Dr Steve Kelly

Research Interests

Photosynthesis, Evolution, Gene expression, Bioinformatics

Photosynthesis is the primary energy source for life on earth. While the biochemistry and cell biology of photosynthesis are well understood, little is known of how the genes that mediate photosynthesis are regulated. Our research aims to address this knowledge gap by identifying the molecular regulators and mechanisms that control the expression of photosynthesis genes in the world’s most important food crops, the grasses. This work combines comparative genomics, evolutionary biology, high-throughput assays and genetic engineering.

For up-to-date details on research interests and publications please see the lab website.

If you are interested in joining our group please get in touch by email including your CV and a short paragraph outlining the project area that you are interested in.

Publications

  • Gene Duplication Accelerates the Pace of Protein Gain and Loss from Plant Organelles.

    2020
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    Journal article
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    Molecular biology and evolution
    Organelle biogenesis and function is dependent on the concerted action of both organellar-encoded (if present) and nuclear-encoded proteins. Differences between homologous organelles across the Plant Kingdom arise, in part, as a result of differences in the cohort of nuclear-encoded proteins that are targeted to them. However, neither the rate at which differences in protein targeting accumulate nor the evolutionary consequences of these changes are known. Using phylogenomic approaches coupled to ancestral state estimation, we show that the plant organellar proteome has diversified in proportion with molecular sequence evolution such that the proteomes of plant chloroplasts and mitochondria lose or gain on average 3.6 proteins per million years. We further demonstrate that changes in organellar protein targeting are associated with an increase in the rate of molecular sequence evolution and that such changes predominantly occur in genes with regulatory rather than metabolic functions. Finally, we show that gain and loss of protein target signals occurs at a higher rate following gene duplication, revealing that gene and genome duplication are a key facilitator of plant organelle evolution.

  • Subdivision of Light Signaling Networks Contributes to Partitioning of C4 Photosynthesis.

    2020
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    Journal article
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    Plant physiology
    Plants coordinate the expression of photosynthesis-related genes in response to growth and environmental changes. In species that conduct two-cell C4 photosynthesis, expression of photosynthesis genes is partitioned such that leaf mesophyll and bundle sheath cells accumulate different components of the photosynthetic pathway. The identities of the regulatory networks that facilitate this partitioning are unknown. Here, we show that differences in light perception between mesophyll and bundle sheath cells facilitate differential regulation and accumulation of photosynthesis gene transcripts in the C4 crop maize (Zea mays). Key components of the photosynthesis gene regulatory network differentially accumulated between mesophyll and bundle sheath cells, indicative of differential network activity across cell types. We further show that blue (but not red) light is necessary and sufficient to activate photosystem II assembly in mesophyll cells in etiolated maize. Finally, we demonstrate that 61% of all light-induced mesophyll and bundle sheath genes were induced only by blue light or only by red light, but not both. These findings provide evidence that subdivision of light signaling networks is a component of cellular partitioning of C4 photosynthesis in maize.

  • Metabolic quirks and the colourful history of the Euglena gracilis secondary plastid.

    2020
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    Journal article
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    New Phytol
    Euglena spp. are phototrophic flagellates with considerable ecological presence and impact. Euglena gracilis harbours secondary green plastids, but an incompletely characterised proteome precludes accurate understanding of both plastid function and evolutionary history. Using subcellular fractionation, an improved sequence database and MS we determined the composition, evolutionary relationships and hence predicted functions of the E. gracilis plastid proteome. We confidently identified 1345 distinct plastid protein groups and found that at least 100 proteins represent horizontal acquisitions from organisms other than green algae or prokaryotes. Metabolic reconstruction confirmed previously studied/predicted enzymes/pathways and provided evidence for multiple unusual features, including uncoupling of carotenoid and phytol metabolism, a limited role in amino acid metabolism, and dual sets of the SUF pathway for FeS cluster assembly, one of which was acquired by lateral gene transfer from Chlamydiae. Plastid paralogues of trafficking-associated proteins potentially mediating fusion of transport vesicles with the outermost plastid membrane were identified, together with derlin-related proteins, potential translocases across the middle membrane, and an extremely simplified TIC complex. The Euglena plastid, as the product of many genomes, combines novel and conserved features of metabolism and transport.
    Euglena gracilis , SUF pathway, lateral gene transfer, metabolic reconstruction, plastid, protein import, proteome, shopping bag hypothesis

  • Gene expression data support the hypothesis that Isoetes rootlets are true roots and not modified leaves

    2019
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    Journal article
    <jats:title>Abstract</jats:title><jats:p>Rhizomorphic lycopsids are the land plant group that includes the first giant trees to grow on Earth and extant species in the genus <jats:italic>Isoetes</jats:italic>. Two mutually exclusive hypotheses account for the evolution of terminal rooting axes called rootlets among the rhizomorphic lycopsids. One hypothesis states that rootlets are true roots, like roots in other lycopsids. The other states that rootlets are modified leaves. Here we test predictions of each hypothesis by investigating gene expression in the leaves and rootlets of <jats:italic>Isoetes echinospora</jats:italic>. We assembled the <jats:italic>de-novo</jats:italic> transcriptome of axenically cultured <jats:italic>I. echinospora</jats:italic>. Gene expression signatures of <jats:italic>I. echinospora</jats:italic> rootlets and leaves were different. Furthermore, gene expression signatures of <jats:italic>I. echinospora</jats:italic> rootlets were similar to gene expression signatures of true roots of <jats:italic>Selaginella moellendorffii</jats:italic> and <jats:italic>Arabidopsis thaliana</jats:italic>. RSL genes which positively regulate cell differentiation in roots were either exclusively or preferentially expressed in the <jats:italic>I. echinospora</jats:italic> rootlets, S. <jats:italic>moellendorffii</jats:italic> roots and <jats:italic>A. thaliana</jats:italic> roots compared to the leaves of each respective species. Taken together, gene expression data from the <jats:italic>de-novo</jats:italic> transcriptome of <jats:italic>I. echinospora</jats:italic> are consistent with the hypothesis that <jats:italic>Isoetes</jats:italic> rootlets are true roots and not modified leaves.</jats:p>

  • OrthoFinder: phylogenetic orthology inference for comparative genomics.

    2019
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    Journal article
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    Genome biology
    Here, we present a major advance of the OrthoFinder method. This extends OrthoFinder's high accuracy orthogroup inference to provide phylogenetic inference of orthologs, rooted gene trees, gene duplication events, the rooted species tree, and comparative genomics statistics. Each output is benchmarked on appropriate real or simulated datasets, and where comparable methods exist, OrthoFinder is equivalent to or outperforms these methods. Furthermore, OrthoFinder is the most accurate ortholog inference method on the Quest for Orthologs benchmark test. Finally, OrthoFinder's comprehensive phylogenetic analysis is achieved with equivalent speed and scalability to the fastest, score-based heuristic methods. OrthoFinder is available at https://github.com/davidemms/OrthoFinder.
    Animals, Genomics, Phylogeny, Algorithms, Software

  • A taxonomic monograph of Ipomoea integrated across phylogenetic scales.

    2019
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    Journal article
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    Nature plants
    Taxonomic monographs have the potential to make a unique contribution to the understanding of global biodiversity. However, such studies, now rare, are often considered too daunting to undertake within a realistic time frame, especially as the world's collections have doubled in size in recent times. Here, we report a global-scale monographic study of morning glories (Ipomoea) that integrated DNA barcodes and high-throughput sequencing with the morphological study of herbarium specimens. Our approach overhauled the taxonomy of this megadiverse group, described 63 new species and uncovered significant increases in net diversification rates comparable to the most iconic evolutionary radiations in the plant kingdom. Finally, we show that more than 60 species of Ipomoea, including sweet potato, independently evolved storage roots in pre-human times, indicating that the storage root is not solely a product of human domestication but a trait that predisposed the species for cultivation. This study demonstrates how the world's natural history collections can contribute to global challenges in the Anthropocene.
    Ipomoea, DNA, Plant, Sequence Analysis, DNA, Evolution, Molecular, Phylogeny, Biological Specimen Banks, DNA Barcoding, Taxonomic, Phylogeography

  • Neofunctionalisation of basic helix-loop-helix proteins occurred when embryophytes colonised the land.

    2019
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    Journal article
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    New Phytol
    ROOT HAIR DEFECTIVE SIX-LIKE (RSL) genes control the development of structures from single cells at the surface of embryophytes (land plants) such as rhizoids and root hairs. RSL proteins constitute a subclass (VIIIc) of the basic helix-loop-helix (bHLH) class VIII transcription factor family. The Charophyceae form the only class of streptophyte algae with tissue-like structures and rhizoids. To determine if the function of RSL genes in the control of cell differentiation in embryophytes was inherited from a streptophyte algal ancestor, we identified the single class VIII bHLH gene from the charophyceaen alga Chara braunii (CbbHLHVIII). CbbHLHVIII is sister to the RSL proteins; they constitute a monophyletic group. Expression of CbbHLHVIII does not compensate for loss of RSL functions in Marchantia polymorpha or Arabidopsis thaliana. In C. braunii CbbHLHVIII is expressed at sites of morphogenesis but not in rhizoids. This finding indicates that C. braunii class VIII protein is functionally different from land plant RSL proteins. This result suggests that the function of RSL proteins in cell differentiation at the plant surface evolved by neofunctionalisation in the land plants lineage after its divergence from its last common ancestor with C. braunii, at or before the colonisation of the land by embryophytes.
    Chara braunii , Coleochate nitellarum , ROOT HAIR DEFECTIVE SIX-LIKE (RSL), basic helix−loop−helix (bHLH), filamentous rooting cells, land plants, neofunctionalisation, streptophyte algae, Amino Acid Motifs, Amino Acid Sequence, Arabidopsis, Basic Helix-Loop-Helix Transcription Factors, Conserved Sequence, Embryophyta, Gene Expression Regulation, Plant, Genome, Plant, Mutation, Phylogeny, Plant Proteins, Plant Roots, RNA, Messenger, Transcriptome

  • Transcriptome, proteome and draft genome of Euglena gracilis.

    2019
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    Journal article
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    BMC biology
    BACKGROUND:Photosynthetic euglenids are major contributors to fresh water ecosystems. Euglena gracilis in particular has noted metabolic flexibility, reflected by an ability to thrive in a range of harsh environments. E. gracilis has been a popular model organism and of considerable biotechnological interest, but the absence of a gene catalogue has hampered both basic research and translational efforts. RESULTS:We report a detailed transcriptome and partial genome for E. gracilis Z1. The nuclear genome is estimated to be around 500 Mb in size, and the transcriptome encodes over 36,000 proteins and the genome possesses less than 1% coding sequence. Annotation of coding sequences indicates a highly sophisticated endomembrane system, RNA processing mechanisms and nuclear genome contributions from several photosynthetic lineages. Multiple gene families, including likely signal transduction components, have been massively expanded. Alterations in protein abundance are controlled post-transcriptionally between light and dark conditions, surprisingly similar to trypanosomatids. CONCLUSIONS:Our data provide evidence that a range of photosynthetic eukaryotes contributed to the Euglena nuclear genome, evidence in support of the 'shopping bag' hypothesis for plastid acquisition. We also suggest that euglenids possess unique regulatory mechanisms for achieving extreme adaptability, through mechanisms of paralog expansion and gene acquisition.
    Cell Nucleus, Plastids, Euglena gracilis, Proteome, Genome, Transcriptome
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Graduate Students
Contact Details
E: steven.kelly@plants.ox.ac.uk
 

+44 (0) 1865 275123
  Lab website