Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (6): 1034-1048.doi: 10.3864/j.issn.0578-1752.2024.06.002

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Analysis of Transposable Element Associated Epigenetic Regulation under Drought in Maize

GAO ChenXi(), HAO LuYang, HU Yue, LI YongXiang, ZHANG DengFeng, LI ChunHui, SONG YanChun, SHI YunSu, WANG TianYu, LI Yu(), LIU XuYang()   

  1. Institute of Crop Sciences, Chinese Academy of Agricultural Sciences/State Key Laboratory of Crop Gene Resources and Breeding, Beijing 100081
  • Received:2023-08-30 Accepted:2023-10-23 Online:2024-03-16 Published:2024-03-25
  • Contact: LI Yu, LIU XuYang

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Abstract:

【Objective】 Drought is one of the serious abiotic stresses influencing maize production worldwide. Understanding the molecular mechanisms underlying drought tolerance is of great importance in maize improvement. 【Method】 In the present study, representative maize inbred lines were selected for field drought experiment and the drought tolerance was estimated based on leaf relative water content and anthesis-silking interval. Two inbred lines with contrasting drought tolerance was used for genome resequencing and transposable element insertions were identified. The DNA methylation level of leaf and root tissues under different water treatments of the two lines were measured using Whole Genome Bisulfite Sequencing (WGBS). And the gene expression profiles of these samples were detected by RNA sequencing. The integrative atlas of transposable element insertion/deletion variants, differentially methylated regions and differentially expressed genes in the two lines were constructed. In addition, the transposable element insertion/deletion variant mediated epigenetic regulation of ZCN7, which has been conferred the drought tolerance function in our previous study, was analyzed. 【Result】 The field experiment showed inbred line H082183 showed highest drought tolerance, in which the leaf relative water content and anthesis-silking interval had no significant difference between drought and well-watered treatments. While the Lü28 displayed lowest leaf relative water content and largest anthesis-silking interval under drought. Thus, these two lines were selected for further analysis. A total of 333 754 and 333 296 transposable element insertions were identified in the genome of H082183 and Lü28, respectively. And 89 954 transposable element insertions were polymorphism between two lines. The transposable element insertions, introns and promoters showed higher CG and CHG methylation level than exons and untranslated regions. Furthermore, 41 352 differentially methylated regions were identified between H082183 and Lü28. And 60% of the differentially methylated regions were located in the transposable element insertion\deletion variants and 5 kb flanking regions. The gene expression level showed negatively correlated with CG and CHG methylation. Differentially expression analysis between H082183 and Lü28 obtained 4 196 and 3 500 differentially expressed genes in leaf and root under drought, respectively. The 19.5% and 19.7% of these differentially expressed genes were located in differentially methylated regions. Three LTR transposable element insertions were identified in the 34 kb region of ZCN7 in Lü28 but absent in the genome H082183. And the DNA methylation levels of CG and CHG in this genomic region were significantly higher in Lü28 than H082183 under both drought and well-watered environments, which conferred higher ZCN7 expression in the drought tolerant line H082183. 【Conclusion】 Our results highlight the important role of interplay of transposable element insertions, DNA methylation and gene expression under drought. And gene expression regulation mechanism of ZCN7 relied on the transposable element insertion/deletion variants mediated DNA methylation was proposed.

Key words: maize (Zea mays L.), drought tolerance, transposable element, DNA methylation, transcriptome

Fig. 1

Drought tolerance-related phenotype and genomic distribution of variable transposable element insertions and DNA methylation levels A: The leaf relative water content performance of eight lines in different water treatments. *: P<0.05, **: P<0.01; NS: No significant difference. WS and WW are drought and well-watered treatments, respectively. B: The anthesis-silking interval of eight lines in different water treatments. C: The genomic distribution of transposable element (TE) insertion presence/absence variations (PAVs), methylation levels and differentially methylated regions (DMRs) in 3 Mb size sliding widow were plotted. The blue bars and lines were for H082183, and the red ones were for Lü28"

Table 1

Transposable element insertions of each superfamily in H082183 and Lü28 genomes"

转座子分类
Subclass		 转座子家族
Superfamily		 简写代码
Code		 H082183基因组数量
No. in H082183 genome		 旅28基因组数量
No. in Lü28 genome		 2个基因组共有数量
No. in both genomes
Retrotransposons
LTR Copia RLC 123957 121858 108237
Gypsy RLG 170353 165861 140809
Unkown LTR RLX 26778 25969 21611
LINE L1 RIL 1545 1529 1306
RTE RIT 600 570 502
SINE RST RST 638 575 439
DNA transposons
TIR hAT DTA 14696 13966 11300
CACTA DTC 22130 21366 17714
PIF-Harbinger DTH 5295 4965 3671
Mutator DTM 6197 5915 4967
Tc1-Mariner DTT 542 526 352
Helitron Helitron DHH 3621 3451 2803

Fig. 2

DNA methylation levels in different genomic regions A: The average percentage of CG, CHG and CHH methylation sites in all methylation C sites of all libraries. B-D show the methylation levels of the CG (B), CHG (C) and CHH (D) contexts in terms of different genomic regions. L_HC and L_HD mean leaf of H082183 under control and drought, respectively. L_LC and L_LD mean leaf of Lü28 under control and drought, respectively. R_HC, R_HD, R_LC and R_LD are the corresponding samples of root. The same as below"

Fig. 3

DNA methylation levels around transposable element and differentially methylated regions A: Genome wide distribution of CG and CHG methylation levels in relation to the transposable element insertion. The X-axis is 100 kb flanking regions of transposable element insertion sites and Y-axis is density of normalized scores of average methylation levels. B: The total numbers of differentially methylated regions (DMRs) detected in leaf or root between H082183 and Lü28. C: The proportions of DMRs identified in genes, 2 kb upstream promoters or intergenic regions. D: The proportions of differentially methylated regions located in transposable element insertion (TEI) PAVs, 5 kb flank regions of TEI PAVs or other regions"

Fig. 4

Comparison analysis of differentially methylated regions and differentially expressed genes A: Distribution of methylation levels with genes in different expression levels. The different methylation levels were defined based on the Quartile1 (Q1, 25%) and Quartile3 (Q3, 75%) of the distribution of gene expression. B: Correlation of CG/CHG methylation differences with gene expression differences. C: Differentially expressed genes associated with methylation variation under drought. The overlap of genotypic differentially expressed genes and differentially methylated regions in leaf or root. The mH+ presents the mCG or mCHG methylation level were higher in H082183 and vice versa. The eH+ presents gene showed higher expression level in H082183 under drought and vice versa. D: GO analysis of the differentially expressed genes associated with differentially methylated regions. The top five most significant GO terms are showed"

Fig. 5

Expression levels of DNA methyltransferase and demethylase genes ** and * represent significant level of FDR<0.01 and FDR<0.05, respectively. The ns means non-significant. The H and L in x-axis are H082183 and Lü28, and D and C are drought and well-watered control treatments, respectively"

Fig. 6

Transposable element insertion associated epigenetic regulation of ZCN7 A: The transposable element insertions and DNA methylation near ZCN7. The dots present single base CG and CHG methylation levels. The green dots revealed higher methylation in Lü28 and orange dot showed higher methylation in H082183. The pink regions present regions with higher methylation in Lü28 and the green regions were higher methylated in H082183. B: The gene expression of ZCN7 in H082183 and Lü28 obtained by RNA-Seq. C: The gene expression of ZCN7 based on another indipendant experiment using RT-qPCR. D: The co-expressed genes with ZCN7 in maize leaves. The gene co-expression networks were constructed using WGCNA and the top 30 genes that were co-expressed with ZCN7 were shown. E: The transposable element insertion/deletion variant mediated epigenetic regulation of ZCN7 based on the results of the present study"

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