Transcriptome Analysis and RNA Interference Reveal GhGDH2 Regulating Cotton Resistance to Verticillium Wilt by JA and SA Signaling Pathways

Xian-Peng Xiong; Shi-Chao Sun; Qian-Hao Zhu; Xin-Yu Zhang; Feng Liu; Yan-Jun Li; Fei Xue; Jie Sun

doi:10.3389/fpls.2021.654676

journal article Open Access Jun 11, 2021

Transcriptome Analysis and RNA Interference Reveal GhGDH2 Regulating Cotton Resistance to Verticillium Wilt by JA and SA Signaling Pathways

Xian-Peng Xiong Shi-Chao Sun Qian-Hao Zhu Xin-Yu Zhang

Feng Liu

Yan-Jun Li Fei Xue

Jie Sun

Frontiers in Plant Science Vol. 12 · Frontiers Media SA

View at Publisher Save 10.3389/fpls.2021.654676

Abstract

Verticillium wilt, caused by Verticillium dahliae, is one of the most damaging and widespread soil-borne cotton diseases. The molecular mechanisms underlying the cotton defense against V. dahliae remain largely elusive. Here, we compared the transcriptional differences between Upland cotton cultivars: one highly resistant (HR; Shidalukang 1) and one highly susceptible (HS; Junmian 1). This was done at multiple time points after V. dahliae inoculation, which identified 2010 and 1275 differentially expressed genes (DEGs) in HR and HS, respectively. Plant hormone signal transduction-related genes were enriched in HR, whereas genes related to lignin biosynthesis were enriched in both HR and HS. Weighted gene co-expression network analysis (WGCNA) using the 2868 non-redundant genes differentially expressed between the V. dahliae infected and uninfected samples in HR or HS identified 10 different gene network modules and 22 hub genes with a potential role in regulating cotton defense against V. dahliae infection. GhGDH2, encoding glutamate dehydrogenase (GDH), was selected for functional characterization. Suppressing the expression level of GhGDH2 by virus-induced gene silencing (VIGS) in HS led to inhibition of the salicylic acid (SA) biosynthesis/signaling pathways and activation of the jasmonic acid (JA) biosynthesis/signaling pathways, which resulted in an increase of 42.1% JA content and a reduction of 78.9% SA content in cotton roots, and consequently enhanced V. dahliae resistance. Our finding provides new insights on the molecular mechanisms of cotton resistance to V. dahliae infection and candidate genes for breeding V. dahliae resistance cotton cultivars by genetic modification.

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References

65

[1]

Amorim "Transcription factors involved in plant resistance to pathogens." Curr. Protein Pept. Sci. (2016) 10.2174/1389203717666160619185308

[2]

Attaran "Temporal dynamics of growth and photosynthesis suppression in response to jasmonate signaling." Plant Physiol. (2014) 10.1104/pp.114.239004

[3]

Lignin Biosynthesis

Wout Boerjan, John Ralph, Marie Baucher

Annual Review of Plant Biology 2003 10.1146/annurev.arplant.54.031902.134938

[4]

Trimmomatic: a flexible trimmer for Illumina sequence data

Anthony M. Bolger, Marc Lohse, Bjoern Usadel

Bioinformatics 2014 10.1093/bioinformatics/btu170

[5]

Cai "Molecular research and genetic engineering of resistance to Verticillium wilt in cotton: a review." Afr. J. Biotechnol. (2009) 10.5897/ajb2009.000-9571

[6]

de Torres Zabala "Chloroplasts play a central role in plant defence and are targeted by pathogen effectors." Nat. Plants (2015) 10.1038/nplants.2015.74

[7]

Dhar "Hormone signaling and its interplay with development and defense responses in Verticillium-plant interactions." Front. Plant Sci. (2020) 10.3389/fpls.2020.584997

[8]

RNA-Sequencing, Physiological and RNAi Analyses Provide Insights into the Response Mechanism of the ABC-Mediated Resistance to Verticillium dahliae Infection in Cotton

Qi Dong, Richard Odongo Magwanga, Xiaoyan Cai et al.

Genes 2019 10.3390/genes10020110

[9]

Du "Identification of regulatory networks and hub genes controlling soybean seed set and size using RNA sequencing analysis." J. Exp. Bot. (2017) 10.1093/jxb/erw460

[10]

Duan "Characterization of a novel cotton subtilase gene GbSBT1 in response to extracellular stimulations and its role in Verticillium resistance." PLoS One (2016) 10.1371/journal.pone.0153988

[11]

Dulermo "Amino acid changes during sunflower infection by the necrotrophic fungus B. cinerea." Plant Signal. Behav. (2009) 10.4161/psb.4.9.9397

[12]

SYSTEMIC ACQUIRED RESISTANCE

W.E. Durrant, X. Dong

Annual Review of Phytopathology 2004 10.1146/annurev.phyto.42.040803.140421

[13]

Ellendorff "RNA silencing is required for Arabidopsis defence against Verticillium wilt disease." J. Exp. Bot. (2009) 10.1093/jxb/ern306

[14]

Fontaine "Characterization of a NADH-dependent glutamate dehydrogenase mutant of Arabidopsis demonstrates the key role of this enzyme in root carbon and nitrogen metabolism." Plant Cell (2012) 10.1105/tpc.112.103689

[15]

Fradin "Interfamily transfer of tomato Ve1 mediates Verticillium resistance in Arabidopsis." Plant Physiol. (2011) 10.1104/pp.111.180067

[16]

Proteomic and Virus-induced Gene Silencing (VIGS) Analyses Reveal That Gossypol, Brassinosteroids, and Jasmonic acid Contribute to the Resistance of Cotton to Verticillium dahliae

Wei Gao, Lu Long, Long-Fu Zhu et al.

Molecular & Cellular Proteomics 10.1074/mcp.m113.031013

[17]

Gao "Cotton GhBAK1 mediates Verticillium wilt resistance and cell death." J. Integr. Plant Biol. 10.1111/jipb.12064

[18]

Guo "An ethylene response-related factor, GbERF1-like, from Gossypium barbadense improves resistance to Verticillium dahliae via activating lignin synthesis." Plant Mol. Biol. (2016) 10.1007/s11103-016-0467-466

[19]

He "GhJAZ2 attenuates cotton resistance to biotic stresses via the inhibition of the transcriptional activity of GhbHLH171." Mol. Plant. Pathol. (2018) 10.1111/mpp.12575

[20]

Hu "Laccase GhLac1 modulates broad-spectrum biotic stress tolerance via manipulating phenylpropanoid pathway and jasmonic acid synthesis." Plant Physiol. (2018) 10.1104/pp.17.01628

[21]

Hu "Proteome and metabolome analyses reveal differential responses in tomato -Verticillium dahliae-interactions." J. Proteomics (2019) 10.1016/j.jprot.2019.103449

[22]

Huot "Growth-defense tradeoffs in plants: a balancing act to optimize fitness." Mol. Plant. (2014) 10.1093/mp/ssu049

[23]

Kachroo "Plastidial fatty acid signaling modulates salicylic acid- and jasmonic acid-mediated defense pathways in the Arabidopsis ssi2 mutant." Plant Cell (2003) 10.1105/tpc.017301

[24]

Kachroo "The Arabidopsis stearoyl-acyl carrier protein-desaturase family and the contribution of leaf isoforms to oleic acid synthesis." Plant Mol. Biol. (2007) 10.1007/s11103-006-9086-y

[25]

Koornneef "Cross talk in defense signaling." Plant Physiol. (2008) 10.1104/pp.107.112029

[26]

WGCNA: an R package for weighted correlation network analysis

Peter Langfelder, Steve Horvath

BMC Bioinformatics 2008 10.1186/1471-2105-9-559

[27]

Li "Melatonin enhances cotton immunity to Verticillium wilt via manipulating lignin and gossypol biosynthesis." Plant J. (2019) 10.1111/tpj.14477

[28]

Li "Cotton WRKY1 mediates the plant defense-to-development transition during infection of cotton by Verticillium dahliae by activating JASMONATE ZIM-DOMAIN1 expression." Plant Physiol. (2014) 10.1104/pp.114.246694

[29]

Li "BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling." Cell (2002) 10.1016/s0092-8674(02)00812-817

[30]

Li "Transcriptomic and biochemical analysis of upland cotton (Gossypium hirsutum) and a chromosome segment substitution line from G. hirsutum x G. barbadense in response to Verticillium dahliae infection." BMC plant Biol. (2019) 10.1186/s12870-018-1619-1614

[31]

Li "Genome-wide association study discovered candidate genes of Verticillium wilt resistance in upland cotton (Gossypium hirsutum L.)." Plant Biotechnol. J. (2017) 10.1111/pbi.12734

[32]

Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method

Kenneth J. Livak, Thomas D. Schmittgen

Methods 2001 10.1006/meth.2001.1262

[33]

Love "Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2." Genome Biol. (2014) 10.1186/s13059-014-0550-558

[34]

Pageau "The two senescence-related markers, GS1 (cytosolic glutamine synthetase) and GDH (glutamate dehydrogenase), involved in nitrogen mobilization, are differentially regulated during pathogen attack and by stress hormones and reactive oxygen species in Nicotiana tabacum L. leaves." J. Exp. Bot. (2006) 10.1093/jxb/erj035

[35]

Seifi "Glutamate metabolism in plant disease and defense: friend or foe?" Mol. Plant Microbe Interact. (2013) 10.1094/mpmi-07-12-0176-cr

[36]

Shaban "Physiological and molecular mechanism of defense in cotton against Verticillium dahliae." Plant Physiol. Biochem. (2018) 10.1016/j.plaphy.2018.02.011

[37]

Shim "AtMYB44 regulates WRKY70 expression and modulates antagonistic interaction between salicylic acid and jasmonic acid signaling." Plant J. (2013) 10.1111/tpj.12051

[38]

Sun "Cotton cytochrome P450 CYP82D regulates systemic cell death by modulating the octadecanoid pathway." Nat. Commun. (2014) 10.1038/ncomms6372

[39]

Sun "Analysis of sea-island cotton and upland cotton in response to Verticillium dahliae infection by RNA sequencing." BMC Genomics (2013) 10.1186/1471-2164-14-852

[40]

Sun "Transcriptome sequencing and metabolome analysis reveal genes involved in pigmentation of green-colored cotton fibers." Int. J. Mol. Sci. (2019) 10.3390/ijms20194838

[41]

Tan "Co-expression network analysis of the transcriptomes of rice roots exposed to various cadmium stresses reveals universal cadmium-responsive genes." BMC Plant Biol. (2017) 10.1186/s12870-017-1143-y

[42]

Tavernier "The plant nitrogen mobilization promoted by Colletotrichum lindemuthianum in Phaseolus leaves depends on fungus pathogenicity." J. Exp. Bot. (2007) 10.1093/jxb/erm182

[43]

Thaler "Evolution of jasmonate and salicylate signal crosstalk." Trends Plant. Sci. (2012) 10.1016/j.tplants.2012.02.010

[44]

Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation

Cole Trapnell, Brian A Williams, Geo Pertea et al.

Nature Biotechnology 2010 10.1038/nbt.1621

[45]

Tsai "Ethylene-regulated glutamate dehydrogenase fine-tunes metabolism during anoxia-reoxygenation." Plant Physiol. (2016) 10.1104/pp.16.00985

[46]

Lignin Biosynthesis and Structure

Ruben Vanholme, Brecht Demedts, Kris Morreel et al.

Plant Physiology 2010 10.1104/pp.110.155119

[47]

Wang "iTRAQ-based proteomics analysis of autophagy-mediated immune responses against the vascular fungal pathogen Verticillium dahliae in Arabidopsis." Autophagy (2018) 10.1080/15548627.2017.1423438

[48]

Wang "Proteomic analysis of the sea-island cotton roots infected by wilt pathogen Verticillium dahliae." Proteomics (2011) 10.1002/pmic.201100062

[49]

Wang "Significant improvement of cotton Verticillium wilt resistance by manipulating the expression of Gastrodia antifungal proteins." Mol. Plant. (2016) 10.1016/j.molp.2016.06.013

[50]

RNA-Seq: a revolutionary tool for transcriptomics

Zhong Wang, Mark Gerstein, Michael Snyder

Nature Reviews Genetics 2009 10.1038/nrg2484

Showing 50 of 65 references

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References

Details

Published: Jun 11, 2021
Vol/Issue: 12
License: View

Authors

Qingdao University

Funding

National Key Research and Development Program of China

Cite This Article

Xian-Peng Xiong, Shi-Chao Sun, Qian-Hao Zhu, et al. (2021). Transcriptome Analysis and RNA Interference Reveal GhGDH2 Regulating Cotton Resistance to Verticillium Wilt by JA and SA Signaling Pathways. Frontiers in Plant Science, 12. https://doi.org/10.3389/fpls.2021.654676

Transcriptome Analysis and RNA Interference Reveal GhGDH2 Regulating Cotton Resistance to Verticillium Wilt by JA and SA Signaling Pathways

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