Skip to main content
Top
Published in: Virology Journal 1/2022

Open Access 01-12-2022 | Research

Integrated next-generation sequencing and comparative transcriptomic analysis of leaves provides novel insights into the ethylene pathway of Chrysanthemum morifolium in response to a Chinese isolate of chrysanthemum virus B

Authors: Xueting Zhong, Lianlian Yang, Jiapeng Li, Zhaoyang Tang, Choufei Wu, Liqin Zhang, Xueping Zhou, Yaqin Wang, Zhanqi Wang

Published in: Virology Journal | Issue 1/2022

Login to get access

Abstract

Background

Chrysanthemum virus B (CVB), a key member of the genus Carlavirus, family Betaflexiviridae, causes severe viral diseases in chrysanthemum (Chrysanthemum morifolium) plants worldwide. However, information on the mechanisms underlying the response of chrysanthemum plants to CVB is scant.

Methods

Here, an integrated next-generation sequencing and comparative transcriptomic analysis of chrysanthemum leaves was conducted to explore the molecular response mechanisms of plants to a Chinese isolate of CVB (CVB-CN) at the molecular level.

Results

In total, 4934 significant differentially expressed genes (SDEGs) were identified to respond to CVB-CN, of which 4097 were upregulated and 837 were downregulated. Gene ontology and functional classification showed that the majority of upregulated SDEGs were categorized into gene cohorts involved in plant hormone signal transduction, phenylpropanoid and flavonoid biosynthesis, and ribosome metabolism. Enrichment analysis demonstrated that ethylene pathway-related genes were significantly upregulated following CVB-CN infection, indicating a strong promotion of ethylene biosynthesis and signaling. Furthermore, disruption of the ethylene pathway in Nicotiana benthamiana, a model plant, using virus-induced gene silencing technology rendered them more susceptible to cysteine-rich protein of CVB-CN induced hypersensitive response, suggesting a crucial role of this pathway in response to CVB-CN infection.

Conclusion

This study provides evidence that ethylene pathway has an essential role of plant in response to CVB and offers valuable insights into the defense mechanisms of chrysanthemum against Carlavirus.
Appendix
Available only for authorised users
Literature
1.
go back to reference Su J, Jiang J, Zhang F, Liu Y, Ding L, Chen S, et al. Current achievements and future prospects in the genetic breeding of chrysanthemum: a review. Hortic Res. 2019;6:109.PubMedPubMedCentralCrossRef Su J, Jiang J, Zhang F, Liu Y, Ding L, Chen S, et al. Current achievements and future prospects in the genetic breeding of chrysanthemum: a review. Hortic Res. 2019;6:109.PubMedPubMedCentralCrossRef
2.
go back to reference Liu H, Luo C, Chen D, Wang Y, Guo S, Chen X, et al. Whole-transcriptome analysis of differentially expressed genes in the mutant and normal capitula of Chrysanthemum morifolium. BMC Genom Data. 2021;22:2.PubMedPubMedCentralCrossRef Liu H, Luo C, Chen D, Wang Y, Guo S, Chen X, et al. Whole-transcriptome analysis of differentially expressed genes in the mutant and normal capitula of Chrysanthemum morifolium. BMC Genom Data. 2021;22:2.PubMedPubMedCentralCrossRef
3.
go back to reference Wang Y, Li J, Xu Z, Li M, Wang K, Pang S, et al. The formation process of green substances in Chrysanthemum morifolium tea. Food Chem. 2020;326:127028.PubMedCrossRef Wang Y, Li J, Xu Z, Li M, Wang K, Pang S, et al. The formation process of green substances in Chrysanthemum morifolium tea. Food Chem. 2020;326:127028.PubMedCrossRef
4.
go back to reference Li Y, Yang P, Luo Y, Gao B, Sun J, Lu W, et al. Chemical compositions of chrysanthemum teas and their anti-inflammatory and antioxidant properties. Food Chem. 2019;286:8–16.PubMedCrossRef Li Y, Yang P, Luo Y, Gao B, Sun J, Lu W, et al. Chemical compositions of chrysanthemum teas and their anti-inflammatory and antioxidant properties. Food Chem. 2019;286:8–16.PubMedCrossRef
5.
go back to reference Sun J, Wang Z, Chen L, Sun G. Hypolipidemic effects and preliminary mechanism of chrysanthemum flavonoids, its main components luteolin and luteoloside in hyperlipidemia rats. Antioxidants. 2021;10:1309.PubMedPubMedCentralCrossRef Sun J, Wang Z, Chen L, Sun G. Hypolipidemic effects and preliminary mechanism of chrysanthemum flavonoids, its main components luteolin and luteoloside in hyperlipidemia rats. Antioxidants. 2021;10:1309.PubMedPubMedCentralCrossRef
6.
go back to reference Yan K, Du X, Mao B. Production of virus-free chrysanthemum (Chrysanthemum morifolium Ramat) by tissue culture techniques. Methods Mol Biol. 2022;2400:171–86.PubMedCrossRef Yan K, Du X, Mao B. Production of virus-free chrysanthemum (Chrysanthemum morifolium Ramat) by tissue culture techniques. Methods Mol Biol. 2022;2400:171–86.PubMedCrossRef
7.
go back to reference Gobatto D, de Oliveira LA, de Siqueira Franco DA, Velásquez N, Daròs JA, Eiras M. Surveys in the chrysanthemum production areas of Brazil and Colombia reveal that weeds are potential reservoirs of chrysanthemum stunt viroid. Viruses. 2019;11:355.PubMedCentralCrossRef Gobatto D, de Oliveira LA, de Siqueira Franco DA, Velásquez N, Daròs JA, Eiras M. Surveys in the chrysanthemum production areas of Brazil and Colombia reveal that weeds are potential reservoirs of chrysanthemum stunt viroid. Viruses. 2019;11:355.PubMedCentralCrossRef
8.
go back to reference Zhao X, Liu X, Ge B, Li M, Hong B. A multiplex RT-PCR for simultaneous detection and identification of five viruses and two viroids infecting chrysanthemum. Arch Virol. 2015;160:1145–52.PubMedCrossRef Zhao X, Liu X, Ge B, Li M, Hong B. A multiplex RT-PCR for simultaneous detection and identification of five viruses and two viroids infecting chrysanthemum. Arch Virol. 2015;160:1145–52.PubMedCrossRef
9.
go back to reference Wang R, Dong J, Wang Z, Zhou T, Li Y, Ding W. Complete nucleotide sequence of a new carlavirus in chrysanthemums in China. Arch Virol. 2018;163:1973–6.PubMedCrossRef Wang R, Dong J, Wang Z, Zhou T, Li Y, Ding W. Complete nucleotide sequence of a new carlavirus in chrysanthemums in China. Arch Virol. 2018;163:1973–6.PubMedCrossRef
10.
go back to reference Singh L, Hallan V, Jabeen N, Singh AK, Ram R, Martin DP, et al. Coat protein gene diversity among chrysanthemum virus B isolates from India. Arch Virol. 2007;152:405–13.PubMedCrossRef Singh L, Hallan V, Jabeen N, Singh AK, Ram R, Martin DP, et al. Coat protein gene diversity among chrysanthemum virus B isolates from India. Arch Virol. 2007;152:405–13.PubMedCrossRef
11.
go back to reference Ohkawa A, Yamada M, Sayama H, Sugiyama N, Okuda S, Natsuaki T. Complete nucleotide sequence of a Japanese isolate of chrysanthemum virus B (genus Carlavirus). Arch Virol. 2007;152:2253–8.PubMedCrossRef Ohkawa A, Yamada M, Sayama H, Sugiyama N, Okuda S, Natsuaki T. Complete nucleotide sequence of a Japanese isolate of chrysanthemum virus B (genus Carlavirus). Arch Virol. 2007;152:2253–8.PubMedCrossRef
12.
go back to reference Verma N, Sharma A, Ram R, Hallan V, Zaidi AA, Garg ID. Detection, identification and incidence of chrysanthemum B carlavirus in chrysanthemum in India. Crop Prot. 2003;22:425–9.CrossRef Verma N, Sharma A, Ram R, Hallan V, Zaidi AA, Garg ID. Detection, identification and incidence of chrysanthemum B carlavirus in chrysanthemum in India. Crop Prot. 2003;22:425–9.CrossRef
13.
go back to reference Singh L, Hallan V, Martin DP, Ram R, Zaidi AA. Genomic sequence analysis of four new chrysanthemum virus B isolates: evidence of RNA recombination. Arch Virol. 2012;157:531–7.PubMedCrossRef Singh L, Hallan V, Martin DP, Ram R, Zaidi AA. Genomic sequence analysis of four new chrysanthemum virus B isolates: evidence of RNA recombination. Arch Virol. 2012;157:531–7.PubMedCrossRef
14.
go back to reference Lukhovitskaya NI, Ignatovich IV, Savenkov EI, Schiemann J, Morozov SY, Solovyev AG. Role of the zinc-finger and basic motifs of chrysanthemum virus B p12 protein in nucleic acid binding, protein localization and induction of a hypersensitive response upon expression from a viral vector. J Gen Virol. 2009;90:723–33.PubMedCrossRef Lukhovitskaya NI, Ignatovich IV, Savenkov EI, Schiemann J, Morozov SY, Solovyev AG. Role of the zinc-finger and basic motifs of chrysanthemum virus B p12 protein in nucleic acid binding, protein localization and induction of a hypersensitive response upon expression from a viral vector. J Gen Virol. 2009;90:723–33.PubMedCrossRef
15.
go back to reference Lukhovitskaia NI, Solov’eva AG, Koshkina TE, Zavriev SK, Morozov S. Interaction of cysteine-rich protein of Carlavirus with plant defense system. Mol Biol. 2005;39:896–904. Lukhovitskaia NI, Solov’eva AG, Koshkina TE, Zavriev SK, Morozov S. Interaction of cysteine-rich protein of Carlavirus with plant defense system. Mol Biol. 2005;39:896–904.
16.
go back to reference Lukhovitskaya NI, Solovieva AD, Boddeti SK, Thaduri S, Solovyev AG, Savenkov EI. An RNA virus-encoded zinc-finger protein acts as a plant transcription factor and induces a regulator of cell size and proliferation in two tobacco species. Plant Cell. 2013;25:960–73.PubMedPubMedCentralCrossRef Lukhovitskaya NI, Solovieva AD, Boddeti SK, Thaduri S, Solovyev AG, Savenkov EI. An RNA virus-encoded zinc-finger protein acts as a plant transcription factor and induces a regulator of cell size and proliferation in two tobacco species. Plant Cell. 2013;25:960–73.PubMedPubMedCentralCrossRef
17.
go back to reference Fujita N, Komatsu K, Ayukawa Y, Matsuo Y, Hashimoto M, Netsu O, et al. N-terminal region of cysteine-rich protein (CRP) in carlaviruses is involved in the determination of symptom types. Mol Plant Pathol. 2018;19:180–90.PubMedCrossRef Fujita N, Komatsu K, Ayukawa Y, Matsuo Y, Hashimoto M, Netsu O, et al. N-terminal region of cysteine-rich protein (CRP) in carlaviruses is involved in the determination of symptom types. Mol Plant Pathol. 2018;19:180–90.PubMedCrossRef
18.
go back to reference Vetukuri RR, Kalyandurg PB, Saripella GV, Sen D, Gil JF, Lukhovitskaya NI, et al. Effect of RNA silencing suppression activity of chrysanthemum virus B p12 protein on small RNA species. Arch Virol. 2020;165:2953–9.PubMedPubMedCentralCrossRef Vetukuri RR, Kalyandurg PB, Saripella GV, Sen D, Gil JF, Lukhovitskaya NI, et al. Effect of RNA silencing suppression activity of chrysanthemum virus B p12 protein on small RNA species. Arch Virol. 2020;165:2953–9.PubMedPubMedCentralCrossRef
19.
go back to reference Ohkawa A, Ishikawa-Suehiro N, Okuda S, Natsuaki T. Construction of an infectious full-length cDNA clone of chrysanthemum virus B. J Gen Plant Pathol. 2008;74:434–7.CrossRef Ohkawa A, Ishikawa-Suehiro N, Okuda S, Natsuaki T. Construction of an infectious full-length cDNA clone of chrysanthemum virus B. J Gen Plant Pathol. 2008;74:434–7.CrossRef
20.
go back to reference Lai Y, Wu X, Lv L, Weng J, Han K, Chen Z, et al. Gynura japonica: a new host of apple stem grooving virus and chrysanthemum virus B in China. Plant Dis. 2021;105:3770.CrossRef Lai Y, Wu X, Lv L, Weng J, Han K, Chen Z, et al. Gynura japonica: a new host of apple stem grooving virus and chrysanthemum virus B in China. Plant Dis. 2021;105:3770.CrossRef
21.
go back to reference Chirkov SN, Sheveleva A, Snezhkina A, Kudryavtseva A, Krasnov G, Zakubanskiy A, et al. Highly divergent isolates of chrysanthemum virus B and chrysanthemum virus R infecting chrysanthemum in Russia. PeerJ. 2022;10:e12607.PubMedPubMedCentralCrossRef Chirkov SN, Sheveleva A, Snezhkina A, Kudryavtseva A, Krasnov G, Zakubanskiy A, et al. Highly divergent isolates of chrysanthemum virus B and chrysanthemum virus R infecting chrysanthemum in Russia. PeerJ. 2022;10:e12607.PubMedPubMedCentralCrossRef
22.
go back to reference Liu Y, Du Z, Wang H, Zhang S, Cao M, Wang X. Identification and characterization of wheat yellow striate virus, a novel leafhopper-transmitted nucleorhabdovirus infecting wheat. Front Microbiol. 2018;9:468.PubMedPubMedCentralCrossRef Liu Y, Du Z, Wang H, Zhang S, Cao M, Wang X. Identification and characterization of wheat yellow striate virus, a novel leafhopper-transmitted nucleorhabdovirus infecting wheat. Front Microbiol. 2018;9:468.PubMedPubMedCentralCrossRef
23.
go back to reference Zhang S, Yang L, Ma L, Tian X, Li R, Zhou C, et al. Virome of Camellia japonica: discovery of and molecular characterization of new viruses of different taxa in camellias. Front Microbiol. 2020;11:945.PubMedPubMedCentralCrossRef Zhang S, Yang L, Ma L, Tian X, Li R, Zhou C, et al. Virome of Camellia japonica: discovery of and molecular characterization of new viruses of different taxa in camellias. Front Microbiol. 2020;11:945.PubMedPubMedCentralCrossRef
24.
go back to reference Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat Biotechnol. 2011;29:644–52.PubMedPubMedCentralCrossRef Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat Biotechnol. 2011;29:644–52.PubMedPubMedCentralCrossRef
26.
go back to reference Luo C, Wang ZQ, Liu X, Zhao L, Zhou X, Xie Y. Identification and analysis of potential genes regulated by an alphasatellite (TYLCCNA) that contribute to host resistance against tomato yellow leaf curl China virus and its betasatellite (TYLCCNV/TYLCCNB) infection in Nicotiana benthamiana. Viruses. 2019;11:442.PubMedCentralCrossRef Luo C, Wang ZQ, Liu X, Zhao L, Zhou X, Xie Y. Identification and analysis of potential genes regulated by an alphasatellite (TYLCCNA) that contribute to host resistance against tomato yellow leaf curl China virus and its betasatellite (TYLCCNV/TYLCCNB) infection in Nicotiana benthamiana. Viruses. 2019;11:442.PubMedCentralCrossRef
27.
go back to reference Huang J, Gu L, Zhang Y, Yan T, Kong G, Kong L, et al. An oomycete plant pathogen reprograms host pre-mRNA splicing to subvert immunity. Nat Commun. 2017;8:2051.PubMedPubMedCentralCrossRef Huang J, Gu L, Zhang Y, Yan T, Kong G, Kong L, et al. An oomycete plant pathogen reprograms host pre-mRNA splicing to subvert immunity. Nat Commun. 2017;8:2051.PubMedPubMedCentralCrossRef
28.
go back to reference Liu X, Xu J, Zhu J, Du P, Sun A. Combined transcriptome and proteome analysis of RpoS regulon reveals its role in spoilage potential of Pseudomonas fluorescens. Front Microbiol. 2019;10:94.PubMedPubMedCentralCrossRef Liu X, Xu J, Zhu J, Du P, Sun A. Combined transcriptome and proteome analysis of RpoS regulon reveals its role in spoilage potential of Pseudomonas fluorescens. Front Microbiol. 2019;10:94.PubMedPubMedCentralCrossRef
29.
go back to reference Du J, Wang S, He C, Zhou B, Ruan YL, Shou H. Identification of regulatory networks and hub genes controlling soybean seed set and size using RNA sequencing analysis. J Exp Bot. 2017;68:1955–72.PubMedPubMedCentral Du J, Wang S, He C, Zhou B, Ruan YL, Shou H. Identification of regulatory networks and hub genes controlling soybean seed set and size using RNA sequencing analysis. J Exp Bot. 2017;68:1955–72.PubMedPubMedCentral
30.
go back to reference Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12:59–60.PubMedCrossRef Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12:59–60.PubMedCrossRef
32.
go back to reference Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-seq. Nat Methods. 2008;5:621–8.PubMedCrossRef Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-seq. Nat Methods. 2008;5:621–8.PubMedCrossRef
33.
go back to reference Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods. 2017;14:417–9.PubMedPubMedCentralCrossRef Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods. 2017;14:417–9.PubMedPubMedCentralCrossRef
34.
go back to reference Yu C, Guo H, Zhang Y, Song Y, Pi E, Yu C, et al. Identification of potential genes that contributed to the variation in the taxoid contents between two Taxus species (Taxus media and Taxus mairei). Tree Physiol. 2017;37:1659–71.PubMedCrossRef Yu C, Guo H, Zhang Y, Song Y, Pi E, Yu C, et al. Identification of potential genes that contributed to the variation in the taxoid contents between two Taxus species (Taxus media and Taxus mairei). Tree Physiol. 2017;37:1659–71.PubMedCrossRef
35.
go back to reference Weight CM, Venturini C, Pojar S, Jochems SP, Reiné J, Nikolaou E, et al. Microinvasion by Streptococcus pneumoniae induces epithelial innate immunity during colonisation at the human mucosal surface. Nat Commun. 2019;10:3060.PubMedPubMedCentralCrossRef Weight CM, Venturini C, Pojar S, Jochems SP, Reiné J, Nikolaou E, et al. Microinvasion by Streptococcus pneumoniae induces epithelial innate immunity during colonisation at the human mucosal surface. Nat Commun. 2019;10:3060.PubMedPubMedCentralCrossRef
36.
go back to reference Bajay SK, Cruz MV, da Silva CC, Murad NF, Brandão MM, de Souza AP. Extremophiles as a model of a natural ecosystem: transcriptional coordination of genes reveals distinct selective responses of plants under climate change scenarios. Front Plant Sci. 2018;9:1376.PubMedPubMedCentralCrossRef Bajay SK, Cruz MV, da Silva CC, Murad NF, Brandão MM, de Souza AP. Extremophiles as a model of a natural ecosystem: transcriptional coordination of genes reveals distinct selective responses of plants under climate change scenarios. Front Plant Sci. 2018;9:1376.PubMedPubMedCentralCrossRef
37.
go back to reference Zhou T, Luo X, Yu C, Zhang C, Zhang L, Song YB, et al. Transcriptome analyses provide insights into the expression pattern and sequence similarity of several taxol biosynthesis-related genes in three Taxus species. BMC Plant Biol. 2019;19:33.PubMedPubMedCentralCrossRef Zhou T, Luo X, Yu C, Zhang C, Zhang L, Song YB, et al. Transcriptome analyses provide insights into the expression pattern and sequence similarity of several taxol biosynthesis-related genes in three Taxus species. BMC Plant Biol. 2019;19:33.PubMedPubMedCentralCrossRef
38.
go back to reference Liu Y, Schiff M, Dinesh-Kumar SP. Virus-induced gene silencing in tomato. Plant J. 2002;31:777–86.PubMedCrossRef Liu Y, Schiff M, Dinesh-Kumar SP. Virus-induced gene silencing in tomato. Plant J. 2002;31:777–86.PubMedCrossRef
39.
go back to reference Wang S, Han K, Peng J, Zhao J, Jiang L, Lu Y, et al. NbALD1 mediates resistance to turnip mosaic virus by regulating the accumulation of salicylic acid and the ethylene pathway in Nicotiana benthamiana. Mol Plant Pathol. 2019;20:990–1004.PubMedPubMedCentralCrossRef Wang S, Han K, Peng J, Zhao J, Jiang L, Lu Y, et al. NbALD1 mediates resistance to turnip mosaic virus by regulating the accumulation of salicylic acid and the ethylene pathway in Nicotiana benthamiana. Mol Plant Pathol. 2019;20:990–1004.PubMedPubMedCentralCrossRef
40.
go back to reference Zhong X, Wang ZQ, Xiao R, Wang Y, Xie Y, Zhou X. iTRAQ analysis of the tobacco leaf proteome reveals that RNA-directed DNA methylation (RdDM) has important roles in defense against geminivirus-betasatellite infection. J Proteom. 2017;152:88–101.CrossRef Zhong X, Wang ZQ, Xiao R, Wang Y, Xie Y, Zhou X. iTRAQ analysis of the tobacco leaf proteome reveals that RNA-directed DNA methylation (RdDM) has important roles in defense against geminivirus-betasatellite infection. J Proteom. 2017;152:88–101.CrossRef
41.
go back to reference Zhong X, Wang ZQ, Xiao R, Cao L, Wang Y, Xie Y, et al. Mimic phosphorylation of a βC1 protein encoded by TYLCCNB impairs its functions as a viral suppressor of RNA silencing and a symptom determinant. J Virol. 2017;91:e00300-e317.PubMedPubMedCentralCrossRef Zhong X, Wang ZQ, Xiao R, Cao L, Wang Y, Xie Y, et al. Mimic phosphorylation of a βC1 protein encoded by TYLCCNB impairs its functions as a viral suppressor of RNA silencing and a symptom determinant. J Virol. 2017;91:e00300-e317.PubMedPubMedCentralCrossRef
42.
go back to reference Lu R, Malcuit I, Moffett P, Ruiz MT, Peart J, Wu AJ, et al. High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J. 2003;22:5690–9.PubMedPubMedCentralCrossRef Lu R, Malcuit I, Moffett P, Ruiz MT, Peart J, Wu AJ, et al. High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J. 2003;22:5690–9.PubMedPubMedCentralCrossRef
43.
go back to reference Wang ZQ, Zhao QM, Zhong X, Xiao L, Ma LX, Wu CF, et al. Comparative analysis of maca (Lepidium meyenii) proteome profiles reveals insights into response mechanisms of herbal plants to high-temperature stress. BMC Plant Biol. 2020;20:431.PubMedPubMedCentralCrossRef Wang ZQ, Zhao QM, Zhong X, Xiao L, Ma LX, Wu CF, et al. Comparative analysis of maca (Lepidium meyenii) proteome profiles reveals insights into response mechanisms of herbal plants to high-temperature stress. BMC Plant Biol. 2020;20:431.PubMedPubMedCentralCrossRef
44.
go back to reference Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative CT method. Nat Protoc. 2008;3:1101–8.PubMedCrossRef Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative CT method. Nat Protoc. 2008;3:1101–8.PubMedCrossRef
45.
go back to reference Shi B, Lin L, Wang S, Guo Q, Zhou H, Rong L, et al. Identification and regulation of host genes related to rice stripe virus symptom production. New Phytol. 2016;209:1106–19.PubMedCrossRef Shi B, Lin L, Wang S, Guo Q, Zhou H, Rong L, et al. Identification and regulation of host genes related to rice stripe virus symptom production. New Phytol. 2016;209:1106–19.PubMedCrossRef
46.
go back to reference Wang L, Sun J, Ren L, Zhou M, Han X, Ding L, et al. CmBBX8 accelerates flowering by targeting CmFTL1 directly in summer chrysanthemum. Plant Biotechnol J. 2020;18:1562–72.PubMedPubMedCentralCrossRef Wang L, Sun J, Ren L, Zhou M, Han X, Ding L, et al. CmBBX8 accelerates flowering by targeting CmFTL1 directly in summer chrysanthemum. Plant Biotechnol J. 2020;18:1562–72.PubMedPubMedCentralCrossRef
47.
go back to reference Tang QY, Zhang CX. Data processing system (DPS) software with experimental design, statistical analysis and data mining developed for use in entomological research. Insect Sci. 2013;20:254–60.PubMedCrossRef Tang QY, Zhang CX. Data processing system (DPS) software with experimental design, statistical analysis and data mining developed for use in entomological research. Insect Sci. 2013;20:254–60.PubMedCrossRef
49.
go back to reference Ascencio-Ibáñez JT, Sozzani R, Lee TJ, Chu TM, Wolfinger RD, Cella R, et al. Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol. 2008;148:436–54.PubMedPubMedCentralCrossRef Ascencio-Ibáñez JT, Sozzani R, Lee TJ, Chu TM, Wolfinger RD, Cella R, et al. Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol. 2008;148:436–54.PubMedPubMedCentralCrossRef
50.
go back to reference Martin K, Singh J, Hill JH, Whitham SA, Cannon SB. Dynamic transcriptome profiling of bean common mosaic virus (BCMV) infection in common bean (Phaseolus vulgaris L.). BMC Genom. 2016;17:613.CrossRef Martin K, Singh J, Hill JH, Whitham SA, Cannon SB. Dynamic transcriptome profiling of bean common mosaic virus (BCMV) infection in common bean (Phaseolus vulgaris L.). BMC Genom. 2016;17:613.CrossRef
51.
go back to reference Hanley-Bowdoin L, Bejarano ER, Robertson D, Mansoor S. Geminiviruses: masters at redirecting and reprogramming plant processes. Nat Rev Microbiol. 2013;11:777–88.PubMedCrossRef Hanley-Bowdoin L, Bejarano ER, Robertson D, Mansoor S. Geminiviruses: masters at redirecting and reprogramming plant processes. Nat Rev Microbiol. 2013;11:777–88.PubMedCrossRef
52.
go back to reference Wang A. Dissecting the molecular network of virus-plant interactions: the complex roles of host factors. Annu Rev Phytopathol. 2015;53:45–66.PubMedCrossRef Wang A. Dissecting the molecular network of virus-plant interactions: the complex roles of host factors. Annu Rev Phytopathol. 2015;53:45–66.PubMedCrossRef
53.
go back to reference Wu M, Ding X, Fu X, Lozano-Duran R. Transcriptional reprogramming caused by the geminivirus tomato yellow leaf curl virus in local or systemic infections in Nicotiana benthamiana. BMC Genom. 2019;20:542.CrossRef Wu M, Ding X, Fu X, Lozano-Duran R. Transcriptional reprogramming caused by the geminivirus tomato yellow leaf curl virus in local or systemic infections in Nicotiana benthamiana. BMC Genom. 2019;20:542.CrossRef
54.
go back to reference Li K, Wu G, Li M, Ma M, Du J, Sun M, et al. Transcriptome analysis of Nicotiana benthamiana infected by tobacco curly shoot virus. Virol J. 2018;15:138.PubMedPubMedCentralCrossRef Li K, Wu G, Li M, Ma M, Du J, Sun M, et al. Transcriptome analysis of Nicotiana benthamiana infected by tobacco curly shoot virus. Virol J. 2018;15:138.PubMedPubMedCentralCrossRef
55.
go back to reference Amorim L, da Fonseca Dos Santos R, Neto J, Guida-Santos M, Crovella S, Benko-Iseppon AM. Transcription factors involved in plant resistance to pathogens. Curr Protein Pept Sci. 2017;18:335–51.PubMedCrossRef Amorim L, da Fonseca Dos Santos R, Neto J, Guida-Santos M, Crovella S, Benko-Iseppon AM. Transcription factors involved in plant resistance to pathogens. Curr Protein Pept Sci. 2017;18:335–51.PubMedCrossRef
56.
go back to reference Huh SU, Lee GJ, Jung JH, Kim Y, Kim YJ, Paek KH. Capsicum annuum transcription factor WRKYa positively regulates defense response upon TMV infection and is a substrate of CaMK1 and CaMK2. Sci Rep. 2015;5:7981.PubMedPubMedCentralCrossRef Huh SU, Lee GJ, Jung JH, Kim Y, Kim YJ, Paek KH. Capsicum annuum transcription factor WRKYa positively regulates defense response upon TMV infection and is a substrate of CaMK1 and CaMK2. Sci Rep. 2015;5:7981.PubMedPubMedCentralCrossRef
57.
go back to reference Lim JH, Park CJ, Huh SU, Choi LM, Lee GJ, Kim YJ, et al. Capsicum annuum WRKYb transcription factor that binds to the CaPR-10 promoter functions as a positive regulator in innate immunity upon TMV infection. Biochem Biophys Res Commun. 2011;411:613–9.PubMedCrossRef Lim JH, Park CJ, Huh SU, Choi LM, Lee GJ, Kim YJ, et al. Capsicum annuum WRKYb transcription factor that binds to the CaPR-10 promoter functions as a positive regulator in innate immunity upon TMV infection. Biochem Biophys Res Commun. 2011;411:613–9.PubMedCrossRef
58.
go back to reference Huh SU, Choi LM, Lee GJ, Kim YJ, Paek KH. Capsicum annuum WRKY transcription factor d (CaWRKYd) regulates hypersensitive response and defense response upon tobacco mosaic virus infection. Plant Sci. 2012;197:50–8.PubMedCrossRef Huh SU, Choi LM, Lee GJ, Kim YJ, Paek KH. Capsicum annuum WRKY transcription factor d (CaWRKYd) regulates hypersensitive response and defense response upon tobacco mosaic virus infection. Plant Sci. 2012;197:50–8.PubMedCrossRef
59.
go back to reference Jiang Y, Zheng W, Li J, Liu P, Zhong K, Jin P, et al. NbWRKY40 positively regulates the response of Nicotiana benthamiana to tomato mosaic virus via salicylic acid signaling. Front Plant Sci. 2021;11:603518.PubMedPubMedCentralCrossRef Jiang Y, Zheng W, Li J, Liu P, Zhong K, Jin P, et al. NbWRKY40 positively regulates the response of Nicotiana benthamiana to tomato mosaic virus via salicylic acid signaling. Front Plant Sci. 2021;11:603518.PubMedPubMedCentralCrossRef
60.
go back to reference Fischer U, Dröge-Laser W. Overexpression of NtERF5, a new member of the tobacco ethylene response transcription factor family enhances resistance to tobacco mosaic virus. Mol Plant Microbe Interact. 2004;17:1162–71.PubMedCrossRef Fischer U, Dröge-Laser W. Overexpression of NtERF5, a new member of the tobacco ethylene response transcription factor family enhances resistance to tobacco mosaic virus. Mol Plant Microbe Interact. 2004;17:1162–71.PubMedCrossRef
62.
go back to reference Sun Y, Fan M, He Y. Transcriptome analysis of watermelon leaves reveals candidate genes responsive to cucumber green mottle mosaic virus infection. Int J Mol Sci. 2019;20:610.PubMedCentralCrossRef Sun Y, Fan M, He Y. Transcriptome analysis of watermelon leaves reveals candidate genes responsive to cucumber green mottle mosaic virus infection. Int J Mol Sci. 2019;20:610.PubMedCentralCrossRef
63.
go back to reference Aparicio F, Pallás V. The coat protein of alfalfa mosaic virus interacts and interferes with the transcriptional activity of the bHLH transcription factor ILR3 promoting salicylic acid-dependent defence signalling response. Mol Plant Pathol. 2017;18:173–86.PubMedCrossRef Aparicio F, Pallás V. The coat protein of alfalfa mosaic virus interacts and interferes with the transcriptional activity of the bHLH transcription factor ILR3 promoting salicylic acid-dependent defence signalling response. Mol Plant Pathol. 2017;18:173–86.PubMedCrossRef
64.
go back to reference Sun D, Zhang X, Zhang Q, Ji X, Jia Y, Wang H, et al. Comparative transcriptome profiling uncovers a Lilium regale NAC transcription factor, LrNAC35, contributing to defence response against cucumber mosaic virus and tobacco mosaic virus. Mol Plant Pathol. 2019;20:1662–81.PubMedPubMedCentralCrossRef Sun D, Zhang X, Zhang Q, Ji X, Jia Y, Wang H, et al. Comparative transcriptome profiling uncovers a Lilium regale NAC transcription factor, LrNAC35, contributing to defence response against cucumber mosaic virus and tobacco mosaic virus. Mol Plant Pathol. 2019;20:1662–81.PubMedPubMedCentralCrossRef
66.
go back to reference Zhu T, Zhou X, Zhang JL, Zhang WH, Zhang LP, You CX, et al. Ethylene-induced NbMYB4L is involved in resistance against tobacco mosaic virus in Nicotiana benthamiana. Mol Plant Pathol. 2022;23:16–31.PubMedCrossRef Zhu T, Zhou X, Zhang JL, Zhang WH, Zhang LP, You CX, et al. Ethylene-induced NbMYB4L is involved in resistance against tobacco mosaic virus in Nicotiana benthamiana. Mol Plant Pathol. 2022;23:16–31.PubMedCrossRef
67.
go back to reference Pattyn J, Vaughan-Hirsch J, Van de Poel B. The regulation of ethylene biosynthesis: a complex multilevel control circuitry. New Phytol. 2021;229:770–82.PubMedCrossRef Pattyn J, Vaughan-Hirsch J, Van de Poel B. The regulation of ethylene biosynthesis: a complex multilevel control circuitry. New Phytol. 2021;229:770–82.PubMedCrossRef
69.
go back to reference Zhao H, Yin CC, Ma B, Chen SY, Zhang JS. Ethylene signaling in rice and Arabidopsis: new regulators and mechanisms. J Integr Plant Biol. 2021;63:102–25.PubMedCrossRef Zhao H, Yin CC, Ma B, Chen SY, Zhang JS. Ethylene signaling in rice and Arabidopsis: new regulators and mechanisms. J Integr Plant Biol. 2021;63:102–25.PubMedCrossRef
70.
go back to reference Huh SU. Functional analysis of hot pepper ethylene responsive factor 1A in plant defense. Plant Signal Behav. 2022;22:2027137.CrossRef Huh SU. Functional analysis of hot pepper ethylene responsive factor 1A in plant defense. Plant Signal Behav. 2022;22:2027137.CrossRef
71.
go back to reference Wu Q, Ding SW, Zhang Y, Zhu S. Identification of viruses and viroids by next-generation sequencing and homology-dependent and homology-independent algorithms. Annu Rev Phytopathol. 2015;53:425–44.PubMedCrossRef Wu Q, Ding SW, Zhang Y, Zhu S. Identification of viruses and viroids by next-generation sequencing and homology-dependent and homology-independent algorithms. Annu Rev Phytopathol. 2015;53:425–44.PubMedCrossRef
72.
go back to reference Pecman A, Kutnjak D, Gutiérrez-Aguirre I, Adams I, Fox A, Boonham N, et al. Next generation sequencing for detection and discovery of plant viruses and viroids: comparison of two approaches. Front Microbiol. 2017;8:1998.PubMedPubMedCentralCrossRef Pecman A, Kutnjak D, Gutiérrez-Aguirre I, Adams I, Fox A, Boonham N, et al. Next generation sequencing for detection and discovery of plant viruses and viroids: comparison of two approaches. Front Microbiol. 2017;8:1998.PubMedPubMedCentralCrossRef
73.
go back to reference Díaz-Cruz GA, Smith CM, Wiebe KF, Villanueva SM, Klonowski AR, Cassone BJ. Applications of next-generation sequencing for large-scale pathogen diagnoses in soybean. Plant Dis. 2019;103:1075–83.PubMedCrossRef Díaz-Cruz GA, Smith CM, Wiebe KF, Villanueva SM, Klonowski AR, Cassone BJ. Applications of next-generation sequencing for large-scale pathogen diagnoses in soybean. Plant Dis. 2019;103:1075–83.PubMedCrossRef
74.
go back to reference Aimone CD, Hoyer JS, Dye AE, Deppong DO, Duffy S, Carbone I, et al. An experimental strategy for preparing circular ssDNA virus genomes for next-generation sequencing. J Virol Methods. 2022;300:114405.PubMedCrossRef Aimone CD, Hoyer JS, Dye AE, Deppong DO, Duffy S, Carbone I, et al. An experimental strategy for preparing circular ssDNA virus genomes for next-generation sequencing. J Virol Methods. 2022;300:114405.PubMedCrossRef
75.
go back to reference Lu J, Du ZX, Kong J, Chen LN, Qiu YH, Li GF, et al. Transcriptome analysis of Nicotiana tabacum infected by cucumber mosaic virus during systemic symptom development. PLoS ONE. 2012;7:e43447.PubMedPubMedCentralCrossRef Lu J, Du ZX, Kong J, Chen LN, Qiu YH, Li GF, et al. Transcriptome analysis of Nicotiana tabacum infected by cucumber mosaic virus during systemic symptom development. PLoS ONE. 2012;7:e43447.PubMedPubMedCentralCrossRef
76.
go back to reference Choi H, Jo Y, Lian S, Jo KM, Chu H, Yoon JY, et al. Comparative analysis of chrysanthemum transcriptome in response to three RNA viruses: cucumber mosaic virus, tomato spotted wilt virus and potato virus X. Plant Mol Biol. 2015;88:233–48.PubMedCrossRef Choi H, Jo Y, Lian S, Jo KM, Chu H, Yoon JY, et al. Comparative analysis of chrysanthemum transcriptome in response to three RNA viruses: cucumber mosaic virus, tomato spotted wilt virus and potato virus X. Plant Mol Biol. 2015;88:233–48.PubMedCrossRef
77.
go back to reference Zhang L, Shang J, Wang W, Du J, Li K, Wu X, et al. Comparison of transcriptome differences in soybean response to soybean mosaic virus under normal light and in the shade. Viruses. 2019;11:793.PubMedCentralCrossRef Zhang L, Shang J, Wang W, Du J, Li K, Wu X, et al. Comparison of transcriptome differences in soybean response to soybean mosaic virus under normal light and in the shade. Viruses. 2019;11:793.PubMedCentralCrossRef
78.
go back to reference Murphy JF, Hallmark HT, Ramaraj T, Sundararajan A, Schilkey F, Rashotte AM. Three strains of tobacco etch virus distinctly alter the transcriptome of apical stem tissue in Capsicum annuum during infection. Viruses. 2021;13:741.PubMedPubMedCentralCrossRef Murphy JF, Hallmark HT, Ramaraj T, Sundararajan A, Schilkey F, Rashotte AM. Three strains of tobacco etch virus distinctly alter the transcriptome of apical stem tissue in Capsicum annuum during infection. Viruses. 2021;13:741.PubMedPubMedCentralCrossRef
79.
go back to reference Alazem M, Lin NS. Roles of plant hormones in the regulation of host-virus interactions. Mol Plant Pathol. 2015;16:529–40.PubMedCrossRef Alazem M, Lin NS. Roles of plant hormones in the regulation of host-virus interactions. Mol Plant Pathol. 2015;16:529–40.PubMedCrossRef
80.
go back to reference Zhao S, Hong W, Wu J, Wang Y, Ji S, Zhu S, et al. A viral protein promotes host SAMS1 activity and ethylene production for the benefit of virus infection. Elife. 2017;6:e27529.PubMedPubMedCentralCrossRef Zhao S, Hong W, Wu J, Wang Y, Ji S, Zhu S, et al. A viral protein promotes host SAMS1 activity and ethylene production for the benefit of virus infection. Elife. 2017;6:e27529.PubMedPubMedCentralCrossRef
81.
go back to reference Zhu F, Xi DH, Deng XG, Peng XJ, Tang H, Chen YJ, et al. The chilli veinal mottle virus regulates expression of the tobacco mosaic virus resistance gene N and jasmonic acid/ethylene signaling is essential for systemic resistance against Chilli veinal mottle virus in tobacco. Plant Mol Biol Rep. 2014;32:382–94.CrossRef Zhu F, Xi DH, Deng XG, Peng XJ, Tang H, Chen YJ, et al. The chilli veinal mottle virus regulates expression of the tobacco mosaic virus resistance gene N and jasmonic acid/ethylene signaling is essential for systemic resistance against Chilli veinal mottle virus in tobacco. Plant Mol Biol Rep. 2014;32:382–94.CrossRef
82.
go back to reference Chandan RK, Singh AK, Patel S, Swain DM, Tuteja N, Jha G. Silencing of tomato CTR1 provides enhanced tolerance against tomato leaf curl virus infection. Plant Signal Behav. 2019;14:e1565595.PubMedPubMedCentralCrossRef Chandan RK, Singh AK, Patel S, Swain DM, Tuteja N, Jha G. Silencing of tomato CTR1 provides enhanced tolerance against tomato leaf curl virus infection. Plant Signal Behav. 2019;14:e1565595.PubMedPubMedCentralCrossRef
Metadata
Title
Integrated next-generation sequencing and comparative transcriptomic analysis of leaves provides novel insights into the ethylene pathway of Chrysanthemum morifolium in response to a Chinese isolate of chrysanthemum virus B
Authors
Xueting Zhong
Lianlian Yang
Jiapeng Li
Zhaoyang Tang
Choufei Wu
Liqin Zhang
Xueping Zhou
Yaqin Wang
Zhanqi Wang
Publication date
01-12-2022
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2022
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-022-01890-3

Other articles of this Issue 1/2022

Virology Journal 1/2022 Go to the issue