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

doi:10.3864/j.issn.0578-1752.2019.08.002

Abstract

Abstract:

【Objective】It is one of the most efficient ways to utilize cytoplasmic male sterile (CMS) lines in hybrid seed production, which could improve the purity of seeds, reduce the cost in creating hybrid seeds and enhance the competitiveness of Chinese seed companies. The comparative transcriptome analysis of the anthers at different development stages from the CMS line, the maintainer line and the restorer line (the three lines) were performed in order to understand the mechanism of sterility and restoration of CMS-C in maize, and also to elucidate the regulation network between the restorer gene and the sterile gene, which will provide the fundamental basis for the employment of maize CMS in hybrid seed production.【Method】The transcriptome sequencing was carried out on the anthers at the prophaseⅠ, the metaphaseⅠand the tetrad stage from the three lines based on the elite inbred line Yu87-1. Method of comparative analysis was used to deal with all the transcripts by the tools such as hisat2, ballgown and DESeq2, and to predict genes involved in the regulation network between the sterile gene and the restorer gene, between the different development stages and through the development time series. qRT-PCR was used to verify the differentially expressed genes. The activity of ATPase was quantified with by the spectrophotometric method for the verification of the putative hypothesis.【Result】Transcriptome sequencing totally produced 156.59 Gb sequence data. After mapping and assembling, 53035 Unigenes were obtained. A total of 5676 differentially expressed (DE) genes were identified from the pairwise comparisons (except for comparisons between the restorer lines and the maintainer lines) in the anthers at the different stages from the three lines. Of those, 4705 DE genes between the comparisons of the development stages, 2693 DE genes between the comparisons of the different lines and 135 DE genes related to the time series. The GO molecular functional analysis showed that the genes related to ATP binding, DNA binding and zinc ion binding were highly enriched, in cell component analysis, genes located in integral component of membrane, nucleus and plasma membrane were enriched, and in biological process, genes involved in DNA-templated transcription, regulation of transcription, oxidation-reduction process and primary metabolic process were enriched. KEGG pathway analysis indicated that the oxidative phosphorylation pathways, the carbon metabolism pathways and glycolysis pathways were mostly enriched. Compared to the maintainer lines, several genes involving in the oxidative phosphorylation pathways were significantly down-regulated in the sterile lines, while those down-regulated genes were recovered, besides other genes in the same pathways were also coordinately regulated. The expression trend determined by qRT-PCR on the selected DE genes was in accordance with that in the transcriptome data. The enzyme activity results show that the activity of ATPase in the sterile line was greatly reduced compared to the maintainer line, while in the restorer line, the activities the ATPase were restored due to the existence of the restorer gene.【Conclusion】 The onset of the changes in the gene expression caused by the sterile gene in the anthers of CMS-C maize may happen after metaphaseⅠ and before telophase Ⅱ in meiosis before visible phenotype occurred. The energy deficiency model may account for the mechanism of the sterility in maize CMS-C, and the energy requirements were compensated by the restorer gene through direct or indirect manner.

Key words: Zea mays, cytoplasmic male sterility, transcriptome, differentially expressed gene, regulation network

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.

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Figures/Tables 13

Table 1

Table 2

Fig. 1

Table 3

Fig. 2

Table 4

Table 5

Differential expression of the genes involved in oxidative phosphorylation pathway"

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

Table 5

Fig. 3

Fig. 4

Fig. 5

Table 6

Expression of cytochrome P450 genes"

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
		下调Down	-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	-	-	-	-
	Nr/Cr	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
		上调Up	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
	CR/Cr	下调Down	-	-	-	-

Table 6

Fig. 6

Fig. 7

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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

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

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
CrM1/CrP1	下调Down	73	CRP1/CrP1	下调Down	160
CrT2/CrM1	上调Up	85	CRM1/CrM1	上调Up	273
CrT2/CrM1	下调Down	329	CRM1/CrM1	下调Down	380
CrT2/CrP1	上调Up	230	CRT2/CrT2	上调Up	975
CrT2/CrP1	下调Down	1088	CRT2/CrT2	下调Down	454
CRM1/CRP1	上调Up	233	NrP1/CrP1	上调Up	50
CRM1/CRP1	下调Down	192	NrP1/CrP1	下调Down	53
CRT2/CRM1	上调Up	142	NrM1/CrM1	上调Up	99
CRT2/CRM1	下调Down	188	NrM1/CrM1	下调Down	64
CRT2/CRP1	上调Up	732	NrT2/CrT2	上调Up	723
CRT2/CRP1	下调Down	775	NrT2/CrT2	下调Down	409
NrM1/NrP1	上调Up	52	发育时序 Time Series	NA/无	135
NrM1/NrP1	下调Down	54	发育时序 Time Series	NA/无	135
NrT2/NrM1	上调Up	356	NrT2/NrP1	上调Up	786
NrT2/NrM1	下调Down	560	NrT2/NrP1	下调Down	1078

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

Comparative Transcriptome Analysis Among the Three Line of Cytoplasmic Male Sterility in Maize

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