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作物学报 ›› 2021, Vol. 47 ›› Issue (12): 2324-2334.doi: 10.3724/SP.J.1006.2021.04269

• 作物遗传育种·种质资源·分子遗传学 • 上一篇    下一篇

红麻DNA甲基化响应镉胁迫及甲基化差异基因的表达分析

卢海1(), 李增强1, 唐美琼1, 罗登杰1, 曹珊1, 岳娇1, 胡亚丽1, 黄震1, 陈涛2, 陈鹏1,*()   

  1. 1广西大学农学院 / 广西高校植物遗传育种重点实验室, 广西南宁 530004
    2广西壮族自治区亚热带作物研究所, 广西南宁 530004
  • 收稿日期:2020-12-09 接受日期:2021-04-14 出版日期:2021-12-12 网络出版日期:2021-05-14
  • 通讯作者: 陈鹏
  • 作者简介:E-mail: 294856020@qq.com
  • 基金资助:
    国家自然科学基金项目(31560341);国家自然科学基金项目(31960368);国家现代农业产业技术体系建设专项(CARS-16-E14)

DNA methylation in response to cadmium stress and expression of different methylated genes in kenaf

LU Hai1(), LI Zeng-Qiang1, TANG Mei-Qiong1, LUO Deng-Jie1, CAO Shan1, YUE Jiao1, HU Ya-Li1, HUANG Zhen1, CHEN Tao2, CHEN Peng1,*()   

  1. 1College of Agriculture, Guangxi University / Guangxi Colleges and Universities Key Laboratory of Plant Genetics and Breeding, Nanning 530004, Guangxi, China
    2Guangxi Subtropical Crops Research Institute, Nanning 530004, Guangxi, China
  • Received:2020-12-09 Accepted:2021-04-14 Published:2021-12-12 Published online:2021-05-14
  • Contact: CHEN Peng
  • Supported by:
    National Natural Science Foundation of China(31560341);National Natural Science Foundation of China(31960368);China Agriculture Research System of MOF and MARA(CARS-16-E14)

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摘要：

DNA甲基化是植物重要的表观遗传修饰方式之一, 在响应逆境胁迫中具有重要作用, 但是有关镉胁迫下植物DNA甲基化水平变化的报道甚少。本研究以红麻P3A为材料, 采用水培法对幼苗进行300 μmol L-1的CdCl2处理, 测定幼苗农艺性状及镉含量; 利用甲基化敏感扩增多态性技术(methylation-sensitive amplification polymorphism, MSAP)分析镉胁迫下根系DNA甲基化水平变化; 回收甲基化差异片段并克隆测序, 采用qRT-PCR技术对DNA甲基化差异基因的表达量进行分析。结果表明, CdCl2胁迫显著抑制红麻幼苗的株高、茎粗、根长、根表面积以及全鲜重。对照及镉处理下幼苗根系的DNA甲基化率分别为62.78%、68.23%, 其中全甲基化率分别为37.50%、36.36%, 半甲基化率分别为25.28%、31.87%, 表明镉胁迫显著提高红麻幼苗根系的DNA甲基化水平。qRT-PCR分析表明, 7个与抗性密切相关的DNA甲基化差异基因也存在表达量的差异, 推测DNA甲基化水平变化在响应红麻镉胁迫中发挥重要作用。本结果为深入探索DNA甲基化响应植物镉胁迫的潜在机制提供了理论基础。

关键词: 红麻, 镉胁迫, DNA甲基化, 甲基化敏感扩增多态性(MSAP), 实时荧光定量PCR (qRT-PCR)

Abstract:

DNA methylation is one of the important epigenetic modifications in plants and plays an important role in response to stress. However, there are few reports of the changes of DNA methylation levels in plants under cadmium stress. The seedlings of kenaf P3A were treated with 300 μmol L-1 CdCl2 by hydroponics, the agronomic traits and cadmium contents were investigated. The changes of DNA methylation level of root under cadmium stress were analyzed by using methylation sensitive amplified polymorphism (MSAP) method. In addition, the differential methylation fragments were recovered, cloned, and sequenced. The relative expression levels of differential methylated genes revealed that Cd stress significantly inhibited the plant height, stem diameter, root length, root surface area, and total fresh weight of kenaf seedlings. The whole DNA methylation ratio in root was 68.23% and 62.78% under cadmium and control treatments, respectively. Among them the total methylation ratio was 37.50% and 36.36%, and the semi-methylation ratio was 25.28% and 31.87%, respectively. These results indicated that cadmium stress significantly increased the DNA methylation level of roots DNA. Seven differential methylated genes which involved in stress resistance were characterized differentially expressed under cadmium stress, suggesting that the change of DNA methylation played an important role in response to cadmium stress. This study provides a theoretical basis for further exploring the potential mechanism of DNA methylation in response to cadmium stress in plants.

Key words: kenaf, cadmium stresses, DNA methylation, methylation-sensitive amplified polymorphism (MSAP), real-time fluorescent quantitative PCR (qRT-PCR)

表1

接头和引物序列"

引物类型
Primer type		 引物名称及序列 Primer name and sequence (5′-3′)
EcoR I (E) Hpa II/Msp I (HM)
接头
Adapter		 EA1 CTCGTAGACTGCGTACC HMA1 GACGATGAGTCTAGAA
EA2 AATTGGTACGCAGTC HMA2 CGTTCTAGACTCATC
预扩增 E0 GACTGCGTACCAATTCA HM0 GATGAGTCTAGAACGGT
Pre-amplification E1 GACTGCGTACCAATTCAAC HM1 GATGAGTCTAGAACGGTAG
E2 GACTGCGTACCAATTCAAG HM2 GATGAGTCTAGAACGGTAC
E3 GACTGCGTACCAATTCACA HM3 GATGAGTCTAGAACGGTTG
选择性扩增 E4 GACTGCGTACCAATTCACT HM4 GATGAGTCTAGAACGGTTC
Selective amplification E5 GACTGCGTACCAATTCACC HM5 GATGAGTCTAGAACGGTGT
E6 GACTGCGTACCAATTCACG HM6 GATGAGTCTAGAACGGTGC
E7 GACTGCGTACCAATTCAGC HM7 GATGAGTCTAGAACGGTCT
E8 GACTGCGTACCAATTCAGG HM8 GATGAGTCTAGAACGGTCG

表2

实时荧光定量PCR引物序列"

引物名称
Primer name		 正向引物
Forward sequence (5′-3′)		 反向引物
Reverse sequence (5′-3′)
GH3.1 GACCGCCGTCTGTAACTCG GGTTCCACAACTCCGCCC
GrKCS1 GCCGCCAGTGTGATGGATAT CGGTGCTCGGTTCTCCATT
NADP-ME TTCATCTTCCCTTCGCCTT CATCCCAACAACACCTTCCT
ABCG26 ATTGGTACGCAGTCACGATG TTCACCTTCATTTGACACGG
L-AAOh AAGCCTTTCCGATTGTTCTGC GGAGTTAGATTTTTGTTGTTGGGAG
LRR-RLK GCATATACACGATAAGAAACCGC CATGAAGATATTCCAAGCCCC
GaTPPD CCTTCCTCCCTTGGGTTAGT TTCTGTTCGCCTGTGGTTTT
XlCGF8.2DB GACTGCGTACCAATTCAAGGC AATTGTTGCCATATTTCTCCCAT
His3 (reference gene) GTGGAGTCAAGAAGCCTCACAG ATGGCTCTGGAAACGCAAA

表3

CdCl2胁迫对红麻幼苗农艺性状的影响"

CdCl2浓度
Concentration of CdCl2 (μmol L-1)		 株高
Plant height
(cm)		 茎粗
Stem diameter (mm)		 全鲜重
Fresh weight
(g)		 根鲜重
Root fresh weight (g)		 根长
Root length
(cm)		 根表面积
Root surface area (cm2)
0 29.24 a 2.49 a 21.19 a 9.27 a 275.32 a 23.68 a
300 19.94 b 1.70 b 9.54 b 5.50 b 186.74 b 8.98 b

表4

CdCl2胁迫对红麻幼苗农艺性状的相对抑制率"

CdCl2浓度
Concentration of CdCl2 (μmol L-1)		 株高
Plant height		 茎粗
Stem diameter		 全鲜重
Fresh weight		 根鲜重
Root fresh weight		 根长
Root length		 根表面积
Root surface area
0 0 0 0 0 0 0
300 21.52 21.07 54.93 40.67 64.27 49.66

图1

CdCl2胁迫对红麻不同部位镉含量的影响 不同小写字母表示在0.05水平差异显著。"

图2

MSAP聚丙烯酰胺凝胶电泳图 泳道M代表BM50 DNA marker; 泳道1和3代表EcoR I/Hpa II酶切; 泳道2和4代表EcoR I/Msp I酶切。1和2: 0 μmol L-1 CdCl2; 3和4: 300 μmol L-1 CdCl2。蓝色方框; I型(无甲基化); 黑色方框; II型(半甲基化); 白色方框; III型(全甲基化); 红色方框; IV型(全甲基化)。"

表5

DNA甲基化水平统计分析"

甲基化类型
Methylation type		 各类型的条带数和比率
Band numbers and ratio of each type		 变化比率(上升↑, 下降↓)
Exchange rate (up↑, down↓)
0 μmol L-1 300 μmol L-1
类型I (无甲基化) Type I (Unmethylation) 356 304 ↓ 14.61
类型II (半甲基化) Type II (Hemi-methylation) 242 305 ↑ 26.03
类型III, IV (全甲基化) Type III and IV (Full methylation) 359 348 ↓ 3.06
半甲基化率Hemi-methylated ratio (%) 25.28 31.87 ↑ 26.07
全甲基化率Fully methylated ratio (%) 37.50 36.36 ↓ 3.04
甲基化率/MSAP Total methylated ratio/MSAP (%) 62.78 68.23 ↑ 8.68

表6

甲基化差异片段比对分析"

序列编号
Sequence number		 甲基化差异片段比对结果
Comparisons of differentially methylated sequences		 功能注释
Functional annotation
1 Leucine-rich repeat receptor-like kinases, (LRR-RLK) At5g15730, Gossypium 充当胞外信号的受体, 参与各种环境及发育信号的感知和传递[22]。
As the receptor of extracellular signal, it participates in the perception and transmission of various environmental and developmental signals[22].
2 Zinc finger protein XlCGF8.2DB-like
(XlCGF8.2DB), Bemisia tabaci gastrula		 参与一些重要的调控过程, 如; 形态建成、花粉发育、胚发育、胁迫反应等[23]。
Widely involved in regulatory of important processes, such as morphogenesis, pollen development, embryo development, stress response, and so on[23].
3 Ankyrin-3-like, Gossypium arboreum 尚未见报道。
Has not been reported.
4 Trehalose-phosphate phosphatase D (GaTPPD), Gossypium arboreum 海藻糖磷酸磷酸酶在植物生长和胁迫反应中起重要作用[24]。
Trehalose phosphatase plays an important role in plant growth and stress response[24].
5 Serine/threonine-protein kinase, Gossypium raimondii 丝氨酸/苏氨酸蛋白激酶, 催化多种功能蛋白的磷酸化, 调控植物非生物胁迫[25]。
Serine/threonine protein kinases, catalyze the phosphorylation of various functional proteins and regulate abiotic stress in plants[25].
6 Peroxidasin (Pxdn) transcript variant X6, Castor canadensis 过氧化物酶, 植物抗逆过程中的关键酶之一[26]。
Peroxidase is one of the key enzymes in plant stress resistance[26].
7 Protein NRT1/ PTR FAMILY 2.7 (NPF2.7), Gossypium hirsutum NRT1/PTR家族蛋白参与转运植物激素及次生代谢物合成过程。
NRT1/PTR family proteins is involved in the transport of plant hormones and the synthesis of secondary metabolites.
8 60S ribosomal protein L16(RPL16), Gossypium hirsutum 参与细胞中蛋白质合成及调控基因表达[27]。
It is involved in protein synthesis and gene expression regulation[27].
9 Receptor-like protein kinase At2g46850, Durio zibethinus 类受体激酶通过接收和传递胞外信号调控细胞的生理反应, 参与植物生长发育过程。
Receptor like kinases are involved in plant growth and development by receiving and transmitting extracellular signals to regulate cell physiological responses.
10 Transcript variant X2, Gossypium raimondii 转录变异体X2, 参与细胞增殖及细胞周期活动的调节。
Transcription variant X2 is involved in the regulation of cell proliferation and cell cycle activity.
11 3-ketoacyl-CoA synthase 1 (GrKCS1), Gossypium raimondii 3-酮脂酰辅酶A合成酶, 在抵抗干旱和盐害等非生物胁迫过程中起着重要的作用。
3-ketoacyl coenzyme A synthetase plays an important role in abiotic stresses such as drought and salt stress.
12 L-ascorbate oxidase homolog (L-AAOh), Gossypium hirsutum 抗坏血酸氧化酶, 在调节植物发育过程和应激反应方面发挥重要作用[21]。
L-Ascorbic acid oxidase plays an important role in regulating plant development and stress response[21].
13 Indole-3-acetic acid-amido synthetase (GH3.1), Camellia sinensis 吲哚-3醋酸-酰胺合成酶, 通过调节植物体内激素的动态平衡, 参与调控植物的生长发育过程[18]。
Indole-3 acetate amide synthetase is involved in the regulation of plant growth and development by regulating the dynamic balance of hormones in plants[18].
14 Acyl-CoA-binding domain-containing protein 4 (ACBD4) 酰基辅酶A结合域蛋白, 在植物的生长发育、生物和非生物胁迫应答中起重要的作用。
Acyl-CoA-binding domain proteins play an important role in plant growth and development, biological and abiotic stress response.
序列编号
Sequence number		 甲基化差异片段比对结果
Comparisons of differentially methylated sequences		 功能注释
Functional annotation
15 ABC transporter G family member 26 (ABCG26), Gossypium arboreum ABC 转运蛋白G家族参与植物信号转导、次生代谢物运输和非生物胁迫响应等过程[20]。
ABC transporter G family are involved in plant signal transduction, secondary metabolite transport and abiotic stress response[20].
16 NADP-dependent malic enzyme (NADP-ME) At1G65930, Gossypium hirsutum NADP依赖苹果酸酶, 通过苹果酸代谢来平衡细胞内的pH来防御生物和非生物胁迫[19]。
NADP relies on malic acid enzyme to balance intracellular pH through malate metabolism to protect against biotic and abiotic stresses[19].
17 NAC domain-containing protein 71 (GrNAC71) NAC转录因子, 在逆境胁迫信号转导过程中发挥重要作用[28]。
NAC transcription factor plays an important role in stress signal transduction[28].
18 F-box protein At3g07870, Gossypium raimondii 参与调控胞内蛋白降解、受体识别和信号传导[29]。
It is involved in the regulation of intracellular protein degradation, receptor recognition and signal transduction[29].
19 Pentatricopeptide repeat-containing
protein (PPRC) At5g55740, Gossypium arboreum		 从RNA剪切、编辑、降解和翻译等多个方面影响细胞器中RNA的新陈代谢[30]。
RNA metabolism in organelles is affected by RNA splicing, editing, degradation, and translation[30].
20 Ethylene-responsive transcription factor 2 (ERF2) 乙烯转录因子(AP2/ERFs)调控激素响应非生物胁迫[31]。
Ethylene transcription factors (AP2/ERFs), widely involved in plant hormone regulation and thus response to abiotic stress[31].

图3

甲基化差异基因的qRT-PCR分析 不同小写字母表示处理在0.05水平差异显著。"

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