Abstract
Aging is associated with the accumulation of DNA damage. High expression of DNA repair genes has been suggested to contribute to prolonged lifespan in several organisms. However, the crucial DNA repair genes contributing to longevity remain unknown. Termite kings have an extraordinary long lifespan compared with that of non-reproductive individuals such as workers despite being derived from the same genome, thus providing a singular model for identifying longevity-related genes. In this study, we demonstrated that termite kings express higher levels of the breast cancer susceptibility gene BRCA1 than other castes. Using RNA sequencing, we identified 21 king-specific genes among 127 newly annotated DNA repair genes in the termite Reticulitermes speratus. Using quantitative PCR, we revealed that some of the highly expressed king-specific genes were significantly upregulated in reproductive tissue (testis) compared to their expression in somatic tissue (fat body). Notably, BRCA1 gene expression in the fat body was more than 4-fold higher in kings than in workers. These results suggest that BRCA1 partly contributes to DNA repair in somatic and reproductive tissues in termite kings. These findings provide important insights into the linkage between BRCA1 gene expression and the extraordinary lifespan of termite kings.
Highlights
Genomic instability and DNA damage are hallmarks of aging and number of aging-linked diseases in multicellular organisms [1]
Aging-associated DNA damage including abnormal bases, abasic sites, 8-oxoguanine, single-strand breaks (SSBs), bulky adducts, pyrimidine dimers, doublestrand breaks (DSBs), interstrand cross-links, and genomic mismatches are generally repaired by various damage response (DDR, middle), and the most relevant DNA repair pathways responsible for the removal of the lesions
Using RNA sequencing (RNA-seq), we identified 127 putative DNA repair genes including 50 DNA damage response (DDR) genes, 26 homologous recombination (HR) genes, 16 nucleotide excision repair (NER) genes, 11 non-homologous end-joining (NHEJ) genes, 9 alkylation damage repair (ADR) genes, 7 MMR genes, 4 genes related to various DNA repair-related pathways, 3 base excision repair (BER) genes, and 1 SSB repair (SSBR) gene in R. speratus (Tables S1 and S2)
Summary
Genomic instability and DNA damage are hallmarks of aging and number of aging-linked diseases in multicellular organisms [1]. Aging-associated DNA damage is normally repaired by various DNA repair proteins [4]. These proteins are highly conserved in many organisms, and they play important roles in organismal aging and longevity [4]. Overexpression of several DNA repair genes contributes to the extension of lifespan in the fly Drosophila melanogaster [6]. These studies suggest that efficient DNA repair system contributes to extended longevity. The crucial DNA repair genes contributing to extraordinary longevity are unclear
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