Structural and biochemical characterization of the key components of an auxin degradation operon from the rhizosphere bacterium Variovorax

PLoS Biol. 2023 Jul 17;21(7):e3002189. doi: 10.1371/journal.pbio.3002189. eCollection 2023 Jul.

Abstract

Plant-associated bacteria play important regulatory roles in modulating plant hormone auxin levels, affecting the growth and yields of crops. A conserved auxin degradation (iad) operon was recently identified in the Variovorax genomes, which is responsible for root growth inhibition (RGI) reversion, promoting rhizosphere colonization and root growth. However, the molecular mechanism underlying auxin degradation by Variovorax remains unclear. Here, we systematically screened Variovorax iad operon products and identified 2 proteins, IadK2 and IadD, that directly associate with auxin indole-3-acetic acid (IAA). Further biochemical and structural studies revealed that IadK2 is a highly IAA-specific ATP-binding cassette (ABC) transporter solute-binding protein (SBP), likely involved in IAA uptake. IadD interacts with IadE to form a functional Rieske non-heme dioxygenase, which works in concert with a FMN-type reductase encoded by gene iadC to transform IAA into the biologically inactive 2-oxindole-3-acetic acid (oxIAA), representing a new bacterial pathway for IAA inactivation/degradation. Importantly, incorporation of a minimum set of iadC/D/E genes could enable IAA transformation by Escherichia coli, suggesting a promising strategy for repurposing the iad operon for IAA regulation. Together, our study identifies the key components and underlying mechanisms involved in IAA transformation by Variovorax and brings new insights into the bacterial turnover of plant hormones, which would provide the basis for potential applications in rhizosphere optimization and ecological agriculture.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacteria / metabolism
  • Indoleacetic Acids* / metabolism
  • Operon / genetics
  • Plant Growth Regulators / metabolism
  • Plants / metabolism
  • Rhizosphere*

Substances

  • Indoleacetic Acids
  • Plant Growth Regulators

Grants and funding

This work was supported by the National Natural Science Foundation of China (32071218 to H.Z.; 32200496 to G.Y.; 22007072 to H.S. and 32201004 to Z.L.) and the Ministry of Science and Technology, 2022YFA0911800 to Z.L.. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.