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. 2019 Dec 12;20(1):974.
doi: 10.1186/s12864-019-6348-z.

From bud formation to flowering: transcriptomic state defines the cherry developmental phases of sweet cherry bud dormancy

Noémie Vimont  1   2   3 , Mathieu Fouché  1 , José Antonio Campoy  4   5   6 , Meixuezi Tong  3 , Mustapha Arkoun  2 , Jean-Claude Yvin  2 , Philip A Wigge  7 , Elisabeth Dirlewanger  1 , Sandra Cortijo  8 , Bénédicte Wenden  9
Affiliations

From bud formation to flowering: transcriptomic state defines the cherry developmental phases of sweet cherry bud dormancy

Noémie Vimont et al. BMC Genomics. .

Abstract

Background: Bud dormancy is a crucial stage in perennial trees and allows survival over winter to ensure optimal flowering and fruit production. Recent work highlighted physiological and molecular events occurring during bud dormancy in trees. However, they usually examined bud development or bud dormancy in isolation. In this work, we aimed to further explore the global transcriptional changes happening throughout bud development and dormancy onset, progression and release.

Results: Using next-generation sequencing and modelling, we conducted an in-depth transcriptomic analysis for all stages of flower buds in several sweet cherry (Prunus avium L.) cultivars that are characterized for their contrasted dates of dormancy release. We find that buds in organogenesis, paradormancy, endodormancy and ecodormancy stages are defined by the expression of genes involved in specific pathways, and these are conserved between different sweet cherry cultivars. In particular, we found that DORMANCY ASSOCIATED MADS-box (DAM), floral identity and organogenesis genes are up-regulated during the pre-dormancy stages while endodormancy is characterized by a complex array of signalling pathways, including cold response genes, ABA and oxidation-reduction processes. After dormancy release, genes associated with global cell activity, division and differentiation are activated during ecodormancy and growth resumption. We then went a step beyond the global transcriptomic analysis and we developed a model based on the transcriptional profiles of just seven genes to accurately predict the main bud dormancy stages.

Conclusions: Overall, this study has allowed us to better understand the transcriptional changes occurring throughout the different phases of flower bud development, from bud formation in the summer to flowering in the following spring. Our work sets the stage for the development of fast and cost effective diagnostic tools to molecularly define the dormancy stages. Such integrative approaches will therefore be extremely useful for a better comprehension of complex phenological processes in many species.

Keywords: Prediction; Prunus avium L.; RNA sequencing; Seasonal timing; Time course; Transcriptomic.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Dormancy status under environmental conditions and RNA-seq sampling dates. a Evaluation of bud break percentage under forcing conditions was carried out for three sweet cherry cultivars displaying different flowering dates: ‘Cristobalina’, ‘Garnet’ and ‘Regina’ for the early, medium and late flowering cultivars, respectively. The dashed and dotted lines correspond to the dormancy release date, estimated at 50% of buds at BBCH stage 53 [35], and the flowering date, respectively. b Pictures of the sweet cherry buds corresponding to the different sampling dates. c Sampling time points for the transcriptomic analysis are represented by coloured stars. Red for ‘Cristobalina, green for ‘Garnet’ and blue for ‘Regina’
Fig. 2
Fig. 2
Separation of samples by dormancy stage using differentially expressed genes . The principal component analysis was conducted on the TPM (transcripts per millions reads) values for the differentially expressed genes in the cultivar ‘Garnet’ flower buds, sampled on three trees between July and March. Samples in organogenesis are red points, samples in paradormancy are yellow points, samples in endodormancy are dark blue points, samples at dormancy release are light blue points and samples in ecodormancy are green points. Each point corresponds to one sampling time in a single tree
Fig. 3
Fig. 3
Clusters of expression patterns for differentially expressed genes in the sweet cherry cultivar ‘Garnet’. Heatmap for ‘Garnet’ differentially expressed genes during bud development. Each column corresponds to the gene expression for flower buds from one single tree at a given date. Each row corresponds to the expression pattern across samples for one gene. Clusters of genes are ordered based on the chronology of the expression peak (from earliest – July, 1-dark green cluster – to latest – March, 9 and 10). Expression values were normalized and z-scores are represented here
Fig. 4
Fig. 4
Enrichments in gene ontology terms for biological processes and average expression patterns in the different clusters in the sweet cherry cultivar ‘Garnet’. a Using the topGO package [36], we performed an enrichment analysis on GO terms for biological processes based on a classic Fisher algorithm. Enriched GO terms with the lowest p-value were selected for representation. Dot size represents the number of genes belonging to the clusters associated with the GO term. b Average z-score values for each cluster. The coloured dotted line corresponds to the estimated date of dormancy release
Fig. 5
Fig. 5
Expression patterns of key genes involved in sweet cherry bud dormancy. Expression patterns, expressed in transcripts per million reads (TPM) were analysed for the cultivar ‘Garnet’ from August to March, covering bud organogenesis (O), paradormancy (P), endodormancy (Endo), and ecodormancy (Eco). Dash lines represent the estimated date of dormancy release
Fig. 6
Fig. 6
Separation of samples by dormancy stage and cultivar using differentially expressed genes. The principal component analysis was conducted on the TPM (transcripts per millions reads) values for the differentially expressed genes in the flower buds of the cultivars ‘Cristobalina’ (filled squares), ‘Garnet’ (empty circles) and ‘Regina’ (stars). Samples in organogenesis are red points, samples in paradormancy are yellow points, samples in endodormancy are dark blue points, samples at dormancy release are light blue points and samples in ecodormancy are green points. Each point corresponds to one sampling time in a single tree
Fig. 7
Fig. 7
Expression patterns in the ten clusters for the three cultivars. Expression patterns were analysed from August to March, covering bud organogenesis (O), paradormancy (P), endodormancy (Endo), and ecodormancy (Eco). Dash lines represent the estimated date of dormancy release, in red for ‘Cristobalina’, green for ‘Garnet’ and blue for ‘Regina’. Average z-score patterns (line) and standard deviation (ribbon), calculated using the TPM values from the RNA-seq analysis, for the genes belonging to the ten clusters
Fig. 8
Fig. 8
Expression patterns for the seven marker genes in the three cultivars. Expression patterns were analysed from August to March, covering bud organogenesis (O), paradormancy (P), endodormancy (Endo), and ecodormancy (Eco). Dash lines represent the estimated date of dormancy release, in red for ‘Cristobalina’, green for ‘Garnet’ and blue for ‘Regina’. TPM were obtained from the RNA-seq analysis for the seven marker genes from clusters 1, 4, 5, 7, 8, 9 and 10. Lines represent the average TPM, dots are the actual values from the biological replicates. SRP: STRESS RESPONSIVE PROTEIN; TCX2: TESMIN/TSO1-like CXC 2; CSLG3: Cellulose Synthase like G3; GH127: Glycosyl Hydrolase 127; PP2C: Phosphatase 2C; UDP-GalT1: UDP-Galactose transporter 1; MEE9: maternal effect embryo arrest 9
Fig. 9
Fig. 9
Expression for the seven marker genes allows accurate prediction of the bud dormancy stages in the late flowering cultivar ‘Fertard’ during two bud dormancy cycles. a Relative expressions were obtained by RT-qPCR and normalized by the expression of two reference constitutively expressed genes PavRPII and PavEF1. Data were obtained for two bud dormancy cycles: 2015/2016 (orange lines and symbols) and 2017/2018 (blue lines and symbols). b Evaluation of the dormancy status in ‘Fertard’ flower buds during the two seasons using the percentage of open flower buds (BBCH stage 53). c Predicted vs experimentally estimated bud stages. SRP: STRESS RESPONSIVE PROTEIN; TCX2: TESMIN/TSO1-like CXC 2; CSLG3: Cellulose Synthase like G3; GH127: Glycosyl Hydrolase 127; PP2C: Phosphatase 2C; UDP-GalT1: UDP-Galactose transporter 1; MEE9: maternal effect embryo arrest 9
Fig. 10
Fig. 10
From bud formation to flowering: transcriptomic regulation of flower bud dormancy. Our results highlighted seven main expression patterns corresponding to the main dormancy stages. During organogenesis and paradormancy (July to September), signalling pathways associated with flower organogenesis and ABA signalling are upregulated. Distinct groups of genes are activated during different phases of endodormancy, including targets of transcription factors involved in ABA signalling, cold response and circadian clock. ABA: abscisic acid
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