An inosine triphosphate pyrophosphatase safeguards plant nucleic acids from aberrant purine nucleotides

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Original languageEnglish
Pages (from-to)1759-1775
Number of pages17
JournalNew Phytologist
Volume237
Issue number5
Early online date4 Dec 2022
Publication statusPublished - 2 Feb 2023

Abstract

In plants, inosine is enzymatically introduced in some tRNAs, but not in other RNAs or DNA. Nonetheless, our data show that RNA and DNA from Arabidopsis thaliana contain (deoxy)inosine, probably derived from nonenzymatic adenosine deamination in nucleic acids and usage of (deoxy)inosine triphosphate (dITP and ITP) during nucleic acid synthesis. We combined biochemical approaches, LC–MS, as well as RNA-Seq to characterize a plant INOSINE TRIPHOSPHATE PYROPHOSPHATASE (ITPA) from A. thaliana, which is conserved in many organisms, and investigated the sources of deaminated purine nucleotides in plants. Inosine triphosphate pyrophosphatase dephosphorylates deaminated nucleoside di- and triphosphates to the respective monophosphates. ITPA loss-of-function causes inosine di- and triphosphate accumulation in vivo and an elevated inosine and deoxyinosine content in RNA and DNA, respectively, as well as salicylic acid (SA) accumulation, early senescence, and upregulation of transcripts associated with immunity and senescence. Cadmium-induced oxidative stress and biochemical inhibition of the INOSINE MONOPHOSPHATE DEHYDROGENASE leads to more IDP and ITP in the wild-type (WT), and this effect is enhanced in itpa mutants, suggesting that ITP originates from ATP deamination and IMP phosphorylation. Inosine triphosphate pyrophosphatase is part of a molecular protection system in plants, preventing the accumulation of (d)ITP and its usage for nucleic acid synthesis.

Keywords

    abiotic stress, damaged metabolites, deaminated purine nucleotides, inosine triphosphate, inosine triphosphate pyrophosphatase, plant nucleotide metabolism, senescence

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An inosine triphosphate pyrophosphatase safeguards plant nucleic acids from aberrant purine nucleotides. / Straube, Henryk; Straube, Jannis; Rinne, Jannis et al.
In: New Phytologist, Vol. 237, No. 5, 02.02.2023, p. 1759-1775.

Research output: Contribution to journalArticleResearchpeer review

Straube H, Straube J, Rinne J, Fischer L, Niehaus M, Witte CP et al. An inosine triphosphate pyrophosphatase safeguards plant nucleic acids from aberrant purine nucleotides. New Phytologist. 2023 Feb 2;237(5):1759-1775. Epub 2022 Dec 4. doi: 10.1111/nph.18656, 10.15488/13961
Straube, Henryk ; Straube, Jannis ; Rinne, Jannis et al. / An inosine triphosphate pyrophosphatase safeguards plant nucleic acids from aberrant purine nucleotides. In: New Phytologist. 2023 ; Vol. 237, No. 5. pp. 1759-1775.
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abstract = "In plants, inosine is enzymatically introduced in some tRNAs, but not in other RNAs or DNA. Nonetheless, our data show that RNA and DNA from Arabidopsis thaliana contain (deoxy)inosine, probably derived from nonenzymatic adenosine deamination in nucleic acids and usage of (deoxy)inosine triphosphate (dITP and ITP) during nucleic acid synthesis. We combined biochemical approaches, LC–MS, as well as RNA-Seq to characterize a plant INOSINE TRIPHOSPHATE PYROPHOSPHATASE (ITPA) from A. thaliana, which is conserved in many organisms, and investigated the sources of deaminated purine nucleotides in plants. Inosine triphosphate pyrophosphatase dephosphorylates deaminated nucleoside di- and triphosphates to the respective monophosphates. ITPA loss-of-function causes inosine di- and triphosphate accumulation in vivo and an elevated inosine and deoxyinosine content in RNA and DNA, respectively, as well as salicylic acid (SA) accumulation, early senescence, and upregulation of transcripts associated with immunity and senescence. Cadmium-induced oxidative stress and biochemical inhibition of the INOSINE MONOPHOSPHATE DEHYDROGENASE leads to more IDP and ITP in the wild-type (WT), and this effect is enhanced in itpa mutants, suggesting that ITP originates from ATP deamination and IMP phosphorylation. Inosine triphosphate pyrophosphatase is part of a molecular protection system in plants, preventing the accumulation of (d)ITP and its usage for nucleic acid synthesis.",
keywords = "abiotic stress, damaged metabolites, deaminated purine nucleotides, inosine triphosphate, inosine triphosphate pyrophosphatase, plant nucleotide metabolism, senescence",
author = "Henryk Straube and Jannis Straube and Jannis Rinne and Lisa Fischer and Markus Niehaus and Witte, {Claus Peter} and Marco Herde",
note = "Funding Information: We would like to express our gratitude to Holger Eubel and Bj{\"o}rn Heinemann for providing the hydroponic system and Andr{\'e} Specht for technical assistance. We also like to thank Anke Steppuhn (University of Hohenheim) for the donation of the phytohormone isotope standards. We furthermore like to express our gratitude to S{\"o}ren Budig and Frank Schaarschmidt (Leibniz University, Hannover) for advice on the statistical analysis. We like to acknowledge the support by the Deutsche Forschungsgemeinschaft (grant no. HE 5949/4‐1 to MH), (grant no. WI3411/7‐1 and WI3411/8‐1 to C‐PW), and (grant no. INST 187/741‐1 FUGG). Open Access funding enabled and organized by Projekt DEAL. ",
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AU - Straube, Henryk

AU - Straube, Jannis

AU - Rinne, Jannis

AU - Fischer, Lisa

AU - Niehaus, Markus

AU - Witte, Claus Peter

AU - Herde, Marco

N1 - Funding Information: We would like to express our gratitude to Holger Eubel and Björn Heinemann for providing the hydroponic system and André Specht for technical assistance. We also like to thank Anke Steppuhn (University of Hohenheim) for the donation of the phytohormone isotope standards. We furthermore like to express our gratitude to Sören Budig and Frank Schaarschmidt (Leibniz University, Hannover) for advice on the statistical analysis. We like to acknowledge the support by the Deutsche Forschungsgemeinschaft (grant no. HE 5949/4‐1 to MH), (grant no. WI3411/7‐1 and WI3411/8‐1 to C‐PW), and (grant no. INST 187/741‐1 FUGG). Open Access funding enabled and organized by Projekt DEAL.

PY - 2023/2/2

Y1 - 2023/2/2

N2 - In plants, inosine is enzymatically introduced in some tRNAs, but not in other RNAs or DNA. Nonetheless, our data show that RNA and DNA from Arabidopsis thaliana contain (deoxy)inosine, probably derived from nonenzymatic adenosine deamination in nucleic acids and usage of (deoxy)inosine triphosphate (dITP and ITP) during nucleic acid synthesis. We combined biochemical approaches, LC–MS, as well as RNA-Seq to characterize a plant INOSINE TRIPHOSPHATE PYROPHOSPHATASE (ITPA) from A. thaliana, which is conserved in many organisms, and investigated the sources of deaminated purine nucleotides in plants. Inosine triphosphate pyrophosphatase dephosphorylates deaminated nucleoside di- and triphosphates to the respective monophosphates. ITPA loss-of-function causes inosine di- and triphosphate accumulation in vivo and an elevated inosine and deoxyinosine content in RNA and DNA, respectively, as well as salicylic acid (SA) accumulation, early senescence, and upregulation of transcripts associated with immunity and senescence. Cadmium-induced oxidative stress and biochemical inhibition of the INOSINE MONOPHOSPHATE DEHYDROGENASE leads to more IDP and ITP in the wild-type (WT), and this effect is enhanced in itpa mutants, suggesting that ITP originates from ATP deamination and IMP phosphorylation. Inosine triphosphate pyrophosphatase is part of a molecular protection system in plants, preventing the accumulation of (d)ITP and its usage for nucleic acid synthesis.

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KW - damaged metabolites

KW - deaminated purine nucleotides

KW - inosine triphosphate

KW - inosine triphosphate pyrophosphatase

KW - plant nucleotide metabolism

KW - senescence

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