Two Young Genes Reshape a Novel Interaction Network in Brassica napus.

New genes often drive the evolution of gene interaction networks. In Brassica napus, the widely used genic male sterile breeding system 7365ABC is controlled by two young genes, Bnams4(b) and BnaMs3. However, the interaction mechanism of these two young genes remains unclear. Here, we confirmed that Bnams4(b) interacts with the nuclear localised E3 ligase BRUTUS (BTS). Ectopic expression of AtBRUTUS (AtBTS) and comparison between Bnams4(b)-transgenic Arabidopsis and bts mutants suggested that Bnams4(b) may drive translocation of BTS to cause various toxic defects. BnaMs3 gained an exclusive interaction with the plastid outer-membrane translocon Toc33 compared with Bnams3 and AtTic40, and specifically compensated for the toxic effects of Bnams4(b). Heat shock treatment also rescued the sterile phenotype, and high temperature suppressed the interaction between Bnams4(b) and BTS in yeast. Furthermore, the ubiquitin system and TOC (translocon at the outer envelope membrane of chloroplasts) component accumulation were affected in Bnams4(b)-transgenic Arabidopsis plants. Taken together, these results indicate that new chimeric Bnams4(b) carries BTS from nucleus to chloroplast, which may disrupt the normal ubiquitin-proteasome system to cause toxic effects, and these defects can be compensated by BnaMs3-Toc33 interaction or environmental heat shock. It reveals a scenario in which two population-specific coevolved young genes reshape a novel interaction network in plants.