Strigolactones Regulate Plant Growth in Arabidopsis via Degradation of the DWARF53-Like Proteins SMXL6, 7, and 8

Strigolactones (SLs) secreted from roots mediate symbiosis with arbuscular mycorrhizal fungi and can trigger germination of parasitic plants (reviewed in Al-Babili and Bouwmeester, 2015). SLs also influence shoot branching, root growth, and leaf shape (reviewed in Williams and Yamaguchi, 2015). In SL signaling in rice (Oryza sativa), the DWARF3 F-box protein acts with the SL receptor DWARF14 as part of an Skp-Cullin-F-box complex in ubiquitin-mediated proteolysis. The targets of this complex include DWARF53, an EAR domain-containing protein that may act as a transcriptional regulator, and possibly the DWARF14 SL receptor (likely as part of a negative feedback mechanism). In Arabidopsis thaliana, the DWARF3 ortholog MORE AXILLARY GROWTH2 (MAX2) also acts in SL signaling. Arabidopsis has eight DWARF53 homologs, which make up the SUPPRESSOR OF MAX2 1 (SMAX1)/SMAX1-LIKE (SMXL) family. To examine SL signaling in Arabidopsis, two studies ( Soundappan et al., 2015; Wang et al., 2015 ) examined smxl6, smxl7, and smxl8 mutants. The smxl6/7/8 triple mutant suppressed the branched phenotype of the max2 mutants (see figure) and also suppressed the auxin transport, PIN1 accumulation, and root branching phenotypes of max2. Expression of a degradation-resistant, dominant form of SMXL6 caused a branched phenotype. Thus, SMXL6/7/8 appear to act downstream of MAX2 in SL signaling. The smxl6/7/8 triple mutant suppresses the branching phenotype of max2. Adult wild-type and mutant plants show the “bushy” phenotype of max2 mutants. (Reprinted from Soundappan et al. [2015], Figure 2A.) Analogy to the rice DWARF3-DWARF53 interaction suggested that Arabidopsis MAX2 might target SMXL6/7/8 for degradation. The authors found that the synthetic SL analog GR24 induces polyubiquitination and degradation of SMXL6/7/8. The degradation of SMXL6/7/8 requires MAX2 and DWARF14; GR24 triggers the association of DWARF14 with SMXL6/7/8, raising the possibility that this event could precede their recruitment into a complex with MAX2. Members of the TOPLESS-RELATED PROTEIN (TPR) family of transcriptional corepressors also interact with SMXL6/7/8. The TPR and SMXL6/7/8 proteins can repress transcription, including of the SL-induced gene BRANCHED1. Thus, these studies found many parallels between D53 in rice and SMXL6/7/8 in Arabidopsis: First, D53/SMXL6/7/8 interact with DWARF3/MAX2 and are polyubiquitinated and degraded in response to induction of SL signaling. Moreover, D53/SMXL6/7/8 interact with TPR proteins to repress transcription (directly or indirectly); degradation of D53/SMXL6/7/8 releases this repression to induce SL signaling. These studies indicate that SMXL6/7/8 function redundantly in response to SLs, but MAX2 may target other SMAX1/SMXL family members in response to other signals. For example, MAX2 also acts in the response to karrikins, compounds found in smoke. Karrikins are structurally related to SL and promote germination in many plants. The authors used KAR1 to activate the karrikin pathway, but KAR1 treatment did not induce degradation of SMXL6/7/8. Rather, activation of the karrikin pathway proceeded through MAX2 and SMAX1, which also interacts with TPR proteins and functions in germination and hypocotyl elongation. Interestingly, SMAX1 and SMXL6/7/8 have different effects on leaf shape, indicating that the members of this family have different functions in response to different signaling molecules. The functions of many of these SMAX1/SMAXL proteins remain to be explored. Identification of the mechanism by which SL regulates shoot branching reveals intriguing similarities to the auxin and jasmonate responses and provides an interesting example of both the conservation of this pathway in monocots and dicots as well as the evolution of the components of this pathway to respond to different signals.