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. 2024 Jun 1;25(11):6127.
doi: 10.3390/ijms25116127.

Gene Regulatory Network Controlling Flower Development in Spinach (Spinacia oleracea L.)

Yaying Ma  1   2 , Wenhui Fu  1 , Suyan Wan  2 , Yikai Li  2 , Haoming Mao  2 , Ehsan Khalid  2 , Wenping Zhang  3 , Ray Ming  2
Affiliations

Gene Regulatory Network Controlling Flower Development in Spinach (Spinacia oleracea L.)

Yaying Ma et al. Int J Mol Sci. .

Abstract

Spinach (Spinacia oleracea L.) is a dioecious, diploid, wind-pollinated crop cultivated worldwide. Sex determination plays an important role in spinach breeding. Hence, this study aimed to understand the differences in sexual differentiation and floral organ development of dioecious flowers, as well as the differences in the regulatory mechanisms of floral organ development of dioecious and monoecious flowers. We compared transcriptional-level differences between different genders and identified differentially expressed genes (DEGs) related to spinach floral development, as well as sex-biased genes to investigate the flower development mechanisms in spinach. In this study, 9189 DEGs were identified among the different genders. DEG analysis showed the participation of four main transcription factor families, MIKC_MADS, MYB, NAC, and bHLH, in spinach flower development. In our key findings, abscisic acid (ABA) and gibberellic acid (GA) signal transduction pathways play major roles in male flower development, while auxin regulates both male and female flower development. By constructing a gene regulatory network (GRN) for floral organ development, core transcription factors (TFs) controlling organ initiation and growth were discovered. This analysis of the development of female, male, and monoecious flowers in spinach provides new insights into the molecular mechanisms of floral organ development and sexual differentiation in dioecious and monoecious plants in spinach.

Keywords: Spinacia oleracea L.; dioecious; floral development; monoecious; transcriptomics.

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Conflict of interest statement

The authors declare no conflicts of interest.

Figures

Figure 1
Figure 1
Global transcriptome changes in five developmental stages of spinach female and male flowers. (A) The morphology of spinach male and female flowers in the five flowering stages. FM: floral meristem; Cp: carpel primordium; Sep: sepal primordia; Se: sepals; Ant: anther; Sty: style. (B) Transcriptional dynamics during spinach female and male flower development showing the number of DEGs at five stages. F: female; M: male; S: stage. (C) The number of up-regulated (red font) and down-regulated (green font) DEGs in female and male flower development.
Figure 2
Figure 2
Analysis and comparison of DEGs in female and male development. (A) Number of DEGs involved in phytohormone pathways in flower development. (B) Statistics of TF family members as DEGs during female and male development. (C) Gene expression patterns of MIKCc and ABCDE models of various organs of spinach. Expression values were scaled by log2(FPKM + 1), in which FPKM is fragments per kilobase of exon per million mapped reads. F: female; M: male; S: stage.
Figure 3
Figure 3
(A) Specifically expressed TFs in dioecious spinach female and male flower development. F: female; M: male; S: stage. (B) Target high-frequency DEGs regulated by floral regulators. w: the whole stage of flower development; e: the early stage of flower development; l: the late stage of flower development.
Figure 4
Figure 4
Transcriptomic profiles during the early-stage development of female, male, and monoecious axillary buds. (A) The morphology of flowers during early-stage development in female, male, and monoecious plants. (B) The chromosomal distributions of sex-biased genes in female, male, and monoecious axillary buds. (C) Number of sex-biased transcription factors. Fe: female; M: male; Mo: monoecious. (D) Expression profiles of specific DEGs of female, male, and monoecious. Expression values were scaled by log2(FPKM + 1), in which FPKM is the fragments per kilobase of exon per million mapped reads. AB: axillary bud.
Figure 5
Figure 5
Transcriptomic profiles during the mature stage development of female, male, and monoecious flowers in spinach. (A) The morphology of spinach monoecious flowers in the mature stage. (B,C) DEGs among female, male, and monoecious flowers. F: female; M: male; Mo: monoecious; S: stage. (D) Number of differentially expressed transcription factors. (E) Expression profiles of major transcription factor families. Blue line: Genes significantly expressed in monoecious mature flowers.
Figure 6
Figure 6
Validation of selected genes expression. (A,B) Relative expression levels of selected genes from RT-qPCR analysis. (C) SpTFIIB expression patterns in axillary buds of male, female, and monoecious flowers. In situ hybridization was performed with antisense and sense SpTFIIB RNA probes. Bar = 100 μm.
Figure 7
Figure 7
Key regulatory TFs throughout spinach flower development. (A) Schema depicting the key regulatory transcription factors in the flower developmental stages of flower formation, including floral primordia (S2), organ specification and differentiation (S3–4), and flower maturation (S5–6). S: stage; Red font: regulatory female TFs; blue font: regulatory male TFs. (B) Network showing organ or tissue-specific TFs during spinach flower development.
Figure 8
Figure 8
Schematic diagram of the regulatory mechanism for floral development in dioecious spinach. stp: stamen primordia; cp: carpel primordia.
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