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A small family of LLS1-related non-heme oxygenases in plants with an origin amongst oxygenic photosynthesizers

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Abstract

Conservation of Lethal-leaf spot 1 (Lls1) lesion mimic gene in land plants including moss is consistent with its recently reported function as pheophorbide a oxygenase (Pao) which catalyzes a key step in chlorophyll degradation (Pruzinska et al., 2003). A bioinformatics survey of complete plant genomes reveals that LLS1(PAO) belongs to a small 5-member family of non-heme oxygenases defined by the presence of Rieske and mononuclear iron-binding domains. This gene family includes chlorophyll a oxygenase (Cao), choline monooxygenase (Cmo), the gene for a 55 kDa protein associated with protein transport through the inner chloroplast membrane (Tic55) and a novel 52 kDa protein isolated from chloroplasts (Ptc52). Analysis of gene structure reveals that these genes diverged prior to monocot/dicot divergence. Homologues of LLS1(PAO), CAO, TIC55 and PTC52 but not CMO are found in the genomes of several cyanobacteria. LLS1(PAO), PTC52, TIC55 and a set of related cyanobacterial homologues share an extended carboxyl terminus containing a novel F/Y/W-x2-H-x3-C-x2-C motif not present in CAO. These proteins appear to have evolved during the transition to oxygenic photosynthesis to play various roles in chlorophyll metabolism. In contrast, CMO homologues are found only in plants and are most closely related to aromatic ring-hydroxylating enzymes from soil-dwelling bacteria, suggesting a more recent evolution of this enzyme, possibly by horizontal gene transfer. Our phylogenetic analysis of 95 extant non-heme dioxygenases provides a useful framework for the classification of LLS1(PAO)-related non-heme oxygenases.

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Authors and Affiliations

  1. Department of Biological Sciences, University of Toledo, 2801 West Bancroft Street, Toledo, OH, 43606, USA

    John Gray, Ellen Wardzala, Manli Yang & Steve Haller

  2. Laboratoire de Génétique Moléculaire des Plantes, Université Joseph Fourier et CNRS, CERMO, BP 53, 38041, Grenoble, France

    Steffen Reinbothe

  3. Department of Genetics, School of Medicine, Stanford University, Stanford, CA, 94305, USA

    Florencia Pauli

Authors
  1. John Gray
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  2. Ellen Wardzala
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  4. Steffen Reinbothe
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  5. Steve Haller
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  6. Florencia Pauli
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Correspondence to John Gray.

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Gray, J., Wardzala, E., Yang, M. et al. A small family of LLS1-related non-heme oxygenases in plants with an origin amongst oxygenic photosynthesizers. Plant Mol Biol 54, 39–54 (2004). https://doi.org/10.1023/B:PLAN.0000028766.61559.4c

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  • DOI: https://doi.org/10.1023/B:PLAN.0000028766.61559.4c

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