Widespread Transcriptional Scanning in the Testis Modulates Gene Evolution Rates

Bo Xia, Yun Yan, Maayan Baron, Florian Wagner, Dalia Barkley, Marta Chiodin, Sang Y. Kim, David L. Keefe, Joseph P. Alukal, Jef D. Boeke, Itai Yanai

Research output: Contribution to journalArticlepeer-review

Abstract

The testis expresses the largest number of genes of any mammalian organ, a finding that has long puzzled molecular biologists. Our single-cell transcriptomic data of human and mouse spermatogenesis provide evidence that this widespread transcription maintains DNA sequence integrity in the male germline by correcting DNA damage through a mechanism we term transcriptional scanning. We find that genes expressed during spermatogenesis display lower mutation rates on the transcribed strand and have low diversity in the population. Moreover, this effect is fine-tuned by the level of gene expression during spermatogenesis. The unexpressed genes, which in our model do not benefit from transcriptional scanning, diverge faster over evolutionary timescales and are enriched for sensory and immune-defense functions. Collectively, we propose that transcriptional scanning shapes germline mutation signatures and modulates mutation rates in a gene-specific manner, maintaining DNA sequence integrity for the bulk of genes but allowing for faster evolution in a specific subset.

Original languageEnglish (US)
Pages (from-to)248-262.e21
JournalCell
Volume180
Issue number2
DOIs
StatePublished - Jan 23 2020

ASJC Scopus subject areas

  • General Biochemistry, Genetics and Molecular Biology

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