Altered Transcription and Neofunctionalization of Duplicated Genes Rescue the Harmful Effects of a Chimeric Gene in Brassica napus

Chimeric genes contribute to the evolution of diverse functions in plants and animals. However, new chimeric genes also increase the risk of developmental defects. Here, we show that the chimeric gene Brassica napus male sterile 4 (Bnams4 b) is responsible for genic male sterility in the widely used canola line 7365A (Bnams3 ms3ms4 b ms4 b). Bnams4 b originated via exon shuffling ~4.6 million years ago. It causes defects in the normal functions of plastids and induces aborted anther formation and/or albino leaves and buds. Evidence of the age of the mutation, its tissue expression pattern, and its sublocalization indicated that it coevolved with BnaC9.Tic40 (BnaMs3). In Arabidopsis thaliana, Bnams4 b results in complete male sterility that can be rescued by BnaC9.Tic40, suggesting that BnaC9.Tic40 might restore fertility through effects on protein level. Another suppressor gene, Bnams4 a, rescues sterility by reducing the level of transcription of Bnams4 b. Our results suggest that Brassica plants have coevolved altered transcription patterns and neofunctionalization of duplicated genes that can block developmental defects resulting from detrimental chimeric genes.