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

Abstract

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, BRC1a(Long) and BRC1a(Short), encoded by unspliced and spliced mRNA, respectively. The BRC1a(Long) C-terminal region has a strong activation domain, whereas that of BRC1a(S) lacks an activation domain and is predicted to form an amphipathic helix, the H domain, which prevents protein nuclear targeting. BRC1a(Short) is thus mainly cytoplasmic, while BRC1a(Long) is mainly nuclear. BRC1a(Long) functions as a transcriptional activator, whereas BRC1a(Short) appears to have no transcriptional activity. Moreover, BRC1a(Short) can heterodimerize with BRC1a(Long) and act as a dominant-negative factor; it increases BRC1a(Long) 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.

Ideal crop plant architecture is mediated by tassels replace upper ears1, a BTB/POZ ankyrin repeat gene directly targeted by TEOSINTE BRANCHED1

“…For example, in potato, the ratio of red to far red light and auxin levels appear to cause alternative splicing of the BRC1 homolog, leading to production of dominant negative forms of the protein and subsequent changes in branching and plant morphology (18). Finally, in other grasses such as sorghum, the tb1 ortholog is sensitive to far red light signals that induce the shade avoidance response known to suppress axillary bud growth (19).…”

Abscisic acid signaling is controlled by a BRANCHED1/HD-ZIP I cascade in Arabidopsis axillary buds

“…However, when ectopically expressed in seedlings, BRC1 also can cause a rapid growth cessation in shoot and root apical meristem and leaf primordia (3). Likewise, generalized overexpression of the Solanum tuberosum ortholog, StBRC1a, produces dwarf plants with very small leaves and short internodes in potato (5). Despite these remarkable effects on growth and development and their wellknown, critical role in the suppression of shoot branching, the downstream pathways by which BRC1-like genes promote bud dormancy are still largely unknown.…”

Mechanisms of vegetative propagation in bulbs : a molecular approach

“…TB1(monocots)/BRC1(dicots) is a TCP transcription factor mainly expressed in dormant axillary meristems inhibiting their outgrowth Takeda et al 2003;Hubbard et al 2002). Given the role of TB1/BRC1 as integrator of multiple signals involved in bud outgrowth, mayor attention has been given to this gene in recent years (Martín-Trillo et al 2011;Nicolas et al 2015;Braun et al 2012;González-Grandío et al 2017).…”

“…The TCP transcription factor family, named after its founder members TEOSINTE BRANCHED1, CYCLOIDEA, and PROLIFERATING CELL FACTOR, has in general around 25-30 members in eudicots (Nicolas et al 2015). TCP genes are expressed in a wide range of tissues and they control flower, leaf, and lateral shoot growth by activating or inhibiting cell proliferation (Martín-Trillo and Cubas 2010) (Nicolas et al 2015) (Mondragón-Palomino and Trontin 2011). Furthermore, evidence from Arabidopsis expression studies indicates that several TCP members are lowly expressed in the above ground tissues (Danisman et al 2013).…”