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. 2022 Jul 25:13:945379.
doi: 10.3389/fpls.2022.945379. eCollection 2022.

Integrative analysis of transcriptome and miRNAome reveals molecular mechanisms regulating pericarp thickness in sweet corn during kernel development

Caiyun Xiong  1 , Hu Pei  1 , Yahui Zhang  1 , Wenchuang Ren  1 , Ziwei Ma  1 , Yunqi Tang  1 , Jun Huang  1
Affiliations

Integrative analysis of transcriptome and miRNAome reveals molecular mechanisms regulating pericarp thickness in sweet corn during kernel development

Caiyun Xiong et al. Front Plant Sci. .

Abstract

Pericarp thickness affects the edible quality of sweet corn (Zea mays L. saccharata Sturt.). Therefore, breeding varieties with a thin pericarp is important for the quality breeding of sweet corn. However, the molecular mechanisms underlying the pericarp development remain largely unclear. We performed an integrative analysis of mRNA and miRNA sequencing to elucidate the genetic mechanism regulating pericarp thickness during kernel development (at 15 days, 19 days, and 23 days after pollination) of two sweet corn inbred lines with different pericarp thicknesses (M03, with a thinner pericarp and M08, with a thicker pericarp). A total of 2,443 and 1,409 differentially expressed genes (DEGs) were identified in M03 and M08, respectively. Our results indicate that phytohormone-mediated programmed cell death (PCD) may play a critical role in determining pericarp thickness in sweet corn. Auxin (AUX), gibberellin (GA), and brassinosteroid (BR) signal transduction may indirectly mediate PCD to regulate pericarp thickness in M03 (the thin pericarp variety). In contrast, abscisic acid (ABA), cytokinin (CK), and ethylene (ETH) signaling may be the key regulators of pericarp PCD in M08 (the thick pericarp variety). Furthermore, 110 differentially expressed microRNAs (DEMIs) and 478 differentially expressed target genes were identified. miRNA164-, miRNA167-, and miRNA156-mediated miRNA-mRNA pairs may participate in regulating pericarp thickness. The expression results of DEGs were validated by quantitative real-time PCR. These findings provide insights into the molecular mechanisms regulating pericarp thickness and propose the objective of breeding sweet corn varieties with a thin pericarp.

Keywords: kernel development; miRNAome; pericarp thickness; sweet corn; transcriptome.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
SEM analyses of the changes in pericarp thickness between M03 and M08. (A) The pericarp thickness of M03 at 15 (A1), 19 (A2), and 23 (A3) DAP. (B) The pericarp thickness of M08 at 15 (B1), 19 (B2), and 23 (B3) DAP. (C) The changes in pericarp thickness in sweet corn lines M03 and M08. Asterisks indicate significant differences between M03 and M08 lines using Student’s t-test; *P < 0.05; ***P < 0.001.
FIGURE 2
FIGURE 2
Differentially expressed genes and miRNAs at different stages during kernel development. (A) The numbers of upregulated and downregulated DEGs (A1) and DEMIs (A2) in the different comparison groups. (B) Venn diagrams of DEGs in the M03 (B1), M08 (B2), and M03M08 (B3) groups. (C) Venn diagrams of DEMIs in the M03 (C1), M08 (C2), and M03M08 (C3) groups.
FIGURE 3
FIGURE 3
Cystoscope regulatory networks of DEMIs and DEGs. Yellow graphics represent miRNAs, and pink graphics represent genes.
FIGURE 4
FIGURE 4
GO annotation and KEGG pathway enrichment analyses of target genes. (A) GO annotation. GO terms were classified into three categories: biological process (BP), cellular component (CC), and molecular function (MF). (B) KEGG pathway analysis.
FIGURE 5
FIGURE 5
GO and KEGG pathway analysis of DEGs. (A) GO annotation of DEGs. In each block of the heatmap, the number represents the gene numbers, and the red coloring represents a P-value of ≤0.05. (B) KEGG pathway analysis of DEGs. GO terms and KEGG pathway enrichment with P-value ≤ 0.05 were identified as significantly enriched.
FIGURE 6
FIGURE 6
Heatmaps of DEGs and corresponding DEMIs in important pathways. (A) Plant hormone signal transduction. (B) MAPK signaling pathway. (C) Starch and sucrose metabolism. (D) Terpenoid backbone biosynthesis. (E) Glycine, serine, and threonine metabolism.
FIGURE 7
FIGURE 7
Heatmap of differentially expressed TFs and their corresponding DEMIs.
FIGURE 8
FIGURE 8
Validation of eight DEGs using RT-qPCR. Error bars represent the standard deviation of three replicates. Heatmaps were generated using transcriptome data; red indicates high expression levels, and green indicates low expression levels. Lowercase letters above the columns represent statistical differences with the same inbred line (P < 0.05).
FIGURE 9
FIGURE 9
Hypothetical mechanisms regulating sweet corn pericarp thickness.
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