Differential expression of recently duplicated PTOX genes in Glycine max during plant development and stress conditions

  • Rachel Alves Maia
  • Kátia Daniella da Cruz Saraiva
  • André Luiz Maia Roque
  • Karine Leitão Lima Thiers
  • Clesivan Pereira dos Santos
  • João Hermínio Martins da Silva
  • Daniel Ferreira Feijó
  • Birgit Arnholdt-Schmitt
  • José Hélio CostaEmail author


Plastid terminal oxidase (PTOX) is a chloroplast enzyme that catalyzes oxidation of plastoquinol (PQH2) and reduction of molecular oxygen to water. Its function has been associated with carotenoid biosynthesis, chlororespiration and environmental stress responses in plants. In the majority of plant species, a single gene encodes the protein and little is known about events of PTOX gene duplication and their implication to plant metabolism. Previously, two putative PTOX (PTOX1 and 2) genes were identified in Glycine max, but the evolutionary origin and the specific function of each gene was not explored. Phylogenetic analyses revealed that this gene duplication occurred apparently during speciation involving the Glycine genus ancestor, an event absent in all other available plant leguminous genomes. Gene expression evaluated by RT-qPCR and RNA-seq data revealed that both PTOX genes are ubiquitously expressed in G. max tissues, but their mRNA levels varied during development and stress conditions. In development, PTOX1 was predominant in young tissues, while PTOX2 was more expressed in aged tissues. Under stress conditions, the PTOX transcripts varied according to stress severity, i.e., PTOX1 mRNA was prevalent under mild or moderate stresses while PTOX2 was predominant in drastic stresses. Despite the high identity between proteins (97%), molecular docking revealed that PTOX1 has higher affinity to substrate plastoquinol than PTOX2. Overall, our results indicate a functional relevance of this gene duplication in G. max metabolism, whereas PTOX1 could be associated with chloroplast effectiveness and PTOX2 to senescence and/or apoptosis.


Docking Gene duplication Gene expression PTOX Soybean 



The authors gratefully thank the National Council for Scientific and Technological Development for financial support (CNPq, grant 455327/2014-9). Maia RA, Thiers KLL and Santos CP were supported by master and doctoral grants from CNPq. Roque ALM and Feijó DF were supported by master and post-doctoral grants from Council for Advanced Professional Training (CAPES), respectively. Costa JH received support from CNPq through Researcher fellowship (CNPq grant 309795/2017-6).

Author contribution statement

Maia RA and Saraiva KDC conducted the RT- qPCR experiments, Maia RA, Roque ALM, Feijó DF and Santos CP interpreted the experimental and in silico data, Thiers KLL and Silva JHM realized the molecular docking. Maia RA, Costa JH, Feijó DF and Arnholdt-Schmitt B designed the study and wrote the manuscript (with input from all authors). All authors read and approved the final version of the paper.

Compliance with ethical standards

Conflict of interests

The authors declare that have no conflict of interest.

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Rachel Alves Maia
    • 1
  • Kátia Daniella da Cruz Saraiva
    • 1
    • 2
  • André Luiz Maia Roque
    • 1
  • Karine Leitão Lima Thiers
    • 1
  • Clesivan Pereira dos Santos
    • 1
  • João Hermínio Martins da Silva
    • 3
  • Daniel Ferreira Feijó
    • 1
  • Birgit Arnholdt-Schmitt
    • 1
    • 4
    • 5
  • José Hélio Costa
    • 1
    • 4
    Email author
  1. 1.Functional Genomics and Bioinformatics, Department of Biochemistry and Molecular BiologyFederal University of CearáFortalezaBrazil
  2. 2.Federal Institute of Education, Science and Technology of Paraíba - IFPB, Campus Princesa IsabelPrincesa IsabelBrazil
  3. 3.Computational Modeling Group – FIOCRUZ – CEFortalezaBrazil
  4. 4.Functional Cell Reprogramming and Organism Plasticity (FunCrop – virtual network), EU Marie Curie Chair, ICAAMUniversity of ÉvoraÉvoraPortugal
  5. 5.Science and Technology Park Alentejo (PACT)ÉvoraPortugal

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