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Lim3  encodes an RNA polymerase II transcription factor with a key role in neuron specification. It was also identified as a candidate gene that affects lifespan. These pleiotropic effects indicate the fundamental significance of the potential interplay between neural development and lifespan control. The goal of this study was to analyze the causal relationships between  Lim3  structural variations, and gene expression and lifespan changes, and to provide insights into regulatory pathways controlling lifespan. Fifty substitution lines containing second chromosomes from a  Drosophila  natural population were used to analyze the association between lifespan and sequence variation in the 5′-regulatory region, and first exon and intron of  Lim3A , in which we discovered multiple transcription start sites (TSS). The core and proximal promoter organization for  Lim3A  and a previously unknown mRNA named  Lim3C  were described. A haplotype of two markers in the  Lim3A  regulatory region was significantly associated with variation in lifespan. We propose that polymorphisms in the regulatory region affect gene transcription, and consequently lifespan. Indeed, five polymorphic markers located within 380 to 680 bp of the  Lim3A  major TSS, including two markers associated with lifespan variation, were significantly associated with the level of  Lim3A  transcript, as evaluated by real time RT-PCR in embryos, adult heads, and testes. A naturally occurring polymorphism caused a six-fold change in gene transcription and a 25% change in lifespan. Markers associated with long lifespan and intermediate  Lim3A  transcription were present in the population at high frequencies. We hypothesize that polymorphic markers associated with  Lim3A  expression are located within the binding sites for proteins that regulate gene function, and provide general rather than tissue-specific regulation of transcription, and that intermediate levels of  Lim3A  expression confer a selective advantage and longer lifespan.

A Naturally Occurring Polymorphism at Drosophila melanogaster Lim3 Locus, a Homolog of Human LHX3/4, Affects Lim3 Transcription and Fly Lifespan