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

ABSTRACT: Self-incompatibility (SI) is used by many angiosperms to prevent self-fertilization and inbreeding. In 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) signals 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; untreated pollen had virtually none. Our data provide the first analysis of the protein targets of ROS in the context of SI-induction and represent a milestone because currently there are few reports of irreversible oxPTMs in plants. Strikingly, cytoskeletal proteins and enzymes involved in energy metabolism are a prominent target. 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 show that this can affect protein function. We suggest that this reduction in cellular activity could lead to PCD.

INSTRUMENT(S): LTQ Orbitrap Velos

ORGANISM(S): Papaver Rhoeas (ncbitaxon:33128)

SUBMITTER: Vernonica Franklin-Tong

PROVIDER: MSV000085216 | MassIVE | Thu Apr 02 03:10:00 BST 2020

REPOSITORIES: MassIVE

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Project description:Background: Tomato (Solanum lycopersicum) self-compatibility (SC) is defined as self-pollen tubes that can penetrate their own stigma, elongate in the style and fertilize their own ovules. Self-incompatibility (SI) is defined as self-pollen tubes that are prevented from developing in the style. To determine the influence of gene expression on style self-pollination, a transcriptome-wide comparative analysis of SC and SI tomato unpollinated/pollinated styles was performed using RNA-sequencing (RNA-seq) data. Results: Transcriptome profiles of 24-h unpollination (UP) and self-pollination (P) styles from SC and SI tomato species were generated using high-throughput next generation sequencing. From the comparison of SC self-pollinated and unpollinated styles, 1341 differentially expressed genes (DEGs) were identified, of which 753 were downregulated and 588 were upregulated. From the comparison of SI self-pollinated and unpollinated styles, 804 DEGs were identified, of which 215 were downregulated and 589 were upregulated. Nine gene ontology (GO) terms were enriched significantly in SC and 78 GO terms were enriched significantly in SI. A total of 105 enriched Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways were identified in SC and 80 enriched KEGG pathways were identified in SI, among which “Cysteine and methionine metabolism pathway” and “Plant hormone signal transduction pathway” were significantly enriched in SI. Conclusions: This study is the first global transcriptome-wide comparative analysis of SC and SI tomato unpollinated/pollinated styles. Advanced bioinformatic analysis of DEGs uncovered the pathways of “Cysteine and methionine metabolism” and “Plant hormone signal transduction”, which are likely to play important roles in the control of pollen tubes growth in SI species. 24-h unpollination (UP) and self-pollination (P) styles mRNA profiles from SC and SI tomato species were generated by deep sequencing, in triplicate, using Illumina Hiseq 2500 platform.

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

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