Scientia Agricultura Sinica ›› 2020, Vol. 53 ›› Issue (7): 1381-1396.doi: 10.3864/j.issn.0578-1752.2020.07.008

• PLANT PROTECTION • Previous Articles     Next Articles

Differential Expression of LncRNAs in Nicotiana tabacum var. Samsun NN Infected by TMV at Different Temperatures

HaiYan JIA1,LiYun SONG1,Xiang XU1,Yi XIE1,ChaoQun ZHANG2,TianBo LIU3,CunXiao ZHAO4,LiLi SHEN1,Jie WANG1,Ying LI1,FengLong WANG1,JinGuang YANG1   

  1. 1.Tobacco Research Institute, Chinese Academy of Agricultural Sciences/Key Laboratory of Tobacco Disease and Pest Monitoring, Controlling & Integrated Management, Qingdao 266101, Shandong;
    2. Tobacco Science Institute of Jiangxi Province, Nanchang 330029
    3. Central South Agricultural Experimental Station of China National Tobacco Corporation, Changsha 410128
    4. Qingyang Tobacco Company of Gansu Provincial Company, Qingyang 745099, Gansu
  • Received:2019-09-16 Accepted:2019-11-06 Online:2020-04-01 Published:2020-04-14

Abstract: 【Objective】 The objective of this study is to screen out the differentially expressed lncRNAs in Nicotiana tabacum var. Samsun NN after Tobacco mosaic virus (TMV) infection at different temperatures, and to investigate the role of identified lncRNAs in Samsun NN’s resistance response.【Method】 The temperature sensitivity of N gene makes Samsun NN have the resistance to TMV at 25℃, but lose it at 31℃. TMV and phosphate buffered saline (PBS) were mechanically inoculated into Samsun NN at 25℃ and 31℃. Total RNAs were extracted from systemic leaves at 48 hpi (hours post infection). Deep sequencing was performed after strand-specific database construction, and the sequencing results were filtered to get clean reads. Using N. tabacum var. TN90 as a reference, HTseq was employed to compare obtained reads. LncRNAs were screened out, and their expression levels were estimated by FPKM method. Differentially expressed lncRNAs (DElncRNAs) were then identified by edgeR and verified by qRT-PCR. The target genes of DElncRNAs were predicted by co-localization and co-expression analyses. Gene annotations, GO and KEGG pathways were analyzed for functional prediction of target genes. 【Result】 Altogether, 80 million clean reads were detected for each of 12 samples from 4 treatments by lncRNA-seq. A total of 4 737 annotated lncRNAs and 40 169 novel lncRNAs were obtained. Among them, 64 lncRNAs were differentially expressed after TMV infection at different temperatures. qRT-PCR results showed that the sequencing accuracy of these DElncRNAs was about 80%, which indicated the sequencing data obtained in this study had high reliability. Importantly, some target genes were simultaneously targeted by DElncRNAs that were down-regulated at 25℃ and up-regulated at 31℃. Gene annotations showed that DElncRNAs’ target genes involved in many functions, such as plant resistance, hormone and metabolic pathways. Particularly, some lncRNAs that may be associated with hormone pathways showed a down-regulation trend after TMV infection at 25℃, while up-regulated at 31℃. Furthermore, GO enrichment analysis showed that target genes were mainly involved in the composition of membranes, vesicles, and acted as calcium and potassium ion channel inhibitor activity, so that consequently the corresponding ions could be transported to their sites of action to trigger subsequent reactions. Moreover, these genes were also involved in pathogenesis, antigen processing and presentation, cytokinin metabolism and other physiological processes. The plant hormone signaling pathway was significantly enriched by target genes during KEGG pathway analysis. DElncRNAs related genes down-regulated at 25℃ and up-regulated at 31℃ were simultaneously enriched in pathways such as hormone signaling, ABC transporters, and phenylpropanoid biosynthesis.【Conclusion】 LncRNAs were differentially expressed in Samsun NN after TMV infection at different temperatures (25℃ and 31℃). DElncRNAs participated in host plant systemic acquired resistance by acting on hormone signaling transduction, substance transport and other processes. Taken together, this study lays a foundation for further research on lncRNA’s regulatory function in plant systemic acquired resistance and the development of new strategies to overcome virus invasion into host plant.

Key words: Tobacco mosaic virus (TMV), N gene, Nicotiana tabacum var. Samsun NN, long non-coding RNA (lncRNA), systemic acquired resistance, deep sequencing, affinity enrichment analysis

Fig. 1

Samsun NN before and after TMV inoculation at different temperatures"

Table 1

Primer sequences of differentially expressed lncRNAs at 25℃"

转录本ID
Transcript ID
基因ID
Gene ID
正向引物序列
Forward primer sequence (5′ to 3′)
反向引物序列
Reverse primer sequence (5′ to 3′)
LNC_000098 XLOC_000472 CCCTCCACGCAGTTCTTCTGA TGCCGGGAGTTTCGGGTTTA
LNC_000799 XLOC_003050 GCCTTCTGCCGAATTGTTGG GCTCAAAGGAGGCCAAGTCC
LNC_001093 XLOC_004138 ATGCGTCAGTTTGCATGGGA GAAATCTCAAGGGTAGCTGTACCA
LNC_006130 XLOC_023441 GCCTTCGACTTGTCGTTTGCT ATCCGCAAATCAGCCCTTCC
LNC_012986 XLOC_049416 CCTCTGCCTCAGGCTGTCTCG TTCTGCCGCTTCCGTTATTGCTG
LNC_019285 XLOC_073034 GGATTGAATCTAAGATGAATGCTTGGT ACAGTCACAAGGGTCTAGAAGG
LNC_028742 XLOC_108482 ACGCTGGCGAACGATAATAGAACC ACGGTCGAGATTCTCCTGGTCAG
LNC_037710 XLOC_141968 TCTCTTTCTACCGGGAATTTAAAAAGT CCATTACGTATTGATTGGTGAGCT
XR_001643474.1 107765638 CCACTTGCATGGGCAGTGAT GCCACCACACCAACTTCCTC
XR_001643621.1 107766213 CGGAGAGGTGGAATGGCAAGTG TCCGAGATGTGCCTCCAAGACC
XR_001644424.1 107769516 AACATTCACGGCCAGCAGAACC CTGAAGGCGCGACTGAGATTAGC
XR_001645141.1 107772701 TCATTCTCAGGTCCTCCGTTGT TCTCTCTGTGCTTTCCGCCT
XR_001650509.1 107796801 CGCCCATGTACCCGATTCTG CTTGTTCCAGATGCGCCAGT
XR_001654053.1 107812073 CACTGCCTACACAACCTACACGTC AACAACATGCTGCGAAGAGACTCC
XR_001657220.1 107826167 AATGGCTTTGTCTGCCTCGG AGGCGCGTTGATGAAAGAGG
LNC_001159 XLOC_004417 GACACAGGTACTTGGTTCGCTC AAGAACCGGCACAATACGCC
LNC_003116 XLOC_011996 GGTTTGCAGCGATAACTCGG TGGCTTCAACTATTCCCGCA
LNC_004594 XLOC_017602 AGTGAATGTAACGGAGGCAGCAAC ACACAGAAGAGGATCGAGGTCGTC
LNC_015076 XLOC_057288 CTCTTGCAGGAAGGTTGGCT CCTCATACGGCTCCTCCCTT
LNC_015077 XLOC_057288 CTCTTGCAGGAAGGTTGGCT CCTCATACGGCTCCTCCCTT
LNC_028743 XLOC_108482 ACGCTGGCGAACGATAATAGAACC ACGGTCGAGATTCTCCTGGTCAG
LNC_030105 XLOC_113591 TCCCAACGTGTTACATAAGGCA GCACGGTGTTCTTCGACTCA
LNC_036321 XLOC_136711 CTCTGTCATTCTTCGGTGCCGATG TGAGCTGCCATGCCATGATACAAG
LNC_038081 XLOC_143307 GCTTAGTGTGTGACTCGTTGGT TGCGAAGTGATGGGTTGGTT
XR_001643840.1 107767123 GTTAGTTCGAGGCTGCGGTCAAG CATCGGCGGCGGACAATTACC
XR_001646643.1 107779549 GGTTGGATCAGCAGCAGCAGTAG AGCAGCAGTCTCATTAGCAGCAAC
XR_001648910.1 107789767 ATCCGAACGACCACTCCCAG TTGCAAGTCATCACCGTCCG
XR_001649452.1 107792124 TGTTGGAGAAGGCTGGGACT CGGCATCTGCTGCTTCTAGT
XR_001651797.1 107802252 GGCATCAATCACACATGCCGT AGCAGCCACTGACTTGGAAAC
XR_001654265.1 107813134 GCACTCGAACCAGAAGGCAA CAGCAGAAGCTCGACCACAA
XR_001654587.1 107814577 GTTCATCGCCTTCTTCTGCCTCTC AAGCACCGAGAGCAACCAACATAG
XR_001655076.1 107816953 AATGGCTTTGTCTGCCTCGG AGGCGCGTTGATGAAAGAGG
XR_001657217.1 107826167 GTGGATGGCGAATGCGATCT CTGAGGTCCAGCTGCCAATG
XR_001657841.1 107829108 GTGGTGGTGCATGGCCGTTC TAGCAGGCTGAGGTCTCGTTCG
XR_001658459.1 107831913 GTGGTGGTGCATGGCCGTTC TAGCAGGCTGAGGTCTCGTTCG

Table 2

Primer sequences of differentially expressed lncRNAs at 31℃"

转录本ID
Transcript ID
基因ID
Gene ID
正向引物序列
Forward primer sequence (5′ to 3′)
反向引物序列
Reverse primer sequence (5′ to 3′)
LNC_008396 XLOC_031876 GCGATCTGCCGAAGCTGTGG TGCGTTACTCAAGCCGACATTCTC
LNC_008562 XLOC_032544 TCCTGTTGCTTCATTGCTGCT ACAGATGAACACAGCGCAGG
LNC_008815 XLOC_033553 GACTGTGAAACTGCGAATGGC GCATCCCTTCCAGAAGTCGG
LNC_010207 XLOC_038635 AGACGAACAACTGCGAAAGCA CTGGTCGGCATCGTTTATGGT
LNC_013541 XLOC_051547 AGCACCATCCTCACTTCCACCAG CGCAGGCTGCCTCACAACTTG
LNC_016042 XLOC_060869 GATTAAGACAGCAGGACGGTGGTC GGCTAGTTGATTCGGCAGGTGAG
LNC_018096 XLOC_068634 AGCCAAGCGTTCATAGCGAC AACCCAGCTCACGTTCCCTA
LNC_024626 XLOC_093025 ACCACCTGTGGCTCCAGTTACC TAGGCGGACCTCGCAGAATCTTAG
LNC_033085 XLOC_124537 AGCGAGCAGTCTGGACTCCTATG ACGAGTAACCAGCGCAATTGGAG
LNC_033563 XLOC_126355 GTGGTGGTGCATGGCCGTTC TAGCAGGCTGAGGTCTCGTTCG
LNC_036321 XLOC_136711 CTCTGTCATTCTTCGGTGCCGATG TGAGCTGCCATGCCATGATACAAG
LNC_037998 XLOC_143050 GATTAAGACAGCAGGACGGTGGTC GGCTAGTTGATTCGGCAGGTGAG
LNC_038712 XLOC_145744 CAACCGCTCAGCCATCTCTC GGGGTATCCACCCCTATGGC
XR_001648128.1 107786374 GGAGGGAAGCTGGGTCGTAT GGCAATTCTCCATCGGCTCC
XR_001655221.1 107817578 GAGAGTCGGGCTGCAACTTC GGGAAGCATGGCACCAACAA
XR_001655293.1 107817783 GTCTGAGGTTGCGGTGAAGGC ATTGGCGGCAGAGAATTGACAGAG
XR_001656793.1 107824145 TCTCATGTGGGATGGCACGA CATTCCACTGCGCACCTCTC
XR_001657266.1 107826393 TTGAGGCCACTGTTCAAGACTTGG CGCGAGCAAGGTCATCAGAGC
LNC_018541 XLOC_070302 ACTTCACAAGCAGCAGCTAGTTCC GTAATGCGCCAGGTGCCGTAG
LNC_034892 XLOC_131403 GTGGGTTCCAGACCACAACC AGATGGAAGGGGCAGGTGTT
XR_001644489.1 107769825 CCGTGGACGTGACAACATTGGAG CGGTGACTGTCGCTGAGATACTTG
XR_001646112.1 107776988 TCGCTGCTGATTGTTGCTGTCTC GACTCGTCGGCAACCTCAACTG
XR_001647877.1 107785495 ATCAATGTGGGAGCTTGCCT GCTTGTGCGTGTCTCGACTA
XR_001647999.1 107785872 GCGGATGAGGTATGGTTCACAGC AGCTGCTTCCATAGTCTGTTGCTG
XR_001648126.1 107786374 ATGAGAGTGGAGTGGGGCAG TGCGCCCAATAGGTTATGCG
XR_001649356.1 107791865 ACGTTGCTTTACACTTTACCCTG TGGAGGAAGAAACCAAGCGT
XR_001654070.1 107812109 TCCGTTCAAGTCCACCTGAAGTTC GCAGCTCACCGTGGAAGTCTC
XR_001656841.1 107824342 CAAGCCATCATGCCTCACAGT CCGGAGTCTACCACCCATTCT
XR_001656939.1 107824792 CTGCTGGTCCAGAAGCCGTTAAG AATGTCGTCACGAGTTCGGTCATG
XR_001658441.1 107831745 CAGACGAGGGGTGGAGATGT GCAAATGCCAACAAACAGGGA

Table 3

Overview of sequencing data"

样本名称
Sample name
原始读段
Raw reads
有效读段
Clean reads
测序错误率
Error rate (%)
可定位序列总数及占比
Total mapped
多定位序列计数及占比
Multiple mapped
单定位序列计数及占比
Uniquely mapped
PBS_25_1 81285872 80011202 0.02 76771937 (95.95%) 36818251 (46.02%) 39953686 (49.94%)
PBS_25_2 79744462 78438974 0.02 75316854 (96.02%) 36751852 (46.85%) 38565002 (49.17%)
PBS_25_3 82086686 81323058 0.02 78074493 (96.01%) 38211722 (46.99%) 39862771 (49.02%)
PBS_31_1 112775324 110071878 0.01 106555280 (96.81%) 51925797 (47.17%) 54629483 (49.63%)
PBS_31_2 110922928 108381110 0.01 105100267 (96.97%) 51096062 (47.14%) 54004205 (49.83%)
PBS_31_3 111456946 109144098 0.01 105971578 (97.09%) 51922061 (47.57%) 54049517 (49.52%)
TMV_25_1 82779880 81084374 0.02 77865206 (96.03%) 38330300 (47.27%) 39534906 (48.76%)
TMV_25_2 81397982 79800752 0.02 76525369 (95.90%) 36994028 (46.36%) 39531341 (49.54%)
TMV_25_3 84779126 83206166 0.02 79834756 (95.95%) 40768694 (49.00%) 39066062 (46.95%)
TMV_31_1 86454182 85145676 0.02 81734255 (95.99%) 39993324 (46.97%) 41740931 (49.02%)
TMV_31_2 82671238 81754880 0.01 78713311 (96.28%) 35893618 (43.90%) 42819693 (52.38%)
TMV_31_3 96258450 93993096 0.02 90712104 (96.51%) 44629779 (47.48%) 46082325 (49.03%)

Fig. 2

LncRNA-seq results analysis"

Fig. 3

DElncRNA analysis"

Fig. 4

Validation of differentially expressed lncRNAs at 25℃ by qRT-PCR"

Fig. 5

Validation of differentially expressed lncRNAs at 31℃ by qRT-PCR"

Table 4

Number of DElncRNA target genes enriched in GO terms"

条目类型
Term type
GO条目
GO term
比较组合
Comparison group
基因数
Number of genes
生物过程
Biological process
(BP)
单组织进程Single-organism process TMV_25_vs_PBS_25 133
单组织细胞进程Single-organism cellular process TMV_25_vs_PBS_25 113
氮化合物代谢过程Nitrogen compound metabolic process TMV_25_vs_PBS_25 108
有机环状化合物代谢过程Organic cyclic compound metabolic process TMV_25_vs_PBS_25 105
细胞氮化合物代谢过程Cellular nitrogen compound metabolic process TMV_25_vs_PBS_25 104
单组织进程Single-organism process TMV_31_vs_PBS_31 21
囊泡介导的运输Vesicle-mediated transport TMV_31_vs_PBS_31 20
细胞对刺激的反应Cellular response to stimulus TMV_31_vs_PBS_31 9
自RNA聚合酶II启动子转录Transcription from RNA polymerase II promoter TMV_31_vs_PBS_31 8
端粒维持Telomere maintenance TMV_31_vs_PBS_31 7
细胞组分
Cellular component
(CC)
细胞Cell TMV_25_vs_PBS_25 188
细胞组分Cell part TMV_25_vs_PBS_25 188
细胞内组分Intracellular part TMV_25_vs_PBS_25 166
细胞内膜结合细胞器Intracellular membrane-bounded organelle TMV_25_vs_PBS_25 114
膜结合细胞器Membrane-bounded organelle TMV_25_vs_PBS_25 114
质膜组分Plasma membrane part TMV_31_vs_PBS_31 8
微管组织中心Microtubule organizing center TMV_31_vs_PBS_31 4
反式高尔基体转运囊泡膜Trans-Golgi network transport vesicle membrane TMV_31_vs_PBS_31 2
网格蛋白囊膜Clathrin vesicle coat TMV_31_vs_PBS_31 2
网格蛋白外壳Clathrin coat TMV_31_vs_PBS_31 3
分子功能
Molecular function
(MF)
阳离子结合Cation binding TMV_25_vs_PBS_25 69
锌离子结合Zinc ion binding TMV_25_vs_PBS_25 41
糖基转移酶活性Transferase activity, transferring glycosyl groups TMV_25_vs_PBS_25 31
己糖基转移酶活性Transferase activity, transferring hexosyl groups TMV_25_vs_PBS_25 23
DNA解旋酶活性DNA helicase activity TMV_25_vs_PBS_25 13
UDP-糖基转移酶活性UDP-glycosyltransferase activity TMV_31_vs_PBS_31 8
抗氧化活性Antioxidant activity TMV_31_vs_PBS_31 8
过氧化物酶活性Peroxidase activity TMV_31_vs_PBS_31 7
作为受体作用于过氧化物的氧化还原酶活性
Oxidoreductase activity, acting on peroxide as acceptor
TMV_31_vs_PBS_31 7
翻译监管活动Translation regulator activity TMV_31_vs_PBS_31 5

Table 5

Comparison of the number of DElncRNA target genes enriched in KEGG pathways"

通路 Pathway TMV_25_vs_PBS_25 TMV_31_vs_PBS_31
植物激素信号转导Plant hormone signal transduction 22 15
苯丙烷类生物合成Phenylpropanoid biosynthesis 12 9
mRNA监测途径mRNA surveillance pathway 11 6
嘧啶代谢Pyrimidine metabolism 10 6
ABC运输蛋白ABC transporters 3 3
非同源末端连接Non-homologous end-joining 3 1
RNA转运RNA transport 6 _
碱基切除修复Base excision repair 5 _
错配修复Mismatch repair 4 _
氨酰基-tRNA生物合成Aminoacyl-tRNA biosynthesis 4 _
缬氨酸、亮氨酸和异亮氨酸的生物合成Valine, leucine and isoleucine biosynthesis 3 _
缬氨酸、亮氨酸和异亮氨酸降解Valine, leucine and isoleucine degradation 3 _
同源重组Homologous recombination 3 _
一个叶酸碳库One carbon pool by folate 3 _
二萜生物合成Diterpenoid biosynthesis 1 _
苯丙氨酸代谢Phenylalanine metabolism _ 7
水泡运输中的SNARE相互作用SNARE interactions in vesicular transport _ 1
磷脂酰肌醇信号系统Phosphatidylinositol signaling system _ 1
肌醇磷酸代谢Inositol phosphate metabolism _ 1
酮体的合成和降解Synthesis and degradation of ketone bodies _ 1
丁酸代谢Butanoate metabolism _ 1
鞘脂代谢Sphingolipid metabolism _ 1
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