Although the main players of the strigolactone (SL) signaling pathway have been characterized genetically, how they regulate plant development is still poorly understood. Of central importance are the SUPPRESSOR OF MAX2 1-LIKE (SMXL) proteins that belong to a family of eight members in Arabidopsis thaliana, of which one subclade is involved in SL signaling and another one in the pathway of the chemically related karrikins. Through proteasomal degradation of these SMXLs, triggered by either DWARF14 (D14) or KARRIKIN INSENSITIVE2 (KAI2), several physiological processes are controlled, such as, among others, shoot and root architecture, seed germination, and seedling photomorphogenesis. Yet another clade has been shown to be involved in vascular development, independently of the D14 and KAI2 actions and not relying on proteasomal degradation. Despite their role in several aspects of plant development, the exact molecular mechanisms by which SMXLs regulate them are not completely unraveled. To fill the major knowledge gap in understanding D14 and KAI2 signaling, SMXLs are intensively studied, making it challenging to combine all the insights into a coherent characterization of these important proteins. To this end, this review provides an in-depth exploration of the recent data regarding their physiological function, evolution, structure, and molecular mechanism. In addition, we propose a selection of future perspectives, focusing on the apparent localization of SMXLs in subnuclear speckles, as observed in transient expression assays, which we couple to recent advances in the field of biomolecular condensates and liquid–liquid phase separation.

Although the division of the pericycle cells initiates both the lateral root development and the root-derived callus formation, these developmental processes are affected differently in the strigolactone (SL) and karrikin (KAR)/KAI2 ligand (KL) signalling mutant, more axillary growth 2 (max2). Whereas max2 produces more lateral roots than the wild type, it is defective in the regeneration of shoots from root explants. We suggest that the decreased shoot regeneration of max2 originates from a delayed callus primordium formation, yielding less callus material to regenerate shoots. Indeed, when incubated on callus-inducing medium, the pericycle cell division was reduced in max2 and the early gene expression varied when compared to the wild type, as determined by a transcriptomics analysis. Furthermore, the expression of the LATERAL ORGAN BOUNDARIES DOMAIN genes and of callus induction genes was modified in correlation with the max2 phenotype, suggesting a role for MAX2 in the regulation of the interplay between cytokinin, auxin, and light signalling in callus initiation. Additionally, we found that the in vitro shoot regeneration phenotype of max2 might be caused by a defect in KAI2, rather than D14, signalling. Nevertheless, the shoot regeneration assays revealed that also the SL biosynthesis mutants max3 and max4 play a minor role.

Under specific conditions, the germination of Arabidopsis thaliana is dependent on the activation of the KARRIKIN INSENSITIVE 2 (KAI2) signalling pathway by the KAI2-dependent perception of karrikin (KAR) or the artificial strigolactone analogue rac-GR24. To regulate induction of germination, the KAI2 signalling pathway relies on MORE AXILLARY BRANCHED 2 (MAX2)-dependent ubiquitination and proteasomal degradation of the repressor protein SUPPRESSOR OF MAX2 1 (SMAX1). It is not yet known how degradation of SMAX1 proteins eventually results in the regulation of seed germination, but it has been hypothesized that SMAX1-LIKE (SMXL) generally function as transcriptional repressors through the recruitment of co-repressors TOPLESS (TPL) and TPL-related, which in turn interact with histone deacetylases (HDACs). Here we show the involvement of histone deacetylases HDA6, HDA9, HDA19, and HDT1 in MAX2-dependent germination of Arabidopsis, and more specifically, that HDA6 is required for the induction of DLK2 expression in response to rac-GR24 treatment.