichloë hybrida, sp. nov., an emerging model system for investigating fungal allopolyploidy

“…lolii, in contrast to the single rDNA sequence type that is similar to E. typhina. Because of its similarity to the E. festucae-like genome in E. hybrida, together with its discovery in the same sample collection, the nonhybrid haploid strain AR5 has often been used as a proxy for the E. festucae parent (Cox et al 2014). For the other homeologous genome within E. hybrida, only two strains of E. typhina are known to have been isolated from perennial ryegrass: the first from a golf course in Massachusetts, USA (strain E8), and the second from a batch of the perennial ryegrass cultivar Callan in France (strain E432) (Leuchtmann and Schardl 1998).…”

“…Strain E8 has often been used as a proxy for the E. typhina parent, although E8 is genetically more distant from the true E. typhina parent than strain AR5 is from the true E. festucae var. lolii parent (Cox et al 2014). Epichloë hybrida Lp1, together with E. festucae var.…”

“…lolii and E. typhina, and full genomes appear to be retained from both parent species (Cox et al 2014). Although the date when the hybridization event occurred is unknown, genetic work has put an upper bound of approximately 300 000 years (Cox et al 2014). On the basis of isozyme analysis, Lp1 was assigned early on to a larger taxonomic group called LpTG-2 (Lolium perenne taxonomic group 2) (Christensen et al 1993), and the new species definition provided in this report likely applies to all other LpTG-2 strains, such as those listed by Van Zijll de Jong et al (2008).…”

“…Lp1 is an allodiploid originating from the hybridization of two haploid parent species, E. festucae var. lolii and E. typhina, and full genomes appear to be retained from both parent species (Cox et al 2014). Although the date when the hybridization event occurred is unknown, genetic work has put an upper bound of approximately 300 000 years (Cox et al 2014).…”

“…Although Lp1 has been used as an agricultural strain, commercial releases have been limited (Barker et al 1997;Kerr et al 2012). It has, however, become a model system for exploring the outcomes of interspecific hybridization in filamentous fungi, including genomic (Ganley and Scott 1998) and transcriptomic (Cox et al 2014) responses.…”