Strigolactone Signaling in Arabidopsis Regulates Shoot Development by Targeting D53-Like SMXL Repressor Proteins for Ubiquitination and Degradation

Strigolactones (<a id="xref-def-1-1" class="xref-list" href="#def-1">SLs</a>) are carotenoid-derived phytohormones that control many aspects of plant development, including shoot branching, leaf shape, stem secondary thickening, and lateral root growth. In rice (<em>Oryza sativa</em>), <a id="xref-def-1-2" class="xref-list" href="#def-1">SL</a> signaling requires the degradation of DWARF53 (D53), mediated by a complex including D14 and D3, but in <em>Arabidopsis thaliana</em>, the components and mechanism of <a id="xref-def-1-3" class="xref-list" href="#def-1">SL</a> signaling involving the D3 ortholog MORE AXILLARY GROWTH2 (MAX2) are unknown. Here, we show that <a id="xref-def-1-4" class="xref-list" href="#def-1">SL</a>-dependent regulation of shoot branching in Arabidopsis requires three D53-like proteins, SUPPRESSOR OF MORE AXILLARY GROWTH2-LIKE6 (SMXL6), SMXL7, and SMXL8. The <em>smxl6 smxl7 smxl8</em> triple mutant suppresses the highly branched phenotypes of <em>max2</em> and the <a id="xref-def-1-5" class="xref-list" href="#def-1">SL</a>-deficient mutant <em>max3.</em> Overexpression of a mutant form of SMXL6 that is resistant to <a id="xref-def-1-6" class="xref-list" href="#def-1">SL</a>-induced ubiquitination and degradation enhances shoot branching. Exogenous application of the <a id="xref-def-1-7" class="xref-list" href="#def-1">SL</a> analog <em>rac</em>-GR24 causes ubiquitination and degradation of SMXL6, 7, and 8; this requires D14 and MAX2. D53-like SMXLs form complexes with MAX2 and TOPLESS-RELATED PROTEIN2 (TPR2) and interact with D14 in a GR24-responsive manner. Furthermore, D53-like SMXLs exhibit TPR2-dependent transcriptional repression activity and repress the expression of <em>BRANCHED1</em>. Our findings reveal that in Arabidopsis, D53-like SMXLs act with TPR2 to repress transcription and so allow lateral bud outgrowth but that <a id="xref-def-1-8" class="xref-list" href="#def-1">SL</a>-induced degradation of D53-like proteins activates transcription to inhibit outgrowth.