Comparative transcriptomics uncovers alternative splicing changes and signatures of selection from maize improvement

Alternative splicing (AS) is an important regulatory mechanism that greatly contributes to eukaryotic transcriptome diversity. A substantial amount of evidence has demonstrated that AS complexity is relevant to eukaryotic evolution, development, adaptation, and complexity. In this study, six teosinte and ten maize transcriptomes were sequenced to analyze AS changes and signatures of selection in maize domestication and improvement.

We suggest that both maize and teosinte share similar AS mechanisms, but more genes have increased AS complexity during domestication from teosinte to maize. Importantly, a subset of AS level-increased genes that encode transcription factors and stress-responsive proteins may have been selected during maize improvement.

In maize and teosinte, 13,593 highly conserved genes, including 12,030 multiexonic genes, were detected. By identifying AS isoforms from mutliexonic genes, we found that AS types were not significantly different between maize and teosinte. In addition, the two main AS types (intron retention and alternative acceptor) contributed to more than 60% of the AS events in the two species, but the average unique AS events per each alternatively spliced gene in maize (4.12) was higher than that in teosinte (2.26). Moreover, 94 genes generating 98 retained introns with transposable element (TE) sequences were detected in maize, which is far more than 9 retained introns with TEs detected in teosinte. This indicates that TE insertion might be an important mechanism for intron retention in maize. Additionally, the AS levels of 3864 genes were significantly different between maize and teosinte. Of these, 151 AS level-altered genes that are involved in transcriptional regulation and in stress responses are located in regions that have been targets of selection during maize improvement. These genes were inferred to be putatively improved genes. Conclusions: We suggest that both maize and teosinte share similar AS mechanisms, but more genes have increased AS complexity during domestication from teosinte to maize. Importantly, a subset of AS level-increased genes that encode transcription factors and stress-responsive proteins may have been selected during maize improvement.