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Title: Co-locality to co-functionality: Eukaryotic gene neighborhoods as a resource for function

Abstract

Diverging from the classic paradigm of random gene order in eukaryotes, gene proximity can be leveraged to systematically identify functionally related gene neighborhoods in eukaryotes, utilizing techniques pioneered in bacteria. Current methods of identifying gene neighborhoods typically rely on sequence similarity to characterized gene products. However, this approach is not robust for non model organisms like algae, which are evolutionarily distant from well-characterized model organisms. Here, we utilize a comparative genomic approach to identify evolutionarily conserved Proximal Orthologous Gene (POG) pairs conserved across at least two taxonomic classes of green algae. A total of 317 gene neighborhoods were identified. In some cases, gene proximity appears to have been conserved since before the streptophyte-chlorophyte split, 1,000 million years ago. Using functional inferences derived from reconstructed evolutionary relationships, we identified several novel functional clusters. A putative mycosporine-like amino acid (MAA), "sunscreen", neighborhood contains genes similar to either vertebrate or cyanobacterial pathways, suggesting a novel mosaic biosynthetic pathway in green algae. One of two putative arsenic-detoxification neighborhoods includes an organoarsenical transporter (ArsJ), a glyceraldehyde 3-phosphate dehydrogenase-like gene, homologs of which are involved in arsenic detoxification in bacteria, and a novel algal-specific phosphoglycerate kinase-like gene (PGK). Mutants of the ArsJ-like transporter and PGK-like genesmore » in Chlamydomonas reinhardtii were found to be sensitive to arsenate, providing experimental support for the role of these identified neighbors in resistance to arsenate. Potential evolutionary origins of neighborhoods are discussed, and updated annotations for formerly poorly annotated genes are presented, highlighting the potential of this strategy for functional annotation.« less

Authors:
 [1]; ORCiD logo [1]
  1. Brookhaven National Lab. (BNL), Upton, NY (United States)
Publication Date:
Research Org.:
Brookhaven National Lab. (BNL), Upton, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1659687
Report Number(s):
BNL-216351-2020-JAAM
Journal ID: ISSN 0737-4038
Grant/Contract Number:  
SC0012704
Resource Type:
Accepted Manuscript
Journal Name:
Molecular Biology and Evolution
Additional Journal Information:
Journal Name: Molecular Biology and Evolution; Journal ID: ISSN 0737-4038
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Foflonker, Fatima, and Blaby-Haas, Crysten E. Co-locality to co-functionality: Eukaryotic gene neighborhoods as a resource for function. United States: N. p., 2020. Web. https://doi.org/10.1093/molbev/msaa221.
Foflonker, Fatima, & Blaby-Haas, Crysten E. Co-locality to co-functionality: Eukaryotic gene neighborhoods as a resource for function. United States. https://doi.org/10.1093/molbev/msaa221
Foflonker, Fatima, and Blaby-Haas, Crysten E. Fri . "Co-locality to co-functionality: Eukaryotic gene neighborhoods as a resource for function". United States. https://doi.org/10.1093/molbev/msaa221. https://www.osti.gov/servlets/purl/1659687.
@article{osti_1659687,
title = {Co-locality to co-functionality: Eukaryotic gene neighborhoods as a resource for function},
author = {Foflonker, Fatima and Blaby-Haas, Crysten E.},
abstractNote = {Diverging from the classic paradigm of random gene order in eukaryotes, gene proximity can be leveraged to systematically identify functionally related gene neighborhoods in eukaryotes, utilizing techniques pioneered in bacteria. Current methods of identifying gene neighborhoods typically rely on sequence similarity to characterized gene products. However, this approach is not robust for non model organisms like algae, which are evolutionarily distant from well-characterized model organisms. Here, we utilize a comparative genomic approach to identify evolutionarily conserved Proximal Orthologous Gene (POG) pairs conserved across at least two taxonomic classes of green algae. A total of 317 gene neighborhoods were identified. In some cases, gene proximity appears to have been conserved since before the streptophyte-chlorophyte split, 1,000 million years ago. Using functional inferences derived from reconstructed evolutionary relationships, we identified several novel functional clusters. A putative mycosporine-like amino acid (MAA), "sunscreen", neighborhood contains genes similar to either vertebrate or cyanobacterial pathways, suggesting a novel mosaic biosynthetic pathway in green algae. One of two putative arsenic-detoxification neighborhoods includes an organoarsenical transporter (ArsJ), a glyceraldehyde 3-phosphate dehydrogenase-like gene, homologs of which are involved in arsenic detoxification in bacteria, and a novel algal-specific phosphoglycerate kinase-like gene (PGK). Mutants of the ArsJ-like transporter and PGK-like genes in Chlamydomonas reinhardtii were found to be sensitive to arsenate, providing experimental support for the role of these identified neighbors in resistance to arsenate. Potential evolutionary origins of neighborhoods are discussed, and updated annotations for formerly poorly annotated genes are presented, highlighting the potential of this strategy for functional annotation.},
doi = {10.1093/molbev/msaa221},
journal = {Molecular Biology and Evolution},
number = ,
volume = ,
place = {United States},
year = {2020},
month = {9}
}

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