Details
| Original language | English |
|---|---|
| Pages (from-to) | 1759-1775 |
| Number of pages | 17 |
| Journal | New Phytologist |
| Volume | 237 |
| Issue number | 5 |
| Early online date | 4 Dec 2022 |
| Publication status | Published - 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
ASJC Scopus subject areas
- Biochemistry, Genetics and Molecular Biology(all)
- Physiology
- Agricultural and Biological Sciences(all)
- Plant Science
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In: New Phytologist, Vol. 237, No. 5, 02.02.2023, p. 1759-1775.
Research output: Contribution to journal › Article › Research › peer review
}
TY - JOUR
T1 - An inosine triphosphate pyrophosphatase safeguards plant nucleic acids from aberrant purine nucleotides
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.
AB - 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.
KW - abiotic stress
KW - damaged metabolites
KW - deaminated purine nucleotides
KW - inosine triphosphate
KW - inosine triphosphate pyrophosphatase
KW - plant nucleotide metabolism
KW - senescence
UR - http://www.scopus.com/inward/record.url?scp=85145297744&partnerID=8YFLogxK
U2 - 10.1111/nph.18656
DO - 10.1111/nph.18656
M3 - Article
C2 - 36464781
AN - SCOPUS:85145297744
VL - 237
SP - 1759
EP - 1775
JO - New Phytologist
JF - New Phytologist
SN - 0028-646X
IS - 5
ER -