Lineage-specific genes are clustered with HET-domain genes and respond to environmental and genetic manipulations regulating reproduction in Neurospora.

Lineage-specific genes (LSGs) have long been postulated to play roles in the establishment of genetic barriers to intercrossing and speciation. In the genome of Neurospora crassa, most of the 670 Neurospora LSGs that are aggregated adjacent to the telomeres are clustered with 61% of the HET-domain genes, some of which regulate self-recognition and define vegetative incompatibility groups. In contrast, the LSG-encoding proteins possess few to no domains that would help to identify potential functional roles. Possible functional roles of LSGs were further assessed by performing transcriptomic profiling in genetic mutants and in response to environmental alterations, as well as examining gene knockouts for phenotypes. Among the 342 LSGs that are dynamically expressed during both asexual and sexual phases, 64% were detectable on unusual carbon sources such as furfural, a wildfire-produced chemical that is a strong inducer of sexual development, and the structurally-related furan 5-hydroxymethyl furfural (HMF). Expression of a significant portion of the LSGs was sensitive to light and temperature, factors that also regulate the switch from asexual to sexual reproduction. Furthermore, expression of the LSGs was significantly affected in the knockouts of adv-1 and pp-1 that regulate hyphal communication, and expression of more than one quarter of the LSGs was affected by perturbation of the mating locus. These observations encouraged further investigation of the roles of clustered lineage-specific and HET-domain genes in ecology and reproduction regulation in Neurospora, especially the regulation of the switch from the asexual growth to sexual reproduction, in response to dramatic environmental conditions changes. Author summary: A portion of genes within sequenced genomes are lineage-specific. These lineage-specific genes (LSGs) lack evolutionary histories tracking them to ancestors within the genomes of other lineages. Accordingly, they are often classified as new or de novo genes and have long been postulated to play roles in the speciation. Here 670 Neurospora LSGs are reported, most of which are aggregate adjacent to the telomeres and are clustered along with "HET-domain" genes, some of which perform functions in the regulation of self-recognition. In contrast, the LSG-encoding proteins possess few to no domains that would help to identify potential functional roles. We assessed possible functional roles of LSGs by performing transcriptomic profiling in genetic mutants and in distinct environmental conditions, as well as examining gene knockouts for phenotypes. Many LSGs are actively regulated during both asexual and sexual reproduction in response to carbon-resource, light, and temperature-based environmental factors. Furthermore, expression of the LSGs was reported to be significantly affected by perturbation of the genes adv-1, pp-1, and a mating locus that regulates hyphal communication and initiation of sexual reproduction in the fungus. These observations encouraged further investigation of the roles of clustered LSGs and HET-domain genes in ecology and reproduction regulation in Neurospora. [ABSTRACT FROM AUTHOR]