Stem Region of tRNA Genes Favors Transition Substitution Towards Keto Bases in Bacteria

Piyali Sen; Ruksana Aziz; Ramesh C. Deka; Edward J. Feil; Suvendra Kumar Ray; Siddhartha Sankar Satapathy

doi:10.1007/s00239-021-10045-x

Stem Region of tRNA Genes Favors Transition Substitution Towards Keto Bases in Bacteria

Piyali Sen, Ruksana Aziz, Ramesh C. Deka, Edward J. Feil, Suvendra Kumar Ray, Siddhartha Sankar Satapathy

Research output: Contribution to journal › Article › peer-review

Abstract

Transversion and transition mutations have variable effects on the stability of RNA secondary structure considering that the former destabilizes the double helix geometry to a greater extent by introducing purine:purine (R:R) or pyrimidine:pyrimidine (Y:Y) base pairs. Therefore, transversion frequency is likely to be lower than that of transition in the secondary structure regions of RNA genes. Here, we performed an analysis of transition and transversion frequencies in tRNA genes defined well with secondary structure and compared with the intergenic regions in five bacterial species namely Escherichia coli, Klebsiella pneumoniae, Salmonella enterica, Staphylococcus aureus and Streptococcus pneumoniae using a large genome sequence data set. In general, the transversion frequency was observed to be lower than that of transition in both tRNA genes and intergenic regions. The transition to transversion ratio was observed to be greater in tRNA genes than that in the intergenic regions in all the five bacteria that we studied. Interestingly, the intraspecies base substitution analysis in tRNA genes revealed that non-compensatory substitutions were more frequent than compensatory substitutions in the stem region. Further, transition to transversion ratio in the loop region was observed to be significantly lesser than that among the non-compensatory substitutions in the stem region. This indicated that the transversion is more deleterious than transition in the stem regions. In addition, substitutions from amino bases (A/C) to keto bases (G/T) were also observed to be more than the reverse substitutions in the stem region. Substitution from amino bases to keto bases are likely to facilitate the stable G:U pairing unlike the reverse substitution that facilitates the unstable A:C pairing in the stem region of tRNA. This work provides additional support that the secondary structure of tRNA molecule is what drives the different substitutions in its gene sequence.

Original language	English
Pages (from-to)	114-123
Number of pages	10
Journal	Journal of Molecular Evolution
Volume	90
Issue number	1
Early online date	27 Jan 2022
DOIs	https://doi.org/10.1007/s00239-021-10045-x
Publication status	Published - 28 Feb 2022

Keywords

Base substitution
Intergenic region
Transition
Transversion
tRNA secondary structure

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Molecular Biology
Genetics

Access to Document

10.1007/s00239-021-10045-x

Cite this

@article{6099f7c99bb244dfa9174e845d15b565,

title = "Stem Region of tRNA Genes Favors Transition Substitution Towards Keto Bases in Bacteria",

abstract = "Transversion and transition mutations have variable effects on the stability of RNA secondary structure considering that the former destabilizes the double helix geometry to a greater extent by introducing purine:purine (R:R) or pyrimidine:pyrimidine (Y:Y) base pairs. Therefore, transversion frequency is likely to be lower than that of transition in the secondary structure regions of RNA genes. Here, we performed an analysis of transition and transversion frequencies in tRNA genes defined well with secondary structure and compared with the intergenic regions in five bacterial species namely Escherichia coli, Klebsiella pneumoniae, Salmonella enterica, Staphylococcus aureus and Streptococcus pneumoniae using a large genome sequence data set. In general, the transversion frequency was observed to be lower than that of transition in both tRNA genes and intergenic regions. The transition to transversion ratio was observed to be greater in tRNA genes than that in the intergenic regions in all the five bacteria that we studied. Interestingly, the intraspecies base substitution analysis in tRNA genes revealed that non-compensatory substitutions were more frequent than compensatory substitutions in the stem region. Further, transition to transversion ratio in the loop region was observed to be significantly lesser than that among the non-compensatory substitutions in the stem region. This indicated that the transversion is more deleterious than transition in the stem regions. In addition, substitutions from amino bases (A/C) to keto bases (G/T) were also observed to be more than the reverse substitutions in the stem region. Substitution from amino bases to keto bases are likely to facilitate the stable G:U pairing unlike the reverse substitution that facilitates the unstable A:C pairing in the stem region of tRNA. This work provides additional support that the secondary structure of tRNA molecule is what drives the different substitutions in its gene sequence.",

keywords = "Base substitution, Intergenic region, Transition, Transversion, tRNA secondary structure",

author = "Piyali Sen and Ruksana Aziz and Deka, {Ramesh C.} and Feil, {Edward J.} and Ray, {Suvendra Kumar} and Satapathy, {Siddhartha Sankar}",

note = "Funding Information: We are highly grateful to anonymous reviewers and Prof. Paul Higgs for their kind suggestions that improved the quality of the manuscript significantly. We thank Dr. Harry Thrope for providing the sequence data. PS is thankful to UGC, GoI New Delhi for the JRF. SSS and SKR are thankful to DBT, GoI for the twinning Grant (BT/PR16361/NER/95/192/2015 date 18-10-2016) to them. SKR and RCD are thankful to DBT, GoI for the twinning Grant BT/PR16182/NER/95/92/2015. SSS is thankful to DBT for the NE Overseas Associateship, which helped him to work in University of Bath. EF, SSS, RCD and SKR are thankful to the society for Molecular Biology and Evolution (SMBE) for holding the satellite meeting at Kaziranga, Assam, India on Dec 14th?6th, 2017, which helped the authors to have collaboration on this work. ",

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doi = "10.1007/s00239-021-10045-x",

language = "English",

volume = "90",

pages = "114--123",

journal = "Journal of Molecular Evolution",

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T1 - Stem Region of tRNA Genes Favors Transition Substitution Towards Keto Bases in Bacteria

AU - Sen, Piyali

AU - Aziz, Ruksana

AU - Deka, Ramesh C.

AU - Feil, Edward J.

AU - Ray, Suvendra Kumar

AU - Satapathy, Siddhartha Sankar

N1 - Funding Information: We are highly grateful to anonymous reviewers and Prof. Paul Higgs for their kind suggestions that improved the quality of the manuscript significantly. We thank Dr. Harry Thrope for providing the sequence data. PS is thankful to UGC, GoI New Delhi for the JRF. SSS and SKR are thankful to DBT, GoI for the twinning Grant (BT/PR16361/NER/95/192/2015 date 18-10-2016) to them. SKR and RCD are thankful to DBT, GoI for the twinning Grant BT/PR16182/NER/95/92/2015. SSS is thankful to DBT for the NE Overseas Associateship, which helped him to work in University of Bath. EF, SSS, RCD and SKR are thankful to the society for Molecular Biology and Evolution (SMBE) for holding the satellite meeting at Kaziranga, Assam, India on Dec 14th?6th, 2017, which helped the authors to have collaboration on this work.

PY - 2022/2/28

Y1 - 2022/2/28

N2 - Transversion and transition mutations have variable effects on the stability of RNA secondary structure considering that the former destabilizes the double helix geometry to a greater extent by introducing purine:purine (R:R) or pyrimidine:pyrimidine (Y:Y) base pairs. Therefore, transversion frequency is likely to be lower than that of transition in the secondary structure regions of RNA genes. Here, we performed an analysis of transition and transversion frequencies in tRNA genes defined well with secondary structure and compared with the intergenic regions in five bacterial species namely Escherichia coli, Klebsiella pneumoniae, Salmonella enterica, Staphylococcus aureus and Streptococcus pneumoniae using a large genome sequence data set. In general, the transversion frequency was observed to be lower than that of transition in both tRNA genes and intergenic regions. The transition to transversion ratio was observed to be greater in tRNA genes than that in the intergenic regions in all the five bacteria that we studied. Interestingly, the intraspecies base substitution analysis in tRNA genes revealed that non-compensatory substitutions were more frequent than compensatory substitutions in the stem region. Further, transition to transversion ratio in the loop region was observed to be significantly lesser than that among the non-compensatory substitutions in the stem region. This indicated that the transversion is more deleterious than transition in the stem regions. In addition, substitutions from amino bases (A/C) to keto bases (G/T) were also observed to be more than the reverse substitutions in the stem region. Substitution from amino bases to keto bases are likely to facilitate the stable G:U pairing unlike the reverse substitution that facilitates the unstable A:C pairing in the stem region of tRNA. This work provides additional support that the secondary structure of tRNA molecule is what drives the different substitutions in its gene sequence.

AB - Transversion and transition mutations have variable effects on the stability of RNA secondary structure considering that the former destabilizes the double helix geometry to a greater extent by introducing purine:purine (R:R) or pyrimidine:pyrimidine (Y:Y) base pairs. Therefore, transversion frequency is likely to be lower than that of transition in the secondary structure regions of RNA genes. Here, we performed an analysis of transition and transversion frequencies in tRNA genes defined well with secondary structure and compared with the intergenic regions in five bacterial species namely Escherichia coli, Klebsiella pneumoniae, Salmonella enterica, Staphylococcus aureus and Streptococcus pneumoniae using a large genome sequence data set. In general, the transversion frequency was observed to be lower than that of transition in both tRNA genes and intergenic regions. The transition to transversion ratio was observed to be greater in tRNA genes than that in the intergenic regions in all the five bacteria that we studied. Interestingly, the intraspecies base substitution analysis in tRNA genes revealed that non-compensatory substitutions were more frequent than compensatory substitutions in the stem region. Further, transition to transversion ratio in the loop region was observed to be significantly lesser than that among the non-compensatory substitutions in the stem region. This indicated that the transversion is more deleterious than transition in the stem regions. In addition, substitutions from amino bases (A/C) to keto bases (G/T) were also observed to be more than the reverse substitutions in the stem region. Substitution from amino bases to keto bases are likely to facilitate the stable G:U pairing unlike the reverse substitution that facilitates the unstable A:C pairing in the stem region of tRNA. This work provides additional support that the secondary structure of tRNA molecule is what drives the different substitutions in its gene sequence.

KW - Base substitution

KW - Intergenic region

KW - Transition

KW - Transversion

KW - tRNA secondary structure

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U2 - 10.1007/s00239-021-10045-x

DO - 10.1007/s00239-021-10045-x

M3 - Article

AN - SCOPUS:85123959135

VL - 90

SP - 114

EP - 123

JO - Journal of Molecular Evolution

JF - Journal of Molecular Evolution

SN - 0022-2844

IS - 1

ER -

Stem Region of tRNA Genes Favors Transition Substitution Towards Keto Bases in Bacteria

Abstract

Keywords

ASJC Scopus subject areas

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SpARK - The Rates and Routes of Transmission of Multidrug Resistant Klebsiella Clones into the Clinic from Environmental Sources

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Stem Region of tRNA Genes Favors Transition Substitution Towards Keto Bases in Bacteria

Abstract

Keywords

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Projects

SpARK - The Rates and Routes of Transmission of Multidrug Resistant Klebsiella Clones into the Clinic from Environmental Sources

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