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

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 percei...

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Main Authors: Catriona H. Walker, Karen Siu-Ting, Alysha Taylor, Mary J. O’Connell, Tom Bennett
Format: Article
Language:English
Published: BMC 2019-09-01
Series:BMC Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12915-019-0689-6
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author Catriona H. Walker
Karen Siu-Ting
Alysha Taylor
Mary J. O’Connell
Tom Bennett
author_facet Catriona H. Walker
Karen Siu-Ting
Alysha Taylor
Mary J. O’Connell
Tom Bennett
author_sort Catriona H. Walker
collection DOAJ
description 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.
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spelling doaj.art-3505ad8a3a544598acc5b65906e89ce32022-12-22T00:02:49ZengBMCBMC Biology1741-70072019-09-0117111910.1186/s12915-019-0689-6Strigolactone synthesis is ancestral in land plants, but canonical strigolactone signalling is a flowering plant innovationCatriona H. Walker0Karen Siu-Ting1Alysha Taylor2Mary J. O’Connell3Tom Bennett4School of Biology, Faculty of Biological Sciences, University of LeedsInstitute for Global Food Security, School of Biological Sciences, Queens UniversityComputational and Molecular Evolutionary Biology Research Group, School of Biology, Faculty of Biological Sciences, University of LeedsComputational and Molecular Evolutionary Biology Research Group, School of Biology, Faculty of Biological Sciences, University of LeedsSchool of Biology, Faculty of Biological Sciences, University of LeedsAbstract 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.http://link.springer.com/article/10.1186/s12915-019-0689-6StrigolactonesStrigolactone synthesisStrigolactone signallingPhylogenetics
spellingShingle Catriona H. Walker
Karen Siu-Ting
Alysha Taylor
Mary J. O’Connell
Tom Bennett
Strigolactone synthesis is ancestral in land plants, but canonical strigolactone signalling is a flowering plant innovation
BMC Biology
Strigolactones
Strigolactone synthesis
Strigolactone signalling
Phylogenetics
title Strigolactone synthesis is ancestral in land plants, but canonical strigolactone signalling is a flowering plant innovation
title_full Strigolactone synthesis is ancestral in land plants, but canonical strigolactone signalling is a flowering plant innovation
title_fullStr Strigolactone synthesis is ancestral in land plants, but canonical strigolactone signalling is a flowering plant innovation
title_full_unstemmed Strigolactone synthesis is ancestral in land plants, but canonical strigolactone signalling is a flowering plant innovation
title_short Strigolactone synthesis is ancestral in land plants, but canonical strigolactone signalling is a flowering plant innovation
title_sort strigolactone synthesis is ancestral in land plants but canonical strigolactone signalling is a flowering plant innovation
topic Strigolactones
Strigolactone synthesis
Strigolactone signalling
Phylogenetics
url http://link.springer.com/article/10.1186/s12915-019-0689-6
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