Abstract
Key message
R2R3 MYB transcription factor GhMYB18 is involved in the defense response to cotton aphid by participating in the synthesis of salicylic acid and flavonoids.
Abstract
R2R3 MYB transcription factors (TFs) play crucial roles in plant growth and development as well as response to abiotic and biotic stresses. However, the mechanism of R2R3 MYB TFs in cotton response to aphid infestation remains largely unknown. Here, an R2R3 MYB transcription factor GhMYB18 was identified as a gene up-regulated from upland cotton (Gossypium hirsutum L.) under cotton aphid (Aphis gossypii Glover) infestation. GhMYB18, which has transcription activity, was localized mainly to nucleus and cell membranes. Transient overexpression of GhMYB18 in cotton activates salicylic acid (SA) and phenylpropane signaling pathways and promoted the synthesis of salicylic acid and flavonoids, which leads to enhancing the tolerance to cotton aphid feeding. In contrast, silencing of GhMYB18 increased the susceptibility of G. hirsutum to aphid. Additionally, GhMYB18 significantly promoted the activities of defense-related enzymes including catalase (CAT), peroxidase (POD), polyphenol oxidase (PPO) and phenylalanine ammonia-lyase (PAL). These results collectively suggest that GhMYB18 is involved in cotton defense response to cotton aphid attacks through regulating the synthesis of salicylic acid and flavonoids.
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The data sets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Ambawat S, Sharma P, Yadav NR, Yadav RC (2013) MYB transcription factor genes as regulators for plant responses: an overview. Physiol Mol Biol Pla 19(3):307–321. https://doi.org/10.1007/s12298-013-0179-1
An C, Sheng L, Du X, Wang Y, Zhang Y, Song A, Jiang J, Guan Z, Fang W, Chen F, Chen S (2019) Overexpression of CmMYB15 provides chrysanthemum resistance to aphids by regulating the biosynthesis of lignin. Hortic Res 6:84. https://doi.org/10.1038/s41438-019-0166-y
Bari R, Jones JD (2009) Role of plant hormones in plant defense responses. Plant Mol Biol 69(4):473–488. https://doi.org/10.1007/s11103-008-9435-0
Bernal-Vicente A, Petri C, Hernández JA, Diaz-Vivancos P (2020) Biochemical study of the effect of stress conditions on the mandelonitrile-associated salicylic acid biosynthesis in peach. Plant Biol 22(2):277–286. https://doi.org/10.1111/plb.13066
Berrocal-Lobo M, Molina A (2004) Ethylene response factor 1 mediates Arabidopsis resistance to the soilborne fungus Fusarium oxysporum. Mol Plant Microbe Interact 17(7):763–770. https://doi.org/10.1094/MPMI.2004.17.7.763
Boudet AM (2007) Evolution and current status of research in phenolic compounds. Phytochemistry 68(22–24):2722–2735. https://doi.org/10.1016/j.phytochem.2007.06.012
Chen BS, Niu FF, Liu WZ, Yang B, Zhang JX, Ma JY, Cheng H, Han F, Jiang YQ (2016) Identification, cloning and characterization of R2R3-MYB gene family in canola (Brassica napus L.) identify a novel member modulating ROS accumulation and hypersensitive-like cell death. DNA Res 23(2):101–114. https://doi.org/10.1093/dnares/dsv040
Claudel P, Chesnais Q, Fouché Q, Krieger C, Halter D, Bogaert F, Meyer S, Boissinot S, Hugueney P, Ziegler-Graff V, Ameline A, Brault V (2018) The aphid-transmitted Turnip yellows virus differentially affects volatiles emission and subsequent vector behavior in two Brassicaceae plants. Int J Mol Sci 19(8):2316. https://doi.org/10.3390/ijms19082316
Dautréaux B, Toledano MB (2007) ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 8(10):813–824. https://doi.org/10.1038/nrm2256
De Vos M, Denekamp M, Dicke M, Vuylsteke M, Van Loon L, Smeekens SC, Pieterse CM (2006) The Arabidopsis thaliana transcription factor AtMYB102 functions in defense against the insect herbivore Pieris rapae. Plant Signal Behav 1(6):305–311. https://doi.org/10.4161/psb.1.6.3512
Demeke T, Morris C (2002) Molecular characterization of wheat polyphenol oxidase (PPO). Theor Appl Genet 104(5):813–818. https://doi.org/10.1007/s00122-001-0847-3
Dong NQ, Lin HX (2021) Contribution of phenylpropanoid metabolism to plant development and plant-environment interactions. J Integr Plant Biol 63(1):180–209. https://doi.org/10.1111/jipb.13054
Du L, Ge F, Zhu S, Parajulee MN (2004) Effect of cotton cultivar on development and reproduction of Aphis gossypii (Homoptera: Aphididae) and its predator Propylaea japonica (Coleoptera: Coccinellidae). J Econ Entomo 97(4):1278–1283. https://doi.org/10.1093/jee/97.4.1278
Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15(10):573–581. https://doi.org/10.1016/j.tplants.2010.06.005
Erb M, Reymond P (2019) Molecular interactions between plants and insect herbivores. Annu Rew Plant Biol 70(1):527–557. https://doi.org/10.1146/annurev-arplant-050718-095910
Fu J, Chu J, Sun X, Wang J, Yan C (2012) Simple, rapid, and simultaneous assay of multiple carboxyl containing phytohormones in wounded tomatoes by UPLC-MS/MS using single SPE purification and isotope dilution. Anal Sci 28(11):1081–1087. https://doi.org/10.2116/analsci.28.1081
Gao W, Long L, Zhu LF, Xu L, Gao WH, Sun LQ, Liu LL, Zhang XL (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. https://doi.org/10.1074/mcp.M113.031013
Goggin FL (2007) Plant–aphid interactions: molecular and ecological perspectives. Curr Opin Plant Biol 10(4):399–408. https://doi.org/10.1016/j.pbi.2007.06.004
Han Y, Wang Y, Bi JL, Yang XQ, Huang Y, Zhao X, Hu Y, Cai QN (2009) Constitutive and induced activities of defense-related enzymes in aphid-resistant and aphid-susceptible cultivars of wheat. J Chem Ecol 35(2):176–182. https://doi.org/10.1007/s10886-009-9589-5
He J, Liu Y, Yuan D, Duan M, Liu Y, Shen Z, Yang C, Qiu Z, Liu D, Wen P, Huang J, Fan D, Xiao S, Xin Y, Chen X, Jiang L, Wang H, Yuan L, Wan J (2020) An R2R3 MYB transcription factor confers brown planthopper resistance by regulating the phenylalanine ammonia-lyase pathway in rice. Proc Natl Acad Sci 117(1):271–277. https://doi.org/10.1073/pnas.1902771116
Herrera-Vásquez A, Salinas P, Holuigue L (2015) Salicylic acid and reactive oxygen species interplay in the transcriptional control of defense genes expression. Front Plant Sci 19(6):171. https://doi.org/10.3389/fpls.2015.00171
Hu Q, Min L, Yang X, Jin S, Zhang L, Li Y, Li YY, Ma YZ, Qi XW, Li DQ, Liu HB, Lindsey K, Zhu LF, Zhang XL (2018) Laccase GhLac1 modulates broad-spectrum biotic stress tolerance via manipulating phenylpropanoid pathway and jasmonic acid synthesis. Plant Physiol 176(2):1808–1823. https://doi.org/10.1104/pp.17.01628
Jia H, Zhao P, Wang B, Tariq P, Zhao F, Zhao M, Wang Q, Yang T, Fang J (2016) Overexpression of polyphenol oxidase gene in strawberry fruit delays the fungus infection process. Plant Mol Biol Rep 34(3):592–606. https://doi.org/10.1007/s11105-015-0946-y
Jiang CK, Rao GY (2020) Insights into the diversification and evolution of R2R3-MYB transcription factors in plants. Plant Physiol 183(2):637–655. https://doi.org/10.1104/pp.19.01082
Jiang C, Wang D, Zhang J, Xu Y, Zhang C, Zhang J, Wang X, Wang Y (2021) VqMYB154 promotes polygene expression and enhances resistance to pathogens in Chinese wild grapevine. Hortic Res 8(1):151. https://doi.org/10.1038/s41438-021-00585-0
Karban R, Baldwin IT (2007) Induced responses to herbivory. University of Chicago Press, Chicago
Kaur H, Heinzel N, Schöttner M, Baldwin IT, Gális I (2010) R2R3-NaMYB8 regulates the accumulation of phenylpropanoid-polyamine conjugates, which are essential for local and systemic defense against insect herbivores in Nicotiana attenuate. Plant Physiol 152(3):1731–1747. https://doi.org/10.1104/pp.109.151738
Kim JH, Jander G (2007) Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. Plant J 49(6):1008–1019. https://doi.org/10.1111/j.1365-313X.2006.03019.x
Koornneef A, Pieterse CM (2008) Cross talk in defense signaling. Plant Physiol 146(3):839–844. https://doi.org/10.1104/pp.107.112029
Li BZ, Fan RN, Guo SY, Wang PT, Zhu XH, Fan YT, Chen YX, He KY, Kumar A, Shi JP, Wang Y, Li LH, Hu ZB, Song CP (2019) The Arabidopsis MYB transcription factor, MYB111 modulates salt responses by regulating flavonoid biosynthesis. Environ Exp Bot 166(2):103807. https://doi.org/10.1016/j.envexpbot.2019.103807
Liu Y, Schiff M, Dinesh-Kumar SP (2002) Virus-induced gene silencing in tomato. Plant J 31(6):777–786. https://doi.org/10.1046/j.1365-313x.2002.01394.x
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Lloyd A, Brockman A, Aguirre L, Campbell A, Bean A, Cantero A, Gonzalez A (2017) Advances in the MYB–bHLH–WD repeat (MBW) pigment regulatory model: addition of a WRKY factor and co-option of an anthocyanin MYB for betalain regulation. Plant Cell Physiol 58(9):1431–1441. https://doi.org/10.1093/pcp/pcx075
Loguercio LL, Zhang JQ, Wilkins TA (1999) Differential regulation of six novel MYB-domain genes defines two distinct expression patterns in allotetraploid cotton (Gossypium hirsutum L.). Mol Gen Genet 261(4):660–671. https://doi.org/10.1007/s004380050009
Løvdal T, Olsen KM, Slimestad R, Verheul M, Lillo C (2010) Synergetic effects of nitrogen depletion, temperature, and light on the content of phenolic compounds and gene expression in leaves of tomato. Phytochemistry 71(5–6):605–613. https://doi.org/10.1016/j.phytochem.2009.12.014
Lu BB, Li XJ, Sun WW, Li L, Gao R, Zhu Q, Tian SM, Fu MQ, Yu HL, Tang XM, Zhang CL, Dong HS (2013) AtMYB44 regulates resistance to the green peach aphid and diamondback moth by activating EIN2-affected defenses in Arabidopsis. Plant Biol 15(5):841–850. https://doi.org/10.1111/j.1438-8677.2012.00675.x
Lu N, Roldan M, Dixon RA (2017) Characterization of two TT2-type MYB transcription factors regulating proanthocyanidin biosynthesis in tetraploid cotton, Gossypium Hirsutum. Planta 246(2):323–335. https://doi.org/10.1007/s00425-017-2682-z
Ma Y, Dai X, Xu Y, Luo W, Zheng X, Zeng D, Pan Y, Lin X, Liu H, Zhang D, Xiao J, Guo X, Xu S, Niu Y, Jin J, Zhang H, Xu X, Li L, Wang W, Qian Q, Ge S, Chong K (2015) COLD1 confers chilling tolerance in rice. Cell 160(6):1209–1221. https://doi.org/10.1016/j.cell.2015.01.046
Mohase L, Westhuizen AJ (2002) Salicylic acid is involved in resistance responses in the Russian wheat aphid-wheat interaction. J Plant Physiol 159(6):585–590. https://doi.org/10.1078/0176-1617-0633
Moran PJ, Thompson GA (2001) Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol 125(2):1074–1085. https://doi.org/10.1104/pp.125.2.1074
Nalam V, Louis J, Shah J (2019) Plant defense against aphids, the pest extraordinaire. Plant Sci 279:96–107. https://doi.org/10.1016/j.plantsci.2018.04.027
Nisbet AJ, Woodford JAT, Strang RHC (1994) Quantifying aphid feeding on non-radioactive food sources. Entomol Exp Appl 72:85–89
Qian Y, Lynch JH, Guo L, Rhodes D, Morgan JA, Dudareva N (2019) Completion of the cytosolic post-chorismate phenylalanine biosynthetic pathway in plants. Nat Commun 10(1):1–15. https://doi.org/10.1038/s41467-018-07969-2
Qu J, Ye J, Geng YF, Sun YW, Gao SQ, Zhang BP, Chen W, Chua NH (2012) Dissecting functions of KATANIN and WRINKLED1 in cotton fiber development by virus-induced gene silencing. Plant Physiol 160(2):738–748. https://doi.org/10.1104/pp.112.198564
Ren G, Wang X, Chen D, Wang XR, Liu X (2014) Effects of aphids Myzus persicae on the changes of Ca2+ and H2O2 flux and enzyme activities in tobacco. J Plant Interact 9(1):883–888. https://doi.org/10.1080/17429145.2014.982221
Rohde A, Morreel K, Ralph J, Goeminne G, Hostyn V, De Rycke R, Kushnir S, Van Doorsselaere J, Joseleau JP, Vuylsteke M, Van Driessche G, Van Beeumen J, Messens E, Boerjan W (2004) Molecular phenotyping of the pal1 and pal2 mutants of Arabidopsis thaliana reveals far-reaching consequences on phenylpropanoid, amino acid, and carbohydrate metabolism. Plant Cell 16(10):2749–2771. https://doi.org/10.1105/tpc.104.023705
Shen SJ, Wang YY, Zhang YX, Guo W, Jiao YQ, Zhou XA (2018) Overexpression of the wild soybean R2R3-MYB transcription factor GsMYB15 enhances resistance to salt stress and Helicoverpa Armigera in transgenic Arabidopsis. Int J Mol Sci 19(12):3958. https://doi.org/10.3390/ijms19123958
Singh KB, Foley RC, Oñate-Sánchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5(5):430–436. https://doi.org/10.1016/S1369-5266(02)00289-3
Solekha R, Susanto FA, Joko T, Nuringtyas TR, Purwestri YA (2020) Phenylalanine ammonia lyase (PAL) contributes to the resistance of black rice against Xanthomonas oryzae pv. oryzae. J Plant Pathol 102(2):359–365. https://doi.org/10.1007/s42161-019-00426-z
Stotz HU, Koch T, Biedermann A, Weniger K, Boland W, Mitchell-Olds T (2002) Evidence for regulation of resistance in Arabidopsis to Egyptian cotton worm by salicylic and jasmonic acid signaling pathways. Planta 214(4):648–652. https://doi.org/10.1007/s004250100656
Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4(5):447–456. https://doi.org/10.1016/S1369-5266(00)00199-0
Sultana B, Anwar F, Ashraf M (2009) Effect of extraction solvent/technique on the antioxidant activity of selected medicinal plant extracts. Molecules 14(6):2167–2180. https://doi.org/10.3390/molecules14062167
Sun X, Gong SY, Nie XY, Li Y, Li W, Huang GQ, Li XB (2015) A R2R3-MYB transcription factor that is specifically expressed in cotton (Gossypium hirsutum) fibers affects secondary cell wall biosynthesis and deposition in transgenic Arabidopsis. Physiol Plant 154(3):420–432. https://doi.org/10.1111/ppl.12317
Thipyapong P, Melkonian J, Wolfe DW, Steffens JC (2004) Suppression of polyphenol oxidases increases stress tolerance in tomato. Plant Sci 167(4):693–703. https://doi.org/10.1016/j.plantsci.2004.04.008
Tsuda K, Somssich IE (2015) Transcriptional networks in plant immunity. New Phytol 206(3):932–947. https://doi.org/10.1111/nph.13286
Wang XY, Zhou LH, Xu B, Xing X, Xu GQ (2014) Seasonal occurrence of Aphis glycines and physiological responses of soybean plants to its feeding. Insect Sci 21(3):342–351. https://doi.org/10.1111/1744-7917.12099
Wang Q, Eneji AE, Kong X, Wang K, Dong H (2015) Salt stress effects on secondary metabolites of cotton in relation to gene expression responsible for aphid development. PLoS One 10(6):e0129541. https://doi.org/10.1371/journal.pone.0129541
Wang Y, Sheng L, Zhang H, Du X, An C, Xia X, Chen F, Jiang J, Chen S (2017) CmMYB19 over-expression improves aphid tolerance in Chrysanthemum by promoting lignin synthesis. Int J Mol Sci 18(3):619. https://doi.org/10.3390/ijms18030619
Yang Z, Liu JJ, Luo L, Ye S, Yang YZ, Zhang GH, Wang XP, Zhang JM (2018) The cotton GhRac6 gene encoding a plant ROP/RAC protein improves the plant defense response to aphid feeding. Plant Mol Biol Rep 36(5):888–896. https://doi.org/10.1007/s11105-018-1127-6
Yue Y, Zhang M, Zhang J, Tian X, Duan L, Li Z (2012) Overexpression of the AtLOS5 gene increased abscisic acid level and drought tolerance in transgenic cotton. J Exp Bot 63(10):3741–3748. https://doi.org/10.1093/jxb/ers069
Zahedi A, Razmjou J, Rafiee-Dastjerdi H, Leppla NC, Golizadeh A, Hassanpour M, Ebadollahi A (2019) Tritrophic interactions of cucumber cultivar, Aphis gossypii (Hemiptera: Aphididae), and its predator Hippodamia variegata (Coleoptera: Coccinellidae). J Econ Entomol 112(4):1774–1779. https://doi.org/10.1093/jee/toz072
Zarate SI, Kempema LA, Walling LL (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143(2):866–875. https://doi.org/10.1104/pp.106.090035
Zhai R, Wang Z, Zhang S, Meng G, Song L, Wang Z, Li P, Ma F, Xu L (2016) Two MYB transcription factors regulate flavonoid biosynthesis in pear fruit (Pyrus bretschneideri Rehd.). J Exp Bot 67(5):1275–1284. https://doi.org/10.1093/jxb/erv524
Zhai Y, Li P, Mei Y, Chen M, Chen X, Xu H, Zhou X, Dong H, Zhang C, Jiang W (2017) Three MYB genes co-regulate the phloem-based defense against English grain aphid in wheat. J Exp Bot 68(15):4153–4169. https://doi.org/10.1093/jxb/erx204
Zhang Y, Li X (2019) Salicylic acid: biosynthesis, perception, and contributions to plant immunity. Curr Opin Plant Biol 50:29–36. https://doi.org/10.1016/j.pbi.2019.02.004
Zhang XY, He YQ, Li LY, Liu HR, Hong GJ (2021a) Involvement of the R2R3-MYB transcription factor MYB21 and its homologs in regulating flavonol accumulation in Arabidopsis stamen. J Exp Bot 72(12):4319–4332. https://doi.org/10.1093/jxb/erab156
Zhang S, Liu J, Xu B, Zhou J (2021b) Differential responses of Cucurbita pepo to Podosphaera xanthii reveal the mechanism of powdery mildew disease resistance in pumpkin. Front Plant Sci 12:633221. https://doi.org/10.3389/fpls.2021.633221
Zhong X, Feng P, Ma QQ, Zhang Y, Yang YZ, Zhang JM (2021) Cotton Chitinase gene GhChi6 improves the Arabidopsis defense response to aphid attack. Plant Mol Biol Rep 39(1):251–261. https://doi.org/10.1007/s11105-020-01248-5
Zhou YL, Lu L, Liu N, Cao H, Li H, Gui DP, Wang JH, Zhang CJ (2022) Analysis of MYB genes in four plant species and the detection of genes associated with drought resistance. Botany 99(99):1–14. https://doi.org/10.1139/cjb-2020-0227
Zhu L, Guo J, Ma Z, Wang J, Zhou C (2018) Arabidopsis transcription factor MYB102 increases plant susceptibility to aphids by substantial activation of ethylene biosynthesis. Biomolecules 8(2):39. https://doi.org/10.3390/biom8020039
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This work was supported by the National Natural Science Foundation of China (Grant No. 32172400)
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Funding Open Access funding enabled and organized by JM Zhang. This work was supported by the National Natural Science Foundation of China (Grant No. 32172400) and open Fund from Key Laboratory of Integrated Pests Management on Crops in Central China, Hubei Key Laboratory of Crop Diseases, Insect Pests and Weeds Control.
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JMZ, YZY, HLA, DX, XPW and PW: conceived and designed the research. ZWH, XZ and HRZ: performed the experiments; ZWH, XCL and YXW: analyzed the data and wrote the manuscript. YW, TL and YZ: provided helpful comments and discussions. All authors read and approved the final manuscript.
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299_2022_2961_MOESM4_ESM.tif
Supplementary file4 Fig. S1 Trans-activation assay of BD-nGhMYB18 and BD-cGhMYB18 in yeast. Yeast strains harboring BD control, BD-nGhMYB18 and BD-cGhMYB18 were grown on SD/-Trp (A), SD/-Trp with X-a-Gal (B) and SD/-Trp with AbA and X-a-Gal medium (C) and cultivated at 28 ℃ for 3 days (TIF 28786 KB)
Supplementary file5 Fig. S2 The aphid honeydew was collected with Whatman filter paper (TIF 1967 KB)
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Supplementary file6 Fig. S3 The content of free gossypol in GhMYB18 transiently expressed cotton (A) and GhMYB18-silenced cotton (B). Those bars indicate the standard errors, the alphabets represent the level of significant difference (p < 0.05) (TIF 27653 KB)
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Supplementary file7 Fig. S4 The expression level of genes related to lignin synthesis pathway in GhMYB18 transiently expressed cotton (A) and GhMYB18-silenced cotton (B). Those bars indicate the standard errors, the alphabets represent the level of significant difference (p < 0.05) (TIF 27894 KB)
299_2022_2961_MOESM8_ESM.tif
Supplementary file8 Fig. S5 Phenotypic analysis of GhMYB18 transiently expressed cotton (A, B) and GhMYB18-silenced (C, D) cotton (TIF 28906 KB)
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Hu, Z., Zhong, X., Zhang, H. et al. GhMYB18 confers Aphis gossypii Glover resistance through regulating the synthesis of salicylic acid and flavonoids in cotton plants. Plant Cell Rep 42, 355–369 (2023). https://doi.org/10.1007/s00299-022-02961-z
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DOI: https://doi.org/10.1007/s00299-022-02961-z