Phytoglobins in the nuclei, cytoplasm and chloroplasts modulate nitric oxide signaling and interact with abscisic acid

Plant J. 2019 Oct;100(1):38-54. doi: 10.1111/tpj.14422. Epub 2019 Jul 8.

Abstract

Symbiotic hemoglobins provide O2 to N2 -fixing bacteria within legume nodules, but the functions of non-symbiotic hemoglobins or phytoglobins (Glbs) are much less defined. Immunolabeling combined with confocal microscopy of the Glbs tagged at the C-terminus with green fluorescent protein was used to determine their subcellular localizations in Arabidopsis and Lotus japonicus. Recombinant proteins were used to examine nitric oxide (NO) scavenging in vitro and transgenic plants to show S-nitrosylation and other in vivo interactions with NO and abscisic acid (ABA) responses. We found that Glbs occur in the nuclei, chloroplasts and amyloplasts of both model plants, and also in the cytoplasm of Arabidopsis cells. The proteins show similar NO dioxygenase activities in vitro, are nitrosylated in Cys residues in vivo, and scavenge NO in the stomatal cells. The Cys/Ser mutation does not affect NO dioxygenase activity, and S-nitrosylation does not significantly consume NO. We demonstrate an interaction between Glbs and ABA on several grounds: Glb1 and Glb2 scavenge NO produced in stomatal guard cells following ABA supply; plants overexpressing Glb1 show higher constitutive expression of the ABA responsive genes Responsive to ABA (RAB18), Responsive to Dehydration (RD29A) and Highly ABA-Induced 2 (HAI2), and are more tolerant to dehydration; and ABA strongly upregulates class 1 Glbs. We conclude that Glbs modulate NO and interact with ABA in crucial physiological processes such as the plant's response to dessication.

Keywords: Arabidopsis thaliana; Lotus japonicus; abscisic acid; nitric oxide; phytoglobins.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Abscisic Acid / metabolism*
  • Arabidopsis / genetics
  • Arabidopsis / metabolism
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / metabolism
  • Cell Nucleus / metabolism*
  • Chloroplasts / metabolism*
  • Cytoplasm / metabolism*
  • Gene Expression Profiling / methods
  • Gene Expression Regulation, Plant
  • Hemoglobins / genetics*
  • Hemoglobins / metabolism
  • Lotus / genetics
  • Lotus / metabolism
  • Microscopy, Immunoelectron
  • Nitric Oxide / metabolism*
  • Plant Stomata / genetics
  • Plant Stomata / metabolism
  • Plant Stomata / ultrastructure
  • Plants, Genetically Modified
  • Protein Binding
  • Signal Transduction

Substances

  • AHB1 protein, Arabidopsis
  • Arabidopsis Proteins
  • Hemoglobins
  • phytoglobin 2 protein, Arabidopsis
  • Nitric Oxide
  • Abscisic Acid