基于二代和三代转录组测序揭示甘蔗重要亲本对黑穗病菌侵染的响应机制

doi:10.3724/SP.J.1006.2023.24228

作物学报 ›› 2023, Vol. 49 ›› Issue (9): 2412-2432.doi: 10.3724/SP.J.1006.2023.24228

• 作物遗传育种·种质资源·分子遗传学 • 上一篇下一篇

基于二代和三代转录组测序揭示甘蔗重要亲本对黑穗病菌侵染的响应机制

胡鑫(), 罗正英, 李纯佳, 吴转娣, 李旭娟, 刘新龙()

云南省农业科学院甘蔗研究所 / 云南甘蔗遗传改良重点试验室 / 农业农村部甘蔗生物学与遗传育种重点实验室(云南), 云南开远 661699

收稿日期:2022-10-12 接受日期:2023-02-21 出版日期:2023-09-12 网络出版日期:2023-03-10
通讯作者: *刘新龙, E-mail: lxlgood868@163.com
作者简介:胡鑫, E-mail: sugarhuxin@163.com
基金资助:
云南基础研究计划项目(2019FA016);云南基础研究计划项目(202201AU070200);云南省种子种业联合实验室项目(202205AR070001-09)

Comparative transcriptome analysis of elite ‘ROC’ sugarcane parents for exploring genes involved in Sporisorium scitamineum infection by using Illumina- and SMRT-based RNA-seq

HU Xin(), LUO Zheng-Ying, LI Chun-Jia, WU Zhuan-Di, LI Xu-Juan, LIU Xin-Long()

Sugarcane Research Institute, Yunnan Academy of Agricultural Sciences / Yunnan Key Laboratory of Sugarcane Genetic Improvement / Key Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs (Yunnan), Kaiyuan 661699, Yunnan, China

Received:2022-10-12 Accepted:2023-02-21 Published:2023-09-12 Published online:2023-03-10
Supported by:
Yunnan Fundamental Research Projects(2019FA016);Yunnan Fundamental Research Projects(202201AU070200);Yunnan Seeds and Seed Industry Joint Laboratory Project(202205AR070001-09)

摘要/Abstract

摘要：

黑穗病是甘蔗生产中的主要病害, 严重影响甘蔗产量。解析甘蔗重要亲本与黑穗病菌相互作用的分子机制及筛选抗病基因对抗黑穗病优良品种的培育具有重要意义。本研究选用我国甘蔗育种中的重要亲本新台糖ROC25 (抗黑穗病)及其姊妹系ROC22 (感黑穗病)为研究对象, 采用单分子实时测序技术(三代测序)和二代转录组测序技术分析和鉴定2个亲本感染黑穗病菌后的转录组谱及差异转录本。三代转录组测序分析共获得79,885条转录本序列, 其中含60,115条完整开放阅读框、3692个可变剪接事件、1799个LncRNA、29,139个SSR和7794个转录因子, 共有74,066个转录本得到注释, 占总数的92.72%。通过对二代测序数据分析, 在抗病亲本中筛选出9716个差异转录本, 在感病亲本中筛选出2033个差异转录本。差异转录本的GO和KEGG富集分析结果表明抗病亲本中共富集到的GO条目和KEGG通路均要多于感病亲本, 且植物MAPK信号通路、苯丙素生物合成、植物-病原互作、亚油酸代谢和蔗糖和淀粉代谢等代谢通路在抗感亲本中均被显著富集, 为抗感亲本对黑穗病的共同抗病途径。进一步, 对植物MAPK信号通路的分析表明, MAPK超家族基因成员在抗感亲本中呈现不同的表达方式, 在抗病亲本中具有更多差异表达的MEKK1和MKK4的转录本, 且MKK5、MPK10和MPK12基因仅在抗病品种中发生显著表达变化, 推测其可能与亲本的抗病表型关联。此外, 抗感亲本中众多WRKY、MYB、NAC和AP2/ERF-ERF等抗病相关转录因子响应了黑穗病菌胁迫, 且主要表现为上调表达。与感病亲本相比, 抗病亲本显示出更多的差异表达转录因子, 推测这些抗病亲本特有的转录因子可能对防御黑穗病菌具有积极作用。本研究完善了新台糖亲本基因组注释信息, 为解析新台糖优异亲本与黑穗病菌互作机制以及抗黑穗病基因资源的挖掘利用提供指导。

关键词: 甘蔗, 黑穗病菌, 全长转录组, RNA-seq, 新台糖

Abstract:

Sugarcane smut, caused by the fungus Sporisorium scitamineum, is the most challenging disease of sugarcane, causing significant losses in cane yield. There is a dearth of information on smut resistance mechanism in elite parents for the development of smut-resistant varieties. In the present study, we adopted joint Illumina- and Single Molecule Real-Time (SMRT)-based RNA-seq analysis to identify transcript expression in an smut-resistant and -susceptible parents (ROC25 and ROC22) infected with S. scitamineum. A total of 79,885 high-quality transcripts was obtained, including 60,115 open reading frames, 3692 alternate splicing isoforms, 1799 long non-coding RNAs, 29,139 simple sequence repeats, and 7794 transcription factors. About 92.72% of the total transcripts were annotated, which should have increased the available data amount for transcriptome profile analysis. There were 2033 and 9716 differentially expressed transcripts (DETs) in ROC22 and ROC25, respectively. The analyses of GO and KEGG enrichment showed that more GO terms and KEGG pathways were observed in ROC25 than ROC22. It was found that MAPK signalling pathway-plant, phenylpropanoid biosynthesis, plant-pathogen interaction, linoleic acid metabolism, and starch and sucrose metabolism were enriched both in resistant and susceptible parents. In addition, MAPK superfamily genes were differentially regulated in different parents, more DETs of MEKK1 and MKK4 were detected in resistant parent, and the relative expression levels of MKK5, MPK10, and MPK12 genes were specifically altered in resistant parent. It suggested that MAPK superfamily genes might play the important roles in the regulation of sugarcane response to S. scitamineum infection. Moreover, lots of transcription factors (TFs) associated with plant disease resistance were found to respond to S. scitamineum infection in both ROC22 and ROC25 parents, including WRKY, MYB, NAC, and AP2/ERF-ERF. Majority of the TFs were up-regulated. Compared to the susceptible ROC22 parent, the number of activated transcription factors in the resistant ROC25 parent was higher, indicating that these extra TFs might have positive effects in the defense against S. scitamineum. This study provides a comprehensive set of reference transcripts for sugarcane and thus increases our understanding on the interactions between sugarcane and S. scitamineum, which should be helpful in guiding on exploitation and utilization of smut-resistance gene resources.

Key words: sugarcane, Sporisorium scitamineum, full-length transcriptomes, RNA-seq, ROC

胡鑫, 罗正英, 李纯佳, 吴转娣, 李旭娟, 刘新龙. 基于二代和三代转录组测序揭示甘蔗重要亲本对黑穗病菌侵染的响应机制[J]. 作物学报, 2023, 49(9): 2412-2432.

HU Xin, LUO Zheng-Ying, LI Chun-Jia, WU Zhuan-Di, LI Xu-Juan, LIU Xin-Long. Comparative transcriptome analysis of elite ‘ROC’ sugarcane parents for exploring genes involved in Sporisorium scitamineum infection by using Illumina- and SMRT-based RNA-seq[J]. Acta Agronomica Sinica, 2023, 49(9): 2412-2432.

图/表 15

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附图1

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表5

ROC22 and ROC25感染黑穗病菌后差异表达的MAPK超级家族基因"

转录本名称 Transcritp ID	基因名 Gene ID	log₂(FC)
转录本名称 Transcritp ID	基因名 Gene ID	SW5d-vs-SS5d	SW8d-vs-SS8d	SW11d-vs-SS11d	RW5d-vs-RS5d	RW8d-vs-RS8d	RW11d-vs-RS11d
F01_transcript_115924	MEKK1	-0.1614	-0.0838	-0.2729	0.1979	1.1462^**	0.1635
F01_transcript_120122	MEKK1	0.3479	-0.1157	0.0410	0.1525	1.1749^**	0.0612
F01_transcript_41431	MEKK1	1.0244	-0.2638	-0.0968	0.6841	1.8470^**	0.2169
F01_transcript_6191	MEKK1	0.3943	0.0512	0.1264	0.1595	1.3689^**	0.1557
F01_transcript_68151	MEKK1	0.1510	0.3081	0.3105	0.2617	1.3543^**	0.1533
F01_transcript_7538	MEKK1	0.1827	0.2544	-0.0911	0.1083	1.1495^**	0.1818
F01_transcript_88331	MEKK1	0.2773	-0.0902	-0.0362	0.0474	1.1993^**	0.1769
F01_transcript_23414	MEKK1	1.2139^**	-0.3284	0.2417	0.3994	0.9609^**	-0.8091
F01_transcript_62670	MKK5	0.4105	0.1947	-0.2444	0.7258^*	1.3829^**	0.1018
F01_transcript_66954	MKK5	0.5368	0.2693	-0.1905	0.5021	1.1541^**	0.3214
F01_transcript_100608	MPK4	1.0335^**	0.0591	0.2897	0.8256^**	2.0799^**	-0.1261
F01_transcript_108403	MPK4	0.6234	0.0827	0.0487	0.2481	1.4680^**	-1.1494^**
F01_transcript_124690	MPK4	0.5862	0.2034	-0.2955	0.0533	1.8433^**	-0.6117
F01_transcript_44325	MPK4	-0.0594	-0.0003	-0.0301	-0.0253	1.0736^**	-1.1649^**
F01_transcript_50250	MPK4	0.3101	0.0442	0.0138	0.0402	1.2023^**	-1.0936^**
F01_transcript_100187	MPK5	1.4254^**	0.2182	0.4447	0.4336	2.6910^**	0
F01_transcript_114847	MPK5	0.9429	0.5651	-0.5916	-0.2143	2.9083^**	-0.1926
F01_transcript_21269	MPK5	1.4307^**	0.3602	0.0160	0.2160	2.4543^**	-1.0587^*
F01_transcript_22098	MPK5	1.3170^**	0.4901	-0.0618	0.2325	2.9756^**	-1.0525^**
F01_transcript_50394	MPK5	0.9511	-0.0242	1.8625	0.7534	2.9206^*	-0.2538
F01_transcript_92541	MPK5	1.4680^**	0.3570	0.1825	0.0913	2.5695^**	-1.3285^*
F01_transcript_79030	MPK10	0.0748	0.1538	-0.0760	0.6273^*	1.1745^**	0.2728
F01_transcript_103525	MPK12	0.9006	-0.0089	0.9832	0.4093	2.3050^**	-1.4729
F01_transcript_110871	MPK12	0.6251	0.5034	0.0290	0.6422	2.5462^**	0.5090
F01_transcript_55631	MPK12	0.6746	0.4856	0.6111	0.4327	1.9302^**	-0.0233
F01_transcript_6660	MPK12	0.2403	0.1333	-0.0408	0.1689	1.4939^**	-0.3976
F01_transcript_6996	MPK12	-0.1050	0.3137	-0.6515	0.2966	1.6429^**	-0.3540
F01_transcript_72629	MPK12	0.3551	-0.2691	1.1131	0.6586	1.8283^**	-0.5795
F01_transcript_98181	MPK12	1.2283	0.2168	-0.6781	0.3370	3.3959^*	-1.3219

表5

表6

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品种 Variety	处理方式 Treatment	接种后天数 Days after inoculation (d)	样品编号 Samples no.	生物重复样品编号 Number of biological duplicate sample
ROC25	黑穗病孢子侵染S. scitamineum inoculation	5	RS5d	RS5dR1, RS5dR2, RS5dR3
	黑穗病孢子侵染S. scitamineum inoculation	8	RS8d	RS8dR1, RS8dR2, RS8dR3
	黑穗病孢子侵染S. scitamineum inoculation	11	RS11d	RS11dR1, RS11dR2, RS11dR3
	清水处理Water inoculation	5	RW5d	RW5dR1, RW5dR2, RW5dR3
	清水处理Water inoculation	8	RW8d	RW8dR1, RW8dR2, RW8dR3
	清水处理Water inoculation	11	RW11d	RW11dR1, RW11dR2, RW11dR3
ROC22	黑穗病孢子侵染S. scitamineum inoculation	5	SS5d	SS5dR1, SS5dR1, SS5dR2
	黑穗病孢子侵染S. scitamineum inoculation	8	SS8d	SS8dR1, SS8dR1, SS8dR2
	黑穗病孢子侵染S. scitamineum inoculation	11	SS11d	SS11dR1, SS11dR1, SS11dR2
	清水处理Water inoculation	5	SW5d	SW5dR1, SW5dR2, SW5dR3
	清水处理Water inoculation	8	SW8d	SW8dR1, SW8dR2, SW8dR3
	清水处理Water inoculation	11	SW11d	SW11dR1, SW11dR2, SW11dR3

基因编号 Gene ID	正向引物序列 Forward sequences (5°-3')	反向引物序列 Reverse sequences (5°-3')
25S RNA-1	ATAACCGCATCAGGTCTCCAAG	CCTCAGAGCCAATCCTTTTCC
25S RNA-2	GCAGCCAAGCGTTCATAGC	CCTATTGGTGGGTGAACAATCC
GAPDH	CACGGCCACTGGAAGCA	TCCTCAGGGTTCCTGATGCC
actin	CTGGAATGGTCAAGGCTGGT	TCCTTCTGTCCCATCCCTACC
tubulin	CCAAGTTCTGGGAGGTGATCTG	TTGTAGTAGACGTTGATGCGCTC
F01_transcript_48016	CGAATCCGAACTACTTTAACCCC	GTAGTCCTTGCCCTCCTTCGTC
F01_transcript_95850	TTCTACAATGGACCAGCGATG	ACGGTACAGGGAACGCTCTAAT
F01_transcript_47889	AGGACCAGTGGAAGGAGACGG	TGACCCTGCTGACGCCTCTTG
F01_transcript_100210	CACCACTACTGCTCTTCCTCCCC	GAGCTGTAGCCGAAGCGAGAC
F01_transcript_114120	GCACGCACAAGTCAGACCAGG	GATGAGCGGGATCGTCGAGGG
F01_transcript_122916	CCACCTGTGATGAGCATGAAGA	GGGTCCTGCATCCACTCCTG
F01_transcript_36883	GGGGATAAGGTGCTGGTGGT	CTTCTCCCTGGACGAGTGCC
F01_transcript_4165	TCAAGCACAAACGACGAATAGT	CCCTGACCACCTTCTCCAATG
F01_transcript_102327	TGAATGAAGCCCTGCGAGAA	TTGTGATGCTGAGCCTGGTG
F01_transcript_106895	GGAGACCGGGAACACTGACCTG	CGAAGAACGTGCTGCATGGGT
F01_transcript_116870	CCGATGTCCATGTTCGGGATG	CGAGCGTGCTGCCGTTGTAG
F01_transcript_123150	TACCTCCGACCACTCTTCTCC	CTGTTCTGCCTTCCCACGAGA
F01_transcript_124105	ATGGGCAAACTTGGGACACTC	GGCAAGAAGAGCACGAGAAGC
F01_transcript_124126	ATTGTCAAGGAGGCAAGAACC	GCGAACCTCCCTAACCCTCTT
F01_transcript_21134	GACCGGGTGCCTGAAGAAGT	GGCGTGTAGTAGTCGGCGTAG

数据库名称 Annotated databases	转录本数目 Isoform number	占比 Proportion in total (%)
Nr	73,781	92.36
eggNOG	70,639	88.43
GO	62,274	77.95
Pfam	58,475	73.20
Swiss-Prot	51,974	65.06
KOG	39,415	49.34
KEGG	31,331	39.22
COG	25,455	31.86
All	74,066	92.72

eggNOG注释分类 eggNOG_class	频率 Frequency	占比 Proportion in total (%)
未知功能Function unknown	35,891	50.81
信号转导机制Signal transduction mechanisms	4924	6.97
翻译后修饰、蛋白质折叠和伴侣蛋白Posttranslational modification, protein turnover, and chaperones	4856	6.87
转录Transcription	3435	4.86
碳水化合物转运代谢Carbohydrate transport and metabolism	3117	4.41
胞内转运、分泌和小泡运输Intracellular trafficking, secretion, and vesicular transport	2447	3.46
氨基酸转运代谢Amino acid transport and metabolism	2223	3.15
复制、重组和修复Replication, recombination, and repair	2157	3.05
翻译、核糖体结构和生物合成Translation, ribosomal structure, and biogenesis	2128	3.01
脂肪转运代谢Lipid transport and metabolism	1328	1.88
能量生成和转换Energy production and conversion	1327	1.88
无机离子转运代谢Inorganic ion transport and metabolism	1201	1.70
细胞壁/膜/被膜的生物合成Cell wall/membrane/envelope biogenesis	1168	1.65
次级代谢物生物合成、转运和代谢Secondary metabolites biosynthesis, transport, and catabolism	915	1.30
细胞骨架Cytoskeleton	799	1.13
核苷酸转运和代谢Nucleotide transport and metabolism	584	0.83
辅酶转运和代谢Coenzyme transport and metabolism	552	0.78
RNA加工修饰RNA processing and modification	474	0.67
抵御机制Defense mechanisms	469	0.66
细胞周期控制、细胞分裂和染色体分裂Cell cycle control, cell division, and chromosome partitioning	317	0.45
染色质结构和动力学Chromatin structure and dynamics	288	0.41
细胞运动Cell motility	35	0.05
核酸结构Nuclear structure	4	0.01

基于二代和三代转录组测序揭示甘蔗重要亲本对黑穗病菌侵染的响应机制

Comparative transcriptome analysis of elite ‘ROC’ sugarcane parents for exploring genes involved in Sporisorium scitamineum infection by using Illumina- and SMRT-based RNA-seq

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转录因子家族Transcription factor family	检测出转录因子基因数Detected TF family number	差异表达的转录因子基因数 Number of differentially expressed TF family genes			差异表达基因表达模式(上调/下调) Dynamic expression patterns of differentially expressed TF family genes (Up-regulated/Down-regulated)
转录因子家族Transcription factor family	检测出转录因子基因数Detected TF family number	ROC22	ROC25	共同 Shared	SW5d-vs-SS5d	SW8d-vs-SS8d	SW11d-vs-SS11d	RW5d-vs-RS5d	RW8d-vs-RS8d	RW11d-vs-RS11d
AP2/ERF-ERF	34	7	23	6	7/0	0/0	0/0	6/0	12/4	9/4
MYB	24	4	13	3	3/0	0/0	1/0	0/0	4/4	5/4
NAC	25	12	16	10	11/1	0/0	0/0	1/0	10/0	10/1
WRKY	37	15	20	14	15/0	1/1	3/0	4/0	18/0	5/3

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