番木瓜成熟过程中全基因组DNA甲基化和转录组变化分析

doi:10.16420/j.issn.0513-353x.2020-1046

园艺学报 ›› 2022, Vol. 49 ›› Issue (3): 519-532.doi: 10.16420/j.issn.0513-353x.2020-1046

番木瓜成熟过程中全基因组DNA甲基化和转录组变化分析

周陈平¹, 杨敏¹, 郭金菊², 邝瑞彬¹, 杨护¹, 黄炳雄¹, 魏岳荣¹^,^*()

¹广东省农业科学院果树研究所,农业农村部南亚热带果树生物学与遗传资源利用重点实验室,广东省热带亚热带果树研究重点实验室,广州 510640
²广东省农业科学院设施农业研究所,广州 510640

收稿日期:2021-07-19 修回日期:2021-08-20 出版日期:2022-03-25 发布日期:2022-03-25
通讯作者: 魏岳荣 E-mail:weid18@163.com
基金资助:
广东省基础与应用基础研究基金项目(2020A1515011166);广州市科技计划项目(202102020038);广东省现代农业产业技术体系创新团队建设项目(2021KJ116);广州市基础与应用基础研究一般项目(2060206-13)

Dynamic Changes in DNA Methylome and Transcriptome Patterns During Papaya Fruit Ripening

ZHOU Chenping¹, YANG Min¹, GUO Jinju², KUANG Ruibin¹, YANG Hu¹, HUANG Bingxiong¹, WEI Yuerong¹^,^*()

¹Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization,Ministry of Agriculture and Rural Affairs,Guangdong Province Key Laboratory of Tropical and Subtropical Fruit Tree Research,Institute of Fruit Tree Research,Guangdong Academy of Agricultural Sciences,Guangzhou 510640,China
²Institute of Facility Agriculture,Guangdong Academy of Agricultural Sciences,Guangzhou 510640,China

Received:2021-07-19 Revised:2021-08-20 Online:2022-03-25 Published:2022-03-25
Contact: WEI Yuerong E-mail:weid18@163.com

摘要/Abstract

摘要：

采用全基因组DNA甲基化（WGBS）和转录组测序（RNA-seq）技术对番木瓜4个成熟时期（绿熟期、破色期、熟化期、腐熟期）的果实样品进行高通量测序。C位点、CG、CHG和CHH序列平均甲基化水平分别为17.15%、49.33%、34.30%和8.28%。全基因组DNA甲基化水平在果实成熟过程中持续下降,同时差异表达基因（DEG）数量逐渐上升。全基因组DNA甲基化和转录组数据联合分析表明,基因表达水平与启动子及基因体甲基化水平呈显著正相关。筛选出CpACO4、CpPDS、CpXTH30和CpXTH31等4个番木瓜果实成熟差异表达候选基因,利用荧光定量PCR和McrBC-PCR分别检测其表达水平和相应DMR序列甲基化水平,结果分别同转录组和全基因组DNA甲基化一致,推测这些基因在番木瓜果实成熟过程中起重要作用。

关键词: 番木瓜, 果实, 成熟, 全基因组, DNA甲基化, 基因, 差异表达

Abstract:

The whole genome bisulfite sequencing（WGBS）and transcriptome sequencing（RNA-seq）techniques were used to sequence papaya fruit samples at four stages,namely green stage,color break stage,half yellow stage and full yellow stage. The average methylation level of C locus,CG,CHG,and CHH sequence contexts were 17.15%,49.33%,34.30%,and 8.28%,respectively. The level of genome-wide DNA methylation decreased with the ripening of fruit,accompanied by the increased number of differentially expressed genes（DEGs）. Combined analysis of genome-wide DNA methylation and transcriptome data showed that the gene expression presented an obvious positive correlation with promoter and genebody methylation. Four differentially expressed candidate genes possibly responsible for papaya fruit ripening,namely CpACO4,CpPDS,CpXTH30 and CpXTH31,were screened out. Their expression levels and DMRs methylation levels obtained by RT-qPCR and McrBC-PCR matched well with the results of the transcriptome and methylome,respectively. These genes might play an important role in papaya fruit ripening.

Key words: Carica papaya, fruit, ripening, whole genome, DNA methylation, gene, differentially expression

中图分类号:

S667.9

周陈平, 杨敏, 郭金菊, 邝瑞彬, 杨护, 黄炳雄, 魏岳荣. 番木瓜成熟过程中全基因组DNA甲基化和转录组变化分析[J]. 园艺学报, 2022, 49(3): 519-532.

ZHOU Chenping, YANG Min, GUO Jinju, KUANG Ruibin, YANG Hu, HUANG Bingxiong, WEI Yuerong. Dynamic Changes in DNA Methylome and Transcriptome Patterns During Papaya Fruit Ripening[J]. Acta Horticulturae Sinica, 2022, 49(3): 519-532.

图/表 11

图1 不同成熟时期的番木瓜果实

Fig. 1 Different maturation stages of papaya fruits

表1 McrBC-PCR和实时定量PCR引物

Table 1 Primers used for McrBC-PCR and qRT-PCR

用途 Application	基因名称 Gene name	上游引物（5′-3′） Forward primer	下游引物（5′-3′） Reverse primer
McrBC-PCR	CpXTH30	GGTTGGCTAATGATTGT	AGAAGGAAGGAGGGTGC
	CpPDS	CTAGTTTCTAACTGCGTAT	AACCATTATCATGTGGG
	CpACO4	GAAGACCATTAGCCACA	TTCGCTTAACTTAAACAC
	CpXTH31	ATGAAGTAGGGTGAGAA	ATGGTGGAATAAGTGTT
qRT-PCR	CpXTH30	GTTCCATCGGTATAGCAT	CTTTGTATCTTCCACCTGA
	CpPDS	AGTTGGCGTCCCTGTTA	GGATTGATTTGGGTTGTA
	CpACO4	CACGAGCAGCCAAACGA	TCACCCACCCATCCCAC
	CpXTH31	GGGAACCCTACACTTTG	CTTGGATACCTCCGAAT

表2 番木瓜果实不同成熟时期全基因组DNA甲基化测序数据统计情况

Table 2 Summary of WGBS data of papaya fruits at different ripening stages

成熟期 Stage	序列总数量 Total reads	对比参考基因组获得的序列数量 Mapped reads	匹配率/% Mapping rate	重复序列占比/% Duplication rate	≥ Q30/%	测序深度 Sequencing depth	甲基化C位点数量Number of Methylated C site	平均甲基化水平/% Mean methylation level
成熟期 Stage	序列总数量 Total reads	对比参考基因组获得的序列数量 Mapped reads	匹配率/% Mapping rate	重复序列占比/% Duplication rate	≥ Q30/%	测序深度 Sequencing depth	甲基化C位点数量Number of Methylated C site	C	CG	CHG	CHH
绿熟期 Green	49 375 154	35 135 889	70.97	14.37	92.78	21.87	251 784 698	17.79	51.22	35.59	8.62
破色期 Color break	49 361 724	34 881 444	70.67	12.75	91.56	22.08	258 718 931	17.51	50.64	35.09	8.44
熟化期 Half yellow	49 461 069	34 774 513	70.36	12.62	92.57	21.95	232 054 629	17.04	48.60	33.76	8.26
腐熟期 Full yellow	48 863 321	34 071 375	70.61	10.79	92.19	22.54	233 578 504	16.26	46.88	32.77	7.81

图2 不同成熟期番木瓜果实的基因（gene）和转座子（TE）DNA甲基化水平（A）和C、CG、CHG和CHH序列的甲基化水平（B） GS：绿熟期;CB：破色期;HY：熟化期;FY：腐熟期;-2K和2K：基因上游和下游2 kb区域;5′和3′：基因5′和3′侧翼区域;rep1和rep2：2个生物学重复。下同。

Fig. 2 DNA methylation levels of genes and TEs（A）and C,CG,CHG,and CHH contexts（B）at different ripening stages of papaya fruits GS：Green stage;CB：Color break stage;HY：Half yellow stage;FY：Full yellow stage;-2K and 2K：2 kb upstream and downstream regions of genes;5′ and 3′：5′ and 3′ flanking regions of genes;rep1 and rep2：Two biological replicates. The same below.

图3 破色期（CB）、熟化期（HY）、腐熟期（FY）与绿熟期（GS）比较差异甲基化胞嘧啶数量（A）和区域数量（B）

Fig. 3 Number of DMCs（A）and DMRs（B）in CB vs. GS,HY vs. GS,and FY vs. GS

图4 20条基因组骨架甲基化密度circos图图谱外圈编号：20条基因组骨架的编号;5mC/RNA、TE和Gene热标：分别为CG、CHG、CHH序列甲基化密度、RNA丰度、转座子重复序列比例和基因数量由低到高。

Fig. 4 Circos plot of twenty genome scaffold methylation density Number on outer rim：Number of the twenty genome scaffolds;Scales of 5mC/RNA,TE and Gene：The methylation levels of CG,CHG,CHH sequence context,RNA abundance,the ratio of transposon repeats and gene number were from low to high,respectively.

图5 3种序列甲基化水平在基因体及其上、下游2 kb区域的分布（A）和基因体及启动子甲基化水平与基因表达水平关系（B） -2K和2K：基因上游和下游2 kb区域;表达水平：FPKM值 < 1基因的FPKM值为无（不表达）,FPKM值 ≥ 1基因的FPKM值由小到大排列,求得上下四分位处的FPKM值;甲基化水平等级：基因体或启动子甲基化水平值由小到大排列,求得第20/40/60/80百分位处的甲基化水平值。

Fig. 5 Relationship between distribution of methylation levels in three contexts within the genebody,upstream,and downstream 2 kb rigions（A）and methylation levels of genebody and promoterwith the gene expression levels（B） -2K and 2K：2 kb upstream and downstream regions of genes;Expression：genes with FPKM value < 1 were considered as none（non-expressed）,expressed genes（FPKM value ≥ 1）were ranked from small to large and divided into three groups based on the upper and lower quartile;Methylation group：Methylation levels of genebodies or promoters were ranked from small to large and divided into quinitiles.

图6 番木瓜不同成熟时期比较组中上、下调差异表达基因数量

Fig. 6 Number of up-and down-regulated DEGs in different ripening stages

图7 番木瓜DNA甲基化基因的同源比对（A）及其在不同成熟时期表达变化（B）热标：由蓝到红表示基因表达量由低到高。1 ~ 3：3个生物学重复。*：P < 0.05;-：无显著差异。

Fig. 7 Homologous alignment of DNA methylation genes（A）and their expression changes at different ripening stages in papaya fruits（B） Scale：From blue to red represent the gene expression levels was from low to high. 1-3：Three biological replicates.*：P < 0.05;-：No significant difference.

图8 类胡萝卜素生物合成基因在番木瓜果实不同成熟时期的表达变化热标：由蓝到红表示基因表达量由低到高;1 ~ 3：3个生物学重复。

Fig. 8 Expression changes of carotenoid biosynthetic-related genes at different ripening stages of papaya fruits Scale：From blue to red represent the gene expression levels was from low to high;1-3：Three biological replicates.

图9 4个候选基因DMR甲基化水平及其在番木瓜不同成熟时期的表达分析 A：CpACO4、CpXTH30和CpXTH31启动子及CpPDS基因体DMR甲基化水平;B：McrBC-PCR验证（M：McrBC酶切的PCR产物,Un：未被酶切的PCR产物）;C：表达倍数（FC）;D：qRT-PCR验证。

Fig. 9 The DMRs methylation and expression levels of four candidate genes at different maturation stages of papaya fruits A：DMRs methylation levels of CpACO4,CpXTH30 and CpXTH31 promoters and CpPDS genebody;B：The McrBC-PCR validation（M：PCR products been digested by McrBC,Un：PCR products not been digested）;C：Fold change（FC）;D：qRT-PCR validation.

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番木瓜成熟过程中全基因组DNA甲基化和转录组变化分析

Dynamic Changes in DNA Methylome and Transcriptome Patterns During Papaya Fruit Ripening

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番木瓜成熟过程中全基因组DNA甲基化和转录组变化分析

Dynamic Changes in DNA Methylome and Transcriptome Patterns During Papaya Fruit Ripening

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