Comparative transcriptome revealed the molecular responses of Aconitum carmichaelii Debx. to downy mildew at different stages of disease development.
Aconitum carmichaelii
Downy mildew
Plant hormones
Responses
Transcriptomic analysis
Journal
BMC plant biology
ISSN: 1471-2229
Titre abrégé: BMC Plant Biol
Pays: England
ID NLM: 100967807
Informations de publication
Date de publication:
25 Apr 2024
25 Apr 2024
Historique:
received:
20
11
2023
accepted:
19
04
2024
medline:
26
4
2024
pubmed:
26
4
2024
entrez:
25
4
2024
Statut:
epublish
Résumé
Aconitum carmichaelii Debx. has been widely used as a traditional medicinal herb for a long history in China. It is highly susceptible to various dangerous diseases during the cultivation process. Downy mildew is the most serious leaf disease of A. carmichaelii, affecting plant growth and ultimately leading to a reduction in yield. To better understand the response mechanism of A. carmichaelii leaves subjected to downy mildew, the contents of endogenous plant hormones as well as transcriptome sequencing were analyzed at five different infected stages. The content of 3-indoleacetic acid, abscisic acid, salicylic acid and jasmonic acid has changed significantly in A. carmichaelii leaves with the development of downy mildew, and related synthetic genes such as 9-cis-epoxycarotenoid dioxygenase and phenylalanine ammonia lyase were also significant for disease responses. The transcriptomic data indicated that the differentially expressed genes were primarily associated with plant hormone signal transduction, plant-pathogen interaction, the mitogen-activated protein kinase signaling pathway in plants, and phenylpropanoid biosynthesis. Many of these genes also showed potential functions for resisting downy mildew. Through weighted gene co-expression network analysis, the hub genes and genes that have high connectivity to them were identified, which could participate in plant immune responses. In this study, we elucidated the response and potential genes of A. carmichaelii to downy mildew, and observed the changes of endogenous hormones content at different infection stages, so as to contribute to the further screening and identification of genes involved in the defense of downy mildew.
Sections du résumé
BACKGROUND
BACKGROUND
Aconitum carmichaelii Debx. has been widely used as a traditional medicinal herb for a long history in China. It is highly susceptible to various dangerous diseases during the cultivation process. Downy mildew is the most serious leaf disease of A. carmichaelii, affecting plant growth and ultimately leading to a reduction in yield. To better understand the response mechanism of A. carmichaelii leaves subjected to downy mildew, the contents of endogenous plant hormones as well as transcriptome sequencing were analyzed at five different infected stages.
RESULTS
RESULTS
The content of 3-indoleacetic acid, abscisic acid, salicylic acid and jasmonic acid has changed significantly in A. carmichaelii leaves with the development of downy mildew, and related synthetic genes such as 9-cis-epoxycarotenoid dioxygenase and phenylalanine ammonia lyase were also significant for disease responses. The transcriptomic data indicated that the differentially expressed genes were primarily associated with plant hormone signal transduction, plant-pathogen interaction, the mitogen-activated protein kinase signaling pathway in plants, and phenylpropanoid biosynthesis. Many of these genes also showed potential functions for resisting downy mildew. Through weighted gene co-expression network analysis, the hub genes and genes that have high connectivity to them were identified, which could participate in plant immune responses.
CONCLUSIONS
CONCLUSIONS
In this study, we elucidated the response and potential genes of A. carmichaelii to downy mildew, and observed the changes of endogenous hormones content at different infection stages, so as to contribute to the further screening and identification of genes involved in the defense of downy mildew.
Identifiants
pubmed: 38664645
doi: 10.1186/s12870-024-05048-x
pii: 10.1186/s12870-024-05048-x
doi:
Substances chimiques
Plant Growth Regulators
0
Types de publication
Journal Article
Comparative Study
Langues
eng
Sous-ensembles de citation
IM
Pagination
332Informations de copyright
© 2024. The Author(s).
Références
Fu YP, Zou YF, Lei FY, Wangensteen H, Inngjerdingen KT. Aconitum carmichaelii Debeaux: a systematic review on traditional use, and the chemical structures and pharmacological properties of polysaccharides and phenolic compounds in the roots. J Ethnopharmacol. 2022;291:115148.
pubmed: 35240238
doi: 10.1016/j.jep.2022.115148
Fu YP, Li CY, Peng X, Zou YF, Rise F, Paulsen BS, Wangensteen H, Inngjerdingen KT. Polysaccharides from Aconitum carmichaelii leaves: structure, immunomodulatory and anti-inflammatory activities. Carbohyd Polym. 2022;291:119655.
doi: 10.1016/j.carbpol.2022.119655
Zhang W, Lu C, Cai S, Feng Y, Shan J, Di L. Aconiti Lateralis Radix Praeparata as potential anticancer herb: bioactive compounds and molecular mechanisms. Front Pharmacol. 2022;13:870282.
pubmed: 35662730
pmcid: 9158441
doi: 10.3389/fphar.2022.870282
He G, Wang X, Liu W, Li Y, Shao Y, Liu W, Liang X, Bao X. Chemical constituents, pharmacological effects, toxicology, processing and compatibility of Fuzi (lateral root of Aconitum carmichaelii Debx): a review. J Ethnopharmacol. 2023;307:116160.
pubmed: 36773791
doi: 10.1016/j.jep.2023.116160
Zhao L, Sun Z, Yang L, Cui R, Yang W, Li B. Neuropharmacological effects of Aconiti Lateralis Radix Praeparata. Clin Exp Pharmacol Physiol. 2020;47(4):531–42.
pubmed: 31837236
doi: 10.1111/1440-1681.13228
Yang M, Ji X, Zuo Z. Relationships between the toxicities of Radix Aconiti Lateralis Preparata (Fuzi) and the toxicokinetics of its main diester-diterpenoid alkaloids. Toxins. 2018;10(10):391.
pubmed: 30261585
pmcid: 6215299
doi: 10.3390/toxins10100391
Zhou G, Tang L, Zhou X, Wang T, Kou Z, Wang Z. A review on phytochemistry and pharmacological activities of the processed lateral root of Aconitum carmichaelii Debeaux. J Ethnopharmacol. 2015;160:173–93.
pubmed: 25479152
doi: 10.1016/j.jep.2014.11.043
Yang Y, Hu P, Zhou X, Wu P, Si X, Lu B, Zhu Y, Xia Y. Transcriptome analysis of Aconitum carmichaelii and exploration of the salsolinol biosynthetic pathway. Fitoterapia. 2020;140:104412.
pubmed: 31698060
doi: 10.1016/j.fitote.2019.104412
Wang W, Zhang D, Wen H, Wang Q, Peng C, Gao J. Soil fungal biodiversity and pathogen identification of rotten disease in Aconitum carmichaelii (Fuzi) roots. PLoS ONE. 2018;13(10):e0205891.
pubmed: 30379951
pmcid: 6209216
doi: 10.1371/journal.pone.0205891
Rajarammohan S. Transcriptome analysis of the necrotrophic pathogen Alternaria brassicae reveals insights into its pathogenesis in Brassica juncea. Microbiol Spect. 2023;11(2):e0293922.
doi: 10.1128/spectrum.02939-22
Zhao Z, Dong Y, Wang J, Zhang G, Zhang Z, Zhang A, Wang Z, Ma P, Li Y, Zhang X, et al. Comparative transcriptome analysis of melon (Cucumis melo L.) reveals candidate genes and pathways involved in powdery mildew resistance. Sci Rep. 2022;12(1):4936.
pubmed: 35322050
pmcid: 8943038
doi: 10.1038/s41598-022-08763-3
Zhong S, Yin YP, He YN, Li MJ, Zhang M, Li SN, Peng C, Zhang DK, Gao JH. Analysis of transcriptome differences in two leaf-type cultivars of Aconitum carmichaelii. Zhongguo Zhong Yao Za Zhi. 2020;45(7):1633–40.
pubmed: 32489043
Yan W, Jian Y, Duan S, Guo X, Hu J, Yang X, Li G. Dissection of the plant hormone signal transduction network in late blight-resistant potato genotype SD20 and prediction of key resistance genes. Phytopathology. 2023;113(3):528–38.
pubmed: 36173283
doi: 10.1094/PHYTO-04-22-0124-R
Chen J, Xuan Y, Yi J, Xiao G, Yuan P, Li D. Progress in rice sheath blight resistance research. Front Plant Sci. 2023;14:1141697.
pubmed: 37035075
pmcid: 10080073
doi: 10.3389/fpls.2023.1141697
Li X, Niu G, Fan Y, Liu W, Wu Q, Yu C, Wang J, Xiao Y, Hou L, Jin D, et al. Synthetic dual hormone-responsive promoters enable engineering of plants with broad-spectrum resistance. Plant Commun. 2023;4:100596.
pubmed: 36998212
pmcid: 10363552
doi: 10.1016/j.xplc.2023.100596
Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnetjournal. 2011;17:10–2.
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011;29(7):644–52.
pubmed: 21572440
pmcid: 3571712
doi: 10.1038/nbt.1883
Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12(1):59–60.
pubmed: 25402007
doi: 10.1038/nmeth.3176
Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods. 2017;14(4):417–9.
pubmed: 28263959
pmcid: 5600148
doi: 10.1038/nmeth.4197
Chaudhary P, Sharma PC. Distribution of simple sequence repeats, transcription factors, and differentially expressed genes in the NGS-based transcriptome of male and female seabuckthorn (Hippophae salicifolia). J Biomol Struct Dyn. 2023;41(6):2504–17.
pubmed: 35120412
doi: 10.1080/07391102.2022.2034669
Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics. 2008;9:559.
pubmed: 19114008
pmcid: 2631488
doi: 10.1186/1471-2105-9-559
Killcoyne S, Carter GW, Smith J, Boyle J. Cytoscape: a community-based framework for network modeling. Methods Mol Biol (Clifton, NJ). 2009;563:219–39.
doi: 10.1007/978-1-60761-175-2_12
Zeng LF, Li GD, Wang BJ, Wang YB, Cheng JP, Cao XQ, Guan LN, Zhu LY, Qian ZG, Ma XH. Selection of optimal qRT-PCR reference genes for Aconitum vilmorinianum. Zhongguo Zhong Yao Za Zhi. 2021;46(12):3116–22.
pubmed: 34467703
Jin J, Tian F, Yang DC, Meng YQ, Kong L, Luo J, Gao G. PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res. 2017;45(D1):D1040-d1045.
pubmed: 27924042
doi: 10.1093/nar/gkw982
Chen L, Meng Y, Bai Y, Yu H, Qian Y, Zhang D, Zhou Y. Starch and sucrose metabolism and plant hormone signaling pathways play crucial roles in Aquilegia salt stress adaption. Int J Mol Sci. 2023;24:3948.
pubmed: 36835360
pmcid: 9966690
doi: 10.3390/ijms24043948
Li Y, Li Y, Liu Y, Wu Y, Xie Q. The sHSP22 heat shock protein requires the ABI1 protein phosphatase to modulate polar auxin transport and downstream responses. Plant Physiol. 2018;176(3):2406–25.
pubmed: 29288233
doi: 10.1104/pp.17.01206
González-Lamothe R, El Oirdi M, Brisson N, Bouarab K. The conjugated auxin indole-3-acetic acid-aspartic acid promotes plant disease development. Plant Cell. 2012;24(2):762–77.
pubmed: 22374398
pmcid: 3315245
doi: 10.1105/tpc.111.095190
Tan L, Liu Q, Song Y, Zhou G, Luan L, Weng Q, He C. Differential function of endogenous and exogenous abscisic acid during bacterial pattern-induced production of reactive oxygen species in Arabidopsis. Int J Mol Sci. 2019;20(10):2544.
pubmed: 31126160
pmcid: 6566928
doi: 10.3390/ijms20102544
Zou K, Li Y, Zhang W, Jia Y, Wang Y, Ma Y, Lv X, Xuan Y, Du W. Early infection response of fungal biotroph Ustilago maydis in maize. Front Plant Sci. 2022;13:970897.
pubmed: 36161006
pmcid: 9504671
doi: 10.3389/fpls.2022.970897
Yop GS, Gair LHV, da Silva VS, Machado ACZ, Santiago DC, Tomaz JP. ABA is involved in the resistance response of Arabidopsis thaliana against Meloidogyne paranaensis. Plant Dis. 2023;107(9):2778-2783.
Huang R, Li Y, Tang G, Hui S, Yang Z, Zhao J, Liu H, Cao J, Yuan M. Dynamic phytohormone profiling of rice upon rice black-streaked dwarf virus invasion. J Plant Physiol. 2018;228:92–100.
pubmed: 29886196
doi: 10.1016/j.jplph.2018.06.001
Fidler J, Graska J, Gietler M, Nykiel M, Prabucka B, Rybarczyk-Płońska A, Muszyńska E, Morkunas I, Labudda M. PYR/PYL/RCAR receptors play a vital role in the abscisic-acid-dependent responses of plants to external or internal stimuli. Cells. 2022;11(8):1352.
pubmed: 35456031
pmcid: 9028234
doi: 10.3390/cells11081352
Sun L, Li J, Liu Y, Noman A, Chen L, Liu J. Transcriptome profiling in rice reveals a positive role for OsNCED3 in defense against the brown planthopper, Nilaparvata lugens BMC Genomics. 2022;23(1):634.
pubmed: 36064309
pmcid: 9446700
doi: 10.1186/s12864-022-08846-5
Rauf M, Ur-Rahman A, Arif M, Gul H, Ud-Din A, Hamayun M, Lee IJ. Immunomodulatory molecular mechanisms of Luffa cylindrica for downy mildews resistance induced by growth-promoting endophytic fungi. J Fungi (Basel, Switzerland). 2022;8(7):689.
Su Y, Wang G, Huang Z, Hu L, Fu T, Wang X. Silencing GhIAA43, a member of cotton AUX/IAA genes, enhances wilt resistance via activation of salicylic acid-mediated defenses. Plant Sci: Int J Exper Plant Biol. 2022;314:111126.
doi: 10.1016/j.plantsci.2021.111126
Fei C, Chen L, Yang T, Zou W, Lin H, Xi D. The role of phytochromes in Nicotiana tabacum against Chilli veinal mottle virus. Plant Physiol Biochem: PPB. 2019;139:470–7.
pubmed: 30999134
doi: 10.1016/j.plaphy.2019.04.002
Liu N, Wang Y, Li K, Li C, Liu B, Zhao L, Zhang X, Qu F, Gao L, Xia T, et al. Transcriptional analysis of tea plants (Camellia sinensis) in response to salicylic acid treatment. J Agric Food Chem. 2023;71(5):2377–89.
pubmed: 36695193
doi: 10.1021/acs.jafc.2c07046
Yang Y, Li HG, Liu M, Wang HL, Yang Q, Yan DH, Zhang Y, Li Z, Feng CH, Niu M, et al. PeTGA1 enhances disease resistance against Colletotrichum gloeosporioides through directly regulating PeSARD1 in poplar. Int J Biol Macromol. 2022;214:672–84.
pubmed: 35738343
doi: 10.1016/j.ijbiomac.2022.06.099
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(3):e1565595.
pubmed: 30661468
pmcid: 6422369
doi: 10.1080/15592324.2019.1565595
Li Y, Liu K, Tong G, Xi C, Liu J, Zhao H, Wang Y, Ren D, Han S. MPK3/MPK6-mediated phosphorylation of ERF72 positively regulates resistance to Botrytis cinerea through directly and indirectly activating the transcription of camalexin biosynthesis enzymes. J Exp Bot. 2022;73(1):413–28.
pubmed: 34499162
doi: 10.1093/jxb/erab415
Chang M, Chen H, Liu F, Fu ZQ. PTI and ETI: convergent pathways with diverse elicitors. Trends Plant Sci. 2022;27(2):113–5.
pubmed: 34863646
doi: 10.1016/j.tplants.2021.11.013
Wang JP, Xu YP, Munyampundu JP, Liu TY, Cai XZ. Calcium-dependent protein kinase (CDPK) and CDPK-related kinase (CRK) gene families in tomato: genome-wide identification and functional analyses in disease resistance. Mol Genet Genom: MGG. 2016;291(2):661–76.
doi: 10.1007/s00438-015-1137-0
Zhu X, Robe E, Jomat L, Aldon D, Mazars C, Galaud JP. CML8, an Arabidopsis calmodulin-like protein, plays a role in Pseudomonas syringae plant immunity. Plant Cell Physiol. 2017;58(2):307–19.
pubmed: 27837097
Zhang H, Huang Q, Yi L, Song X, Li L, Deng G, Liang J, Chen F, Yu M, Long H. PAL-mediated SA biosynthesis pathway contributes to nematode resistance in wheat. Plant J: Cell Mol Biol. 2021;107(3):698–712.
doi: 10.1111/tpj.15316
Pant S, Huang Y. Genome-wide studies of PAL genes in sorghum and their responses to aphid infestation. Sci Rep. 2022;12(1):22537.
pubmed: 36581623
pmcid: 9800386
doi: 10.1038/s41598-022-25214-1
Kavil S, Otti G, Bouvaine S, Armitage A, Maruthi MN. PAL1 gene of the phenylpropanoid pathway increases resistance to the cassava brown streak virus in cassava. Virol J. 2021;18(1):184.
pubmed: 34503522
pmcid: 8428094
doi: 10.1186/s12985-021-01649-2
Li C, Qin J, Huang Y, Shang W, Chen J, Klosterman SJ, Subbarao KV, Hu X. Verticillium dahliae effector VdCE11 contributes to virulence by promoting accumulation and activity of the aspartic protease GhAP1 from cotton. Microbiol Spect. 2023;11(1):e0354722.
doi: 10.1128/spectrum.03547-22
Figueiredo L, Santos RB, Figueiredo A. The grapevine aspartic protease gene family: characterization and expression modulation in response to Plasmopara viticola J Plant Res. 2022;135(3):501–15.
pubmed: 35426578
doi: 10.1007/s10265-022-01390-z
Widjaja I, Lassowskat I, Bethke G, Eschen-Lippold L, Long HH, Naumann K, Dangl JL, Scheel D, Lee J. A protein phosphatase 2C, responsive to the bacterial effector AvrRpm1 but not to the AvrB effector, regulates defense responses in Arabidopsis. Plant J: Cell Mol Biol. 2010;61(2):249–58.
doi: 10.1111/j.1365-313X.2009.04047.x
Qiu J, Ni L, Xia X, Chen S, Zhang Y, Lang M, Li M, Liu B, Pan Y, Li J, et al. Genome-wide analysis of the protein phosphatase 2C genes in tomato. Genes. 2022;13(4):604.
pubmed: 35456410
pmcid: 9032827
doi: 10.3390/genes13040604
Lan X, Liu Y, Song S, Yin L, Xiang J, Qu J, Lu J. Plasmopara viticola effector PvRXLR131 suppresses plant immunity by targeting plant receptor-like kinase inhibitor BKI1. Mol Plant Pathol. 2019;20(6):765–83.
pubmed: 30945786
pmcid: 6637860
doi: 10.1111/mpp.12790
Mei Y, Wang Y, Hu T, He Z, Zhou X. The C4 protein encoded by tomato leaf curl yunnan virus interferes with mitogen-activated protein kinase cascade-related defense responses through inhibiting the dissociation of the ERECTA/BKI1 complex. New Phytol. 2021;231(2):747–62.
pubmed: 33829507
doi: 10.1111/nph.17387
Hu Z, Fang H, Zhu C, Gu S, Ding S, Yu J, Shi K. Ubiquitylation of phytosulfokine receptor 1 modulates the defense response in tomato. Plant Physiol. 2023;192(3):2507–22.
pubmed: 36946197
pmcid: 10315268
doi: 10.1093/plphys/kiad188
Li W, Zhu Z, Chern M, Yin J, Yang C, Ran L, Cheng M, He M, Wang K, Wang J, et al. A natural allele of a transcription factor in rice confers broad-spectrum blast resistance. Cell. 2017;170(1):114-126.e115.
pubmed: 28666113
doi: 10.1016/j.cell.2017.06.008
Liu J, Shen Y, Cao H, He K, Chu Z, Li N. OsbHLH057 targets the AATCA cis-element to regulate disease resistance and drought tolerance in rice. Plant Cell Rep. 2022;41(5):1285–99.
pubmed: 35278106
doi: 10.1007/s00299-022-02859-w
Li D, Li X, Liu X, Zhang Z. Comprehensive analysis of bZIP gene family and function of RcbZIP17 on Botrytis resistance in rose (Rosa chinensis). Gene. 2023;849:146867.
pubmed: 36115481
doi: 10.1016/j.gene.2022.146867
Wang H, Gong W, Wang Y, Ma Q. Contribution of a WRKY transcription factor, ShWRKY81, to powdery mildew resistance in wild tomato. Int J Mol Sci. 2023;24(3):2583.
pubmed: 36768909
pmcid: 9917159
doi: 10.3390/ijms24032583