The origin of plants: genomes, rocks, and biochemical cycles
Lead Research Organisation:
University of Bristol
Department Name: Earth Sciences
Abstract
There can be no doubt that early land plant evolution transformed the planet but how our knowledge of how this happened is in disarray. The clear coincidence in the first appearance of land plant fossils and formative shifts in atmospheric oxygen and CO2 is an artefact of the absence of earlier terrestrial rocks, and disentangling the timing of land plant bodyplan assembly and its impact on global biogeochemical cycles requires a new understanding of early land plant evolution and the timescale over which it was effected.
Early life on land was mostly microbial, but sometime between about 700 million and 420 million years ago plants moved from water onto land. The timeframe is controversial and as currently understood it is very broad, but a more precise knowledge of the events is key to linking the early evolution of plant life to major environmental change. Ambiguity and uncertainty arise because the principal lines of evidence conflict. Fossils, notably plant microfossils (spores), point to colonization beginning about 470 Ma (million years ago), but the affinities of the early spore producers are controversial. Macrofossils (plant stems, multicellular organ systems, etc) indicate a later colonization, beginning about 430 Ma. Calibrated molecular phylogenies - studies of the timing of divergence of living plant lineages based on molecular sequence data, where the rate of mutation is calibrated to time using fossils - point to an origin and early evolution of life on land that may have begun during the Late Neoproterozoic, long predating the fossil evidence. Recent research has identified difficulties with both molecular phylogenetic and palaeontological approaches, which our proposed research program will address.
We have assembled a multidisciplinary team to conduct research to remedy these shortcomings. We will establish a robust genealogy for living plant lineages based on a genome-scale amount of molecular sequence data (~1,000s genes and, therefore, ~1,000,000s nucleotides). The genealogy will be linked to time by including important and exceptionally preserved fossil species. These will be correctly placed through detailed characterization of their anatomy using state of the art Synchrotron Computed Tomography, a novel approach that we have recently shown to provide valuable new data in a recent proof of concept study. Sedimentary regime is known to affect the age estimate given by fossils, so we will also apply new methods develop by us to assess and to correct for this. Together, these approaches will enable us to develop a robust phylogeny calibrated with greater precision to time, which we will use to investigate the evolutionary assembly of key land plant organs and tissue systems (e.g., roots, stomata, vascular tissue, leaves) and their impact on major biogeochemical cycles. Finally, we will we will explore the implications of our plant evolutionary timescale within a leading computer model of global biogeochemical cycling (GENIE). This will enable us to generate predictions for levels of atmospheric carbon dioxide levels and of organic carbon productivity that we will test against geological observations. Ultimately, we will establish a new scenario for the timing and tempo of early land plant evolution, the assembly of land plant bodyplans, and a new understanding of the effect of this episode upon the evolution of the Earth System.
Early life on land was mostly microbial, but sometime between about 700 million and 420 million years ago plants moved from water onto land. The timeframe is controversial and as currently understood it is very broad, but a more precise knowledge of the events is key to linking the early evolution of plant life to major environmental change. Ambiguity and uncertainty arise because the principal lines of evidence conflict. Fossils, notably plant microfossils (spores), point to colonization beginning about 470 Ma (million years ago), but the affinities of the early spore producers are controversial. Macrofossils (plant stems, multicellular organ systems, etc) indicate a later colonization, beginning about 430 Ma. Calibrated molecular phylogenies - studies of the timing of divergence of living plant lineages based on molecular sequence data, where the rate of mutation is calibrated to time using fossils - point to an origin and early evolution of life on land that may have begun during the Late Neoproterozoic, long predating the fossil evidence. Recent research has identified difficulties with both molecular phylogenetic and palaeontological approaches, which our proposed research program will address.
We have assembled a multidisciplinary team to conduct research to remedy these shortcomings. We will establish a robust genealogy for living plant lineages based on a genome-scale amount of molecular sequence data (~1,000s genes and, therefore, ~1,000,000s nucleotides). The genealogy will be linked to time by including important and exceptionally preserved fossil species. These will be correctly placed through detailed characterization of their anatomy using state of the art Synchrotron Computed Tomography, a novel approach that we have recently shown to provide valuable new data in a recent proof of concept study. Sedimentary regime is known to affect the age estimate given by fossils, so we will also apply new methods develop by us to assess and to correct for this. Together, these approaches will enable us to develop a robust phylogeny calibrated with greater precision to time, which we will use to investigate the evolutionary assembly of key land plant organs and tissue systems (e.g., roots, stomata, vascular tissue, leaves) and their impact on major biogeochemical cycles. Finally, we will we will explore the implications of our plant evolutionary timescale within a leading computer model of global biogeochemical cycling (GENIE). This will enable us to generate predictions for levels of atmospheric carbon dioxide levels and of organic carbon productivity that we will test against geological observations. Ultimately, we will establish a new scenario for the timing and tempo of early land plant evolution, the assembly of land plant bodyplans, and a new understanding of the effect of this episode upon the evolution of the Earth System.
Planned Impact
museum visitors, and the amateur naturalist community. We will reach these diverse audiences through a combination of tailored standard academic practices and innovative means of communication led by experts in science communication at one of our major national museums. The process and results of our research will significantly enhance The Natural History Museum's Science Communication Programme, providing direct educational benefits to secondary school students and cultural benefits to the general public.
Because of the subject matter and the multidisciplinary nature of the proposed research, our results will be of interest to a diverse scientific audience, including both Life Scientists (systematic botanists, molecular systematists, evolutionary and developmental biologists) and Earth Scientists (palaeobotanists, micropalaeontologists, sedimentary geologists, geochemists). The results, novel data and methods in our Time Tree project are relevant to the former, whereas the latter will be most interested in our analyses of the Rock Record. Both groups as well as (palaeo-)climatologists will be interested in the synthesis, which is concerned with how the geochemical carbon cycle is best calibrated in light of a revised time scale for key events in land plant evolution (e.g., rates of carbon sequestration, weathering of surface rocks, soil development). New datasets will be made publicly available via the TimeTree project, DRYAD, TreeBASE and The Paleobiology Database. Results will be disseminated through the scientific press and at scientific meetings, and we will target both Earth and Life Science outlets. Major results will be communicated through the press office at all three partner institutions.
Schools and museum visitors are identified as the major wider beneficiaries, because our central question involves a key event in the history of life. The story of the earliest life on land is accessible to students and to the broader public, and it provides a compelling springboard for showing how scientists approach studying evolution as a process and its impact on the natural environment. Schools and public engagement are therefore a major focus of our Impact Plan. We will draw on expertise in science communication, facilities, and the current diverse programme plan in place at The Natural History Museum. We will be working directly with learning professionals who engage with policy makers on schools policy and UK government public engagement policy.
The Natural History Museum attracts some 150,000 school visitors each year, 25% of whom participate in formal activities. Under the guidance of professional science educators, we (Investigators, PDRAs) will contribute to curriculum linked activities already in place such as "How Science Works", "Science Focus", "A-level Biology Days", and the "Earth Science Fair" for science teachers and school children. PDRAs will participate in the Research Councils' "Researcher in Residence" school program to reinforce their science communication skills developed in the museum and to bring real working science into the classroom. School children will have the opportunity to contribute directly to our data by collecting plants in the UK, which will be used in molecular labwork.
Museum public and amateur naturalists will be engaged in several ways. We will communicate (onsite and remotely via webcam) through our "Nature Live" series presentations at The Natural History Museum and through our Angela Marmont Centre for UK Biodiversity, which plays a key role in supporting networks of societies and other partners working in the field of natural history across the UK.
Because of the subject matter and the multidisciplinary nature of the proposed research, our results will be of interest to a diverse scientific audience, including both Life Scientists (systematic botanists, molecular systematists, evolutionary and developmental biologists) and Earth Scientists (palaeobotanists, micropalaeontologists, sedimentary geologists, geochemists). The results, novel data and methods in our Time Tree project are relevant to the former, whereas the latter will be most interested in our analyses of the Rock Record. Both groups as well as (palaeo-)climatologists will be interested in the synthesis, which is concerned with how the geochemical carbon cycle is best calibrated in light of a revised time scale for key events in land plant evolution (e.g., rates of carbon sequestration, weathering of surface rocks, soil development). New datasets will be made publicly available via the TimeTree project, DRYAD, TreeBASE and The Paleobiology Database. Results will be disseminated through the scientific press and at scientific meetings, and we will target both Earth and Life Science outlets. Major results will be communicated through the press office at all three partner institutions.
Schools and museum visitors are identified as the major wider beneficiaries, because our central question involves a key event in the history of life. The story of the earliest life on land is accessible to students and to the broader public, and it provides a compelling springboard for showing how scientists approach studying evolution as a process and its impact on the natural environment. Schools and public engagement are therefore a major focus of our Impact Plan. We will draw on expertise in science communication, facilities, and the current diverse programme plan in place at The Natural History Museum. We will be working directly with learning professionals who engage with policy makers on schools policy and UK government public engagement policy.
The Natural History Museum attracts some 150,000 school visitors each year, 25% of whom participate in formal activities. Under the guidance of professional science educators, we (Investigators, PDRAs) will contribute to curriculum linked activities already in place such as "How Science Works", "Science Focus", "A-level Biology Days", and the "Earth Science Fair" for science teachers and school children. PDRAs will participate in the Research Councils' "Researcher in Residence" school program to reinforce their science communication skills developed in the museum and to bring real working science into the classroom. School children will have the opportunity to contribute directly to our data by collecting plants in the UK, which will be used in molecular labwork.
Museum public and amateur naturalists will be engaged in several ways. We will communicate (onsite and remotely via webcam) through our "Nature Live" series presentations at The Natural History Museum and through our Angela Marmont Centre for UK Biodiversity, which plays a key role in supporting networks of societies and other partners working in the field of natural history across the UK.
Organisations
Publications
Barba-Montoya J
(2018)
Constraining uncertainty in the timescale of angiosperm evolution and the veracity of a Cretaceous Terrestrial Revolution.
in The New phytologist
Betts HC
(2018)
Integrated genomic and fossil evidence illuminates life's early evolution and eukaryote origin.
in Nature ecology & evolution
Bowles A
(2024)
Cryogenian origins of multicellularity in Archaeplastida
in Genome Biology and Evolution
Bowles AMC
(2023)
The origin and early evolution of plants.
in Trends in plant science
Carlisle EM
(2021)
Experimental taphonomy of organelles and the fossil record of early eukaryote evolution.
in Science advances
Clark J
(2023)
Evolution of phenotypic disparity in the plant kingdom
in Nature Plants
Clark JW
(2018)
Whole-Genome Duplication and Plant Macroevolution.
in Trends in plant science
Clark JW
(2017)
Constraining the timing of whole genome duplication in plant evolutionary history.
in Proceedings. Biological sciences
Clark JW
(2023)
Constraining Whole-Genome Duplication Events in Geological Time.
in Methods in molecular biology (Clifton, N.J.)
Clark JW
(2019)
Origin of horsetails and the role of whole-genome duplication in plant macroevolution.
in Proceedings. Biological sciences
Davies TG
(2017)
Open data and digital morphology.
in Proceedings. Biological sciences
De Baets K
(2016)
Tectonic blocks and molecular clocks.
in Philosophical transactions of the Royal Society of London. Series B, Biological sciences
De Sousa F
(2019)
Nuclear protein phylogenies support the monophyly of the three bryophyte groups (Bryophyta Schimp.).
in The New phytologist
Donoghue P
(2019)
Evolution: The Flowering of Land Plant Evolution.
in Current biology : CB
Donoghue P
(2020)
Plant Evolution: Assembling Land Plants.
in Current biology : CB
Donoghue PC
(2016)
The evolution of methods for establishing evolutionary timescales.
in Philosophical transactions of the Royal Society of London. Series B, Biological sciences
Donoghue PCJ
(2021)
The evolutionary emergence of land plants.
in Current biology : CB
Donoghue PCJ
(2020)
Fossil cells.
in Current biology : CB
Donoghue PCJ
(2024)
Plant evolution: Streptophyte multicellularity, ecology, and the acclimatisation of plants to life on land.
in Current biology : CB
Donoghue Philip C. J.
(2020)
Fossil cells
in CURRENT BIOLOGY
Harris BJ
(2022)
Divergent evolutionary trajectories of bryophytes and tracheophytes from a complex common ancestor of land plants.
in Nature ecology & evolution
Harrison CJ
(2018)
The origin and early evolution of vascular plant shoots and leaves.
in Philosophical transactions of the Royal Society of London. Series B, Biological sciences
Marchadier E
(2016)
Evolution of the Calcium-Based Intracellular Signaling System.
in Genome biology and evolution
Morris JL
(2018)
The timescale of early land plant evolution.
in Proceedings of the National Academy of Sciences of the United States of America
Morris JL
(2018)
Reply to Hedges et al.: Accurate timetrees do indeed require accurate calibrations.
in Proceedings of the National Academy of Sciences of the United States of America
O'Reilly J
(2018)
Empirical realism of simulated data is more important than the model used to generate it: a reply to Goloboff et al .
in Palaeontology
O'Reilly JE
(2016)
Bayesian methods outperform parsimony but at the expense of precision in the estimation of phylogeny from discrete morphological data.
in Biology letters
O'Reilly JE
(2018)
Probabilistic methods surpass parsimony when assessing clade support in phylogenetic analyses of discrete morphological data.
in Palaeontology
O'Reilly JE
(2018)
The Efficacy of Consensus Tree Methods for Summarizing Phylogenetic Relationships from a Posterior Sample of Trees Estimated from Morphological Data.
in Systematic biology
O'Reilly JE
(2020)
The Effect of Fossil Sampling on the Estimation of Divergence Times with the Fossilized Birth-Death Process.
in Systematic biology
O'Reilly JE
(2016)
Tips and nodes are complementary not competing approaches to the calibration of molecular clocks.
in Biology letters
Puttick M
(2018)
Probabilistic methods outperform parsimony in the phylogenetic analysis of data simulated without a probabilistic model
in Palaeontology
Puttick MN
(2018)
The Interrelationships of Land Plants and the Nature of the Ancestral Embryophyte.
in Current biology : CB
Puttick MN
(2017)
Parsimony and maximum-likelihood phylogenetic analyses of morphology do not generally integrate uncertainty in inferring evolutionary history: a response to Brown et al.
in Proceedings. Biological sciences
Puttick MN
(2017)
Uncertain-tree: discriminating among competing approaches to the phylogenetic analysis of phenotype data.
in Proceedings. Biological sciences
Püschel H
(2019)
The impact of fossil stratigraphic ranges on tip-calibration, and the accuracy and precision of divergence time estimates
in Palaeontology
Silvestro D
(2021)
Fossil data support a pre-Cretaceous origin of flowering plants.
in Nature ecology & evolution
Silvestro D
(2021)
Unbiased clade age estimation using a Bayesian Brownian Bridge
Taylor RS
(2017)
MicroRNA annotation of plant genomes - Do it right or not at all.
in BioEssays : news and reviews in molecular, cellular and developmental biology
Warnock RCM
(2017)
Testing the molecular clock using mechanistic models of fossil preservation and molecular evolution.
in Proceedings. Biological sciences
Yang Z
(2016)
Dating species divergences using rocks and clocks.
in Philosophical transactions of the Royal Society of London. Series B, Biological sciences
| Description | We have resolved controversy over the fundamental evolutionary relationships among living land plants and calibrated their evolutionary to geological time. |
| Exploitation Route | Climate modellers can build on our timescale and phylogeny to better understand how the evolution of land plants transformed the planet |
| Sectors | Education |
| Title | Data from: Bayesian and likelihood phylogenetic reconstructions of morphological traits are not discordant when taking uncertainty into consideration: a comment on Puttick et al |
| Description | Puttick et al. (2017 Proc. R. Soc. B 284, 20162290 (doi:10.1098/rspb.2016.2290)) performed a simulation study to compare accuracy among methods of inferring phylogeny from discrete morphological characters. They report that a Bayesian implementation of the Mk model (Lewis 2001 Syst. Biol. 50, 913-925 (doi:10.1080/106351501753462876)) was most accurate (but with low resolution), while a maximum-likelihood (ML) implementation of the same model was least accurate. They conclude by strongly advocating that Bayesian implementations of the Mk model should be the default method of analysis for such data. While we appreciate the authors' attempt to investigate the accuracy of alternative methods of analysis, their conclusion is based on an inappropriate comparison of the ML point estimate, which does not consider confidence, with the Bayesian consensus, which incorporates estimation credibility into the summary tree. Using simulation, we demonstrate that ML and Bayesian estimates are concordant when confidence and credibility are comparably reflected in summary trees, a result expected from statistical theory. We therefore disagree with the conclusions of Puttick et al. and consider their prescription of any default method to be poorly founded. Instead, we recommend caution and thoughtful consideration of the model or method being applied to a morphological dataset. |
| Type Of Material | Database/Collection of data |
| Year Produced | 2017 |
| Provided To Others? | Yes |
| URL | https://datadryad.org/stash/dataset/doi:10.5061/dryad.dh0dv |
| Title | Data from: Bayesian methods outperform parsimony but at the expense of precision in the estimation of phylogeny from discrete morphological data |
| Description | Different analytical methods can yield competing interpretations of evolutionary history and, currently, there is no definitive method for phylogenetic reconstruction using morphological data. Parsimony has been the primary method for analysing morphological data, but there has been a resurgence of interest in the likelihood-based Mk-model. Here, we test the performance of the Bayesian implementation of the Mk-model relative to both equal and implied-weight implementations of parsimony. Using simulated morphological data, we demonstrate that the Mk-model outperforms equal-weights parsimony in terms of topological accuracy, and implied-weights performs the most poorly. However, the Mk-model produces phylogenies that have less resolution than parsimony methods. This difference in the accuracy and precision of parsimony and Bayesian approaches to topology estimation needs to be considered when selecting a method for phylogeny reconstruction. |
| Type Of Material | Database/Collection of data |
| Year Produced | 2016 |
| Provided To Others? | Yes |
| URL | https://datadryad.org/stash/dataset/doi:10.5061/dryad.10qf3 |
| Title | Data from: Bayesian methods outperform parsimony but at the expense of precision in the estimation of phylogeny from discrete morphological data |
| Description | Simulated data matrices from 'Bayesian methods outperform parsimony but at the expense of precision in the estimation of phylogeny from discrete morphological data' |
| Type Of Material | Database/Collection of data |
| Year Produced | 2016 |
| Provided To Others? | Yes |
| URL | http://datadryad.org/resource/doi:10.5061/dryad.10qf3/1 |
| Title | Data from: The efficacy of consensus tree methods for summarising phylogenetic relationships from a posterior sample of trees estimated from morphological data |
| Description | Consensus trees are required to summarise trees obtained through MCMC sampling of a posterior distribution, providing an overview of the distribution of estimated parameters such as topology, branch lengths and divergence times. Numerous consensus tree construction methods are available, each presenting a different interpretation of the tree sample. The rise of morphological clock and sampled-ancestor methods of divergence time estimation, in which times and topology are co-estimated, has increased the popularity of the maximum clade credibility (MCC) consensus tree method. The MCC method assumes that the sampled, fully resolved topology with the highest clade credibility contains an adequate summary of the most probable clades, with parameter estimates from compatible sampled trees used to obtain the marginal distributions of parameters such as clade ages and branch lengths. Using both simulated and empirical data, we demonstrate that MCC trees, and trees constructed using the similar maximum a posteriori (MAP) method, often include poorly supported and incorrect clades when summarising diffuse posterior samples of trees. We demonstrate that the paucity of information in morphological datasets contributes to the inability of MCC and MAP trees to present an accurate summary of the posterior distribution. Conversely, majority-rule consensus (MRC) trees report a lower proportion of incorrect nodes when summarising the same posterior samples of trees. Thus, we advocate the use of MRC trees, in place of MCC or MAP trees, in attempts to summarise the results of Bayesian phylogenetic analyses of morphological data. |
| Type Of Material | Database/Collection of data |
| Year Produced | 2017 |
| Provided To Others? | Yes |
| URL | https://datadryad.org/stash/dataset/doi:10.5061/dryad.66s9h |
| Title | Puttick_et_al_R_script from Uncertain-tree: discriminating among competing approaches to the phylogenetic analysis of phenotype data |
| Description | The R script used to generate the simulated data on which this analysis was based |
| Type Of Material | Database/Collection of data |
| Year Produced | 2016 |
| Provided To Others? | Yes |
| URL | https://rs.figshare.com/articles/dataset/Puttick_et_al_R_script_from_Uncertain-tree_discriminating_a... |
| Title | Puttick_et_al_R_script from Uncertain-tree: discriminating among competing approaches to the phylogenetic analysis of phenotype data |
| Description | The R script used to generate the simulated data on which this analysis was based |
| Type Of Material | Database/Collection of data |
| Year Produced | 2016 |
| Provided To Others? | Yes |
| URL | https://rs.figshare.com/articles/dataset/Puttick_et_al_R_script_from_Uncertain-tree_discriminating_a... |
| Description | Conference presentation |
| Form Of Engagement Activity | A talk or presentation |
| Part Of Official Scheme? | No |
| Geographic Reach | International |
| Primary Audience | Professional Practitioners |
| Results and Impact | Conference presentation |
| Year(s) Of Engagement Activity | 2017 |
| Description | Press release and associated interviews |
| Form Of Engagement Activity | A press release, press conference or response to a media enquiry/interview |
| Part Of Official Scheme? | No |
| Geographic Reach | International |
| Primary Audience | Media (as a channel to the public) |
| Results and Impact | Press releases associated with three consecutive papers and associated interviews |
| Year(s) Of Engagement Activity | 2018 |
| Description | Westbury on Trym C of E primary Academy |
| Form Of Engagement Activity | A talk or presentation |
| Part Of Official Scheme? | No |
| Geographic Reach | Local |
| Primary Audience | Schools |
| Results and Impact | Science Week school presentation |
| Year(s) Of Engagement Activity | 2017 |