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Transcriptome profiling reveals roles of meristem regulators and polarity genes during multicellular fruit trichome development in cucumber (Cucumis sativus L.).

ABSTRACT: Trichomes are the hair-like structures that are widely present on the surface of aerial organs and function in plant defense against biotic and abiotic stresses. Previous studies focus on the single cell trichomes in Arabidopsis and cotton, or multicellular glandular trichomes in tomato, but the developmental process and molecular mechanisms controlling multicellular non-glandular trichome development are largely neglected. Here, we extensively characterized the fruit trichome (spine) development in wild type cucumber and in a tiny branched hair (tbh) mutant that contains a spontaneous mutation and has hairless foliage and smooth fruit surface. Our data indicated that cucumber trichome was multicellular and non-glandular, with no branches or endoreduplication. Further, the major feature of cucumber trichome development was spine base expansion. Transcriptome profiling through Digital Gene Expression indicated that meristem-related genes and transcription factors were implicated in the fruit spine development, and polarity regulators were upregulated during spine base expansion. qRT-PCR verified the reliability of our RNA-SEQ data, and in situ hybridization confirmed the enriched expression of meristem regulators CUP-SHAPED COTYLEDON3 (CUC3) and STM (SHOOT MERISTEMLESS) , as well as the abaxial identity gene KANADI (KAN) in cucumber fruit spine. Together, our results suggest a distinct regulatory pathway involving meristem genes and polarity regulators in multicellular trichome development in cucumber.

ORGANISM(S): Cucumis sativus

PROVIDER: GSE49607 | GEO | 2014/07/01

SECONDARY ACCESSION(S): PRJNA214462

REPOSITORIES: GEO

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Project description:Purpose: Plant trichomes are hair-like protuberances developing from epidermal cells of most terrestrial plants, serve as an excellent system for analyzing the molecular mechanisms underlying cell fate choices, cell cycle control, and cell morphogenesis. Regulation of trichomes in arabidopsis has been well characterized. However, the mechanisms of multicellular trichomes is unclear. To further identify the genes responsible for the SlCycB2-mediated phenotype change, we compared the gene expression profiles of SlCycB2-OE and RNAi plants by RNA-seq. Methods: The transcriptomes of between SlCycB2-OE and RNAi in tomato (Solanum lycopersicum) cultivar Ailsa Craig (AC) by RNA-seq analysis were evaluated using the Illumina HiSeq™ 2500 sequencing platform. Raw sequences were filtered and the resulting sets of clean reads were used for the following analysis by Hisat2 and DEGseq software. qRT-PCR validation was performed using SYBR Green assays. Results: In this study, we determined that SlCycB2 encodes a nuclear localized protein, which is highly expressed in trichomes, stigmas, hypocotyls and stems, and induced by the light, suppressed under the dark. Transgene analysis showed that suppression of SlCycB2 could promote type III and type V trichomes formation. On the contrary, overexpression of SlCycB2 could result in nearly disappearance of all non-glandular trichomes (including type III and V), as well as the glandular ones of type I and type VI. Detection of secondary metabolites indicated that the production of monoterpene and sesquiterpene were significantly decreased in SlCycB2-OE plants, which thus caused the reduction of the defense against Prodenia litura. Transcriptome profile demonstrated that the differential expressed genes mainly participate in the biosynthesis of terpenes, cutin, suberine and wax. Furthermore, we identified several homologs of this gene in many plants, SlCycB3 in tomato, NtCycB2 in tobacco, AtCycB2 in Arabidopsis, which have similar regulatory functions in trichome formation. SlCycB2 overexpression also led to abnormal flower with the unclosed stamen, shortened style and aberrant pollen. Conclusions: The results demonstrate that SlCycB2 play a critical role in multicellular trichome formation, secondary metabolite biosynthesis, Prodenia litura defense and reproductive organ development in tomato. The similar roles of its homologs in multicellular trichome formation suggest that Solanaceous species may share common regulatory pathway.

Project description:Purpose: Cucumber (Cucumis sativus L.) is an economically important vegetable crop worldwide, and cucumber fruit spine density has an important impact on the commercial value. However, little is known about the regulatory mechanism for the fruit spine formation.In this study, the transcriptome analyses of ovaries and pericarps from numerous-spine parent and few-spine parent were conducted to identify the gene regulatory networks involved in the formation and development of numerous fruit spines in cucumber. Methods: Cucumber mRNA profiles of ovaries and pericarps from numerous-spine parent and few-spine parent were generated by deep sequencing, in triplicate, using Illumina HiSeq 4000. Then, clean data (clean reads) were obtained by removing reads containing adapters, reads containing poly-N sequences and low-quality reads from the raw data. Simultaneously, the Q20, Q30 and GC contents of the clean data were calculated. All of the downstream analyses were based on the high-quality clean data. Clean paired-end reads were mapped to the reference genome using TopHat v2.0.12 (Trapnell et al. 2012). Then, the FPKM (fragments per kilobase of transcript sequence per million base pairs sequenced) value of each gene was calculated to estimate gene expression levels (Trapnell et al. 2010). Genes with an adjusted P-value < 0.05 identified by DESeq were assigned as differentially expressed genes(DEGs). Results: We generated 42.96-57.53 million raw reads from each library, and 39.85-54.02 million clean reads were obtained after the removal of low-quality reads and adapter sequences. Among the clean reads, 79.03-80.94% were mapped to the gene database . Based on the KEGG database, pathway enrichment analysis was performed to identify significantly enriched metabolic pathways or signal transduction pathways in DEGs. Plant hormone signal transduction was significantly enriched in up-regulated genes in both F_6DBF compared with M_6DBF and F_0DAA compared with M_0DAA. Conclusions: Based on the transcriptome analysis, we excavated possible biological regulatory networks involved in the formation and development of numerous fruit spines in cucumber. This work will promote the exploration of molecular mechanisms that regulate cucumber fruit spine density.

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Transcriptome profiling reveals roles of meristem regulators and polarity genes during multicellular fruit trichome development in cucumber (Cucumis sativus L.).

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