中国农业科学 ›› 2019, Vol. 52 ›› Issue (8): 1308-1323.doi: 10.3864/j.issn.0578-1752.2019.08.002
所属专题: 作物雄性不育
薛亚东1,杨露1,杨慧丽1,李冰1,林亚楠1,张怀胜1,郭战勇1,汤继华1,2()
收稿日期:
2018-12-10
接受日期:
2019-02-14
出版日期:
2019-04-16
发布日期:
2019-04-26
通讯作者:
汤继华
作者简介:
薛亚东,E-mail:基金资助:
XUE YaDong1,YANG Lu1,YANG HuiLi1,LI Bing1,LIN YaNan1,ZHANG HuaiSheng1,GUO ZhanYong1,TANG JiHua1,2()
Received:
2018-12-10
Accepted:
2019-02-14
Online:
2019-04-16
Published:
2019-04-26
Contact:
JiHua TANG
摘要:
【目的】通过分析玉米C型胞质雄性不育“三系”材料花药不同发育时期的转录组数据,以期阐明玉米C型胞质的不育和恢复机制,并解析不育基因与恢复基因之间相互作用的调控网络,为玉米C型细胞质雄性不育在不育化制种中的利用提供理论依据。【方法】以中国玉米生产上的骨干自交系豫自87-1为背景的C型胞质不育系、保持系、恢复系为材料,通过对3种材料减数分裂的前期Ⅰ、中期Ⅰ及末期Ⅱ(四分体)时期的花药进行转录组测序并利用hisat2、ballgown及DESeq2等工具进行生物信息学分析,寻找三系花药不同时期、相同时期不同材料间以及发育时序中差异表达的基因,预测C型胞质不育机制与育性恢复的调控网络;同时通过实时定量PCR对测序分析结果进行验证;通过酶活测定验证推测的C型胞质不育及恢复假说。【结果】所有材料的转录组测序共产生156.59 Gb的序列数据,比对并组装共得到53 035个基因;在恢复系与不育系、保持系与不育系以及“三系”花药不同时期之间共筛选出非重复差异基因5 676个,其中发育阶段差异基因4 705个,同时期材料间差异基因2 693个,发育时序差异基因135个。GO分子功能分析显示ATP和DNA结合相关的基因和锌离子结合基因得到高度富集;细胞组分中膜基本组分、核内及质膜内的基因得到富集;以DNA为模板的转录、转录调控、氧化还原及初级代谢等生物学过程中的基因得到富集。KEGG分析表明,差异基因主要富集于氧化磷酸化、碳代谢及糖酵解等能量代谢相关的途径中。不育系相对保持系而言,多个与氧化磷酸化相关的基因下调表达,而恢复系中不但相应基因的表达水平得到恢复,而且同时协调调节了同一能量代谢途径中的其他基因,定量分析显示差异基因的表达差异及趋势与转录组测序结果基本一致。ATP酶活结果表明不育系相比保持系,ATP酶活显著降低,恢复系中由于恢复基因的作用其活性得到大幅恢复。【结论】玉米C型胞质不育基因引起基因表达变化可能发生在减数分裂中期Ⅰ之后,末期Ⅱ之前;玉米C型胞质不育的形成可能是由于不育基因引起的能量亏损所致,而恢复基因则通过能量补偿促使育性得以恢复。
薛亚东,杨露,杨慧丽,李冰,林亚楠,张怀胜,郭战勇,汤继华. 玉米C型细胞质雄性不育花药不同发育时期的转录组分析[J]. 中国农业科学, 2019, 52(8): 1308-1323.
XUE YaDong,YANG Lu,YANG HuiLi,LI Bing,LIN YaNan,ZHANG HuaiSheng,GUO ZhanYong,TANG JiHua. Comparative Transcriptome Analysis Among the Three Line of Cytoplasmic Male Sterility in Maize[J]. Scientia Agricultura Sinica, 2019, 52(8): 1308-1323.
表1
差异基因表达分析所用引物"
引物名称 Primer name | 引物序列 Primer sequence (5′-3′) | 作用 Function |
---|---|---|
Zm00001d043834-F | GAGCAAGCTACAGAGCAGCA | Zm00001d043834表达分析 |
Zm00001d043834-R | GCACCACCAAAGAGACCAAT | For the expression of Zm00001d043834 |
Zm00001d009222-F | GAGATCCAGAGCGCCATTT | Zm00001d009222表达分析 |
Zm00001d009222-R | GAGCCCAGGAAGAGGAAGAT | For the expression of Zm00001d009222 |
Zm00001d007966-F | GTGCATCACCAAGCTCTTCC | Zm00001d007966表达分析 |
Zm00001d007966-R | GTGCCACCTCCAATCATCTT | For the expression of Zm00001d007966 |
Zm00001d009727-F | TTGTCTGCACGAGGAATCAG | Zm00001d009727表达表达 |
Zm00001d009727-R | ACCAGACGACATCGTGTTCA | For the expression of Zm00001d009727 |
表2
测序数据统计分析"
样品 Sample | 总序列 Total read pairs | 总碱基数 Total bases (Billion) | GC含量 GC percentage (%) | Q30比例 Q30 percentage (%) | 比对序列比例 Total mapping reads percentage (%) |
---|---|---|---|---|---|
CrP11 | 18374016 | 5.51 | 54.5 | 94.3 | 90.0 |
CrP12 | 16560680 | 4.96 | 54.5 | 93.7 | 91.1 |
CrP13 | 27650293 | 6.91 | 52.5 | 100.0 | 91.3 |
CrM11 | 17989607 | 5.39 | 54.5 | 93.3 | 90.6 |
CrM12 | 16908690 | 5.07 | 53.5 | 95.0 | 90.7 |
CrM13 | 26782609 | 6.69 | 52.0 | 100.0 | 91.5 |
CrT21 | 18705720 | 5.61 | 54.5 | 93.7 | 90.2 |
CrT22 | 17698741 | 5.31 | 54.5 | 95.0 | 90.1 |
CrT23 | 13798055 | 2.48 | 55.0 | 80.5 | 83.6 |
CRP11 | 22127378 | 6.63 | 54.0 | 100.0 | 90.6 |
CRP12 | 24978644 | 7.49 | 54.0 | 100.0 | 90.8 |
CRP13 | 27365104 | 6.84 | 52.0 | 100.0 | 91.7 |
CRM11 | 28575880 | 8.57 | 54.0 | 100.0 | 90.4 |
CRM12 | 18086263 | 5.42 | 55.0 | 97.6 | 89.8 |
CRM13 | 29768530 | 7.44 | 52.5 | 100.0 | 91.3 |
CRT21 | 27996156 | 8.39 | 55.5 | 93.3 | 90.3 |
CRT22 | 20498349 | 6.14 | 55.5 | 94.7 | 90.1 |
CRT23 | 12902671 | 2.32 | 55.0 | 78.9 | 83.1 |
NrP11 | 17959776 | 5.38 | 54.0 | 94.0 | 91.0 |
NrP12 | 18272442 | 5.48 | 55.0 | 94.7 | 90.4 |
NrP13 | 28541683 | 7.13 | 52.0 | 100.0 | 90.8 |
NrM11 | 19324515 | 5.79 | 55.5 | 94.0 | 89.6 |
NrM12 | 18245189 | 5.47 | 55.5 | 94.0 | 89.8 |
NrM13 | 29194399 | 7.29 | 52.5 | 100.0 | 92.1 |
NrT21 | 21652022 | 6.49 | 57.0 | 100.0 | 89.4 |
NrT22 | 20912786 | 6.27 | 56.0 | 100.0 | 90.0 |
表3
差异基因统计分析"
差异比较 Comparison | 表达趋势 Up-/Down regulated | 差异基因数 DE gene numbers | 差异比较 Comparison | 表达趋势 Up-/Down regulated | 差异基因数 DE gene numbers |
---|---|---|---|---|---|
CrM1/CrP1 | 上调Up | 48 | CRP1/CrP1 | 上调Up | 57 |
下调Down | 73 | 下调Down | 160 | ||
CrT2/CrM1 | 上调Up | 85 | CRM1/CrM1 | 上调Up | 273 |
下调Down | 329 | 下调Down | 380 | ||
CrT2/CrP1 | 上调Up | 230 | CRT2/CrT2 | 上调Up | 975 |
下调Down | 1088 | 下调Down | 454 | ||
CRM1/CRP1 | 上调Up | 233 | NrP1/CrP1 | 上调Up | 50 |
下调Down | 192 | 下调Down | 53 | ||
CRT2/CRM1 | 上调Up | 142 | NrM1/CrM1 | 上调Up | 99 |
下调Down | 188 | 下调Down | 64 | ||
CRT2/CRP1 | 上调Up | 732 | NrT2/CrT2 | 上调Up | 723 |
下调Down | 775 | 下调Down | 409 | ||
NrM1/NrP1 | 上调Up | 52 | 发育时序 Time Series | NA/无 | 135 |
下调Down | 54 | ||||
NrT2/NrM1 | 上调Up | 356 | NrT2/NrP1 | 上调Up | 786 |
下调Down | 560 | 下调Down | 1078 |
图2
差异表达GO分类 转运:Transport;翻译:Translation;DNA模板的转录:Transcription, DNA-templated;系统发育:System development;信号发射:Signaling;信号转导:Signal transduction;水缺乏响应:Response to water deprivation;胁迫响应:Response to stress;刺激物响应:Response to stimulus;盐胁迫响应:Response to salt stress;冷响应:Response to cold;化学物响应:Response to chemical;镉离子响应:Response to cadmium ion;脱落酸响应:Response to abscisic acid;转录调节:Regulation of transcription;细胞过程调节:Regulation of cellular process;生物学过程调节:Regulation of biological process;嘌呤核苷酸代谢过程:Purine ribonucleotide catabolic process;嘌呤三磷酸核苷代谢过程:Purine ribonucleoside triphosphate catabolic process;蛋白水解:Proteolysis;蛋白泛素化:Protein ubiquitination;蛋白磷酸化:Protein phosphorylation;初级代谢过程:Primary metabolic process;翻译后蛋白修饰:Post-translational protein modification;胚胎后动物器官发育:Post-embryonic animal organ development;DNA模板的转录正调控:Positive regulation of transcription, DNA-templated;磷酸化:Phosphorylation;氧化还原过程:Oxidation-reduction process;多细胞机体过程:Multicellular organismal process;多细胞生物发育:Multicellular organism development;多生物体过程:Multi-organism process;定位:Localization;基因表达:Gene expression;表皮细胞分化:Epidermal cell differentiation;发育过程:Developmental process;染色体组建:Chromosome organization;细胞过程:Cellular process;细胞氮复合物代谢过程:Cellular nitrogen compound metabolic process;细胞代谢过程:Cellular metabolic process;细胞大分子代谢过程:Cellular macromolecule metabolic process;细胞大分子生物合成过程:Cellular macromolecule biosynthetic process;细胞酮基代谢过程:Cellular ketone metabolic process;细胞组分组建:Cellular component organization;细胞生物合成过程:Cellular biosynthetic process;生物合成过程:Biosynthetic process;生物学调控:Biological regulation;动物器官发育:Animal organ development;解剖结构的形态建成:Anatomical structure morphogenesis;形态建成中解剖结构的形成:Anatomical structure formation involved in morphogenesis;液泡:Vacuole;液泡膜:Vacuolar membrane;蛋白复合体:Protein complex;胞间连丝:Plasmodesma;质膜:Plasma membrane;植物类型细胞壁:Plant-type cell wall;核:Nucleus;核仁:Nucleolus;线粒体:Mitochondrion;膜:Membrane;膜基本组分:Integral component of membrane;高尔基体装置:Golgi apparatus;细胞外区域:Extracellular region;内质网:Endoplasmic reticulum;细胞溶质:Cytosol;细胞质:Cytoplasm;叶绿体基质:Chloroplast stroma;叶绿体:Chloroplast;细胞壁:Cell wall;质外体:Apoplast;锌离子结合:Zinc ion binding;特定序列的DNA结合:Sequence-specific DNA binding;RNA结合:RNA binding;蛋白丝氨酸/苏氨酸激酶活性:Protein serine/threonine kinase activity;蛋白二聚化活性:Protein dimerization activity;核苷酸结合:Nucleotide binding;核酸结合:Nucleic acid binding;金属离子结合:Metal ion binding;DNA结合的转录因子活性:DNA binding transcription factor activity;DNA结合:DNA binding;结合:Binding;ATP结合:ATP binding。BP:生物过程 Biological processes;CC:细胞组分 Cell components;MF:分子功能 Molecular function"
表4
差异表达基因数量最多的15个代谢通路"
代谢通路 Pathway ID | 通路名称 Name of pathways | 通路出现次数 Occurrences of pathways | 基因数目 Counts of genes |
---|---|---|---|
zma01200 | 碳代谢 Carbon metabolism | 1 | 28 |
zma00010 | 糖酵解 Glycolysis/Gluconeogenesis | 1 | 20 |
zma03030 | DNA复制 DNA replication | 1 | 19 |
zma00620 | 丙酮酸盐代谢 Pyruvate metabolism | 2 | 16 |
zma03440 | 同源重组 Homologous recombination | 1 | 15 |
zma00071 | 脂肪酸降解 Fatty acid degradation | 5 | 14 |
zma00130 | 辅酶Q及其他萜-醌合成 Ubiquinone and other terpenoid-quinone biosynthesis | 6 | 13 |
zma00040 | 戊糖与葡萄糖醛酸相互转换 Pentose and glucuronate interconversions | 1 | 9 |
zma00073 | 角质、软木脂及蜡质合成 Cutin, suberine and wax biosynthesis | 12 | 8 |
zma00940 | 苯丙烷合成 Phenylpropanoid biosynthesis | 5 | 6 |
zma00290 | 缬氨酸、亮氨酸和异亮氨酸合成 Valine, leucine and isoleucine biosynthesis | 2 | 5 |
zma02010 | ABC运输 ABC transporters | 1 | 5 |
zma00500 | 淀粉和蔗糖代谢 Starch and sucrose metabolism | 1 | 4 |
zma00770 | 泛酸酯和辅酶A合成 Pantothenate and CoA biosynthesis | 1 | 4 |
zma04016 | 植物MAPK信号途径 MAPK signaling pathway-plant | 1 | 4 |
表5
线粒体氧化磷酸化途径相关基因的表达差异"
基因编号 ID number of gene | 中期Ⅰ恢复系比不育系 CR/Cr-m1 | 四分体恢复系比不育系 CR/Cr-t2 | 四分体保持系比不育系 Nr/Cr-t2 | 不育系四分体比前期Ⅰ Cr-t2/p1 | 保持系四分体比中期Ⅰ Nr-t2/m1 | 保持系四分体比前期Ⅰ Nr-t2/p1 | 恢复系四分体比前期Ⅰ CR-t2/p1 | 染色体 Chr. | 基因功能描述 Description |
---|---|---|---|---|---|---|---|---|---|
Zm00001d033552 | 2.94±0.83 | 3.60±0.83 | 3.78±0.93 | 4.09±0.93 | 5.95±0.93 | 5.15±0.83 | 1 | 腺苷三磷酸酶4, 质膜类型 ATPase 4 plasma membrane-type | |
Zm00001d043834 | 1.33±0.40 | 1.44±0.40 | 1.42±0.40 | 1.07±0.35 | 3 | 类线粒体腺苷三磷酸合成酶贝塔亚基 ATP synthase subunit beta, mitochondrial-like | |||
Zm00001d045122 | 4.60±1.08 | 4.04±1.19 | 9 | 腺苷三磷酸酶8, 质膜类型 ATPase 8 plasma membrane-type | |||||
Zm00001d041214 | 1.74±0.54 | 3 | 腺苷三磷酸酶4, 质膜类型 ATPase 4 plasma membrane-type | ||||||
Zm00001d015569 | 1.64±0.41 | 5 | 液泡质子泵同系物1 Vacuolar proton pump homolog 1 | ||||||
Zm00001d037576 | 2.22±0.6 | 2.54±0.67 | -1.85±0.60 | 6 | 焦磷酸供能的液泡质膜质子泵 Pyrophosphate-energized vacuolar membrane proton pump | ||||
Zm00001d009222 | 3.38±1.07 | -3.61±1.06 | -7.12±1.77 | -7.90±1.77 | 8 | 焦磷酸供能的液泡质膜质子泵 Pyrophosphate-energized vacuolar membrane proton pump | |||
Zm00001d052022 | -5.78±1.58 | 4 | 腺苷三磷酸酶8, 质膜类型 ATPase 8 plasma membrane-type | ||||||
Zm00001d045497 | -2.04±0.59 | 9 | V型质子偶联腺苷三磷酸亚基e1 V-type proton ATPase subunit e1 | ||||||
Zm00001d027304 | -3.2±0.90 | -2.94±1.00 | -3.17±0.90 | 1 | 腺苷三磷酸酶9, 质膜类型 ATPase 9, plasma membrane-type | ||||
Zm00001d007966 | -1.18±0.30 | -1.17±0.30 | 2 | 琥珀酸脱氢酶4 Succinate dehydrogenase4 | |||||
Zm00001d036728 | -4.01±0.95 | 6 | 腺苷三磷酸酶2, 质膜类型 ATPase 2, plasma membrane-type | ||||||
Zm00001d009727 | -8.63±2.86 | 8 | 线粒体细胞色素c氧化酶亚基5b-2 Cytochrome c oxidase subunit 5b-2 mitochondrial |
表6
细胞色素P450基因的表达"
时期 stage | 比较 Comparison | 表达 Expression | 差异倍数log2FLC | 基因ID Gene ID | 染色体 Chr. | 功能描述 Description |
---|---|---|---|---|---|---|
末期2 Telo2 | Nr/Cr | 上调Up | 21.83 | Zm00001d024412 | 10 | NADPH-细胞色素P450还原酶 NADPH-cytochrome P450 reductase |
9.20 | Zm00001d042814 | 3 | 86A1型细胞色素P450 Cytochrome P450 86A1 | |||
7.31 | Zm00001d011932 | 8 | 类89A2型细胞色素P450 Cytochrome P450 89A2-like | |||
6.94 | Zm00001d013862 | 5 | 细胞色素P450大家族蛋白 Cytochrome P450 superfamily protein | |||
6.92 | Zm00001d029526 | 1 | 78A5型细胞色素P450 Cytochrome P450 78A5 | |||
下调Down | -17.05 | Zm00001d039697 | 3 | 类711A1型细胞色素P450 Cytochrome P450 711A1-like | ||
-20.91 | Zm00001d004486 | 2 | 71D7型细胞色素P450 Cytochrome P450 71D7 | |||
CR/Cr | 上调Up | 18.54 | Zm00001d024412 | 10 | 细胞色素P450还原酶 Cytochrome P450 reductase | |
8.54 | Zm00001d042814 | 3 | 86A1型细胞色素P450 Cytochrome P450 86A1 | |||
7.29 | Zm00001d013862 | 5 | 推断的细胞色素P450大家族蛋白 Putative cytochrome P450 superfamily protein | |||
7.23 | Zm00001d011932 | 8 | 类89A2型细胞色素P450 Cytochrome P450 89A2-like | |||
6.46 | Zm00001d012326 | 8 | 细胞色素P450大家族蛋白 Cytochrome P450 superfamily protein | |||
5.82 | Zm00001d029526 | 1 | 78A5型细胞色素P450 Cytochrome P450 78A5 | |||
下调Down | -1.22 | Zm00001d002937 | 2 | 细胞色素P450,72家族,A亚族,多肽8 Cytochrome P450 family 72 subfamily A polypeptide 8 | ||
-20.04 | Zm00001d039697 | 3 | 类711A1型细胞色素P450 Cytochrome P450 711A1-like | |||
-23.94 | Zm00001d004486 | 2 | 71D7型细胞色素P450 Cytochrome P450 71D7 | |||
中期1 Meta1 | Nr/Cr | 上调Up | - | - | - | - |
下调Down | - | - | - | - | ||
CR/Cr | 上调Up | 7.46 | Zm00001d011932 | 8 | 类89A2型细胞色素P450 Cytochrome P450 89A2-like | |
6.79 | Zm00001d013862 | 5 | 推断的细胞色素P450大家族蛋白 Putative cytochrome P450 superfamily protein | |||
3.88 | Zm00001d020673 | 7 | 推断的细胞色素P450大家族蛋白 Putative cytochrome P450 superfamily protein | |||
下调Down | -3.58 | Zm00001d049573 | 4 | 推断的细胞色素P450大家族蛋白 Putative cytochrome P450 superfamily protein | ||
-4.16 | Zm00001d037701 | 6 | 推断的细胞色素P450大家族蛋白 Putative cytochrome P450 superfamily protein | |||
-16.87 | Zm00001d039697 | 3 | 类711A1型细胞色素P450 Cytochrome P450 711A1-like | |||
前期1 Prop1 | Nr/Cr | 上调Up | 19.96 | Zm00001d024412 | 10 | NADPH-细胞色素P450还原酶 NADPH--cytochrome P450 reductase |
17.59 | Zm00001d042814 | 3 | 86A1型细胞色素P450 Cytochrome P450 86A1 | |||
下调Down | - | - | - | - | ||
CR/Cr | 上调Up | 17.44 | Zm00001d042814 | 3 | 86A1型细胞色素P450 Cytochrome P450 86A1 | |
下调Down | - | - | - | - |
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