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

Walker, Catriona; Siu-Ting, Karen; Taylor, Alysha; O'Connell, Mary J,; Bennett, Tom

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.

Citation

Walker, C., Siu-Ting, K., Taylor, A., O'Connell, M. J., & Bennett, T. (2019). Strigolactone synthesis is ancestral in land plants, but canonical strigolactone signalling is a flowering plant innovation. BMC Biology, 17, 1-19. https://doi.org/10.1186/s12915-019-0689-6

• Journal Article Type: Article
• Acceptance Date: Aug 15, 2019
• Online Publication Date: Sep 5, 2019
• Publication Date: Sep 5, 2019
• Deposit Date: Aug 15, 2019
• Publicly Available Date: Sep 12, 2019
• Journal: BMC Biology
• Electronic ISSN: 1741-7007
• Publisher: Springer Verlag
• Peer Reviewed: Peer Reviewed
• Volume: 17
• Article Number: 70
• Pages: 1-19
• DOI: https://doi.org/10.1186/s12915-019-0689-6
• Keywords: Strigolactones; strigolactone synthesis; strigolactone signalling; phylogenetics
• Public URL: https://nottingham-repository.worktribe.com/output/2434674
• Publisher URL: https://bmcbiol.biomedcentral.com/articles/10.1186/s12915-019-0689-6
• Additional Information: Received: 3 July 2019; Accepted: 13 August 2019; First Online: 5 September 2019; : Not applicable.; : Not applicable.; : The authors declare that they have no competing interests.