Functional genomics and structural insights into maize aldo-keto reductase-4 family: Stress metabolism and substrate specificity in embryos

J Biol Chem. 2025 Jul;301(7):110404. doi: 10.1016/j.jbc.2025.110404. Epub 2025 Jun 20.

Abstract

Aldo-keto reductases (AKRs) are ubiquitous in nature and are able to reduce a wide range of substrates, from simple sugars to potentially toxic aldehydes. In plants, AKRs are involved in key metabolic processes including reactive aldehyde detoxification. This study aimed to (i) delineate a maize gene family encoding aldo keto reductase-4s (AKR4s) (ii) help bridge sequence-to-function gaps among them, and (iii) focus on a family member implicated in embryo specific stress metabolism. We employed a genome-wide analysis approach to identify maize genes encoding AKR4s, defining and annotating a 15-member gene family that clustered into three subgroups. Expression profiling, validated through wet lab experiments, revealed distinct functional roles: (i) AKR4C Zm-1 functions in aldehyde detoxification during stress, (ii) AKR4C Zm-2 includes stress-responsive AKRs with diverse substrate affinities, and (iii) AKR4A/B Zm-3 contributes to specialized metabolites like phytosiderophores for iron transport. To investigate the impact of sequence variation on function, we characterized ZmAKR4C13, a representative of AKR4C Zm-1. Its mRNA and protein were predominantly localized in embryos, suggesting a specialized role. Recombinant ZmAKR4C13 efficiently reduced methylglyoxal and small aldehydes but showed poor activity toward aldoses larger than four carbons. Crystallographic analysis identified a size constraint at the active site, attributed to the bulkier LEU residue at position 294. Collectively, our results emphasize how subtle modifications in active-site architecture influence AKR substrate specificity. They also demonstrate a potential role of maize ZmAKR4C13 in detoxifying methylglyoxal and other small metabolites that could contribute to stress signaling in embryos.

Keywords: Zea mays; crystallography; detoxification; enzyme kinetics; functional genomics; fungi; gene expression; protein structure.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aldehyde Reductase
  • Aldo-Keto Reductases
  • Crystallography, X-Ray
  • Gene Expression Regulation, Plant
  • Genomics
  • Multigene Family
  • Plant Proteins* / chemistry
  • Plant Proteins* / genetics
  • Plant Proteins* / metabolism
  • Seeds* / enzymology
  • Seeds* / genetics
  • Seeds* / metabolism
  • Stress, Physiological*
  • Substrate Specificity
  • Zea mays* / embryology
  • Zea mays* / enzymology
  • Zea mays* / genetics

Substances

  • Plant Proteins
  • Aldo-Keto Reductases
  • Aldehyde Reductase

Associated data

  • PDB/5JGW
  • PDB/5JGY