Introns and gene expression: cellular constraints, transcriptional regulation, and evolutionary consequences

Abstract

A gene's "expression profile" denotes the number of transcripts present relative to all other transcripts. The overall rate of transcript production is determined by transcription and RNA processing rates. While the speed of elongating RNA polymerase II has been characterized for many different genes and organisms, gene-architectural features - primarily the number and length of exons and introns - have recently emerged as important regulatory players. Several new studies indicate that rapidly cycling cells constrain gene-architecture toward short genes with a few introns, allowing efficient expression during short cell cycles. In contrast, longer genes with long introns exhibit delayed expression, which can serve as timing mechanisms for patterning processes. These findings indicate that cell cycle constraints drive the evolution of gene-architecture and shape the transcriptome of a given cell type. Furthermore, a tendency for short genes to be evolutionarily young hints at links between cellular constraints and the evolution of animal ontogeny.

Keywords: cell cycle constraints; gene length; macro-evolutionary patterns; splicing.

Figure 1

Transcription and RNA processing take time. A schematic on an intronless (upper panel) and an intron-containing gene (lower panel) are depicted. Pol II transcribes the genes and the RNA is co-transcriptionally capped at the 5′-end as well as spliced (intron-containing gene). The time it takes for Pol II to reach the end of the gene depends on the length of the gene and the elongation rate of Pol II.

Figure 2

Distinct gene architectural features of maternal and zygotic genes. Stick diagram of typical gene architecture for zygotic, maternal, and all annotated transcripts in zebrafish (upper panel) and fly (lower panel). Drawn to scale is the median length of the genes and the first and last exons. For internal exons, the population median for all exons per transcript is drawn. Introns are not to scale; median numbers of introns are shown. Data are from Heyn et al. 2014 [44].

Figure 3

Causative relationships between different levels of biological organization. Blue arrows indicate relationships that propagate from low to high via all the intermediate levels. In contrast, gray arrows indicate potentially new relationships in which fast cell cycles constrain genes to be short, which in turn increases the fraction of young genes that are expressed at specific stages of ontogeny. This alternative path illustrates how causative effects can take different routes as a consequence of the impact of cellular constraints on genomic architectures.