The miRNAome dynamics during developmental and metabolic reprogramming of tomato root infected with potato cyst nematode

• Published in: Plant science (Limerick) Vol. 268; pp. 18 - 29
• Main Authors: Koter, Marek D., Święcicka, Magdalena, Matuszkiewicz, Mateusz, Pacak, Andrzej, Derebecka, Natalia, Filipecki, Marcin
• Format: Journal Article
• Language: English
• Published: Ireland Elsevier B.V 01.03.2018
• Subjects: Animals; auxins; Base Sequence; complementary DNA; cyst nematodes; data collection; developmental stages; Disease Progression; gene expression; gene expression regulation; Gene Expression Regulation, Developmental; Gene Expression Regulation, Plant; genes; giant cells; Globodera rostochiensis; GRAS substances; High-Throughput Nucleotide Sequencing; isomiRs; Lycopersicon esculentum - genetics; Lycopersicon esculentum - growth & development; Lycopersicon esculentum - metabolism; Lycopersicon esculentum - parasitology; meta-analysis; microRNA; MicroRNAs - genetics; MicroRNAs - metabolism; miRNA dynamics; Molecular Sequence Annotation; plant development; Plant Diseases - genetics; Plant Diseases - parasitology; plant diseases and disorders; Plant Roots - genetics; Plant Roots - parasitology; Potato cyst nematode; potatoes; quantitative polymerase chain reaction; rapid amplification of cDNA ends; Real-Time Polymerase Chain Reaction; Reproducibility of Results; reverse transcriptase polymerase chain reaction; RNA Stability - genetics; RNA, Messenger - genetics; RNA, Messenger - metabolism; RNA, Small Interfering - metabolism; roots; sequence analysis; Solanum tuberosum - parasitology; Tomato; tomatoes; Transcription factors; Transcription, Genetic; transcriptome; Tylenchoidea - pathogenicity; isomiRs; Transcription factors; Tomato; miRNA dynamics; Potato cyst nematode
• DOI: 10.1016/j.plantsci.2017.12.003
• ISSN: 0168-9452; 1873-2259

•The tomato root miRNAs differentially regulated during G. rostochensis infection were sequenced by NGS.•Different regulatory potentials for isomiRs were shown.•Direct or indirect evidence for 54 targets cleavage was shown pointing the regulatory pressure on genes involved in defense response and development. Cyst-forming plant-parasitic nematodes are pests threatening many crops. By means of their secretions cyst nematodes induce the developmental and metabolic reprogramming of host cells that lead to the formation of a syncytium, which is the sole food source for growing nematodes. The in depth micro RNA (miRNA) dynamics in the syncytia induced by Globodera rostochiensis in tomato roots was studied. The miRNAomes were obtained from syncytia covering the early and intermediate developmental stages, and were the subject of differential expression analysis. The expression of 1235 miRNAs was monitored. The fold change (log2FC) ranged from −7.36 to 8.38, indicating that this transcriptome fraction was very variable. Moreover, we showed that the DE (differentially expressed) miRNAs do not fully overlap between the selected time points, suggesting infection stage specific regulation by miRNA. The correctness of RNA-seq expression profiling was confirmed by qRT-PCR (quantitative Real Time Polymerase Chain Reaction) for seven miRNA species. Down- and up-regulated miRNA species, including their isomiRs, were further used to identify their potential targets. Among them there are a large number of transcription factors linked to different aspects of plant development belonging to gene families, such as APETALA2 (AP2), SQUAMOSA (MADS-box), MYB, GRAS, and AUXIN RESPONSE FACTOR (ARF). The substantial portion of potential target genes belong to the NB-LRR and RLK (RECEPTOR-LIKE KINASE) families, indicating the involvement of miRNA mediated regulation in defense responses. We also collected the evidence for target cleavage in the case of 29 miRNAs using one of three alternative methods: 5′ RACE (5′ Rapid Amplification of cDNA Ends), a search of tasiRNA within our datasets, and the meta-analysis of tomato degradomes in the GEO (Gene Expression Omnibus) database. Eight target transcripts showed a negative correlation with their respective miRNAs at two or three time points. These results indicate a large regulatory potential for miRNAs in tuning the development and defense responses.