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Polymorphisms in plastoquinol oxidase (PTOX) from Arabidopsis accessions indicate SNP-induced structural variants associated with altitude and rainfall

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Abstract

Plant plastoquinol oxidase (PTOX) is a chloroplast oxidoreductase involved in carotenoid biosynthesis, chlororespiration, and response to environmental stresses. The present study aimed to gain insight of the potential role of nucleotide/amino acid changes linked to environmental adaptation in PTOX gene/protein from Arabidopsis thaliana accessions. SNPs in the single-copy PTOX gene were identified in 1190 accessions of Arabidopsis using the Columbia-0 PTOX as a reference. The identified SNPs were correlated with geographical distribution of the accessions according to altitude, climate, and rainfall. Among the 32 identified SNPs in the coding region of the PTOX gene, 16 of these were characterized as non-synonymous SNPs (in which an AA is altered). A higher incidence of AA changes occurred in the mature protein at positions 78 (31%), 81 (31.4%), and 323 (49.9%). Three-dimensional structure prediction indicated that the AA change at position 323 (D323N) leads to a PTOX structure with the most favorable interaction with the substrate plastoquinol, when compared with the reference PTOX structure (Columbia-0). Molecular docking analysis suggested that the most favorable D323N PTOX-plastoquinol interaction is due to a better enzyme-substrate binding affinity. The molecular dynamics revealed that plastoquinol should be more stable in complex with D323N PTOX, likely due a restraint mechanism in this structure that stabilize plastoquinol inside of the reaction center. The integrated analysis made from accession geographical distribution and PTOX SNPs indicated that AA changes in PTOX are related to altitude and rainfall, potentially due to an adaptive positive environmental selection.

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Acknowledgements

We are grateful to the Weigel laboratory at the Max Planck Institute for Developmental Biology (http://www.weigelworld.org) for providing us with the genomic data that made advancements in the present research possible. The Brazilian authors would also like to thank CAPES (Coordination for the Improvement of Higher Education Personnel), CNPq (National Council of Technological and Scientific Development), and FUNCAP (Ceara Research Support Foundation) for financial support. BAS is thankful to the University of Évora for continuous invitations as a Coordinating Investigator since 2008 to prolong the running of the established EU Marie Curie Chair, financed initially by the European Commission from 2005 to 2008. We also thank Dr. Daniel Ferreira Feijó for his helpful suggestions in reviewing the final article.

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  1. Functional Genomics and Bioinformatics, Department of Biochemistry and Molecular Biology, Federal University of Ceara, Ceara, Fortaleza, 60451-970, Brazil

    Karine Leitão Lima Thiers, Clesivan Pereira dos Santos, Kátia Daniella da Cruz Saraiva, André Luiz Maia Roque, Birgit Arnholdt-Schmitt & José Hélio Costa

  2. Computational Modeling Group – FIOCRUZ – CE, Fortaleza, Brazil

    João Hermínio Martins da Silva & Geraldo Rodrigues Sartori

  3. Federal Institute of Education, Science and Technology, Paraíba, Brazil

    Kátia Daniella da Cruz Saraiva

  4. Functional Cell Reprogramming and Organism Plasticity (FunCrop), EU Marie Curie Chair, ICAAM, University of Évora, Apartado 94, 7002-554, Évora, Portugal

    Birgit Arnholdt-Schmitt

  5. Science and Technology Park Alentejo (PACT), 7005-841, Évora, Portugal

    Birgit Arnholdt-Schmitt

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Thiers, K.L.L., da Silva, J.H.M., Sartori, G.R. et al. Polymorphisms in plastoquinol oxidase (PTOX) from Arabidopsis accessions indicate SNP-induced structural variants associated with altitude and rainfall. J Bioenerg Biomembr 51, 151–164 (2019). https://doi.org/10.1007/s10863-018-9784-6

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