A Recently Evolved Alternative Splice Site in the BRANCHED1a Gene Controls Potato Plant Architecture

• Published in: Current biology Vol. 25; no. 14; pp. 1799 - 1809
• Main Authors: Nicolas, Michael, Rodríguez-Buey, María Luisa, Franco-Zorrilla, José Manuel, Cubas, Pilar
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 20.07.2015
• Subjects: Alternative Splicing; Evolution, Molecular; Plant Proteins - genetics; Plant Proteins - metabolism; Plant Shoots - genetics; Plant Shoots - growth & development; Protein Isoforms - genetics; Protein Isoforms - metabolism; RNA Splice Sites; Solanum; Solanum tuberosum; Solanum tuberosum - genetics; Solanum tuberosum - growth & development; Solanum tuberosum - metabolism; Transcription Factors - genetics; Transcription Factors - metabolism
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2015.05.053

Amplification and diversification of transcriptional regulators that control development is a driving force of morphological evolution. A major source of protein diversity is alternative splicing, which leads to the generation of different isoforms from a single gene. The mechanisms and timing of intron evolution nonetheless remain unclear, and the functions of alternative splicing-generated protein isoforms are rarely studied. In Solanum tuberosum, the BRANCHED1a (BRC1a) gene encodes a TCP transcription factor that controls lateral shoot outgrowth. Here, we report the recent evolution in Solanum of an alternative splice site in BRC1a that leads to the generation of two BRC1a protein isoforms with distinct C-terminal regions, BRC1aLong and BRC1aShort, encoded by unspliced and spliced mRNA, respectively. The BRC1aLong C-terminal region has a strong activation domain, whereas that of BRC1aS lacks an activation domain and is predicted to form an amphipathic helix, the H domain, which prevents protein nuclear targeting. BRC1aShort is thus mainly cytoplasmic, while BRC1aLong is mainly nuclear. BRC1aLong functions as a transcriptional activator, whereas BRC1aShort appears to have no transcriptional activity. Moreover, BRC1aShort can heterodimerize with BRC1aLong and act as a dominant-negative factor; it increases BRC1aLong concentration in cytoplasm and reduces its transcriptional activity. This alternative splicing mechanism is regulated by hormones and external stimuli that control branching. The evolution of a new alternative splicing site and a novel protein domain in Solanum BRC1a led to a multi-level mechanism of post-transcriptional and post-translational BRC1a regulation that effectively modulates its branch suppressing activity in response to environmental and endogenous cues. [Display omitted] •In the Solanum clade, an alternative splice site evolved in the BRC1a gene•Alternative splicing of potato BRC1a renders two proteins with antagonistic functions•BRC1aLong isoform is a transcription factor that prevents shoot and stolon branching•BRC1aShort isoform interacts with and limits BRC1aLong nuclear targeting Nicolas et al. show that a splice site evolved in Solanum adds a novel regulatory level to BRC1a branching function. In potato, BRC1aL is a transcription factor that prevents shoot and stolon branching. In contrast, BRC1aS is cytoplasmic, does not have transcriptional activity, and sequesters BRC1aL to the cytoplasm to antagonize its activity.