GhKWL1 Upregulates GhERF105 but Its Function Is Impaired by Binding with VdISC1, a Pathogenic Effector of Verticillium dahliae
Abstract
:1. Introduction
2. Results
2.1. GhKWL1 Is Induced by V. dahliae and the Protein Is Located in the Nucleus
2.2. Downregulation of GhKWL1 Decreases, While Overexpression of GhKWL1 Increases, Resistance to V. dahliae Infection
2.3. GhKWL1 Upregulates Transcription of GhERFs
2.4. Suppression of GhERF105 Increases the Susceptibility of Cotton to V. dahliae Infection
2.5. VdISC1 Interacts with GhKWL1 and Inhibits Transcription of GhKWL1
3. Discussion
4. Materials and Methods
4.1. Vector Construction and Plant Materials
4.2. Sequence Retrieval, Phylogenetic Analysis, Subcellular Localization Prediction and Sequence Alignment
4.3. Transient Expression in Tobacco Epidermal Cells and BiFC Assay
4.4. Microscopy Observation
4.5. Quantitative RT-PCR Analysis
4.6. Virus-Induced Gene Silencing in Cotton and RNA-Seq Analysis
4.7. Inoculation Method and Disease Assays
4.8. Dual-Luciferase Reporter Assay
4.9. Co-Immunoprecipitation Assay
4.10. Yeast Autoactivation Assay
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Jamshed, M.; Jia, F.; Gong, J.; Palanga, K.K.; Shi, Y.; Li, J.; Shang, H.; Liu, A.; Chen, T.; Zhang, Z.; et al. Identification of stable quantitative trait loci (QTLs) for fiber quality traits across multiple environments in Gossypium hirsutum recombinant inbred line population. BMC Genom. 2016, 17, 1–13. [Google Scholar] [CrossRef] [Green Version]
- Fradin, E.F.; Thomma, B.P.H.J. Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol. Plant Pathol. 2006, 7, 71–86. [Google Scholar] [CrossRef] [PubMed]
- Cai, Y.; Xiaohong, H.; Mo, J.; Sun, Q.; Yang, J.; Liu, J. Molecular research and genetic engineering of resistance to Verticillium wilt in cotton: A review. Afr. J. Biotechnol. 2009, 8, 7363–7372. [Google Scholar] [CrossRef]
- Fang, H.; Zhou, H.; Sanogo, S.; Lipka, A.E.; Fang, D.D.; Percy, R.G.; Hughs, S.E.; Jones, D.C.; Gore, M.A.; Zhang, J. Quantitative trait locus analysis of Verticillium wilt resistance in an introgressed recombinant inbred population of Upland cotton. Mol. Breed. 2013, 33, 709–720. [Google Scholar] [CrossRef]
- Klosterman, S.J.; Atallah, Z.K.; Vallad, G.E.; Subbarao, K.V. Diversity, pathogenicity, and management of Verticillium Species. Annu. Rev. Phytopathol. 2009, 47, 39–62. [Google Scholar] [CrossRef] [Green Version]
- Klimes, A.; Dobinson, K.F.; Thomma, B.P.H.J.; Klosterman, S.J. Genomics spurs rapid advances in our understanding of the biology of vascular wilt pathogens in the genus Verticillium. Annu. Rev. Phytopathol. 2015, 53, 181–198. [Google Scholar] [CrossRef]
- Dangl, J.L.; Klosterman, S.J.; Subbarao, K.V.; Kang, S.; Veronese, P.; Gold, S.E.; Thomma, B.P.H.J.; Chen, Z.; Henrissat, B.; Lee, Y.-H.; et al. Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. PLoS Pathog. 2011, 7, e1002137. [Google Scholar] [CrossRef] [Green Version]
- Jones, J.D.G.; Dangl, J.L. The plant immune system. Nature 2006, 444, 323–329. [Google Scholar] [CrossRef] [Green Version]
- Berens, M.L.; Berry, H.M.; Mine, A.; Argueso, C.T.; Tsuda, K. Evolution of hormone signaling networks in plant defense. Annu. Rev. Phytopathol. 2017, 55, 401–425. [Google Scholar] [CrossRef]
- Shigenaga, A.M.; Argueso, C.T. No hormone to rule them all: Interactions of plant hormones during the responses of plants to pathogens. Semin. Cell Dev. Biol. 2016, 56, 174–189. [Google Scholar] [CrossRef]
- Liu, T.; Song, T.; Zhang, X.; Yuan, H.; Su, L.; Li, W.; Xu, J.; Liu, S.; Chen, L.; Chen, T.; et al. Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis. Nat. Commun. 2014, 5, 4686. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kumar, D. Salicylic acid signaling in disease resistance. Plant Sci. 2014, 228, 127–134. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.B.; Han, L.B.; Wang, H.Y.; Zhang, J.; Sun, S.T.; Feng, D.Q.; Yang, C.L.; Sun, Y.D.; Zhong, N.Q.; Xia, G.X. The thioredoxin GbNRX1 Plays a crucial role in homeostasis of apoplastic reactive oxygen species in response to Verticillium dahliae infection in cotton. Plant Physiol. 2016, 170, 2392–2406. [Google Scholar] [CrossRef] [Green Version]
- Hu, Q.; Min, L.; Yang, X.; Jin, S.; Zhang, L.; Li, Y.; Ma, Y.; Qi, X.; Li, D.; Liu, H.; et al. Laccase GhLac1 modulates broad-spectrum biotic stress tolerance via manipulating phenylpropanoid pathway and jasmonic acid synthesis. Plant Physiol. 2018, 176, 1808–1823. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yang, C.L.; Liang, S.; Wang, H.Y.; Han, L.B.; Wang, F.X.; Cheng, H.Q.; Wu, X.M.; Qu, Z.L.; Wu, J.H.; Xia, G.X. Cotton major latex protein 28 functions as a positive regulator of the ethylene responsive factor 6 in defense against Verticillium dahliae. Mol. Plant 2015, 8, 399–411. [Google Scholar] [CrossRef] [Green Version]
- Gu, Z.; Liu, T.; Ding, B.; Li, F.; Wang, Q.; Qian, S.; Ye, F.; Chen, T.; Yang, Y.; Wang, J.; et al. Two lysin-motif receptor kinases, Gh-LYK1 and Gh-LYK2, contribute to resistance against Verticillium wilt in upland cotton. Front. Plant Sci. 2017, 8, 2133. [Google Scholar] [CrossRef] [Green Version]
- Liu, J.; Wang, Y.; Zhao, G.; Zhao, J.; Du, H.; He, X.; Zhang, H. A novel Gossypium barbadense ERF transcription factor, GbERFb, regulation host response and resistance to Verticillium dahliae in tobacco. Physiol. Mol. Biol. Plants 2017, 23, 125–134. [Google Scholar] [CrossRef] [Green Version]
- Li, C.; He, X.; Luo, X.; Xu, L.; Liu, L.; Min, L.; Jin, L.; Zhu, L.; Zhang, X. 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, 166, 2179–2194. [Google Scholar] [CrossRef] [Green Version]
- He, X.; Zhu, L.; Wassan, G.M.; Wang, Y.; Miao, Y.; Shaban, M.; Hu, H.; Sun, H.; Zhang, X. GhJAZ2 attenuates cotton resistance to biotic stresses via the inhibition of the transcriptional activity of GhbHLH171. Mol. Plant Pathol. 2018, 19, 896–908. [Google Scholar] [CrossRef]
- Cheng, H.Q.; Han, L.B.; Yang, C.L.; Wu, X.M.; Zhong, N.Q.; Wu, J.H.; Wang, F.X.; Wang, H.Y.; Xia, G.X. The cotton MYB108 forms a positive feedback regulation loop with CML11 and participates in the defense response against Verticillium dahliae infection. J. Exp. Bot. 2016, 67, 1935–1950. [Google Scholar] [CrossRef] [Green Version]
- Song, R.; Li, J.; Xie, C.; Jian, W.; Yang, X. An overview of the molecular genetics of plant resistance to the Verticillium Wilt pathogen Verticillium dahliae. Int. J. Mol. Sci. 2020, 21, 1120. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, T.; Zhao, Y.L.; Zhao, J.H.; Wang, S.; Jin, Y.; Chen, Z.Q.; Fang, Y.Y.; Hua, C.L.; Ding, S.W.; Guo, H.S. Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen. Nat. Plants 2016, 2, 16153. [Google Scholar] [CrossRef]
- Huang, P.Y.; Catinot, J.; Zimmerli, L. Ethylene response factors in Arabidopsis immunity. J. Exp. Bot. 2016, 67, 1231–1241. [Google Scholar] [CrossRef] [Green Version]
- Zhu, X.; Qi, L.; Liu, X.; Cai, S.; Xu, H.; Huang, R.; Li, J.; Wei, X.; Zhang, Z. The wheat ethylene response factor transcription factor PATHOGEN-INDUCED ERF1 mediates host responses to both the necrotrophic pathogen Rhizoctonia cerealis and freezing stresses. Plant Physiol. 2014, 164, 1499–1514. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- He, P.; Warren, R.F.; Zhao, T.; Shan, L.; Zhu, L.; Tang, X.; Zhou, J.M. Overexpression of Pti5 in tomato potentiates pathogen-induced defense gene expression and enhances disease resistance to Pseudomonas syringae pv. tomato. Mol. Plant Microbe 2001, 14, 1453–1457. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Abiri, R.; Shaharuddin, N.A.; Maziah, M.; Yusof, Z.N.B.; Atabaki, N.; Sahebi, M.; Valdiani, A.; Kalhori, N.; Azizi, P.; Hanafi, M.M. Role of ethylene and the APETALA2/ethylene response factor superfamily in rice under various abiotic and biotic stress conditions. Environ. Exp. Bot. 2017, 134, 33–44. [Google Scholar] [CrossRef] [Green Version]
- Zhao, Y.; Chang, X.; Qi, D.; Dong, L.; Wang, G.; Fan, S.; Jiang, L.; Cheng, Q.; Chen, X.; Han, D.; et al. A novel soybean ERF transcription factor, GmERF113, increases resistance to Phytophthora sojae infection in soybean. Front. Plant Sci. 2017, 8, 299. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jin, J.H.; Zhang, H.X.; Ali, M.; Wei, A.M.; Luo, D.X.; Gong, Z.H. The CaAP2/ERF064 regulates dual functions in pepper: Plant cell death and resistance to Phytophthora capsici. Int. J. Mol. Sci. 2019, 10, 541. [Google Scholar] [CrossRef] [Green Version]
- Brown, R.L.; Kazan, K.; McGrath, K.C.; Maclean, D.J.; Manners, J.M. A role for the GCC-box in jasmonate-mediated activation of the PDF1.2 gene of Arabidopsis. Plant Physiol. 2003, 132, 1020–1032. [Google Scholar] [CrossRef] [Green Version]
- Meng, X.; Xu, J.; He, Y.; Yang, K.Y.; Mordorski, B.; Liu, Y.; Zhang, S. Phosphorylation of an ERF transcription factor by Arabidopsis MPK3/MPK6 regulates plant defense gene induction and fungal resistance. Plant Cell 2013, 25, 1126–1142. [Google Scholar] [CrossRef] [Green Version]
- Moffat, C.S.; Ingle, R.A.; Wathugala, D.L.; Saunders, N.J.; Knight, H.; Knight, M.R. ERF5 and ERF6 Play Redundant Roles as positive regulators of JA/Et-mediated defense against Botrytis cinerea in Arabidopsis. PLoS ONE 2012, 7, e35995. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Onate-Sanchez, L.; Anderson, J.P.; Young, J.; Singh, K.B. AtERF14, a member of the ERF family of transcription factors, plays a nonredundant role in plant defense. Plant Physiol. 2007, 143, 400–409. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pre, M.; Atallah, M.; Champion, A.; De Vos, M.; Pieterse, C.M.; Memelink, J. The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol. 2008, 147, 1347–1357. [Google Scholar] [CrossRef] [Green Version]
- Zarei, A.; Korbes, A.P.; Younessi, P.; Montiel, G.; Champion, A.; Memelink, J. Two GCC boxes and AP2/ERF-domain transcription factor ORA59 in jasmonate/ethylene-mediated activation of the PDF1.2 promoter in Arabidopsis. Plant Mol. Biol. 2011, 75, 321–331. [Google Scholar] [CrossRef] [Green Version]
- Guo, W.; Jin, L.; Miao, Y.; He, X.; Hu, Q.; Guo, K.; Zhu, L.; Zhang, X. An ethylene response-related factor, GbERF1-like, from Gossypium barbadense improves resistance to Verticillium dahliae via activating lignin synthesis. Plant Mol. Biol. 2016, 91, 305–318. [Google Scholar] [CrossRef]
- Meng, X.; Li, F.; Liu, C.; Zhang, C.; Wu, Z.; Chen, Y. Isolation and characterization of an ERF transcription factor gene from cotton (Gossypium barbadense L.). Plant Mol. Biol. Rep. 2009, 28, 176–183. [Google Scholar] [CrossRef]
- Liu, Y.; Liu, X.; Long, L.; Wang, W.; Sun, Q.; Li, B.; Wang, C.; Cheng, J.; Zhang, Y.; Xie, Y.; et al. GbABR1 is associated with Verticillium wilt resistance in cotton. Biologia 2018, 73, 449–457. [Google Scholar] [CrossRef]
- Tamburrini, M.; Cerasuolo, I.; Carratore, V.; Stanziola, A.A.; Zofra, S.; Romano, L.; Camardella, L.; Ciardiello, M.A. Kiwellin, a novel protein from kiwi fruit. Purification, biochemical characterization and identification as an allergen. Protein J. 2005, 24, 423–429. [Google Scholar] [CrossRef]
- Tuppo, L.; Giangrieco, I.; Palazzo, P.; Bernardi, M.L.; Scala, E.; Carratore, V.; Tamburrini, M.; Mari, A.; Ciardiello, M.A. Kiwellin, a modular protein from green and gold kiwi fruits evidence of in vivo and in vitro processing and IgE binding. J. Agr. Food Chem. 2008, 56, 3812–3817. [Google Scholar] [CrossRef]
- Maddumage, R.; Nieuwenhuizen, N.J.; Bulley, S.M.; Cooney, J.M.; Green, S.A.; Atkinson, R.G. Diversity and relative levels of actinidin, kiwellin, and thaumatin-like allergens in 15 varieties of kiwifruit (Actinidia). J. Agr. Food Chem. 2013, 61, 728–739. [Google Scholar] [CrossRef] [PubMed]
- Bernardi, M.L.; Picone, D.; Tuppo, L.; Giangrieco, I.; Petrella, G.; Palazzo, P.; Ferrara, R.; Tamburrini, M.; Mari, A.; Ciardiello, M.A. Physico-chemical features of the environment affect the protein conformation and the immunoglobulin E reactivity of kiwellin (Act d 5). Clin. Exp. Allergy 2010, 40, 1819–1826. [Google Scholar] [CrossRef]
- Antonietta Ciardiello, M.; Giangreco, I.; Tuppo, L.; Tamburrini, M.; Buccheri, M.; Palazzo, P.; Bernardi, M.L.; Ferrara, R.; Mari, A. Influence of the natural ripening stage, cold storage, and ethylene treatment on the protein and IgE-binding profiles of green and gold kiwi fruit extracts. J. Agr. Food Chem. 2009, 57, 1565. [Google Scholar] [CrossRef]
- Bublin, M.; Pfister, M.; Radauer, C.; Oberhuber, C.; Bulley, S.; Dewitt, A.M.; Lidholm, J.; Reese, G.; Vieths, S.; Breiteneder, H.; et al. Component-resolved diagnosis of kiwifruit allergy with purified natural and recombinant kiwifruit allergens. J. Allergy Clin. Immunol. 2010, 125, 687–694. [Google Scholar] [CrossRef]
- Yin, T.; Mosquera, T.; Alvarez, M.F.; Jiménez-Gómez, J.M.; Muktar, M.S.; Paulo, M.J.; Steinemann, S.; Li, J.; Draffehn, A.; Hofmann, A.; et al. Targeted and untargeted approaches unravel novel candidate genes and diagnostic SNPs for quantitative resistance of the potato (Solanum tuberosum L.) to Phytophthora infestans causing the late blight disease. PLoS ONE 2016, 11, e0156254. [Google Scholar] [CrossRef]
- Quintana-Camargo, M.; Méndez-Morán, L.; Ramirez-Romero, R.; Gurrola-Díaz, C.M.; Carapia-Ruiz, V.; Ibarra-Laclette, E.; Délano-Frier, J.P.; Sánchez-Hernández, C. Identification of genes differentially expressed in husk tomato (Physalis philadelphica) in response to whitefly (Trialeurodes vaporariorum) infestation. Acta Physiol. Plant 2015, 37, 29. [Google Scholar] [CrossRef]
- Ashfaq Ali, E.A.; Sandin, M.; Resjö, S.; Lenman, M.; Hedley, P.; Levander, F.; Andreasson, E. Quantitative proteomics and transcriptomics of potato in response to Phytophthora infestansin compatible and incompatible interactions. BMC Genom. 2014, 15, 497. [Google Scholar] [CrossRef] [Green Version]
- Lanver, D.; Müller, A.N.; Happel, P.; Schweizer, G.; Haas, F.B.; Franitza, M.; Pellegrin, C.; Reissmann, S.; Altmüller, J.; Rensing, S.A.; et al. The biotrophic development of Ustilago maydis studied by RNA-seq analysis. Plant Cell 2018, 30, 300–323. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Han, X.; Altegoer, F.; Steinchen, W.; Binnebesel, L.; Schuhmacher, J.; Glatter, T.; Giammarinaro, P.I.; Djamei, A.; Rensing, S.A.; Reissmann, S.; et al. A kiwellin disarms the metabolic activity of a secreted fungal virulence factor. Nature 2019, 565, 650–653. [Google Scholar] [CrossRef] [PubMed]
- Altegoer, F.; Weiland, P.; Giammarinaro, P.I.; Freibert, S.-A.; Binnebesel, L.; Han, X.; Lepak, A.; Kahmann, R.; Lechner, M.; Bange, G. The two paralogous kiwellin proteins KWL1 and KWL1-b from maize are structurally related and have overlapping functions in plant defense. J. Biol. Chem. 2020, 295, 7816–7825. [Google Scholar] [CrossRef]
- Liu, X.; Zhao, B.; Zheng, H.J.; Hu, Y.; Lu, G.; Yang, C.Q.; Chen, J.D.; Chen, J.J.; Chen, D.Y.; Zhang, L.; et al. Gossypium barbadense genome sequence provides insight into the evolution of extra-long staple fiber and specialized metabolites. Sci. Rep. 2015, 5, 14139. [Google Scholar] [CrossRef]
- Manners, J.M.; Penninckx, I.A.; Vermaere, K.; Kazan, K.; Brown, R.L.; Morgan, A.; Maclean, D.J.; Curtis, M.D.; Cammue, B.P.; Broekaert, W.F. The promoter of the plant defensin gene PDF1.2 from Arabidopsis is systemica. Plant Mol. Biol. 1998, 38, 1071–1080. [Google Scholar] [CrossRef]
- Shin, R. Ectopic expression of Tsi1 in transgenic hot pepper plants enhances host resistance to viral, bacterial, and oomycete pathogens. Mol. Plant-Microbe Interact. 2002, 15, 983–989. [Google Scholar] [CrossRef] [Green Version]
- Zeng, J.; Zhang, M.; Hou, L.; Bai, W.; Yan, X.; Hou, N.; Wang, H.; Huang, J.; Zhao, J.; Pei, Y. Cytokinin inhibits cotton fiber initiation by disrupting PIN3a-mediated asymmetric accumulation of auxin in the ovule epidermis. J. Exp. Bot. 2019, 70, 3139–3151. [Google Scholar] [CrossRef]
- Hellens, R.P.; Allan, A.C.; Friel, E.N.; Bolitho, K.; Grafton, K.; Templeton, M.D.; Karunairetnam, S.; Gleave, A.P.; Laing, W.A. Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 2005, 1, 13. [Google Scholar] [CrossRef] [Green Version]
- Duan, X.; Zhang, Z.; Wang, J.; Zuo, K. Characterization of a novel cotton subtilase gene GbSBT1 in response to extracellular stimulations and its role in Verticillium resistance. PLoS ONE 2016, 11, e0153988. [Google Scholar] [CrossRef] [Green Version]
- Clough, S.J.; Bent, A.F. Floral dip a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998, 16, 735–743. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhu, T.; Liang, C.; Meng, Z.; Sun, G.; Meng, Z.; Guo, S.; Zhang, R. CottonFGD: An integrated functional genomics database for cotton. BMC Plant Biol. 2017, 17, 101. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Burland, T.G. DNASTAR’s Lasergene sequence analysis software. In Bioinformatics Methods and Protocols; Humana Press: Totowa, NJ, USA, 2000. [Google Scholar]
- Nicholas, K.B.; Nicholas, B.H., Jr.; Deerfield, D.W., III. GeneDoc: Analysis and visualization of genetic variation. Embent News 1996, 4, 14. [Google Scholar] [CrossRef] [Green Version]
- Fradin, E.F.; Zhang, Z.; Juarez Ayala, J.C.; Castroverde, C.D.; Nazar, R.N.; Robb, J.; Liu, C.M.; Thomma, B.P. Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiol. 2009, 150, 320–332. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, J.Y.; Liu, C.; Gui, Y.J.; Si, K.W.; Zhang, D.D.; Wang, J.; Short, D.P.G.; Huang, J.Q.; Li, N.Y.; Liang, Y.; et al. Comparative genomics reveals cotton-specific virulence factors in flexible genomic regions in Verticillium dahliae and evidence of horizontal gene transfer from Fusarium. New Phytol. 2018, 217, 756–770. [Google Scholar] [CrossRef] [Green Version]
- Han, L.B.; Li, Y.B.; Wang, F.X.; Wang, W.Y.; Liu, J.; Wu, J.H.; Zhong, N.Q.; Wu, S.J.; Jiao, G.L.; Wang, H.Y.; et al. The cotton apoplastic protein CRR1 stabilizes chitinase 28 to facilitate defense against the fungal pathogen Verticillium dahliae. Plant Cell 2019, 31, 520–536. [Google Scholar] [CrossRef] [PubMed]
- Ellendorff, U.; Fradin, E.F.; de Jonge, R.; Thomma, B.P. RNA silencing is required for Arabidopsis defence against Verticillium wilt disease. J. Exp. Bot. 2009, 60, 591–602. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Song, Y.; Liu, L.; Wang, Y.; Valkenburg, D.J.; Zhang, X.; Zhu, L.; Thomma, B. Transfer of tomato immune receptor Ve1 confers Ave1-dependent Verticillium resistance in tobacco and cotton. Plant Biotechnol. J. 2018, 16, 638–648. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Chen, Y.; Zhang, M.; Wang, L.; Yu, X.; Li, X.; Jin, D.; Zeng, J.; Ren, H.; Wang, F.; Song, S.; et al. GhKWL1 Upregulates GhERF105 but Its Function Is Impaired by Binding with VdISC1, a Pathogenic Effector of Verticillium dahliae. Int. J. Mol. Sci. 2021, 22, 7328. https://doi.org/10.3390/ijms22147328
Chen Y, Zhang M, Wang L, Yu X, Li X, Jin D, Zeng J, Ren H, Wang F, Song S, et al. GhKWL1 Upregulates GhERF105 but Its Function Is Impaired by Binding with VdISC1, a Pathogenic Effector of Verticillium dahliae. International Journal of Molecular Sciences. 2021; 22(14):7328. https://doi.org/10.3390/ijms22147328
Chicago/Turabian StyleChen, Yang, Mi Zhang, Lei Wang, Xiaohan Yu, Xianbi Li, Dan Jin, Jianyan Zeng, Hui Ren, Fanlong Wang, Shuiqing Song, and et al. 2021. "GhKWL1 Upregulates GhERF105 but Its Function Is Impaired by Binding with VdISC1, a Pathogenic Effector of Verticillium dahliae" International Journal of Molecular Sciences 22, no. 14: 7328. https://doi.org/10.3390/ijms22147328