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作物学报 ›› 2025, Vol. 51 ›› Issue (4): 958-968.doi: 10.3724/SP.J.1006.2025.43055

• 作物遗传育种·种质资源·分子遗传学 • 上一篇    下一篇

基于RNA-seq和PER-seq联合分析探究ZmHDZ6表达调控网络

方应浩1(), 周波3(), 陈茹梅2, 杨文竹2,*(), 秦慧民1,*()   

  1. 1工业发酵微生物教育部重点实验室 / 天津市工业微生物重点实验室 / 天津科技大学生物技术学院 / 工业酶国家工程实验室, 天津 300457
    2中国农业科学院生物技术研究所作物功能基因组研究中心, 北京 100081
    3河南省农业科学院粮食作物研究所, 河南郑州 450002
  • 收稿日期:2024-12-01 接受日期:2025-01-23 出版日期:2025-04-12 网络出版日期:2025-02-07
  • 通讯作者: 杨文竹, E-mail: yangwenzhu@caas.cn; 秦慧民, E-mail: huiminqin@tust.edu.cn
  • 作者简介:方应浩, E-mail: 15971341259@163.com;
    周波, E-mail: zb009@126.com第一联系人：

    **同等贡献

  • 基金资助:
    国家自然科学基金项目(32372064)

Integrative analysis of RNA-seq and PER-seq to elucidate regulatory network of ZmHDZ6 expression

FANG Ying-Hao1(), ZHOU Bo3(), CHEN Ru-Mei2, YANG Wen-Zhu2,*(), QIN Hui-Min1,*()   

  1. 1Key Laboratory of Industrial Fermentation Microbiology of the Ministry of Education / Tianjin Key Laboratory of Industrial Microbiology / College of Biotechnology, Tianjin University of Science and Technology / National Engineering Laboratory for Industrial Enzymes, Tianjin 300457, China
    2Crop Functional Genome Research Center, Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China
    3Cereal Crops Institute, Henan Academy of Agricultural Sciences, Zhengzhou 450002, Henan, China
  • Received:2024-12-01 Accepted:2025-01-23 Published:2025-04-12 Published online:2025-02-07
  • Contact: E-mail: yangwenzhu@caas.cn; E-mail: huiminqin@tust.edu.cn
  • About author:First author contact:

    **Contributed equally to this work

  • Supported by:
    National Natural Science Foundation of China(32372064)

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摘要：

玉米是需水量较大的作物, 而干旱是制约玉米生产的主要因素。结合前期研究基础和相关研究进展, 发现ZmHDZ6受干旱诱导强烈, 且过表达植株表现出优良的抗旱性能。为探究玉米转录因子ZmHDZ6的下游调控机制, 通过对ZmHDZ6过表达转基因玉米株系进行RNA-seq测序, 对自交系B73原生质体进行PER-seq (protoplast transient expression-based RNA-sequencing)测序, 并进行联合分析。 结果显示,2种测序策略得到的差异表达基因(DEGs)呈现一致性, 功能主要集中在参与氧化还原反应等GO富集分析条目。KEGG分析显示功能都富集在苯并噁唑嗪酮类化合物代谢途径上。此外, 基于RNA-seq的DEGs在氨基酸和核苷酸代谢途径富集, 而基于PER-seq的DEGs还富集在核糖体生物发生代谢途径。因此, 推测ZmHDZ6可能通过调控与氧化还原相关基因和苯并噁唑嗪酮类化合物的代谢进而增强玉米抗旱性。通过进一步在129个Co-DEGs (Common DEGs)的启动子序列扫描HDZIP I家族的DNA结合基序(motif), 将潜在靶基因缩减至16个, 其中8个基因的功能与玉米抗逆紧密相关。本研究利用转录组学数据分析了ZmHDZ6基因的下游表达调控网络, 为进一步解析抗旱机制提供了参考。

关键词: RNA-seq, PER-seq, 转录因子, ZmHDZ6, 靶基因, motif

Abstract:

Maize is a crop with high water demand, and drought is a major factor limiting its productivity. Building on previous findings and related research, we identified that the ZmHDZ6 gene is strongly induced by drought, and transgenic plants overexpressing ZmHDZ6 exhibit enhanced drought resistance. To investigate the downstream regulatory mechanisms of the maize transcription factor ZmHDZ6, RNA-seq was performed on transgenic maize plants overexpressing ZmHDZ6, while PER-seq (protoplast transient expression-based RNA sequencing) was conducted using protoplasts from the B73 inbred line. An integrative analysis of these datasets revealed that the differentially expressed genes (DEGs) identified by both methods showed consistent results in GO analysis, with their functions primarily associated with redox reactions. KEGG pathway analysis further demonstrated consistency in the benzoxazinoid biosynthesis pathway. Notably, RNA-seq DEGs were additionally enriched in amino acid and nucleotide metabolism pathways, while PER-seq DEGs were enriched in ribosome biogenesis pathways. Based on these findings, we propose that ZmHDZ6 enhances drought resistance in maize by regulating genes involved in redox processes and benzoxazinoid metabolism. Furthermore, through an integrative analysis of DNA binding motifs of the HD-ZIP I family and the promoters of 129 common DEGs (Co-DEGs), combined with gene annotation and motif physical location information, we narrowed potential target genes down to 16, of which 8 are closely associated with stress responses in maize. This study provides a detailed analysis of the regulatory network of ZmHDZ6 expression, offering valuable insights into the drought resistance mechanisms mediated by ZmHDZ6 and a reference for further functional studies.

Key words: RNA-seq, PER-seq, transcription factor, ZmHDZ6, target gene, motif

图1

载体构建图谱和转化体相对表达量检测 A: PER-seq载体构建图; B: 过表达载体构建图; C: 转化体表达量检测。EGFP: 增强型绿色荧光蛋白基因; Ter: 终止子; Bar: 抗除草剂基因; Ltp2: 糊粉层特异性表达启动子; DsRed: 红色荧光蛋白基因; UBI: 组成型启动子; 3×Flag: 蛋白标签; WT: 野生型; OE1/4/12: 过表达ZmHDZ6株系。数据使用平均值±标准差表示; 差异显著性分析采用t检验(**: P < 0.01, ****: P < 0.0001)。"

图2

样品相关性分析热图 A: RNA-seq样品相关性分析; B: PER-seq样品相关性分析。OE12-1/2/3: OE12阳性样品; WT-1/2/3: 野生型样品; ZmHDZ6-1/2/3: ZmHDZ6原生质体转化样品; Control-1/2/3: 原生质体转化对照样品。"

图3

差异表达基因火山图 A: RNA-seq差异表达基因火山图; B: PER-seq差异表达基因火山图。Up regulated genes: 上调基因; Down regulated genes: 下调基因; Non-regulated genes: 非差异基因。每个圆点代表一个差异表达基因, x轴表示两组间表达量的倍数变化取Log2的值, y轴表示t检验的P值取log10的值。"

图4

RNA-seq和PER-seq差异表达基因韦恩图 A: 上调基因韦恩图; B: 下调基因韦恩图。"

图5

差异表达基因富集分析 A: RNA-seq差异表达基因GO富集分析条形图; B: RNA-seq差异表达基因KEGG富集通路气泡图; C: PER-seq差异表达基因GO富集分析条形图; D: PER-seq差异表达基因KEGG富集通路气泡图; E: Co-DEGs GO富集分析条形图; F: Co-DEGs KEGG富集通路气泡图。图A、C、E中x轴表示基因的数目, y轴表示数据库中条目注释信息。图B、D、F中x横表示富集因子, y轴表示数据库中通路注释信息, 圆点大小表示基因数目, 颜色表示t检验的P值取log10的值。"

图6

HDZIP I家族motif x轴表示碱基的相对位置, y轴代表碱基出现的频率。"

表1

16个可能的靶基因功能注释"

基因ID
Gene ID		 离近端启动子区物理位置
Physical location from proximal promoter region (bp)		 描述
Description		 结合位点数量
Number of binding sites		 相关文献
Reference
Zm00001d029747 266 过氧化物酶64 Peroxidase 64 3 [31]
Zm00001d031717 111 转录因子bHLH28 Transcription factor bHLH28 2 [37]
Zm00001d034836 215 未知Unknown 1 —
Zm00001d048985 134 At5g01610蛋白Protein At5g01610 2 [39]
Zm00001d034977 292 突变体相关蛋白SEC22 VAMP protein SEC22 1 [40]
Zm00001d020401 284 肉桂醇脱氢酶 Cinnamyl alcohol dehydrogenase 1 [41]
Zm00001d021632 195 LOC103633229 1 [42]
Zm00001d008173 165 第3类分泌型植物过氧化物酶家族蛋白
Class III secretory plant peroxidase family protein		 4 [32]
Zm00001d009404 275/229 天冬氨酸-谷氨酸消旋酶家族
Aspartate-glutamate racemase family		 5 [43]
Zm00001d046281 286 LOC103638588 1 [44]
Zm00001d047504 151 花青素5,3-葡糖基转移酶
Anthocyanidin 5,3-O-glucosyltransferase		 1 [38]
Zm00001d048437 278 钙调蛋白结合蛋白Calmodulin binding protein 1 [45]
Zm00001d023936 256 类CASP蛋白8 CASP-like protein 8 2 —
Zm00001d025567 212/243 阿拉伯半乳糖蛋白1 Arabinogalactan protein 1 2 —
Zm00001d026398 267 转录因子TGAL6 Transcription factor TGAL6 3 [33]
Zm00001d023673 278 SWEET13b 2 [34⇓-36]

图7

差异表达基因的qRT-PCR验证 WT: 野生型材料; OE: OE12株系材料。RNA-seq: 公司测序数据; qRT-PCR: 试验数据。Leaf: 以叶片为材料进行数据验证; Potoplast: 以原生质体为材料进行数据验证。数据使用平均值±标准差表示; 差异显著性分析采用t检验(**: P < 0.01, ***: P < 0.001, ****: P < 0.0001)。"

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