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Polyamines Involved in Regulating Self-Incompatibility in Apple.

ABSTRACT: Apple exhibits typical gametophytic self-incompatibility, in which self-S-RNase can arrest pollen tube growth, leading to failure of fertilization. To date, there have been few studies on how to resist the toxicity of self-S-RNase. In this study, pollen tube polyamines were found to respond to self-S-RNase and help pollen tubes defend against self-S-RNase. In particular, the contents of putrescine, spermidine, and spermine in the pollen tube treated with self-S-RNase were substantially lower than those treated with non-self-S-RNase. Further analysis of gene expression of key enzymes in the synthesis and degradation pathways of polyamines found that the expression of DIAMINE OXIDASE 4 (MdDAO4) as well as several polyamine oxidases such as POLYAMINE OXIDASES 3 (MdPAO3), POLYAMINE OXIDASES 4 (MdPAO4), and POLYAMINE OXIDASES 6 (MdPAO6) were significantly up-regulated under self-S-RNase treatment, resulting in the reduction of polyamines. Silencing MdPAO6 in pollen tubes alleviates the inhibitory effect of self-S-RNase on pollen tube growth. In addition, exogenous polyamines also enhance pollen tube resistance to self-S-RNase. Transcriptome sequencing data found that polyamines may communicate with S-RNase through the calcium signal pathway, thereby regulating the growth of the pollen tubes. To summarize, our results suggested that polyamines responded to the self-incompatibility reaction and could enhance pollen tube tolerance to S-RNase, thus providing a potential way to break self-incompatibility in apple.

SUBMITTER: Yu J

PROVIDER: S-EPMC8620888 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Non-self gametophytic self-incompatibility (GSI) recognition system is characterized by the presence of multiple F-box genes tandemly located in the S-locus, that regulate pollen specificity. This reproductive barrier is present in Solanaceae, Plantaginacea and Maleae (Rosaceae), but only in Petunia functional assays have been performed to get insight on how this recognition mechanism works. In this system, each of the encoded S-pollen proteins (called SLFs in Solanaceae and Plantaginaceae /SFBBs in Maleae) recognizes and interacts with a sub-set of non-self S-pistil proteins, called S-RNases, mediating their ubiquitination and degradation. In Petunia there are 17 SLF genes per S-haplotype, making impossible to determine experimentally each SLF specificity. Moreover, domain -swapping experiments are unlikely to be performed in large scale to determine S-pollen and S-pistil specificities. Phylogenetic analyses of the Petunia SLFs and those from two Solanum genomes, suggest that diversification of SLFs predate the two genera separation. Here we first identify putative SLF genes from nine Solanum and 10 Nicotiana genomes to determine how many gene lineages are present in the three genera, and the rate of origin of new SLF gene lineages. The use of multiple genomes per genera precludes the effect of incompleteness of the genome at the S-locus. The similar number of gene lineages in the three genera implies a comparable effective population size for these species, and number of specificities. The rate of origin of new specificities is one per 10 million years. Moreover, here we determine the amino acids positions under positive selection, those involved in SLF specificity recognition, using 10 Petunia S-haplotypes with more than 11 SLF genes. These 16 amino acid positions account for the differences of self-incompatible (SI) behavior described in the literature. When SLF and S-RNase proteins are divided according to the SI behavior, and the positively selected amino acids classified according to hydrophobicity, charge, polarity and size, we identified fixed differences between SI groups. According to the in silico 3D structure of the two proteins these amino acid positions interact. Therefore, this methodology can be used to infer SLF/S-RNase specificity recognition.

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Polyamines Involved in Regulating Self-Incompatibility in Apple.

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