Self-incompatibility triggers irreversible oxidative modification of proteins in incompatible pollen

Tamanna Haque, Deborah Eaves, Zongcheng Lin, Gleidiane Zampronio, Helen Cooper, Maurice Bosch, Nicholas Smirnoff, Vernonica E. Franklin-Tong

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7 Citations (SciVal)
101 Downloads (Pure)

Abstract

Self-incompatibility (SI) is used by many angiosperms to prevent self-fertilization and inbreeding. In common poppy (Papaver rhoeas), interaction of cognate pollen and pistil S-determinants triggers programmed cell death (PCD) of incompatible pollen. We previously identified that reactive oxygen species (ROS) signal to SI-PCD. ROS-induced oxidative post-translational modifications (oxPTMs) can regulate protein structure and function. Here we have identified and mapped oxPTMs triggered by SI in incompatible pollen. Notably, SI-induced pollen had numerous irreversible oxidative modifications while untreated pollen had virtually none. Our data provide a valuable analysis of the protein targets of ROS in the context of SI-induction and comprise a benchmark because currently there are few reports of irreversible oxPTMs in plants. Strikingly, cytoskeletal proteins and enzymes involved in energy metabolism are a prominent target of ROS. Oxidative modifications to a phosphomimic form of a pyrophosphatase result in a reduction of its activity. Therefore, our results demonstrate irreversible oxidation of pollen proteins during SI and provide evidence that this modification can affect protein function. We suggest that this reduction in cellular activity could lead to PCD.
Original languageEnglish
Pages (from-to)1391-1404
Number of pages14
JournalPlant Physiology
Volume183
Issue number3
Early online date22 Apr 2020
DOIs
Publication statusPublished - 31 Jul 2020

Keywords

  • Inorganic Pyrophosphatase/metabolism
  • Amino Acid Sequence
  • Pollen/drug effects
  • Proteasome Endopeptidase Complex/metabolism
  • Actins/metabolism
  • Oxidation-Reduction
  • Solubility
  • Pollen Tube/drug effects
  • Amino Acids/metabolism
  • Nitrosation
  • Papaver/drug effects
  • Peptide Hydrolases/metabolism
  • Cytoskeletal Proteins/metabolism
  • Peptides/metabolism
  • Self-Incompatibility in Flowering Plants/drug effects
  • Protein Processing, Post-Translational/drug effects
  • Hydrogen Peroxide/toxicity
  • Plant Proteins/chemistry

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