Molecular evolution and diversification of the SMXL gene family

Abstract

Strigolactones (SLs) are a relatively recent addition to the list of plant hormones that control different aspects of plant development. SL signalling is perceived by an α/β hydrolase, DWARF 14 (D14). A close homolog of D14, KARRIKIN INSENSTIVE2 (KAI2), is involved in perception of an uncharacterized molecule called karrikin (KAR). Recent studies in Arabidopsis identified the SUPPRESSOR OF MAX2 1 (SMAX1) and SMAX1-LIKE 7 (SMXL7) to be potential SCF-MAX2 complex-mediated proteasome targets of KAI2 and D14, respectively. Genetic studies on SMXL7 and SMAX1 demonstrated distinct developmental roles for each, but very little is known about these repressors in terms of their sequence features. In this study, we performed an extensive comparative analysis of SMXLs and determined their phylogenetic and evolutionary history in the plant lineage. Our results show that SMXL family members can be sub-divided into four distinct phylogenetic clades/classes, with an ancient SMAX1. Further, we identified the clade-specific motifs that have evolved and that might act as determinants of SL-KAR signalling specificity. These specificities resulted from functional diversities among the clades. Our results suggest that a gradual co-evolution of SMXL members with their upstream receptors D14/KAI2 provided an increased specificity to both the SL perception and response in land plants.

Impairment in karrikin but not strigolactone sensing enhances root skewing in Arabidopsis thaliana

“…The KAR‐dependent degradation of KAI2 can also occur independently from MAX2, independently of ubiquitination or the activity of the 26S proteasome (Waters et al ., ). More recently, heat‐shock‐related proteins have been identified as degradation targets of MAX2 in rice (Jiang et al ., ; Zhou et al ., ) and Arabidopsis (SMXL, SUPPRESSOR OF MAX2‐1‐LIKE; Stanga et al ., ; Soundappan et al ., ; Moturu et al ., ). Thus far, a dichotomy has been proposed with SMAX1 (SUPPRESSOR OF MAX2‐1) suppressing KAR‐related max2 phenotypes (e.g.…”

Fellowship of the rings: a saga of strigolactones and other small signals

“…5c). Elsewhere, the origin of the DLK23 lineage matches the origin of the SMXL4 lineage; while DLK2/DLK3 in angiosperms have lost key residues for MAX2 interaction, and SMXL4 in angiosperms has lost the degron motif (Bythell-Douglas et al, 2017;Wallner et al, 2017;Moturu et al, 2018;Walker et al, 2019). Although this could be coincidence, the strong likelihood is that DLK23 receptors interact with SMXL4 proteins in seed plants, possibly inhibiting their activity without degradation (Fig.…”

“…Analysis of the SMXL protein family supports this idea in most cases, but also suggests there are some intriguing exceptions to this rule. As a group, SMXL proteins can be found in all land-plant taxa, but have not been identified so far in charophyte algae (Moturu et al, 2018;Walker et al, 2019) (Fig. 4).…”

“…In each nonseed plant group, there is usually a single clade of SMXL proteins, while in gymnosperms, there are two clades, equivalent to SMAX1 and SMXL4, and in all angiosperms there are four major clades, increasing to six in the eudicots (SMAX1, SMXL7, SMXL8, SMXL4, SMXL3 and SMXL9; Fig. 5a) (Moturu et al, 2018;Walker et al, 2019). SMXL proteins have a large, multidomain protein structure which is generally highly conserved across land plants; the degree of conservation varies between the different domains (A-I) (Fig.…”

“…5a,b). Domain H contains a short ERF-associated amphiphilic repression (EAR) motif present in all SMXL proteins (Jiang et al, 2013;Zhou et al, 2013;Moturu et al, 2018;Walker et al, 2019). The final domain (I) of SMXL proteins is also highly conserved, but intriguingly, this domain is absent in flowering plant SMXL3 or SMXL9 proteins, and in monilophyte SMXLJ proteins (Fig.…”