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. 2019 Sep 5;17(1):70.
doi: 10.1186/s12915-019-0689-6.

Strigolactone synthesis is ancestral in land plants, but canonical strigolactone signalling is a flowering plant innovation

Catriona H Walker  1 , Karen Siu-Ting  2   3 , Alysha Taylor  4 , Mary J O'Connell  4   5 , Tom Bennett  6
Affiliations

Strigolactone synthesis is ancestral in land plants, but canonical strigolactone signalling is a flowering plant innovation

Catriona H Walker et al. BMC Biol. .

Abstract

Background: Strigolactones (SLs) are an important class of carotenoid-derived signalling molecule in plants, which function both as exogenous signals in the rhizosphere and as endogenous plant hormones. In flowering plants, SLs are synthesized by a core pathway of four enzymes and are perceived by the DWARF14 (D14) receptor, leading to degradation of SMAX1-LIKE7 (SMXL7) target proteins in a manner dependent on the SCFMAX2 ubiquitin ligase. The evolutionary history of SLs is poorly understood, and it is not clear whether SL synthesis and signalling are present in all land plant lineages, nor when these traits evolved.

Results: We have utilized recently-generated genomic and transcriptomic sequences from across the land plant clade to resolve the origin of each known component of SL synthesis and signalling. We show that all enzymes in the core SL synthesis pathway originated at or before the base of land plants, consistent with the previously observed distribution of SLs themselves in land plant lineages. We also show that the late-acting enzyme LATERAL BRANCHING OXIDOREDUCTASE (LBO) may be considerably more ancient than previously thought. We perform a detailed phylogenetic analysis of SMXL proteins and show that specific SL target proteins only arose in flowering plants. We also assess diversity and protein structure in the SMXL family, identifying several previously unknown clades.

Conclusions: Overall, our results suggest that SL synthesis is much more ancient than canonical SL signalling, consistent with the idea that SLs first evolved as rhizosphere signals and were only recruited much later as hormonal signals.

Keywords: Phylogenetics; Strigolactone signalling; Strigolactone synthesis; Strigolactones.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Optimal phylogeny for D27 family. Maximum likelihood (ML) tree under the MGK+F3X4+R5 codon model in IQtree. Topology rooted with the D27L2 clade. Key bootstrap values are shown along the backbone of the tree. The fully labelled phylogeny is shown in Additional file 3A
Fig. 2
Fig. 2
Optimal phylogeny for CCD7 family. Maximum likelihood (ML) tree with the amino acid dataset under the PROTCATLGX model in RAxML. Topology rooted with the chlorophyte CCD7 clade. Key bootstrap values are shown along the backbone of the tree. The fully labelled phylogeny is shown in Additional file 7C
Fig. 3
Fig. 3
Optimal phylogeny for CCD8 family. Maximum likelihood (ML) tree with the amino acid dataset under the PROTCATLGX model in RAxML. Topology rooted with the hornwort CCD8 clade. Key bootstrap values are shown along the backbone of the tree. The fully labelled phylogeny is shown in Additional file 9C
Fig. 4
Fig. 4
Optimal phylogeny for MAX1 family. Maximum likelihood (ML) tree with the amino acid dataset under the PROTCATLGX model in RAxML. Topology rooted with the algal MAX1 clade. The fully labelled phylogeny is shown in Additional file 11C
Fig. 5
Fig. 5
Optimal phylogeny for LBO family. Maximum likelihood (ML) tree with the amino acid dataset under the PROTCATLGX model in RAxML. Topology rooted with the DOXC55 clade. The fully labelled phylogeny is shown in Additional file 13A
Fig. 6
Fig. 6
Optimal phylogeny for SMXL family. Maximum likelihood (ML) tree with the amino acid dataset under the PROTCATJTTX model in RAxML. Topology rooted at the hornwort clade. a Phylogram, labelled to show the high-order relationships between the major clades. b Cladogram showing more detailed relationships between the clades listed in Table 2, with bootstrap values at key nodes. The fully labelled phylogeny is shown in Additional file 17
Fig. 7
Fig. 7
Reconstruction of SMXL evolution. Schematic depicting the complement of SMXL proteins in major land groups, and their inferred evolutionary origin. Each branch indicates a major land plant group; lycophytes, monilophytes and gymnosperms are further sub-divided into relevant orders/families/etc. The circles on each branch indicate the core complement of proteins in that group or sub-group. Clades which are inferred by parsimony are denoted with a translucent circle, and clades believed to have been lost are shown with a red cross. Letters and numbers in the circles indicate clade names. Circles without symbols at internal branching points represent the minimum inferred SMXL protein complement in the last common ancestor of each major land plant group
Fig. 8
Fig. 8
Models of strigolactone signalling evolution. Three models of land plant evolution, showing the likely origins of different protein families involved in SL/KL synthesis and signalling. a Traditional view [37]. b ‘Hornworts-basal’ model [38]. c ‘Monophyletic bryophytes’ [44]. Depending on the scheme of evolution, the likely origin(s) of SL perception vary considerably. Curved lines represent the innovations (duplications, sub/neo-functionalization) in the DDK and SMXL lineages implied by each scenario. Hor = hornworts, Liv = liverworts, Mos = mosses, Lyc = lycophytes, Mon = monilophytes, Gym = gymnosperms, Ang = angiosperms
Fig. 9
Fig. 9
Ligand and target specificity in D14/KAI2 signalling. Possible models of D14/SMXL signalling in different land plant groups, based on (1) identified D14/KAI2 and SMXL proteins in each taxon, (2) presence or absence of MAX2-interaction residues in D14/KAI2 proteins and (3) predicted shape of ligand binding pockets in D14/KAI2 proteins [29]. In charophyte algae, there may be a KAI2-MAX2 signalling module, but there are no apparent SMXL proteins, and the function of this complex is not clear. In hornworts and liverworts, there is likely to be canonical KAI2 signalling, but there does not seem to be any canonical SL signalling, and SLs may act only as mycorrhizal signals. In mosses, mycorrhizal associations have been lost, and SL may have been independently recruited as a hormonal or ‘quorum sensing’ signal. This may plausibly have occurred by neo-functionalization of DDK and SMXL proteins, but either way is MAX2 independent. In both lycophytes and monilophytes, the status of SL signalling, and whether there is any connection with DDK proteins, is largely unclear. In monilophytes, DDK proteins probably act independently of MAX2, and it is unclear with SMXL proteins interact with the KAI2-MAX2 module. In gymnosperms, canonical D14-mediated SL signalling is present, but both SL and KL probably target the same SMXL protein for degradation. In angiosperms, SL and KL target separate SMXL proteins for degradation. It is unclear whether the downstream targets of the pathways are still shared, or have also separated
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