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作物学报 ›› 2023, Vol. 49 ›› Issue (9): 2398-2411.doi: 10.3724/SP.J.1006.2023.22059

• 作物遗传育种·种质资源·分子遗传学 • 上一篇    下一篇

低温胁迫下组蛋白H3K18cr在水稻全基因组上的动态变化特征解析

刘凯1(), 陈积金1, 刘帅2, 陈旭1, 赵新茹2, 孙尚2, 薛超2, 龚志云1,2,*()   

  1. 1江苏省作物基因组学和分子育种重点实验室 / 植物功能基因组学教育部重点实验室 / 江苏省作物遗传生理重点实验室 / 扬州大学农学院, 江苏扬州 225009
    2江苏省粮食作物现代产业技术协同创新中心 / 扬州大学, 江苏扬州 225009
  • 收稿日期:2022-10-07 接受日期:2023-02-10 出版日期:2023-09-12 网络出版日期:2023-02-27
  • 通讯作者: *龚志云, E-mail: zygong@yzu.edu.cn
  • 作者简介:刘凯, E-mail: lkss1730@foxmail.com
  • 基金资助:
    国家自然科学基金项目(31871232)

Dynamic change profile of histone H3K18cr on rice whole genome under cold stress

LIU Kai1(), CHEN Ji-Jin1, LIU Shuai2, CHEN Xu1, ZHAO Xin-Ru2, SUN Shang2, XUE Chao2, GONG Zhi-Yun1,2,*()   

  1. 1Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding / Key Laboratory of Plant Functional Genomics of the Ministry of Education / Jiangsu Key Laboratory of Crop Genetics and Physiology, Agricultural College of Yangzhou University, Yangzhou 225009, Jiangsu, China
    2Jiangsu Co-innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, Yangzhou 225009, Jiangsu, China
  • Received:2022-10-07 Accepted:2023-02-10 Published:2023-09-12 Published online:2023-02-27
  • Supported by:
    National Natural Science Foundation of China(31871232)

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摘要：

组蛋白修饰在水稻响应非生物胁迫的过程中发挥着重要作用。巴豆酰化是一种新型的组蛋白修饰方式, 其在水稻受到低温逆境时如何变化目前很少有见报道。本研究对正常生长和低温处理的水稻日品种本晴幼苗进行RNA-seq和ChIP-seq高通量测序, 然后联合分析组蛋白H3赖氨酸18特异位点上巴豆酰化修饰(H3K18cr)在低温胁迫下对基因表达的调控特征。研究表明, 在基因组中H3K18cr主要富集在第1外显子和基因间区, 且与基因表达和基因长度呈现正相关。低温胁迫下, H3K18cr在水稻基因组上的分布区域没有变化, 但是蛋白免疫印记和ChIP-seq结果均表明整体修饰水平下降; 差异修饰分析发现低温胁迫后有899个和409个基因分别表现出修饰显著增加和减少。通过与RNA-seq关联分析显示共有199个基因H3K18cr修饰水平增高且表达水平上调, GO富集分析发现这些基因主要参与转录活性的调控等过程。进一步验证表明组蛋白H3K18cr通过调控OsDREB1A、OsEATB、OsAP2-39、OsNAC9等转录因子的表达来参与水稻低温胁迫的响应过程。相关研究结果为解析组蛋白巴豆酰化调控植物响应低温胁迫的表观遗传机制提供理论基础。

关键词: 水稻, 低温胁迫, H3K18cr, 基因表达

Abstract:

Histone modifications play an important role in response to abiotic stresses in rice. Crotonylation is a novel histone modification, and the changes of crotonylation in rice subjected to low temperature stress are rarely reported. In this study, RNA-seq and ChIP-seq were performed on normal-grown and cold-treated rice seedlings of rice variety ‘Nipponbare’, followed by combined analysis of the regulatory characteristics of the crotonylation modification at the histone H3 lysine 18-specific site (H3K18cr) on gene expression under cold stress. The results showed that H3K18cr was mainly enriched in the first exon and intergenic region and had positive correlation with gene expression and gene length. The global distribution of H3K18cr in rice genome did not change under cold stress, but WB and ChIP-seq results indicated that the overall modification level decreased. The differential modification analysis revealed that there were significant increase and decrease of 899 genes and 409 genes in the modification after cold stress, respectively. Association analysis with RNA-seq showed that a total of 199 genes had increased levels of H3K18cr modification and up-regulated expression levels. GO enrichment revealed that these genes were mainly involved in the processes such as the regulation of transcriptional activity. Further analysis indicated that histone H3K18cr was involved in the response process of cold stress by regulating the expression of transcription factors such as OsDREB1A, OsEATB, OsAP2-39, and OsNAC9 in rice. The results provide a theoretical basis for further understanding the epigenetic mechanisms of histone crotonylation in response to cold stress in plants.

Key words: rice, cold stress, H3K18cr, gene expression

表1

本研究所用引物"

引物名称
Primer name		 引物序列
Primer sequence (5'-3')		 引物名称
Primer name		 引物序列
Primer sequence (5'-3')
OsDREB1A-F GACGTCCTGAGTGACATGG OsTPS1-F CATCGTGTCAGAGTTTGTCG
OsDREB1A-R CTAGTAGCTCCAGAGTGGGA OsTPS1-R TCACGTACCTGTAGTGCTTC
OsDREB1B-F GTCCACACTTTTCAGTGCGAG OsLEA5-F CTCACCTACACCCTCAAGTG
OsDREB1B-R AATCTCGCACTGAAAAGTGTGG OsLEA5-R CGAGATGAGGAAGTCGTAGG
OsMYBS3-F CAAGAACCAGAGACCCAAGT OsV5A-F CTTCTGCTGAGAATGGACCT
OsMYBS3-R AAGCTGGAACAATCACTGGA OsV5A-R GAGGGTGGGATGATGAATGT
OsMADS57-F GTTCCAGCACTCCATACAGC ONAC095-F CAGGAGGAGAGGTGGAGG
OsMADS57-R GGCAGATGAAGTCCCAGTTCT ONAC095-R GGGGATGATGTCGAACTTGA

图1

水稻品种日本晴幼苗在低温胁迫下H3K18cr的变化情况 A: 生长2周的水稻幼苗在正常和低温(4℃)处理10 h后的表型; B: 蛋白免疫分析H3K18cr在正常和低温胁迫下的变化情况, 使用ImageJ软件计算灰度值; C: 正常和低温胁迫下H3K18cr peaks的全基因组分布; D: 正常和低温胁迫下H3K18cr在不同类型基因上的分布模式分析, X轴表示不同长度基因转化为百分比的标准化, 包括基因的上下游1 kb区域。Y轴表示H3K18cr的归一化读数。"

表2

ChIP-seq数据统计"

样品名
Sample name		 重复数
Replicate		 总序列数
Total clean reads		 比对序列数
Total aligned reads		 唯一比对序列数
Total unique reads		 Peak数
Total peaks		 共有Peak数
Common peaks		 相关性
Correlation coefficient
H3K18cr-CK 1 45,952,156 45,268,705 (98.51%) 30,248,490 (65.83%) 25,218 20,077 0.92
H3K18cr-CK 2 48,099,538 47,360,155 (98.46%) 32,023,294 (66.58%) 29,127
H3K18cr-Cold 1 47,721,602 46,868,242 (98.21%) 30,382,217 (63.67%) 23,544 17,944 0.92
H3K18cr-Cold 2 48,128,162 47,304,118 (98.29%) 30,250,892 (62.85%) 29,632

图2

低温胁迫下H3K18cr响应基因分析 A: 正常和低温胁迫下被H3K18cr标记基因的数目。红线表示正常生长幼苗, 蓝线表示低温处理10 h的幼苗; B: 正常和低温胁迫下H3K18cr差异修饰基因的数目; C: 低温胁迫下H3K18cr修饰增加基因的GO富集分析。散点图表示对相似GO terms矩阵进行多维缩放得出的二维空间中的聚类图, 气泡颜色和大小使用log10(FDR)表示, X轴和Y轴无实际意义; D: 低温胁迫下H3K18cr修饰降低基因的GO富集分析。Y轴表示富集的GO terms, X轴用-log10(FDR)表示, 图中数字表示富集在该GO terms中的基因数; E: 低温胁迫下H3K18cr修饰增加基因的KEGG富集通路分析。"

表3

RNA-seq数据统计"

样品名
Sample		 重复数
Replicate		 总序列数
Total reads		 比对序列数
Aligned reads		 表达基因数
FPKM>0		 相关性
Correlation coefficient
正常温度Control 1 51,702,548 49,740,100 (92.62%) 26,992 0.94
正常温度Control 2 54,410,846 50,622,035 (93.04%) 24,422
低温Cold 1 61,244,656 52,044,285 (84.98%) 25,474 0.95
低温Cold 2 72,466,862 67,205,195 (92.74%) 27,191

图3

低温胁迫下基因表达情况分析 A: 先前报道的非生物胁迫相关基因的RT-qPCR。红色表示上调基因, 蓝色表示下调基因; B: 正常和低温胁迫下H3K18cr修饰与基因表达的关系; C: 正常和低温胁迫下差异基因的表达情况; D: 表达上调基因的GO和KEGG富集分析; E: 表达下基因的GO和KEGG富集分析。"

图4

低温胁迫下H3K18cr与基因表达关系分析 A: 低温处理后ChIP-seq差异修饰基因和RNA-seq差异表达基因的韦恩图; B: 199个修饰增加且表达上调基因修饰富集热图; C: 199个修饰增加且表达上调基因表达水平的盒形图; D: 199个修饰增加且表达上调基因的GO富集分析。散点图表示对相似GO terms矩阵进行多维缩放得出的二维空间中的聚类图, 气泡颜色和大小使用log10(FDR)表示, X轴和Y轴无实际意义; E: 199个修饰增加且表达上调基因的KEGG富集分析。"

图5

低温胁迫下H3K18cr相关的转录因子分析 A: 199个H3K18cr修饰增加且表达上调基因与水稻中所有转录因子的韦恩图; B: IGV软件显示低温下ERF家族中基因与H3K18cr相关; C: IGV软件显示低温下NAC家族中基因与H3K18cr相关; D: IGV软件显示低温下GRAS家族中基因与H3K18cr相关; E: IGV软件显示低温下DBB家族中基因与H3K18cr相关。"

表4

转录因子功能信息统计"

TF 家族
TF family		 基因 ID
Gene ID		 基因名字
Gene name		 功能
Function		 参考文献References
Dof LOC_Os01g15900 RDD1; OsDof-2 产量相关 Yield-related [45]
LOC_Os10g26620 OsDof-26; OsDof27 非生物逆境抗性 Abiotic stress tolerance [46]
ERF LOC_Os09g35030 OsDREB1A 非生物逆境抗性 Abiotic stress tolerance [28]
LOC_Os09g28440 OsEATB 株高发育; 非生物逆境抗性
Plant growth; Abiotic stress tolerance		 [37-38]
LOC_Os04g52090 OsAP2-39 非生物逆境抗性 Abiotic stress tolerance [39]
ARF LOC_Os04g36054 OsARF9 — —
NAC LOC_Os03g60080 SNAC1; OsNAC9 非生物逆境抗性 Abiotic stress tolerance [41]
LOC_Os07g12340 OsNAC3 非生物逆境抗性 Abiotic stress tolerance [40]
CO-like LOC_Os09g06464 OsCO3 调控光周期 Regulate photoperiodic [47]
LOC_Os02g39710 OsCOL4 调控抽穗期 Regulate heading date [48]
HD-ZIP LOC_Os04g45810 Oshox22 非生物逆境抗性 Abiotic stress tolerance [49]
bZIP LOC_Os02g16680 RITA-1; OsbZIP20 非生物逆境抗性; 重金属胁迫
Abiotic stress tolerance; High metal stress		 [50-51]
HSF LOC_Os02g13800 OsHsfC2a 非生物逆境抗性 Abiotic stress tolerance [52]
DBB LOC_Os02g39360 OsBBX4; OsBBX25 非生物逆境抗性 Abiotic stress tolerance [44]
LOC_Os09g35880 OsBBX29 非生物逆境抗性 Abiotic stress tolerance [43]
LOC_Os04g41560 OsBBX11 非生物逆境抗性 Abiotic stress tolerance [43]
bHLH LOC_Os01g50940 OsMYL1 调控JA信号 Regulate JA signal [53]
LOC_Os04g41229 OsbHLH111 调控糖信号 Regulate sugar signal [54]
LOC_Os09g29930 OsbHLH032 调控BR信号 Regulate BR signal [55]
GRAS LOC_Os02g44360 SCL6-IIb; OsHAM1 非生物逆境抗性 Abiotic stress tolerance [42]
LOC_Os02g45760 OsGRAS-10 — —
LOC_Os01g62460 OsGRAS-2 — —
MYB_related LOC_Os04g49450 OsMYBR1 非生物逆境抗性 Abiotic stress tolerance [56]
LOC_Os02g46030 OsMYB1R 非生物逆境抗性 Abiotic stress tolerance [57]
LOC_Os02g45670 — — —
LOC_Os01g41900 OsDLN13 — —
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