Structural and Biochemical Characterization of Aldehyde Dehydrogenase 12, the Last Enzyme of Proline Catabolism in Plants

David A. Korasick, Radka Končitíková, Martina Kopečná, Eva Hájková, Armelle Vigouroux, Solange Moréra, Donald F Becker, Marek Šebela, John J. Tanner, David Kopečný

Research output: Contribution to journalArticle

2 Citations (Scopus)

Abstract

Heterokonts, Alveolata protists, green algae from Charophyta and Chlorophyta divisions, and all Embryophyta plants possess an aldehyde dehydrogenase (ALDH) gene named ALDH12. Here, we provide a biochemical characterization of two ALDH12 family members from the lower plant Physcomitrella patens and higher plant Zea mays. We show that ALDH12 encodes an NAD+-dependent glutamate γ-semialdehyde dehydrogenase (GSALDH), which irreversibly converts glutamate γ-semialdehyde (GSAL), a mitochondrial intermediate of the proline and arginine catabolism, to glutamate. Sedimentation equilibrium and small-angle X-ray scattering analyses reveal that in solution both plant GSALDHs exist as equilibrium between a domain-swapped dimer and the dimer-of-dimers tetramer. Plant GSALDHs share very low-sequence identity with bacterial, fungal, and animal GSALDHs (classified as ALDH4), which are the closest related ALDH superfamily members. Nevertheless, the crystal structure of ZmALDH12 at 2.2-Å resolution shows that nearly all key residues involved in the recognition of GSAL are identical to those in ALDH4, indicating a close functional relationship with ALDH4. Phylogenetic analysis suggests that the transition from ALDH4 to ALDH12 occurred during the evolution of the endosymbiotic plant ancestor, prior to the evolution of green algae and land plants. Finally, ALDH12 expression in maize and moss is downregulated in response to salt and drought stresses, possibly to maintain proline levels. Taken together, these results provide molecular insight into the biological roles of the plant ALDH12 family.

Original languageEnglish (US)
JournalJournal of Molecular Biology
DOIs
StateAccepted/In press - Jan 1 2019

Fingerprint

Aldehyde Dehydrogenase
Proline
Enzymes
Chlorophyta
Embryophyta
Glutamic Acid
Glutamate-5-Semialdehyde Dehydrogenase
Zea mays
Charophyceae
Alveolata
Stramenopiles
Bryopsida
Viridiplantae
Bryophyta
Droughts
NAD
Arginine
Down-Regulation
Salts
X-Rays

Keywords

  • ALDH12
  • glutamate γ-semialdehyde
  • Physcomitrella patens
  • proline
  • Zea mays

ASJC Scopus subject areas

  • Structural Biology
  • Molecular Biology

Cite this

Korasick, D. A., Končitíková, R., Kopečná, M., Hájková, E., Vigouroux, A., Moréra, S., ... Kopečný, D. (Accepted/In press). Structural and Biochemical Characterization of Aldehyde Dehydrogenase 12, the Last Enzyme of Proline Catabolism in Plants. Journal of Molecular Biology. https://doi.org/10.1016/j.jmb.2018.12.010

Structural and Biochemical Characterization of Aldehyde Dehydrogenase 12, the Last Enzyme of Proline Catabolism in Plants. / Korasick, David A.; Končitíková, Radka; Kopečná, Martina; Hájková, Eva; Vigouroux, Armelle; Moréra, Solange; Becker, Donald F; Šebela, Marek; Tanner, John J.; Kopečný, David.

In: Journal of Molecular Biology, 01.01.2019.

Research output: Contribution to journalArticle

Korasick, DA, Končitíková, R, Kopečná, M, Hájková, E, Vigouroux, A, Moréra, S, Becker, DF, Šebela, M, Tanner, JJ & Kopečný, D 2019, 'Structural and Biochemical Characterization of Aldehyde Dehydrogenase 12, the Last Enzyme of Proline Catabolism in Plants', Journal of Molecular Biology. https://doi.org/10.1016/j.jmb.2018.12.010
Korasick, David A. ; Končitíková, Radka ; Kopečná, Martina ; Hájková, Eva ; Vigouroux, Armelle ; Moréra, Solange ; Becker, Donald F ; Šebela, Marek ; Tanner, John J. ; Kopečný, David. / Structural and Biochemical Characterization of Aldehyde Dehydrogenase 12, the Last Enzyme of Proline Catabolism in Plants. In: Journal of Molecular Biology. 2019.
@article{6aa8ea3d835046db92f5ba76033de739,
title = "Structural and Biochemical Characterization of Aldehyde Dehydrogenase 12, the Last Enzyme of Proline Catabolism in Plants",
abstract = "Heterokonts, Alveolata protists, green algae from Charophyta and Chlorophyta divisions, and all Embryophyta plants possess an aldehyde dehydrogenase (ALDH) gene named ALDH12. Here, we provide a biochemical characterization of two ALDH12 family members from the lower plant Physcomitrella patens and higher plant Zea mays. We show that ALDH12 encodes an NAD+-dependent glutamate γ-semialdehyde dehydrogenase (GSALDH), which irreversibly converts glutamate γ-semialdehyde (GSAL), a mitochondrial intermediate of the proline and arginine catabolism, to glutamate. Sedimentation equilibrium and small-angle X-ray scattering analyses reveal that in solution both plant GSALDHs exist as equilibrium between a domain-swapped dimer and the dimer-of-dimers tetramer. Plant GSALDHs share very low-sequence identity with bacterial, fungal, and animal GSALDHs (classified as ALDH4), which are the closest related ALDH superfamily members. Nevertheless, the crystal structure of ZmALDH12 at 2.2-{\AA} resolution shows that nearly all key residues involved in the recognition of GSAL are identical to those in ALDH4, indicating a close functional relationship with ALDH4. Phylogenetic analysis suggests that the transition from ALDH4 to ALDH12 occurred during the evolution of the endosymbiotic plant ancestor, prior to the evolution of green algae and land plants. Finally, ALDH12 expression in maize and moss is downregulated in response to salt and drought stresses, possibly to maintain proline levels. Taken together, these results provide molecular insight into the biological roles of the plant ALDH12 family.",
keywords = "ALDH12, glutamate γ-semialdehyde, Physcomitrella patens, proline, Zea mays",
author = "Korasick, {David A.} and Radka Končit{\'i}kov{\'a} and Martina Kopečn{\'a} and Eva H{\'a}jkov{\'a} and Armelle Vigouroux and Solange Mor{\'e}ra and Becker, {Donald F} and Marek Šebela and Tanner, {John J.} and David Kopečn{\'y}",
year = "2019",
month = "1",
day = "1",
doi = "10.1016/j.jmb.2018.12.010",
language = "English (US)",
journal = "Journal of Molecular Biology",
issn = "0022-2836",
publisher = "Academic Press Inc.",

}

TY - JOUR

T1 - Structural and Biochemical Characterization of Aldehyde Dehydrogenase 12, the Last Enzyme of Proline Catabolism in Plants

AU - Korasick, David A.

AU - Končitíková, Radka

AU - Kopečná, Martina

AU - Hájková, Eva

AU - Vigouroux, Armelle

AU - Moréra, Solange

AU - Becker, Donald F

AU - Šebela, Marek

AU - Tanner, John J.

AU - Kopečný, David

PY - 2019/1/1

Y1 - 2019/1/1

N2 - Heterokonts, Alveolata protists, green algae from Charophyta and Chlorophyta divisions, and all Embryophyta plants possess an aldehyde dehydrogenase (ALDH) gene named ALDH12. Here, we provide a biochemical characterization of two ALDH12 family members from the lower plant Physcomitrella patens and higher plant Zea mays. We show that ALDH12 encodes an NAD+-dependent glutamate γ-semialdehyde dehydrogenase (GSALDH), which irreversibly converts glutamate γ-semialdehyde (GSAL), a mitochondrial intermediate of the proline and arginine catabolism, to glutamate. Sedimentation equilibrium and small-angle X-ray scattering analyses reveal that in solution both plant GSALDHs exist as equilibrium between a domain-swapped dimer and the dimer-of-dimers tetramer. Plant GSALDHs share very low-sequence identity with bacterial, fungal, and animal GSALDHs (classified as ALDH4), which are the closest related ALDH superfamily members. Nevertheless, the crystal structure of ZmALDH12 at 2.2-Å resolution shows that nearly all key residues involved in the recognition of GSAL are identical to those in ALDH4, indicating a close functional relationship with ALDH4. Phylogenetic analysis suggests that the transition from ALDH4 to ALDH12 occurred during the evolution of the endosymbiotic plant ancestor, prior to the evolution of green algae and land plants. Finally, ALDH12 expression in maize and moss is downregulated in response to salt and drought stresses, possibly to maintain proline levels. Taken together, these results provide molecular insight into the biological roles of the plant ALDH12 family.

AB - Heterokonts, Alveolata protists, green algae from Charophyta and Chlorophyta divisions, and all Embryophyta plants possess an aldehyde dehydrogenase (ALDH) gene named ALDH12. Here, we provide a biochemical characterization of two ALDH12 family members from the lower plant Physcomitrella patens and higher plant Zea mays. We show that ALDH12 encodes an NAD+-dependent glutamate γ-semialdehyde dehydrogenase (GSALDH), which irreversibly converts glutamate γ-semialdehyde (GSAL), a mitochondrial intermediate of the proline and arginine catabolism, to glutamate. Sedimentation equilibrium and small-angle X-ray scattering analyses reveal that in solution both plant GSALDHs exist as equilibrium between a domain-swapped dimer and the dimer-of-dimers tetramer. Plant GSALDHs share very low-sequence identity with bacterial, fungal, and animal GSALDHs (classified as ALDH4), which are the closest related ALDH superfamily members. Nevertheless, the crystal structure of ZmALDH12 at 2.2-Å resolution shows that nearly all key residues involved in the recognition of GSAL are identical to those in ALDH4, indicating a close functional relationship with ALDH4. Phylogenetic analysis suggests that the transition from ALDH4 to ALDH12 occurred during the evolution of the endosymbiotic plant ancestor, prior to the evolution of green algae and land plants. Finally, ALDH12 expression in maize and moss is downregulated in response to salt and drought stresses, possibly to maintain proline levels. Taken together, these results provide molecular insight into the biological roles of the plant ALDH12 family.

KW - ALDH12

KW - glutamate γ-semialdehyde

KW - Physcomitrella patens

KW - proline

KW - Zea mays

UR - http://www.scopus.com/inward/record.url?scp=85059323636&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85059323636&partnerID=8YFLogxK

U2 - 10.1016/j.jmb.2018.12.010

DO - 10.1016/j.jmb.2018.12.010

M3 - Article

JO - Journal of Molecular Biology

JF - Journal of Molecular Biology

SN - 0022-2836

ER -