Comprehensive analysis of the longan transcriptome reveals distinct regulatory programs during the floral transition

Abstract

Background: Longan (Dimocarpus longan Lour.) is an important fruit tree in the subtropical regions of Southeast Asia and Australia. Among the factors affecting D. longan fruit yield, the difficulty and instability of blossoming is one of the most challenging issues. Perpetual flowering (PF) is a crucial trait for fruit trees and is directly linked to production potential. Therefore, studying the molecular regulatory mechanism of longan PF traits is crucial for understanding and solving problems related to flowering. In this study, comparative transcriptome analysis was performed using two longan cultivars that display opposite flowering phenotypes during floral induction.

Results: We obtained 853.72 M clean reads comprising 125.08 Gb. After comparing these data with the longan genome, 27,266 known genes and 1913 new genes were detected. Significant differences in gene expression were observed between the two genotypes, with 6150 and 6202 differentially expressed genes (DEGs) for 'SJ' and 'SX', respectively. The transcriptional landscape of floral transition at the early stage was very different in these two longan genotypes with respect to key hormones, circadian rhythm, sugar metabolism, and transcription factors. Almost all flowering-related DEGs identified are involved in photoperiod and circadian clock pathways, such as CONSTANS-like (COL), two-component response regulator-like (APRRs), gigantea (GI), and early flowering (EFL). In addition, the leafy (LFY) gene, which is the central floral meristem identity gene, may inhibit PF formation in 'SJ'.

Conclusion: This study provides a platform for understanding the molecular mechanisms responsible for changes between PF and seasonal flowering (SF) longan genotypes and may benefit studies on PF trait mechanisms of evergreen fruit trees.

Keywords: Comprehensive transcriptome analysis; Floral transition; Longan; Perpetual flowering.

Fig. 1

Different flowering phenotypes and number of differentially expressed genes during floral induction in ‘SJ’ and ‘SX’ longan. a Different flowering traits of ‘SJ’ and ‘SX’. ‘SJ’ longan blossoms continuously; both terminal and axillary shoots can differentiate into inflorescences, and flowers and fruits can be observed at the same time on one tree. T1 represents the dormant stage (before the emergence of floral primordia), T2 represents the emergence of floral primordium stage, and T3 represents the floral organ formation stage. The red arrows represent comparisons conducted in quantitative analyses. The numbers by the arrows denote the number differentially expressed genes for the specified comparison. b Venn diagram showing the number of DEGs between ‘SJ’ and ‘SX’ longan during the floral induction process. c Venn diagram showing the number of DEGs during floral induction in ‘SJ’. d Venn diagram showing the number of DEGs during floral induction in ‘SX’

Fig. 2

Trend analysis of DEGs with significant changes in expression profiles and KEGG pathway enrichment analysis for ‘SJ’ (a) and ‘SX’ (b). Genes coding for unknown products were not considered in the analysis. Enriched KEGG pathways are listed to the right of each profile

Fig. 3

Expression profiles of sugar-related genes and qRT-PCR identification of sugar-related gene expression levels in flower buds during the floral induction process in ‘SJ’ and ‘SX’ longan. a Heat map of the comparative expression levels of sugar-related genes. Data for gene expression levels were normalized by the Z-score. Red and blue indicate up- and downregulated genes, respectively. b qRT-PCR identification of sugar-related gene expression levels in buds. The bar and line graphs are derived from RNA-Seq and qRT-PCR data, respectively. Values are the means of three replicates ± SE

Fig. 4

Expression profiles of hormone-related genes and qRT-PCR identification of hormone-related gene expression levels in flower buds during the floral induction process in ‘SJ’ and ‘SX’ longan. a Heat map of the comparative expression level of hormone-related genes. Data for gene expression levels were normalized by the Z-score. Red and blue indicate up- and downregulated genes, respectively. b qRT-PCR identification of hormone-related gene expression levels in buds. The bar and line graphs are derived from RNA-Seq and qRT-PCR data, respectively. Values are the means of three replicates ± SE

Fig. 5

Expression profiles of flower-related genes and qRT-PCR identification of flower-related gene expression levels in flower buds during the floral induction process in ‘SJ’ and ‘SX’ longan. a Heat map of the comparative expression level of flower-related genes. Data for gene expression levels were normalized by the Z-score. Red and blue indicate up- and downregulated genes, respectively. b qRT-PCR identification of flower-related gene expression levels in buds. The bar and line graphs are derived from RNA-Seq and qRT-PCR data, respectively. Values are the means of three replicates ± SE

Fig. 6

Expression profiles of transcription factor-related genes and qRT-PCR identification of transcription factor-related gene expression levels in flower buds during the floral induction process in ‘SJ’ and ‘SX’ longan. (a) Heat map of the comparative expression level of transcription factor-related genes. Data for gene expression levels were normalized by the Z-score. Red and blue indicate up- and downregulated genes, respectively. b qRT-PCR identification of transcription factor-related gene expression levels in buds. The bar and line graphs are derived from RNA-Seq and qRT-PCR data, respectively. Values are the means of three replicates ± SE

Fig. 7

Summary of transcriptional-level regulation of longan PF trait formation