Arabidopsis and maize RidA Proteins preempt reactive enamine/imine damage to branched-chain amino acid biosynthesis in plastids

Thomas D. Niehaus, Thuy N D Nguyen, Satinder K. Gidda, Mona ElBadawi-Sidhu, Jennifer A. Lambrecht, Donald R. McCarty, Diana M. Downs, Arthur J L Cooper, Oliver Fiehn, Robert T. Mullen, Andrew D. Hanson

Research output: Contribution to journalArticle

31 Citations (Scopus)

Abstract

RidA (for Reactive Intermediate Deaminase A) proteins are ubiquitous, yet their function in eukaryotes is unclear. It is known that deleting Salmonella enterica ridA causes Ser sensitivity and that S. enterica RidA and its homologs from other organisms hydrolyze the enamine/imine intermediates that Thr dehydratase forms from Ser or Thr. In S. enterica, the Ser-derived enamine/imine inactivates a branched-chain aminotransferase; RidA prevents this damage. Arabidopsis thaliana and maize (Zea mays) have a RidA homolog that is predicted to be plastidial. Expression of either homolog complemented the Ser sensitivity of the S. enterica ridA mutant. The purified proteins hydrolyzed the enamines/imines formed by Thr dehydratase from Ser or Thr and protected the Arabidopsis plastidial branched-chain aminotransferase BCAT3 from inactivation by the Ser-derived enamine/imine. In vitro chloroplast import assays and in vivo localization of green fluorescent protein fusions showed that Arabidopsis RidA and Thr dehydratase are chloroplast targeted. Disrupting Arabidopsis RidA reduced root growth and raised the root and shoot levels of the branched-chain amino acid biosynthesis intermediate 2-oxobutanoate; Ser treatment exacerbated these effects in roots. Supplying Ile reversed the root growth defect. These results indicate that plastidial RidA proteins can preempt damage to BCAT3 and Ile biosynthesis by hydrolyzing the Ser-derived enamine/imine product of Thr dehydratase.

Original languageEnglish (US)
Pages (from-to)3010-3022
Number of pages13
JournalPlant Cell
Volume26
Issue number7
DOIs
StatePublished - 2014

Fingerprint

Branched Chain Amino Acids
Plastids
branched chain amino acids
Imines
Salmonella enterica
Hydro-Lyases
Arabidopsis
Zea mays
plastids
biosynthesis
corn
transaminases
Scrapie
Chloroplasts
root growth
Proteins
proteins
chloroplasts
protein hydrolysates
green fluorescent protein

ASJC Scopus subject areas

  • Plant Science
  • Cell Biology

Cite this

Niehaus, T. D., Nguyen, T. N. D., Gidda, S. K., ElBadawi-Sidhu, M., Lambrecht, J. A., McCarty, D. R., ... Hanson, A. D. (2014). Arabidopsis and maize RidA Proteins preempt reactive enamine/imine damage to branched-chain amino acid biosynthesis in plastids. Plant Cell, 26(7), 3010-3022. https://doi.org/10.1105/tpc.114.126854

Arabidopsis and maize RidA Proteins preempt reactive enamine/imine damage to branched-chain amino acid biosynthesis in plastids. / Niehaus, Thomas D.; Nguyen, Thuy N D; Gidda, Satinder K.; ElBadawi-Sidhu, Mona; Lambrecht, Jennifer A.; McCarty, Donald R.; Downs, Diana M.; Cooper, Arthur J L; Fiehn, Oliver; Mullen, Robert T.; Hanson, Andrew D.

In: Plant Cell, Vol. 26, No. 7, 2014, p. 3010-3022.

Research output: Contribution to journalArticle

Niehaus, TD, Nguyen, TND, Gidda, SK, ElBadawi-Sidhu, M, Lambrecht, JA, McCarty, DR, Downs, DM, Cooper, AJL, Fiehn, O, Mullen, RT & Hanson, AD 2014, 'Arabidopsis and maize RidA Proteins preempt reactive enamine/imine damage to branched-chain amino acid biosynthesis in plastids', Plant Cell, vol. 26, no. 7, pp. 3010-3022. https://doi.org/10.1105/tpc.114.126854
Niehaus, Thomas D. ; Nguyen, Thuy N D ; Gidda, Satinder K. ; ElBadawi-Sidhu, Mona ; Lambrecht, Jennifer A. ; McCarty, Donald R. ; Downs, Diana M. ; Cooper, Arthur J L ; Fiehn, Oliver ; Mullen, Robert T. ; Hanson, Andrew D. / Arabidopsis and maize RidA Proteins preempt reactive enamine/imine damage to branched-chain amino acid biosynthesis in plastids. In: Plant Cell. 2014 ; Vol. 26, No. 7. pp. 3010-3022.
@article{85bf57036e144897993ca8d9a00521b7,
title = "Arabidopsis and maize RidA Proteins preempt reactive enamine/imine damage to branched-chain amino acid biosynthesis in plastids",
abstract = "RidA (for Reactive Intermediate Deaminase A) proteins are ubiquitous, yet their function in eukaryotes is unclear. It is known that deleting Salmonella enterica ridA causes Ser sensitivity and that S. enterica RidA and its homologs from other organisms hydrolyze the enamine/imine intermediates that Thr dehydratase forms from Ser or Thr. In S. enterica, the Ser-derived enamine/imine inactivates a branched-chain aminotransferase; RidA prevents this damage. Arabidopsis thaliana and maize (Zea mays) have a RidA homolog that is predicted to be plastidial. Expression of either homolog complemented the Ser sensitivity of the S. enterica ridA mutant. The purified proteins hydrolyzed the enamines/imines formed by Thr dehydratase from Ser or Thr and protected the Arabidopsis plastidial branched-chain aminotransferase BCAT3 from inactivation by the Ser-derived enamine/imine. In vitro chloroplast import assays and in vivo localization of green fluorescent protein fusions showed that Arabidopsis RidA and Thr dehydratase are chloroplast targeted. Disrupting Arabidopsis RidA reduced root growth and raised the root and shoot levels of the branched-chain amino acid biosynthesis intermediate 2-oxobutanoate; Ser treatment exacerbated these effects in roots. Supplying Ile reversed the root growth defect. These results indicate that plastidial RidA proteins can preempt damage to BCAT3 and Ile biosynthesis by hydrolyzing the Ser-derived enamine/imine product of Thr dehydratase.",
author = "Niehaus, {Thomas D.} and Nguyen, {Thuy N D} and Gidda, {Satinder K.} and Mona ElBadawi-Sidhu and Lambrecht, {Jennifer A.} and McCarty, {Donald R.} and Downs, {Diana M.} and Cooper, {Arthur J L} and Oliver Fiehn and Mullen, {Robert T.} and Hanson, {Andrew D.}",
year = "2014",
doi = "10.1105/tpc.114.126854",
language = "English (US)",
volume = "26",
pages = "3010--3022",
journal = "Plant Cell",
issn = "1040-4651",
publisher = "American Society of Plant Biologists",
number = "7",

}

TY - JOUR

T1 - Arabidopsis and maize RidA Proteins preempt reactive enamine/imine damage to branched-chain amino acid biosynthesis in plastids

AU - Niehaus, Thomas D.

AU - Nguyen, Thuy N D

AU - Gidda, Satinder K.

AU - ElBadawi-Sidhu, Mona

AU - Lambrecht, Jennifer A.

AU - McCarty, Donald R.

AU - Downs, Diana M.

AU - Cooper, Arthur J L

AU - Fiehn, Oliver

AU - Mullen, Robert T.

AU - Hanson, Andrew D.

PY - 2014

Y1 - 2014

N2 - RidA (for Reactive Intermediate Deaminase A) proteins are ubiquitous, yet their function in eukaryotes is unclear. It is known that deleting Salmonella enterica ridA causes Ser sensitivity and that S. enterica RidA and its homologs from other organisms hydrolyze the enamine/imine intermediates that Thr dehydratase forms from Ser or Thr. In S. enterica, the Ser-derived enamine/imine inactivates a branched-chain aminotransferase; RidA prevents this damage. Arabidopsis thaliana and maize (Zea mays) have a RidA homolog that is predicted to be plastidial. Expression of either homolog complemented the Ser sensitivity of the S. enterica ridA mutant. The purified proteins hydrolyzed the enamines/imines formed by Thr dehydratase from Ser or Thr and protected the Arabidopsis plastidial branched-chain aminotransferase BCAT3 from inactivation by the Ser-derived enamine/imine. In vitro chloroplast import assays and in vivo localization of green fluorescent protein fusions showed that Arabidopsis RidA and Thr dehydratase are chloroplast targeted. Disrupting Arabidopsis RidA reduced root growth and raised the root and shoot levels of the branched-chain amino acid biosynthesis intermediate 2-oxobutanoate; Ser treatment exacerbated these effects in roots. Supplying Ile reversed the root growth defect. These results indicate that plastidial RidA proteins can preempt damage to BCAT3 and Ile biosynthesis by hydrolyzing the Ser-derived enamine/imine product of Thr dehydratase.

AB - RidA (for Reactive Intermediate Deaminase A) proteins are ubiquitous, yet their function in eukaryotes is unclear. It is known that deleting Salmonella enterica ridA causes Ser sensitivity and that S. enterica RidA and its homologs from other organisms hydrolyze the enamine/imine intermediates that Thr dehydratase forms from Ser or Thr. In S. enterica, the Ser-derived enamine/imine inactivates a branched-chain aminotransferase; RidA prevents this damage. Arabidopsis thaliana and maize (Zea mays) have a RidA homolog that is predicted to be plastidial. Expression of either homolog complemented the Ser sensitivity of the S. enterica ridA mutant. The purified proteins hydrolyzed the enamines/imines formed by Thr dehydratase from Ser or Thr and protected the Arabidopsis plastidial branched-chain aminotransferase BCAT3 from inactivation by the Ser-derived enamine/imine. In vitro chloroplast import assays and in vivo localization of green fluorescent protein fusions showed that Arabidopsis RidA and Thr dehydratase are chloroplast targeted. Disrupting Arabidopsis RidA reduced root growth and raised the root and shoot levels of the branched-chain amino acid biosynthesis intermediate 2-oxobutanoate; Ser treatment exacerbated these effects in roots. Supplying Ile reversed the root growth defect. These results indicate that plastidial RidA proteins can preempt damage to BCAT3 and Ile biosynthesis by hydrolyzing the Ser-derived enamine/imine product of Thr dehydratase.

UR - http://www.scopus.com/inward/record.url?scp=84907324191&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84907324191&partnerID=8YFLogxK

U2 - 10.1105/tpc.114.126854

DO - 10.1105/tpc.114.126854

M3 - Article

VL - 26

SP - 3010

EP - 3022

JO - Plant Cell

JF - Plant Cell

SN - 1040-4651

IS - 7

ER -