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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()   

  1. 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()   

  1. 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:

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MEKK1MKK4的转录本, 且MKK5MPK10MPK12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

表1

黑穗病菌接种设计和转录组测序样品采取"

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

表2

实时荧光定量PCR的引物序列"

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

图1

全长转录组测序一致性序列度长分布和完整度评估 A为全长转录组测序获得的一致性序列的长度分布, 左侧Y坐标轴对应一致性序列长度频数分布直方图, 右侧Y坐标轴对应一致性序列长度累积频率曲线。B为全长转录组测序获得的一致性序列的完整性评估结果。"

图2

甘蔗全长转录本特征和结构分析 A为基因的可变剪接事件发生次数分析; B为CPC、CNCI、pfam蛋白结构域和CPAT等4种分析方法预测的LncRNA的韦恩分析; C为SSR类型分布作图, c为混合微卫星(2个SSR距离小于100 bp), p1为单碱基, p2为双碱基, p3为三碱基, p4为四碱基, p5为五碱基, p6为六碱基; D为预测的CDS编码蛋白长度分布图; E为排名前20的转录因子类型。"

表3

全长转录本在不同数据库中注释数量统计"

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

图3

甘蔗全长转录本注释及分类统计 A、B和C为Nr、KEGG和GO注释分类统计图。"

表4

全长转录本eggNOG注释分类统计"

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

图4

ROC22和ROC25黑穗病侵染和清水处理的36个样品的相关性分析和主成分分析 A、B、C和D分别为ROC22清水处理生物学样品、ROC22黑穗病侵染生物学样品、ROC25清水处理生物学样品和ROC25黑穗病侵染生物学样品的相关性系数; E和F分别为18个ROC22样品和18个ROC25样品的PCA分析图。"

图5

ROC22和ROC25不同侵染阶段差异基因数量统计和两亲本间差异基因韦恩分析 A为ROC22和ROC25感染黑穗病后5 d、8 d和11 d差异基因数量; B为不同侵染阶段2个亲本差异基因维恩图。"

图6

对15个转录本采取实时荧光定量PCR验证转录组测序结果 对15个转录本(表2)比较各个接种病菌组与清水对照组的的RNA-seq的FPKM值和实时荧光定量PCR中2-ΔΔCt值的差异倍数。"

附图1

RNA-Seq和qRT-PCR相关性"

图7

ROC22和ROC25感染黑穗病菌后差异基因GO富集分析 A和B分别为 ROC22差异基因和ROC25差异基因富集程度排名前20的GO条目。C、D和E为抗感亲本中差异基因富集的生物过程(MP)、细胞组分(CC)和分子功能(MF)条目比较分析。"

图8

ROC22和ROC25感染黑穗病菌后差异基因KEGG富集分析 A和B分别为ROC22和ROC25差异基因富集程度排名前20的KEGG通路。C为不同亲本的差异基因富集的KEGG通路比较分析。"

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)
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6

ROC22 and ROC25感染黑穗病菌后抗病相关转录因子分析"

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)
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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