Evolution of strigolactone receptors by gradual neo-functionalization of KAI2 paralogues

Abstract

BackgroundStrigolactones (SLs) are a class of plant hormones that control many aspects of plant growth. The SL signalling mechanism is homologous to that of karrikins (KARs), smoke-derived compounds that stimulate seed germination. In angiosperms, the SL receptor is an α/β-hydrolase known as DWARF14 (D14); its close homologue, KARRIKIN INSENSITIVE2 (KAI2), functions as a KAR receptor and likely recognizes an uncharacterized, endogenous signal (‘KL’). Previous phylogenetic analyses have suggested that the KAI2 lineage is ancestral in land plants, and that canonical D14-type SL receptors only arose in seed plants; this is paradoxical, however, as non-vascular plants synthesize and respond to SLs.ResultsWe have used a combination of phylogenetic and structural approaches to re-assess the evolution of the D14/KAI2 family in land plants. We analysed 339 members of the D14/KAI2 family from land plants and charophyte algae. Our phylogenetic analyses show that the divergence between the eu-KAI2 lineage and the DDK (D14/DLK2/KAI2) lineage that includes D14 occurred very early in land plant evolution. We show that eu-KAI2 proteins are highly conserved, and have unique features not found in DDK proteins. Conversely, we show that DDK proteins show considerable sequence and structural variation to each other, and lack clearly definable characteristics. We use homology modelling to show that the earliest members of the DDK lineage structurally resemble KAI2 and that SL receptors in non-seed plants likely do not have D14-like structure. We also show that certain groups of DDK proteins lack the otherwise conserved MORE AXILLARY GROWTH2 (MAX2) interface, and may thus function independently of MAX2, which we show is highly conserved throughout land plant evolution.ConclusionsOur results suggest that D14-like structure is not required for SL perception, and that SL perception has relatively relaxed structural requirements compared to KAI2-mediated signalling. We suggest that SL perception gradually evolved by neo-functionalization within the DDK lineage, and that the transition from KAI2-like to D14-like protein may have been driven by interactions with protein partners, rather than being required for SL perception per se.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-017-0397-z) contains supplementary material, which is available to authorized users.

Physcomitrella patens MAX2 characterization suggests an ancient role for this F‐box protein in photomorphogenesis rather than strigolactone signalling

“…Phylogenetic analysis of full‐length predicted MAX2 proteins indicated that, in contrast to previously published phylogenies that used a higher number of expressed sequence tags and full‐length sequences, MAX2 from P. patens , Marchantia polymorpha and Selaginella moellendorffii formed a separate clade to seed plant proteins (Fig. S3a) (Delaux et al ., ; Bythell‐Douglas et al ., ). Thus, the precise relationships between MAX2 homologues in vascular plants and those in nonvascular plants remain ambiguous.…”

KAI2 regulates root and root hair development by modulating auxin distribution

“…In this second pathway MAX2 is thought to interact with KAI2 (KARRIKIN-INSENSITIVE2), a receptor protein of the α/ hydrolase family, which is encoded by an evolutionary older paralog of D14 (Delaux et al, 2012;Toh et al, 2014;Bythell-Douglas et al, 2017). KAI2 was first identified as a receptor for karrikins, a family of butenolide compounds found in the smoke of burnt plant material (Waters et al, 2012b;Guo et al, 2013).…”

The karrikin ‘calisthenics’: Can compounds derived from smoke help in stress tolerance?

“…Furthermore, some non‐conserved amino acids were also found to mediate the unique ligand binding profile of KAI2iB in S. hermonthica and the exertion of evolutionary forces on these residues possibly led to the diversification of KAI2 receptors (Xu et al ). Bythell‐Douglas et al () phylogenetically analyzed 339 members of the D14/KAI2 family from land plants and charophyte algae. The study suggested that SL perception actually evolved via neo‐functionalization of the D14/KAI2 family, and the transition from KAI2‐like to D14‐like proteins was induced by protein interactions rather than by the requirement of SL perception (Bythell‐Douglas et al ).…”

“…Bythell‐Douglas et al () phylogenetically analyzed 339 members of the D14/KAI2 family from land plants and charophyte algae. The study suggested that SL perception actually evolved via neo‐functionalization of the D14/KAI2 family, and the transition from KAI2‐like to D14‐like proteins was induced by protein interactions rather than by the requirement of SL perception (Bythell‐Douglas et al ).…”

“…2016) Bythell-Douglas et al (2017). phylogenetically analyzed 339 members of the D14/KAI2 family from land plants and charophyte algae.…”