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. 2020 Jul 20;21(14):5107.
doi: 10.3390/ijms21145107.

An Integrative Analysis of Transcriptome, Proteome and Hormones Reveals Key Differentially Expressed Genes and Metabolic Pathways Involved in Flower Development in Loquat

Danlong Jing  1   2 , Weiwei Chen  1   2 , Ruoqian Hu  2 , Yuchen Zhang  2 , Yan Xia  1   2 , Shuming Wang  1   2 , Qiao He  1   2 , Qigao Guo  1   2 , Guolu Liang  1   2
Affiliations

An Integrative Analysis of Transcriptome, Proteome and Hormones Reveals Key Differentially Expressed Genes and Metabolic Pathways Involved in Flower Development in Loquat

Danlong Jing et al. Int J Mol Sci. .

Abstract

Flower development is a vital developmental process in the life cycle of woody perennials, especially fruit trees. Herein, we used transcriptomic, proteomic, and hormone analyses to investigate the key candidate genes/proteins in loquat (Eriobotrya japonica) at the stages of flower bud differentiation (FBD), floral bud elongation (FBE), and floral anthesis (FA). Comparative transcriptome analysis showed that differentially expressed genes (DEGs) were mainly enriched in metabolic pathways of hormone signal transduction and starch and sucrose metabolism. Importantly, the DEGs of hormone signal transduction were significantly involved in the signaling pathways of auxin, gibberellins (GAs), cytokinin, ethylene, abscisic acid (ABA), jasmonic acid, and salicylic acid. Meanwhile, key floral integrator genes FLOWERING LOCUS T (FT) and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 (SOC1) and floral meristem identity genes SQUAMOSA PROMOTER BINDING LIKE (SPL), LEAFY (LFY), APETALA1 (AP1), and AP2 were significantly upregulated at the FBD stage. However, key floral organ identity genes AGAMOUS (AG), AP3, and PISTILLATA (PI) were significantly upregulated at the stages of FBE and FA. Furthermore, transcription factors (TFs) such as bHLH (basic helix-loop-helix), NAC (no apical meristem (NAM), Arabidopsis transcription activation factor (ATAF1/2) and cup-shaped cotyledon (CUC2)), MYB_related (myeloblastosis_related), ERF (ethylene response factor), and C2H2 (cysteine-2/histidine-2) were also significantly differentially expressed. Accordingly, comparative proteomic analysis of differentially accumulated proteins (DAPs) and combined enrichment of DEGs and DAPs showed that starch and sucrose metabolism was also significantly enriched. Concentrations of GA3 and zeatin were high before the FA stage, but ABA concentration remained high at the FA stage. Our results provide abundant sequence resources for clarifying the underlying mechanisms of the flower development in loquat.

Keywords: Eriobotrya japonica; flower development; regulatory pathways; transcription factor; transcriptome.

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Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Figure 1
Figure 1
Morphological changes of flower development in loquat (excellent triploid line ‘CB-1 Q11’). (S1) Vegetative apex. (S2) Floral meristem initiation and flower bud differentiation. (S3) Rapid differentiation of floral buds. (S4) Panicle elongation. (S5) Floral bud elongation with visible floral buds. (S6) Elongation of branches in a panicle. (S7) White corollas of floral buds. (S8) Floral anthesis and full bloom. (S9) Petal fall.
Figure 2
Figure 2
Numbers of differentially expressed genes (DEGs) involved in phase changes during flower development of flower bud differentiation (FBD), floral bud elongation (FBE) and floral anthesis (FA). (A) The numbers of DEGs in FBE vs. FBD, FA vs. FBE and FA vs. FBD. (B) The numbers of upregulated DEGs in FBE vs. FBD and FA vs. FBE. (C) The numbers of downregulated DEGs in FBE vs. FBD and FA vs. FBE.
Figure 3
Figure 3
Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analysis of DEGs. (A) Enrichment analysis of DEGs for floral bud elongation (FBE) vs. flower bud differentiation (FBD). The pathway of plant hormone signal transduction was mainly enriched (black arrow). (B) Enrichment analysis of DEGs for floral anthesis (FA) vs. FBE. The pathways of plant hormone signal transduction (black arrow) and starch and sucrose metabolism (green arrow) were mainly enriched. Rich factor is a ratio of the number of DEGs annotated with a pathway relative to the total number of genes annotated with this pathway. The larger value of the rich factor represented, the greater the enrichment of this KEGG pathway.
Figure 4
Figure 4
Expression level changes of the DEGs involved in the auxin, gibberellin (GA), and cytokinin signaling and metabolism pathways in three flower development stages in loquat. (A) Expression levels of DEGs of auxin signaling pathways. (B) Expression levels of DEGs of GA signaling and metabolism pathways. (C) Expression levels of DEGs of cytokinin signaling pathways.
Figure 5
Figure 5
Expression level changes of the DEGs involved in the ethylene-, abscisic acid (ABA)-, jasmonic acid (JA)-, and salicylic acid (SA)-signaling pathways. (A) Expression levels of DEGs of ethylene signaling pathways. (B) Expression levels of DEGs of ABA signaling pathways. (C) Expression levels of DEGs of JA signaling pathways. (D) Expression levels of DEGs of SA signaling pathways.
Figure 6
Figure 6
Expression changes of the genes involved in flowering-related pathways, floral integrator, floral meristem identity, and floral organ identity in flower development. (A) Expression levels of DEGs involved in flowering-related pathways. (B) Expression levels of DEGs encoding SPLs. (C) Expression levels of DEGs involved in floral integrator, floral meristem identity, and floral organ identity.
Figure 7
Figure 7
Gene Ontology (GO) enrichment analysis of the identified proteins.
Figure 8
Figure 8
Correlation for proteome and transcriptome, differentially accumulated proteins (DAPs), and DEGs of FBE vs. FBD, FA vs. FBE, and FA vs. FBD. (A–C) Correlation for proteome and transcriptome of FBE vs. FBD, FA vs. FBE, and FA vs. FBD. (D–F) Correlation for DAPs and DEGs of FBE vs. FBD, FA vs. FBE, and FA vs. FBD.
Figure 9
Figure 9
Combined enrichment of proteome and transcriptome in FBE vs. FBD, FA vs. FBE, and FA vs. FBD. (A) Combined enrichment of proteome and transcriptome in FBE vs. FBD. (B) Combined enrichment of proteome and transcriptome in FA vs. FBE. (C) Combined enrichment of proteome and transcriptome in FA vs. FBD. Starch and sucrose metabolism is marked by red arrows.
Figure 10
Figure 10
Validation of the expression of flower development-related genes by qRT-PCR analysis. Bar charts indicate values of qRT-PCR. Line plots indicate values of fragments per kilobase per million (FPKM). Error bars indicate the standard deviation of three biological replicates.
Figure 11
Figure 11
Changes in GA3, zeatin (ZT), and ABA concentrations during flower development. (A) GA3 concentration. (B) ZT concentration. (C) ABA concentration. Significant differences are indicated by different letters (p < 0.05).
Figure 12
Figure 12
Schematic of the regulatory genes and metabolic pathways in flower development in loquat.
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