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Floral Development Stage-Specific Transcriptomic Analysis Reveals the Formation Mechanism of Different Shapes of Ray Florets in Chrysanthemum.

ABSTRACT: The formation mechanism of different ray floret shapes of chrysanthemum (Chrysanthemum × morifolium) remains elusive due to its complex genetic background. C. vestitum, with the basic ray floret shapes of the flat, spoon, and tubular types, is considered a model material for studying ray floret morphogenesis. In this study, the flat and tubular type lines of C. vestitum at specific stages were used to investigate the key genes that regulate morphological differences in ray florets. We found that the expression levels of genes related to auxin synthesis, transport, and response were generally higher in the tubular type than in the flat type. CvARF3 was highly expressed in the flat type, while CvARF5 and CvARF6 were highly expressed in the tubular type. Additionally, the transcription levels of Class B and E genes closely related to petal development, including CvPI, CvAP3, Cvdefh21, CvSEP3, and CvCDM77, were expressed at higher levels in the tubular type than the flat type. Based on the results, it is proposed that auxin plays a key role in the development of ray florets, and auxin-related genes, especially CvARFs, may be key genes to control the morphological difference of ray florets. Simultaneously, MADS-box genes are involved in the co-regulation of ray floret morphogenesis. The results provide novel insights into the molecular mechanism of different petal type formation and lay a theoretical foundation for the directional breeding of petal type in chrysanthemums.

SUBMITTER: Pu Y

PROVIDER: S-EPMC10048392 | biostudies-literature | 2023 Mar

REPOSITORIES: biostudies-literature

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Floral Development Stage-Specific Transcriptomic Analysis Reveals the Formation Mechanism of Different Shapes of Ray Florets in Chrysanthemum.

Pu Ya Y Liao Minling M Li Junzhuo J Tian Yuankai Y Wang Zhongman Z Song Xiang X Dai Silan S

Genes 20230321 3

The formation mechanism of different ray floret shapes of chrysanthemum (Chrysanthemum × morifolium) remains elusive due to its complex genetic background. C. vestitum, with the basic ray floret shapes of the flat, spoon, and tubular types, is considered a model material for studying ray floret morphogenesis. In this study, the flat and tubular type lines of C. vestitum at specific stages were used to investigate the key genes that regulate morphological differences i ...[more]

PMID: 36981036

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Project description:BackgroundChrysanthemum morifolium is one of the most important global cut flower and pot plants, and has been cultivated worldwide. However, limited genomic resources are available and the molecular mechanisms involved in the two morphologically distinct floret developmental cycles in chrysanthemum remain unclear.ResultsThe transcriptomes of chrysanthemum ray florets, disc florets and leaves were sequenced using Illumina paired-end sequencing technology. In total, 16.9 G reads were assembled into 93,138 unigenes with an average length of 738 bp, of which 44,364 unigenes showed similarity to known proteins in the Swissprot or NCBI non-redundant protein databases. Additionally, 26,320, 22,304 and 13,949 unigenes were assigned to 54 gene ontology (GO) categories, 25 EuKaryotic Orthologous Groups (KOG) categories, and 280 Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways, respectively. A total of 1863 differentially expressed genes (DEGs) (1210 up-regulated and 653 down-regulated) were identified between ray florets and disc florets, including genes encoding transcription factors and protein kinases. GO and KEGG pathway enrichment analyses were performed on the DEGs to identify differences in the biological processes and pathways between ray florets and disc florets. The important regulatory genes controlling flower development and flower organ determination, as well as important functional genes in the anthocyanin biosynthetic pathway, were identified, of which two leucoanthocyanidin dioxygenase-encoding genes showed specific expression in ray florets. Lastly, reverse transcription quantitative PCR was conducted to validate the DEGs identified in our study.ConclusionsComparative transcriptome analysis revealed significant differences in patterns of gene expression and signaling pathways between ray florets and disc florets in Chrysanthemum morifolium. This study provided the first step to understanding the molecular mechanism of the differential development of ray florets and disc florets in chrysanthemum, and also provided valuable genomic resources for candidate genes applicable for the breeding of novel varieties in chrysanthemum.

Project description:BackgroundThe ray and disc florets on the chrysanthemum capitulum are morphologically diverse and have remarkably abundant variant types, resulting in a rich variety of flower types. An anemone shape with pigmented and elongated disk florets is an important trait in flower shape breeding of chrysanthemums. The regulatory mechanism of their anemone-type disc floret formation was not clear, thus limiting the directional breeding of chrysanthemum flower types. In this study, we used morphological observation, transcriptomic analysis, and gene expression to investigate the morphogenetic processes and regulatory mechanisms of anemone-type chrysanthemum.ResultScanning electron microscopy (SEM) observation showed that morphological differences between non-anemone-type disc florets and anemone-type disc florets occurred mainly during the petal elongation period. The anemone-type disc florets elongated rapidly in the later stages of development. Longitudinal paraffin section analysis revealed that the anemone-type disc florets were formed by a great number of cells in the middle layer of the petals with vigorous division. We investigated the differentially expressed genes (DEGs) using ray and disc florets of two chrysanthemum cultivars, 082 and 068, for RNA-Seq and their expression patterns of non-anemone-type and anemone-type disc florets. The result suggested that the CYCLOIDEA2 (CYC2s), MADS-box genes, and phytohormone signal-related genes appeared significantly different in both types of disc florets and might have important effects on the formation of anemone-type disc florets. In addition, it is noteworthy that the auxin and jasmonate signaling pathways might play a vital role in developing anemone-type disc florets.ConclusionsBased on our findings, we propose a regulatory network for forming non-anemone-type and anemone-type disc florets. The results of this study lead the way to further clarify the mechanism of the anemone-type chrysanthemum formation and lay the foundation for the directive breeding of chrysanthemum petal types.

Project description:BackgroundThe ray floret shapes referred to as petal types on the chrysanthemum (Chrysanthemum × morifolium Ramat.) capitulum is extremely abundant, which is one of the most important ornamental traits of chrysanthemum. However, the regulatory mechanisms of different ray floret shapes are still unknown. C. vestitum is a major origin species of cultivated chrysanthemum and has flat, spoon, and tubular type of ray florets which are the three basic petal types of chrysanthemum. Therefore, it is an ideal model material for studying ray floret morphogenesis in chrysanthemum. Here, using morphological, gene expression and transcriptomic analyses of different ray floret types of C. vestitum, we explored the developmental processes and underlying regulatory networks of ray florets.ResultsThe formation of the flat type was due to stagnation of its dorsal petal primordium, while the petal primordium of the tubular type had an intact ring shape. Morphological differences between the two ray floret types occurred during the initial stage with vigorous cell division. Analysis of genes related to flower development showed that CYCLOIDEA genes, including CYC2b, CYC2d, CYC2e, and CYC2f, were differentially expressed in different ray floret types, while the transcriptional levels of others, such as MADS-box genes, were not significantly different. Hormone-related genes, including SMALL AUXIN UPREGULATED RNA (SAUR), GRETCHEN HAGEN3 (GH3), GIBBERELLIN 2-BETA-DIOXYGENASE 1 (GA2OX1) and APETALA2/ETHYLENE RESPONSIVE FACTOR (AP2/ERF), were identified from 1532 differentially expressed genes (DEGs) in pairwise comparisons among the flat, spoon, and tubular types, with significantly higher expression in the tubular type than that in the flat type and potential involvement in the morphogenesis of different ray floret types.ConclusionsOur findings, together with the gene interactional relationships reported for Arabidopsis thaliana, suggest that hormone-related genes are highly expressed in the tubular type, promoting petal cell division and leading to the formation of a complete ring of the petal primordium. These results provide novel insights into the morphological variation of ray floret of chrysanthemum.

Project description:BackgroundChrysanthemum morifolium is one of the most popular ornamental crops. The capitulum, which is the main ornamental part of chrysanthemum plants, consists of ligulate marginal ray florets, an attractive corolla (petals), and radially hermaphroditic disc florets, but no stamens. In Asteraceae species, the zygomorphic ray florets evolved from the actinomorphic disc florets. During this process, the zygomorphic ligulate corolla arose and the stamens were aborted. Although molecular genetic research has clarified ray floret development to some extent, the precise molecular mechanism underlying ray floret development in chrysanthemum remained unclear.ResultsA CYC2-like gene, Cyc2CL, was cloned from C. morifolium 'Fenditan'. Subsequent analyses revealed that the alternative splicing of Cyc2CL, which occurred in the flower differentiation stage, resulted in the production of Cyc2CL-1 and Cyc2CL-2 in the apical buds. Prior to this stage, only Cyc2CL-1 was produced in the apical buds. A fluorescence in situ hybridization analysis of labeled Cyc2CL-1 and Cyc2CL-2 RNA indicated that Cyc2CL-2 was first expressed in the involucre tissue during the final involucre differentiation stage, but was subsequently expressed in the receptacle and floret primordia as the floral bud differentiation stage progressed. Moreover, Cyc2CL-2 was highly expressed in the inflorescence tissue during the corolla formation stage, and the expression remained high until the end of the floral bud differentiation stage. Furthermore, the overexpression of Cyc2CL-1 and Cyc2CL-2 in transgenic Arabidopsis inhibited stamen and petal development. Therefore, both Cyc2CL-1 and Cyc2CL-2 encode candidate regulators of petal development and stamen abortion and are important for the ray floret development in chrysanthemum.ConclusionIn this study, we characterized the alternatively spliced transcripts of the CYC2-like gene that differ subtly regarding expression and function. The data presented herein will be useful for clarifying the regulatory mechanisms associated with the CYC2-like gene and may also be important for identifying the key genes and molecular mechanisms controlling the development of ray florets in chrysanthemum.

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Floral Development Stage-Specific Transcriptomic Analysis Reveals the Formation Mechanism of Different Shapes of Ray Florets in Chrysanthemum.

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Floral Development Stage-Specific Transcriptomic Analysis Reveals the Formation Mechanism of Different Shapes of Ray Florets in Chrysanthemum.

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