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

Authors: WANG, ZHENG - Yale University; WANG, YEN-WEN - Yale University; Kasuga, Takao; LOPEZ-GIRALDEZ, FRANCESC - Yale University; ZHANG, YANG - Chinese Academy Of Sciences; ZHANG, ZHANG - Chinese Academy Of Sciences; WANG, YANING - Chinese Academy Of Sciences; DONG, CAIHONG - Chinese Academy Of Sciences; SIL, ANITA - University Of California San Francisco (UCSF); TRAIL, FRANCES - Michigan State University; YARDEN, ODED - Hebrew University Of Jerusalem; TOWNSEND, JEFFREY - Yale University

Submitted to: PLoS Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/16/2023
Publication Date: 11/7/2023
Citation: Wang, Z., Wang, Y., Kasuga, T., Lopez-Giraldez, F., Zhang, Y., Zhang, Z., Wang, Y., Dong, C., Sil, A., Trail, F., Yarden, O., Townsend, J. 2023. Lineage-specific genes are clustered with HET-domain genes and respond to environmental and genetic manipulations regulating reproduction in Neurospora. PLoS Genetics. 19(11). Article e1011019. https://doi.org/10.1371/journal.pgen.1011019.
DOI: https://doi.org/10.1371/journal.pgen.1011019

Interpretive Summary: Some genes in a fungal genome are shared only within closely related species such as the fungal kingdom, and some genes, called orphan genes, are unique to a particular species. Orphan genes have long been postulated to play roles in the establishment of genetic barriers to intercrossing and speciation. We identified 670 orphan genes in the genome of the fungal model Neurospora crassa were aggregated adjacent to the telomeres, and over 63% of them formed clusters. Among these, 64% were detectable on unusual carbon sources such as furfural and HMF—wildfire-produced chemicals that are a strong inducer of sexual development in N. crassa. Orphan genes are potential targets for the manipulation of fungal growth, a key aspect of both the control of fungal pathogenicity and the iterative improvement of fungal biotechnology.

Technical Abstract: As de novo elements of the genome, orphan genes have long been postulated to play roles in the establishment of genetic barriers to intercrossing and speciation. However, there is a lack of working hypotheses as to what role they play. Systematic investigation of the evolutionary history, genome structures, expression dynamics and regulation of orphan genes in well-studied models can shed light on their functions in reproductive isolation. The 670 orphan genes that we identified in the genome of the fungal model Neurospora crassa were aggregated adjacent to the telomeres, and over 63% of them formed clusters with 61% of the het-like genes—genes that regulate self-recognition and define vegetative compatibility groups. Nearly all orphan-het clusters are syntenic within closely related species, suggesting relatively recent colocalization. Analysis of transcriptomic data from N. crassa conditions associated with growth and reproduction reveals 342 orphan genes that are dynamically expressed during both asexual and sexual phases. Among these, 37% were expressed in a detectable manner when the fungus was cultured on common carbon resources, but 64% were detectable on unusual carbon sources such as furfural and HMF—wildfire-produced chemicals that are a strong inducer of sexual development in N. crassa. Expression of a significant portion of the orphan genes was sensitive to light and temperature, factors that regulate asexual and sexual reproduction, among other fungal activities. Coordinate expression in orphan-het gene clusters was detected during early hyphal branching. Furthermore, orphan genes and clustered het-like genes respond similarly to mutations in transcription factors adv-1 and pp-1 that regulate hyphal communication, and expression of more than one quarter of the orphan genes was affected by a mating locus mutant. Functional interactions between orphan and het-like genes likely consolidate vegetative incompatibility during asexual reproduction, but possibly promote crossings between vegetative compatibility groups during sexual reproduction. Their involvement in the balance between genome homogeneity and heterogeneity in vegetative compatibility likely contribute to Neurospora speciation. Orphan genes are potential targets for the manipulation of fungal growth, a key aspect of both the control of fungal pathogenicity and the iterative improvement of fungal biotechnology.