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GbC4H regulates the metabolic flow of flavonoids and inhibits the occurrence of Fusarium wilt in sea island cotton

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Abstract

Fusarium wilt is a soil-borne fungal disease, and various problems associated with this disease in cotton production in Xinjiang need to be urgently solved. Thus, the breeding of new disease-resistant varieties can effectively solve this problem. Here, the GbC4H gene was cloned from the resistant variety 06–146 and silenced by virus-induced gene silencin (VIGS). By measuring the flavonoid contents, we explored the role of the GbC4H gene in the flavonoid pathway of sea island cotton, and the mechanisms underlying flavonoid accumulation regulated by the GbC4H gene and resistance to Fusarium wilt were evaluated. The resistance of cotton seedlings to Fusarium wilt was significantly reduced by the silencing of GbC4H in 06–146. The expression of genes downstream from GbC4H in cotton seedlings with Fusarium wilt decreased to different degrees. The accumulation of flavonoids may originate from GbC4H gene activity because flavonoid antibacterial compounds were synthesized to inhibit Fusarium wilt under the simultaneous action of downstream genes. Moreover, the Methyl jasmonate (MeJA) and salicylic acid (SA) signaling pathways were found to be involved in the resistance of cotton to Fusarium wilt. Overall, GbC4H may mediate the MeJA and SA signaling pathways and regulate downstream genes to induce the accumulation of a large number of flavonoids and thus inhibit the occurrence of Fusarium wilt in cotton.

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References

  • Barber MS, Mitchell HJ (1997) Regulation of phenylpropanoid metabolism in relation to lignin biosynthesis in plants. Int Rev Cytol 172:243–293

    Article  CAS  Google Scholar 

  • Bari R, Jones JDG (2009) Role of incorporation in plant defence responses. Plant Mol Biol 69(4):473–488

    Article  CAS  PubMed  Google Scholar 

  • Chaturvedi R, Krothapalli K, Makandar R, Nandi A, Sparks AA, Roth MR et al (2008) Plastid ω3-fatty acid desaturase-dependent accumulation of a systemic acquired resistance inducing activity in petiole exudates of Arabidopsis thaliana is independent of jasmonic acid. Plant J 54(1):106–117

    Article  CAS  PubMed  Google Scholar 

  • Chen AH, Chai YR, Li JN, Chen L (2007) Molecular cloning of two genes encoding cinnamate 4-hydroxylase (C4H) from oilseed rape (Brassica napus). BMB Rep 40(2):247–260

    Article  CAS  Google Scholar 

  • Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MS, Wang L (2002) The phenylpropanoid pathway and plant defence-a genomics perspective. Mol Plant Pathol 3(5):371–390

    Article  CAS  PubMed  Google Scholar 

  • Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB et al (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19(7):2225–2245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong X (2004) NPR1, all things considered. Curr Opin Plant Biol 7(5):547–552

    Article  CAS  PubMed  Google Scholar 

  • Du X, Huang G, He S, Yang Z, Sun G, Ma X et al (2018) Resequencing of 243 diploid cotton accessions based on an updated A genome identifies the genetic basis of key agronomic traits. Nat Genet 50(6):796–802

    Article  CAS  PubMed  Google Scholar 

  • Elliger CA, Chan BC, Waiss AC (1980) Flavonoids as larval growth inhibitors. Naturwissenschaften 67(7):358–360

    Article  CAS  Google Scholar 

  • Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10(4):366–371

    Article  CAS  PubMed  Google Scholar 

  • Falcone-Ferreyra ML, Rius S, Casati P (2012) Flavonoids: biosynthesis, biological functions, and biotechnological applications. Front Plant Sci 3:222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao W, Long L, Zhu LF, Xu L, Gao WH, Sun LQ et al (2013) Proteomic and virus-induced gene silencing (VIGS) analyses reveal that gossypol, brassinosteroids, and jasmonic acid contribute to the resistance of cotton to Verticillium dahliae. Mol Cell Proteomics 12(12):3690–3703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao X, Britt-Jr RC, Shan L, He P (2011) Agrobacterium-mediated virus-induced gene silencing assay in cotton. J vis Exp 54:e2938

    Google Scholar 

  • Guo W, Jin L, Miao Y, He X, Hu Q, Guo K et al (2016) An ethylene response-related factor, GbERF1-like, from Gossypium barbadense improves resistance to Verticillium dahliae via activating lignin synthesis. Plant Mol Biol 91(3):305–318

    Article  CAS  PubMed  Google Scholar 

  • Hu Q, Min L, Yang X, Jin S, Zhang L, Li Y et al (2018) Laccase GhLac1 modulates broad-spectrum biotic stress tolerance via manipulating phenylpropanoid pathway and jasmonic acid synthesis. Plant Physiol 176(2):1808–1823

    Article  CAS  PubMed  Google Scholar 

  • Huang Q, Qu Y, Yao Z, Li M, Chen Q (2017) Correlation between Fusarium wilt resistance and expression levels of genes involved in flavonoid metabolism pathway in Gossypium barbadense L. Acta Agron Sin 43(12):1791–1801

    Article  Google Scholar 

  • Huffaker A, Kaplan F, Vaughan MM, Dafoe NJ, Ni X, Rocca JR et al (2011) Novel acidic sesquiterpenoids constitute a dominant class of pathogen-induced phytoalexins in maize. Plant Physiol 156(4):2082–2097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kong JQ, Lu D, Wang ZB (2014) Molecular cloning and yeast expression of cinnamate 4-hydroxylase from Ornithogalum saundersiae baker. Molecules 19(2):1608–1621

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumar R, Vashisth D, Misra A, Akhtar MQ, Jalil SU, Shanker K et al (2016) RNAi down-regulation of cinnamate-4-hydroxylase increases artemisinin biosynthesis in Artemisia annua. Sci Rep 6(1):1–12

    Google Scholar 

  • Li C, He X, Luo X, Xu L, Liu L, Min L et al (2014) Cotton WRKY1 mediates the plant defense-to-development transition during infection of cotton by Verticillium dahliae by activating JASMONATE ZIM-DOMAIN1 expression. Plant Physiol 166(4):2179–2194

    Article  PubMed  PubMed Central  Google Scholar 

  • Li H (2006) Research on international competitiveness of Xinjiang’s Cotton industry in China. Dissertation, Huazhong Agricultural University (in chinese)

  • Li J, Brader G, Kariola T, Tapio-Palva E (2006) WRKY70 modulates the selection of signaling pathways in plant defense. Plant J 46(3):477–491

    Article  CAS  PubMed  Google Scholar 

  • Li W, Yang L, Jiang L, Zhang G, Luo Y (2016) Molecular cloning and functional characterization of a cinnamate 4-hydroxylase-encoding gene from Camptotheca acuminata. Acta Physiol Plant 38(11):1–9

    Article  Google Scholar 

  • Liechti R, Farmer EE (2002) The jasmonate pathway. Science 296(5573):1649–1650

    Article  CAS  PubMed  Google Scholar 

  • Liu S, Zhang X, Xiao S, Ma J, Shi W, Qin T et al (2021) A single-nucleotide mutation in a GLUTAMATE RECEPTOR-LIKE gene confers resistance to Fusarium wilt in Gossypium hirsutum. Adv Sci 8(7):2002723

    Article  CAS  Google Scholar 

  • Lorenzo O, Piqueras R, Sánchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15(1):165–178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mao P, Duan M, Wei C, Li Y (2007) WRKY62 transcription factor acts downstream of cytosolic NPR1 and negatively regulates jasmonate-responsive gene expression. Plant Cell Physiol 48:833–842

    Article  CAS  PubMed  Google Scholar 

  • Nazeer W, Tipu AL, Ahmad S, Mahmood K, Mahmood A, Zhou B (2014) Evaluation of cotton leaf curl virus resistance in BC1, BC2, and BC3 progenies from an interspecific cross between Gossypium arboreum and Gossypium hirsutum. PLoS ONE 9(11):e111861

    Article  PubMed  PubMed Central  Google Scholar 

  • Park JH, Park NI, Xu H, Park SU (2010) Cloning and characterization of phenylalanine ammonia-lyase and cinnamate 4-hydroxylase and pyranocoumarin biosynthesis in Angelica gigas. J Nat Prod 73(8):1394–1397

    Article  CAS  PubMed  Google Scholar 

  • Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318(5847):113–116

    Article  CAS  PubMed  Google Scholar 

  • Peng JL, Qu YY, Wang LP, Wang C, Hao WW, Wang CL (2003) A Study on properties of resistance to Fusarium wilt in leaves of sea island cotton (Gossypium barbadense) and upland cotton (Gossypium hirsutum L.) under different temperature conditions. Xinjiang Agricultural Sciences 50(1):89–93 (in chinese)

  • Ro DK, Mah N, Ellis BE, Douglas CJ (2001) Functional characterization and subcellular localization of poplar (Populus trichocarpa× Populus deltoides) cinnamate 4-hydroxylase. Plant Physiol 126(1):317–329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ru M (2017) Cloning and characterization of genes involved in tyrosine-branched pathway of rosmarinic acid biosynthesis from Prunella Vulgris L.. Dissertation, University of Chinese Academy of Sciences (in chinese)

  • Russell DW, Conn EE (1967) The cinnamic acid 4-hydraxylase of pea seedlings. Arch Biochem Biophys 122(1):256–258

    Article  CAS  PubMed  Google Scholar 

  • Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci 97(21):11655–11660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh K, Kumar S, Rani A, Gulati A, Ahuja PS (2009) Phenylalanine ammonia-lyase (PAL) and cinnamate 4-hydroxylase (C4H) and catechins (flavan-3-ols) accumulation in tea. Funct Integr Genomics 9(1):125–134

    Article  CAS  PubMed  Google Scholar 

  • Smith CM, Chuang WP (2014) Plant resistance to aphid feeding: behavioral, physiological, genetic and molecular cues regulate aphid host selection and feeding. Pest Manag Sci 70(4):528–540

    Article  PubMed  Google Scholar 

  • Spoel SH, Johnson JS, Dong X (2007) Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci 104(47):18842–18847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sudheeran PK, Ovadia R, Galsarker O, Maoz I, Sela N, Maurer D et al (2020) Glycosylated flavonoids: fruit’s concealed antifungal arsenal. New Phytol 225(4):1788–1798

    Article  CAS  PubMed  Google Scholar 

  • Truman W, Bennett MH, Kubigsteltig I, Turnbull C, Grant M (2007) Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc Natl Acad Sci 104(3):1075–1080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuan PA, Park NI, Li X, Xu H, Kim HH, Park SU (2010) Molecular cloning and characterization of phenylalanine ammonia-lyase and cinnamate 4-hydroxylase in the phenylpropanoid biosynthesis pathway in garlic (Allium sativum). J Agric Food Chem 58(20):10911–10917

    Article  CAS  PubMed  Google Scholar 

  • Ulloa M, Hutmacher RB, Davis RM, Wright SD, Percy R, Marsh B (2006) Breeding for Fusarium wilt race 4 resistance in cotton under field and greenhouse conditions. Journal of Cotton Science 10:114–127

    Google Scholar 

  • Ulloa M, Hutmacher RB, Roberts PA, Wright SD, Nichols RL, Michael Davis R (2013) Inheritance and QTL mapping of Fusarium wilt race 4 resistance in cotton. Theor Appl Genet 126(5):1405–1418

    Article  CAS  PubMed  Google Scholar 

  • Ulloa M, Wang C, Hutmacher RB, Wright SD, Davis RM, Saski CA et al (2011) Mapping Fusarium wilt race 1 resistance genes in cotton by inheritance, QTL and sequencing composition. Mol Genet Genomics 286(1):21–36

    Article  CAS  PubMed  Google Scholar 

  • Umemoto N, Nakayasu M, Ohyama K, Yotsu-Yamashita M, Mizutani M, Seki H et al (2016) Two cytochrome P450 monooxygenases catalyze early hydroxylation steps in the potato steroid glycoalkaloid biosynthetic pathway. Plant Physiol 171(4):2458–2467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, Roberts PA (2006) A Fusarium wilt resistance gene in Gossypium barbadense and its effect on root-knot nematode-wilt disease complex. Phytopathology 96(7):727–734

    Article  CAS  PubMed  Google Scholar 

  • Wang HB, Wang PH, Qin JJ, Zhou HL (2018) Research profile of the extraction, purification and determination of flavonoids in plants. J JiLin Univ Chem Technol 35(7):44–47 ((in Chinese))

    CAS  Google Scholar 

  • Wang P, Su L, Qin L, Hu B, Guo W, Zhang T (2009) Identification and molecular mapping of a Fusarium wilt resistant gene in upland cotton. Theor Appl Genet 119(4):733–739

    Article  CAS  PubMed  Google Scholar 

  • Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100(4):681–697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woźniak A, Drzewiecka K, Kęsy J, Marczak Ł, Narożna D, Grobela M et al (2017) The influence of lead on generation of signalling molecules and accumulation of flavonoids in pea seedlings in response to pea aphid infestation. Molecules 22(9):1404

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu H, Park NI, Li X, Kim YK, Lee SY, Park SU (2010) Molecular cloning and characterization of phenylalanine ammonia-lyase, cinnamate 4-hydroxylase and genes involved in flavone biosynthesis in Scutellaria baicalensis. Biores Technol 101(24):9715–9722

    Article  CAS  Google Scholar 

  • Zhang J, Sanogo S, Ma Z, Qu Y (2015) Breeding, genetics, and quantitative trait locus mapping for Fusarium wilt resistance in cotton. Crop Sci 55(6):2435–2452

    Article  CAS  Google Scholar 

  • Zhang K (2019) Cloning and functional analysis of two genes related to verticillium wilt resistance in cotton. Dissertation, Chinese Academy of Agricultural Science (in chinese)

  • Zhang Y, Wang X, Rong W, Yang J, Li Z, Wu L et al (2017) Histochemical analyses reveal that stronger intrinsic defenses in Gossypium barbadense than in G. hirsutum are associated with resistance to Verticillium dahliae. Molecular Plant-Microbe Interactions 30(12):984–996

  • Zhang Y, Wang XF, Ding ZG, Ma Q, Zhang GR, Zhang SL et al (2013) Transcriptome profiling of Gossypium barbadense inoculated with Verticillium dahliae provides a resource for cotton improvement. BMC Genomics 14(1):1–18

    Article  Google Scholar 

  • Zhang YC, He RR, Lian JP, Zhou YF, Zhang F, Li QF et al (2020) OsmiR528 regulates rice-pollen intine formation by targeting an uclacyanin to influence flavonoid metabolism. Proc Natl Acad Sci 117(1):727–732

    Article  CAS  PubMed  Google Scholar 

  • Zu QL, Qu YY, Ni ZY, Zheng K, Chen Q, Chen QJ (2019) The chalcone isomerase family in cotton: whole-genome bioinformatic and expression analyses of the Gossypium barbadense L. response to Fusarium wilt infection. Genes 10(12):1006

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Acknowledgements

The author is especially grateful for the support of the Key Laboratory of Crop Genetic Improvement and Germplasm Innovation of Xinjiang Agricultural University. Thanks to AJE(American Journal Experts) for revising the the grammar of the paper language.

Funding

This work was supported by the Major Special Project of Xinjiang Uygur Autonomous Region (2020A01002–2), New Cultivar Breeding of Transgenic Herbicide Resistance in Cotton (2020ZX08005–005) and the University-level postgraduate Research Innovation Program of Xinjiang Agricultural University in 2021.

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Authors and Affiliations

  1. College of Agronomy, Xinjiang Agricultural University, 311 Nongda East Road Xinjiang, Urumqi, 830052, People’s Republic of China

    Qianli Zu, Yanying Qu, Xuening Su, Kai Zheng, Qin Chen, Xiaojuan Deng, Wenju Gao, Jieyin Zhao & Quanjia Chen

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  1. Qianli Zu
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  2. Yanying Qu
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  3. Xuening Su
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Contributions

Conceived and designed the experiments: Qianli Zu, Yanying Qu and Quanjia Chen. Performed the research: Qianli Zu. Analyzed the data: Qianli Zu. Contributed reagents/materials/analysis tools: Xuening Su, Kai Zheng, Qin Chen, Xiaojuan Deng, Wenju Gao and Jieyin Zhao. Wrote the paper: Qianli Zu. Revised the paper: Quanjia Chen. All authors read and reviewed the final manuscript.

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Correspondence to Quanjia Chen.

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Supplementary Information

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10725_2023_1000_MOESM1_ESM.tif

Supplementary file1 (TIF 40068 KB) Cloning and bioinformatic analysis of the GbC4H gene. A: Amplified product of GbC4H cDNA from 06-146; B: Predicted three-dimensional structure of the GbC4H gene; C: Genomic structure of the GbC4H gene

10725_2023_1000_MOESM2_ESM.tif

Supplementary file2 (TIF 33686 KB) Expression patterns of the GbC4H gene in 06-146 and Xinhai 14 under hormone (MeJA and SA) treatment. Statistical significance: “*” indicates P < 0.05, and “* *” indicates P < 0.01

10725_2023_1000_MOESM3_ESM.tif

Supplementary file3 (TIF 36379 KB) GbC4H gene silencing efficiency test and Fusarium wilt recovery assay. A: The GbC4H gene silencing efficiency test showed that GbC4H gene silencing was successful; B: Fusarium wilt recovery assay. The stems 3 mm above the cotyledon node of the control plants (pTRV2::00) and the GbC4H gene-silenced plants (pTRV2::GbC4H) after infection with Fusarium wilt were taken for the Fusarium wilt recovery assay

10725_2023_1000_MOESM4_ESM.tif

Supplementary file4 Establishment of a rutin standard curve for cotton. Establishment of a standard curve of rutin in cotton (linear regression equation, y = 0.1322x+0.0968; R² = 0.9925). (TIF 25648 KB)

Table S1 qRT‒PCR primers used in this study. (XLSX 15 KB)

Table S2 Specific amplification primers and vector-specific amplification primers used in this study. (XLSX 14 KB)

Table S3 Physical and chemical properties of GbC4H protein (XLSX 16 KB)

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Zu, Q., Qu, Y., Su, X. et al. GbC4H regulates the metabolic flow of flavonoids and inhibits the occurrence of Fusarium wilt in sea island cotton. Plant Growth Regul 101, 87–97 (2023). https://doi.org/10.1007/s10725-023-01000-5

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