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. 2022 Apr 29;23(9):4968.
doi: 10.3390/ijms23094968.

Characteristics of microRNAs and Target Genes in Maize Root under Drought Stress

Qi Tang  1   2   3 , Haozhe Lv  1   2   3 , Qimeng Li  1   2   3 , Xiaoyue Zhang  1   2   3 , Le Li  1   2   3 , Jie Xu  1   2   3 , Fengkai Wu  1   2   3 , Qingjun Wang  1   2   3 , Xuanjun Feng  1   2   3 , Yanli Lu  1   2   3
Affiliations

Characteristics of microRNAs and Target Genes in Maize Root under Drought Stress

Qi Tang et al. Int J Mol Sci. .

Abstract

Maize (Zea mays) is an important multi-functional crop. The growth and yield of maize are severely affected by drought stress. Previous studies have shown that microRNAs (miRNAs) in maize play important roles in response to abiotic stress; however, their roles in response to drought stress in maize roots is unclear. In our study, we found 375 miRNAs in the roots of 16 inbred lines. Of the 16 lines, zma-MIR168, zma-MIR156, and zma-MIR166 were highly expressed, whereas zma-MIR399, zma-MIR2218, and zma-MIR2275 exhibited low expression levels. The expression patterns of miRNA in parental lines and their derived RILs are different. Over 50% of miRNAs exhibited a lower expression in recombinant inbred lines than in parents. The expression of 50 miRNAs was significantly altered under water stress (WS) in at least three inbred lines, and the expression of miRNAs in drought-tolerant lines changed markedly. To better understand the reasons for miRNA response to drought, the degree of histone modifications for miRNA genes was estimated. The methylation level of H3K4 and H3K9 in miRNA precursor regions changed more noticeably after WS, but no such phenomenon was seen for DNA methylation and m6A modification. After the prediction of miRNA targets using psRNATarget and psRobot, we used correlation analysis and qRT-PCR to further investigate the relationship between miRNAs and target genes. We found that 87 miRNA-target pairs were significantly negatively correlated. In addition, a weighted gene co-expression network analysis using miRNAs, as well as their predicted targets, was conducted to reveal that miR159, miR394, and miR319 may be related to maize root growth. The results demonstrated that miRNAs might play essential roles in the response to drought stress.

Keywords: drought stress; maize; miRNA; root; target genes.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
The composition and length distribution of miRNAs identified in maize root. (A) Composition of the identified known miRNAs. (B) Secondary structures of some novel miRNAs. (C) Length distribution of the identified miRNAs. Known, known miRNAs; Novel, novel miRNAs. (D) Venn diagram of parent miRNAs and RIL miRNAs in WW and WS (right); Venn diagram of drought-tolerant miRNAs and drought-sensitive miRNAs in WW and WS (left). The text in the Venn diagram depicts the proportion of miRNAs.
Figure 2
Figure 2
Expression analysis of miRNAs identified in maize root. (A) Distribution of identified miRNA expression in WW and WS. (B) Expression of miRNA families in WW and WS treatments. (C) Expression variation of miRNA families in 16 materials. (D) Expression of miRNAs between parents and RILs. We standardized the expression of miRNAs in 14 RILs. X-axis, values of the expression of RILs minus AC7643 (DT); Y-axis, values of the expression of RILs minus AC7729/TZSRW (DS).
Figure 3
Figure 3
Differential expression of identified miRNAs in maize root. (A) Log2 fold change of miRNAs under WS. Down-Regulated means log2 fold change < −1; Up-Regulated means log2 fold change > 1; Not-Significant, −1≤ log2 fold change ≤ 1. (B) The difference in miRNA expression and log2 fold change between drought-tolerant and drought-sensitive lines. DT, drought-tolerant; DS, drought-sensitive. * for p-value ≤ 0.05, ** for p-value ≤ 0.01. (C) The number of miRNA precursors with epigenetics modification. Chi-square test, * for p-value ≤ 0.05, ** for p-value ≤ 0.01.
Figure 4
Figure 4
The analysis of negatively correlated miRNA/target pairs. (A) The location of miRNA target sites on targets. Chi-square test, ** for p-value ≤ 0.01. (B,C) The target expression and log2 fold change of different miRNA binding site. (D) Fold change distribution of negatively correlated miRNA/target pairs. (E) Comparison of expression and log2 fold change between target genes and other genes. Target, miRNA target genes; Not_Target, the genes were not miRNA target genes. (F) The real-time PCR analysis of expression of miRNAs and targets in AC7643. The expression of each gene in plants grown in WW was set to 1. Y-axis means the relative expression of each gene in plants grown in WS. Data are shown as mean ± SD (n = 3) of three independent biological replicates. From left to right, the target genes are Zm00001d003518, Zm00001d048527, Zm00001d053589, and Zm00001d053545.
Figure 5
Figure 5
Co-expression network analysis in well water and water stress treatments. (A) Network visualization in Cytoscape. The nodes were colored by module membership. (B) Correlations between module eigengenes and root phenotypic traits. The numbers within the heatmap represent correlations and p-value (red, positively correlated; green, negatively correlated) for the module–trait associations (SDW, shoot dry weight; SFW, shoot fresh weight; RL, root length; TRL, total root length; Tips, root branches; Forks, root forks; RSA, root surface area; RV, root volume). (C) The connection between zma-miR394b precursor expression and total dry weight. On the left is the root phenotype of some lines from a natural group containing 368 lines. Red means that the expression of zma-miR394b precursor is higher (right).
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