Abstract
The soil-borne pathogen Verticillium dahliae, also referred as “The Cotton Cancer,” is responsible for causing Verticillium wilt in cotton crops, a destructive disease with a global impact. To infect cotton plants, the pathogen employs multiple virulence mechanisms such as releasing enzymes that degrade cell walls, activating genes that contribute to virulence, and using protein effectors. Conversely, cotton plants have developed numerous defense mechanisms to combat the impact of V. dahliae. These include strengthening the cell wall by producing lignin and depositing callose, discharging reactive oxygen species, and amassing hormones related to defense. Despite the efforts to develop resistant cultivars, there is still no permanent solution to Verticillium wilt due to a limited understanding of the underlying molecular mechanisms that drive both resistance and pathogenesis is currently prevalent. To address this challenge, cutting-edge technologies such as clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated protein 9 (Cas9), host-induced gene silencing (HIGS), and gene delivery via nano-carriers could be employed as effective alternatives to control the disease. This article intends to present an overview of V. dahliae virulence mechanisms and discuss the different cotton defense mechanisms against Verticillium wilt, including morphophysiological and biochemical responses and signaling pathways including jasmonic acid (JA), salicylic acid (SA), ethylene (ET), and strigolactones (SLs). Additionally, the article highlights the significance of microRNAs (miRNAs), circular RNAs (circRNAs), and long non-coding RNAs (lncRNAs) in gene expression regulation, as well as the different methods employed to identify and functionally validate genes to achieve resistance against this disease. Gaining a more profound understanding of these mechanisms could potentially result in the creation of more efficient strategies for combating Verticillium wilt in cotton crops.
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References
Abdurakhmonov IY, Kohel RJ, Yu JZ, Pepper AE, Abdullaev AA, Kushanov FN, Salakhutdinov IB, Buriev ZT, Saha SUKUMAR, Scheffler BE, Jenkins JN (2008) Molecular diversity and association mapping of fiber quality traits in exotic G. hirsutum L. germplasm. Genomics 92(6):478–487
Ahmad S, GORDON‐WEEKS RUTH, Pickett J, Ton J (2010) Natural variation in priming of basal resistance: from evolutionary origin to agricultural exploitation. Molecular plant pathology 11(6):817–827
Akiyama K, Matsuzaki KI, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435(7043):824–827
Andersen EJ, Ali S, Byamukama E, Yen Y, Nepal MP (2018) Disease resistance mechanisms in plants. Genes 9(7):339
Apostol I, Low PS, Heinstein P, Stipanovic RD, Altman DW (1987) Inhibition of elicitor-induced phytoalexin formation in cotton and soybean cells by citrate. Plant Physiology 84(4):1276–1280
Back M, Haydock P, Jenkinson P (2002) Disease complexes involving plant parasitic nematodes and soilborne pathogens. Plant Pathology 51(6):683–697
Barbara D (2003) Verticillium Wilts-GF Pegg and BL Brady; CABI Publishing, CAB International, Wallingford, Oxon OX10 8DE, UK & 10 East 40th Street, Suite 3203, New York, NY 10016, USA, 552 pages. ISBN 0 85199 529 2. Physiological and Molecular Plant Pathology 1(62):51–52
Bardak A, Çelik S, Erdoğan O, Ekinci R, Dumlupinar Z (2021) Association mapping of Verticillium wilt disease in a worldwide collection of cotton (Gossypium hirsutum L.). Plants 10(2):306
Beliën T, Van Campenhout S, Robben J, Volckaert G (2006) Microbial endoxylanases: effective weapons to breach the plant cell-wall barrier or, rather, triggers of plant defense systems? Molecular Plant-Microbe Interactions 19(10):1072–1081
Berrocal-Lobo M, Molina A, Solano R (2002) Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. The Plant Journal 29(1):23–32
Betsuyaku S, Katou S, Takebayashi Y, Sakakibara H, Nomura N, Fukuda H (2018) Salicylic acid and jasmonic acid pathways are activated in spatially different domains around the infection site during effector-triggered immunity in Arabidopsis thaliana. Plant and Cell Physiology 59(1):8–16
Bhat R, Subbarao K (1999) Host range specificity in Verticillium dahliae. Phytopathology 89(12):1218–1225
Block A, Toruño TY, Elowsky CG, Zhang C, Steinbrenner J, Beynon J, Alfano JR (2014) The Pseudomonas syringae type III effector H op D 1 suppresses effector-triggered immunity, localizes to the endoplasmic reticulum, and targets the A rabidopsis transcription factor NTL 9. New phytologist 201(4):1358–1370
Boch J, Bonas U (2010) Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annual review of phytopathology 48:419–436
Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S, Lahaye T, Nickstadt A, Bonas U (2009) Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326(5959):1509–1512
Bocos-Asenjo IT, Niño-Sánchez J, Ginésy M, Diez JJ (2022) New insights on the integrated management of plant diseases by RNA strategies: Mycoviruses and RNA interference. International journal of molecular sciences 23(16):9236
Bok JW, Chiang YM, Szewczyk E, Reyes-Dominguez Y, Davidson AD, Sanchez JF, Lo HC, Watanabe K, Strauss J, Oakley BR, Wang CC (2009) Chromatin-level regulation of biosynthetic gene clusters. Nature chemical biology 5(7):462–464
Boller T, Felix G (2009) A renaissance of elicitors: perception of Microbe–associated molecular patterns and danger signals by pattern-recognition. Annual review of plant biology 60:379–406
Boller T, He SY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324(5928):742–744
Braatz J, Harloff HJ, Mascher M, Stein N, Himmelbach A, Jung C (2017) CRISPR-Cas9 targeted mutagenesis leads to simultaneous modification of different homoeologous gene copies in polyploid oilseed rape (Brassica napus). Plant Physiology 174(2):935–942. https://doi.org/10.1104/pp.17.00426
Brooks C, Nekrasov V, Lippman ZB, Van Eck J (2014) Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiology 166(3):1292–1297. https://doi.org/10.1104/pp.114.247577
Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G (2010) A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proceedings of the National Academy of Sciences 107(20):9452–9457
Bu B, Qiu D, Zeng H, Guo L, Yuan J, Yang X (2014) A fungal protein elicitor PevD1 induces Verticillium wilt resistance in cotton. Plant Cell Reports 33(3):461–470
Buchner V, Nachmias A, Burstein Y (1982) Isolation and partial characterization of a phytotoxic glycopeptide from a protein—lipopolysaccharide complex produced by a potato isolate of Verticillium dahliae. FEBS letters 138(2):261–264
Buchner V, Burstein Y, Nachmias A (1989) Comparison of Verticillium dahliae-produced phytotoxic peptides purified from culture fluids and infected potato stems. Physiological and Molecular Plant Pathology 35(3):253–269
Cai CP, Li C, Sun RR, Zhang BH, Nichols RL, Hake KD, Pan XP (2021) Small RNA and degradome deep sequencing reveals important roles of microRNAs in cotton (Gossypium hirsutum L.) response to root-knot nematode Meloidogyne incognita infection. Genomics 113(3):1146–1156 https://doi.org/10.1016/j.ygeno.2021.02.018
Cai Y, Cai X, Wang Q, Wang P, Zhang Y, Cai C, Xu Y, Wang K, Zhou Z, Wang C, Geng S (2020) Genome sequencing of the Australian wild diploid species Gossypium australe highlights disease resistance and delayed gland morphogenesis. Plant Biotechnology Journal 18(3):814–828
Cai Y, Chen L, Liu X, Guo C, Sun S, Wu C, Jiang B, Han T, Hou W (2018) CRISPR/Cas9-mediated targeted mutagenesis of GmFT2a delays flowering time in soya bean. Plant Biotechnology Journal 16(1):176–185. https://doi.org/10.1111/pbi.12758
Cai Y, Xiaohong H, Mo J, Sun Q, Yang J, Liu J (2009) Molecular research and genetic engineering of resistance to Verticillium wilt in cotton: a review. African journal of Biotechnology 8:25
Cao TY, Qin MH, Zhu S, Li YB (2022) Silencing of a cotton actin-binding protein GhWLIM1C decreases resistance against Verticillium dahliae infection. Plants-Basel 11(14):1828. https://doi.org/10.3390/plants11141828
Catinot J, Huang JB, Huang PY, Tseng MY, Chen YL, Gu SY, Lo WS, Wang LC, Chen YR, Zimmerli L (2015) Ethylene response factor 96 positively regulates A rabidopsis resistance to necrotrophic pathogens by direct binding to GCC elements of jasmonate–and ethylene-responsive defence genes. Plant, cell & environment 38(12):2721–2734
Chen P, Lee B, Robb J (2004) Tolerance to a non-host isolate of Verticillium dahliae in tomato. Physiological and Molecular Plant Pathology 64(6):283–291
Chen X, Lu X, Shu N, Wang S, Wang J, Wang D, Guo L, Ye W (2017) Targeted mutagenesis in cotton (Gossypium hirsutum L.) using the CRISPR/Cas9 system. Scientific reports 7:1–7. https://doi.org/10.1038/srep44304
Chen Y, Zhang M, Wang L, Yu X, Li X, Jin D, Zeng J, Ren H, Wang F, Song S, Yan X (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(14):7328. https://doi.org/10.3390/ijms22147328
Cheng HQ, Han LB, Yang CL, Wu XM, Zhong NQ, Wu JH, Wang FX, Wang HY, Xia GX (2016) The cotton MYB108 forms a positive feedback regulation loop with CML11 and participates in the defense response against Verticillium dahliae infection. Journal of experimental botany 67(6):1935–1950
Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F, Hummel A, Bogdanove AJ, Voytas DF (2010) Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186(2):757–761
Coego A, Ramirez V, Gil MJ, Flors V, Mauch-Mani B, Vera P (2005) An Arabidopsis homeodomain transcription factor, overexpressor of cationic peroxidase3, mediates resistance to infection by necrotrophic pathogens. The Plant Cell 17(7):2123–2137
Correll J, Gordon T, McCain A (1988) Vegetative compatibility and pathogenicity of Verticillium albo-atrum. Phytopathology 78(8):1017–1021
Cui H, Tsuda K, Parker JE (2015) Effector-triggered immunity: from pathogen perception to robust defense. Annual review of plant biology 66(487):10.1146
Daayf F (2015) Verticillium wilts in crop plants: pathogen invasion and host defence responses. Canadian journal of plant pathology 37(1):8–20
Dadd-Daigle P, Kirkby K, Chowdhury PR, Labbate M, Chapman TA (2021) The Verticillium wilt problem in Australian cotton. Australasian Plant Pathology 50:129–135
De Jonge R, Peter van Esse H, Maruthachalam K, Bolton MD, Santhanam P, Saber MK, Zhang Z, Usami T, Lievens B, Subbarao KV, Thomma BP (2012) Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proceedings of the National Academy of Sciences 109(13):5110–5115
del Pozo O, Pedley KF, Martin GB (2004) MAPKKKα is a positive regulator of cell death associated with both plant immunity and disease. The EMBO journal 23(15):3072–3082
Deng S, Wang CY, Zhang X, Wang Q, Lin L (2015) VdNUC-2, the key regulator of phosphate responsive signaling pathway, is required for Verticillium dahliae infection. PloS one 10:e0145190
Deng C, Wang Y, Huang F, Lu S, Zhao L, Ma X, Kai G (2020) SmMYB2 promotes salvianolic acid biosynthesis in the medicinal herb Salvia miltiorrhiza. Journal of integrative plant biology 62(11):1688–1702
Deng YH, Chen QJ, Qu YY (2022) Protein S-acyl transferase GhPAT27 was associated with Verticillium wilt resistance in cotton. Plants-Basel 11(20):2758. https://doi.org/10.3390/plants11202758
Deniz E, Erman B (2017) Long noncoding RNA (lincRNA), a new paradigm in gene expression control. Functional & integrative genomics 17:135–143
Dodds PN, Lawrence GJ, Catanzariti A-M, Ayliffe MA, Ellis JG (2004) The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. The Plant Cell 16(3):755–768
Doehlemann G, Van Der Linde K, Aßmann D, Schwammbach D, Hof A, Mohanty A, Jackson D, Kahmann R (2009) Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS pathogens 5(2):e1000290
Dong X (2004) NPR1, all things considered. Current Opinion in Plant Biology 7(5):547–552
Duan X, Zhang Z, Wang J, Zuo K (2016) Characterization of a novel cotton subtilase gene GbSBT1 in response to extracellular stimulations and its role in Verticillium resistance. PloS one 11(4):e0153988
Dubery IA, Slater V (1997) Induced defence responses in cotton leaf disks by elicitors from Verticillium dahliae. Phytochemistry 44(8):1429–1434
Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends in plant science 15(10):573–581
Faulkner C, Robatzek S (2012) Plants and pathogens: putting infection strategies and defence mechanisms on the map. Current Opinion in Plant Biology 15(6):699–707
Feng Z, Zhang B, Ding W, Liu X, Yang DL, Wei P, Cao F, Zhu S, Zhang F, Mao Y, Zhu JK (2013) Efficient genome editing in plants using a CRISPR/Cas system. Cell Research 23(10):1229–1232. https://doi.org/10.1038/cr.2013.114
Feng Z, Mao Y, Xu N, Zhang B, Wei P, Yang DL, Wang Z, Zhang Z, Zheng R, Yang L, Zeng L (2014) Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 111(12):4632–4637. https://doi.org/10.1073/pnas.1400822111
Feng H, Li C, Zhou J, Yuan Y, Feng Z, Shi Y, Zhao L, Zhang Y, Wei F, Zhu H (2021) A cotton WAKL protein interacted with a DnaJ protein and was involved in defense against Verticillium dahliae. International Journal of Biological Macromolecules 167:633–643. https://doi.org/10.1016/j.ijbiomac.2020.11.191
Ferrari S, Plotnikova JM, De Lorenzo G, Ausubel FM (2003) Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. The Plant Journal 35(2):193–205
Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. The Plant Cell 17(7):1866–1875
Fradin EF, Thomma BP (2006) Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Molecular plant pathology 7(2):71–86
Fradin EF, Abd-El-Haliem A, Masini L, van den Berg GC, Joosten MH, Thomma BP (2011) Interfamily transfer of tomato Ve1 mediates Verticillium resistance in Arabidopsis. Plant Physiology 156(4):2255–2265
Frye CA, Tang D, Innes RW (2001) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proceedings of the National Academy of Sciences 98(1):373–378
Galletti R, Ferrari S, De Lorenzo G (2011) Arabidopsis MPK3 and MPK6 play different roles in basal and oligogalacturonide-or flagellin-induced resistance against Botrytis cinerea. Plant Physiology 157(2):804–814
Gao F, Zhou BJ, Li GY, Jia PS, Li H, Zhao YL, Zhao P, Xia GX, Guo HS (2010) A glutamic acid-rich protein identified in Verticillium dahliae from an insertional mutagenesis affects microsclerotial formation and pathogenicity. PloS one 5:e15319
Gao X, Wheeler T, Li Z, Kenerley CM, He P, Shan L (2011) Silencing GhNDR1 and GhMKK2 compromises cotton resistance to Verticillium wilt. The Plant Journal 66(2):293–305
Gao W, Long L, Zhu LF, Xu L, Gao WH, Sun LQ, Liu LL, Zhang XL (2013a) Proteomic and virus-induced gene silencing (VIGS) analyses reveal that gossypol, brassinosteroids, and jasmonic acid contribute to the resistance of cotton to Verticillium dahliae. Molecular & Cellular Proteomics 12(12):3690–3703
Gao X, Li F, Li M, Kianinejad AS, Dever JK, Wheeler TA, Li Z, He P, Shan L (2013b) Cotton GhBAK1 mediates Verticillium wilt resistance and cell death. Journal of integrative plant biology 55(7):586–596
Gao W, Long L, Xu L, Lindsey K, Zhang X, Zhu L (2016) Suppression of the homeobox gene HDTF1 enhances resistance to Verticillium dahliae and Botrytis cinerea in cotton. Journal of integrative plant biology 58(5):503–513
Gao F, Zhang BS, Zhao JH, Huang JF, Jia PS, Wang S, Zhang J, Zhou JM, Guo HS (2019) Deacetylation of chitin oligomers increases virulence in soil-borne fungal pathogens. Nature Plants 5(11):1167–1176
Gaspar YM, McKenna JA, McGinness BS, Hinch J, Poon S, Connelly AA, Anderson MA, Heath RL (2014) Field resistance to Fusarium oxysporum and Verticillium dahliae in transgenic cotton expressing the plant defensin NaD1. Journal of experimental botany 65(6):1541–1550
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48(12):909–930
Gimenez-Ibanez S, Boter M, Fernández-Barbero G, Chini A, Rathjen JP, Solano R (2014) The bacterial effector HopX1 targets JAZ transcriptional repressors to activate jasmonate signaling and promote infection in Arabidopsis. PLoS biology 12(2):e1001792
Göhre V, Robatzek S (2008) Breaking the barriers: microbial effector molecules subvert plant immunity. Annual review of phytopathology 46:189–215
Gold J, Robb J (1995) The role of the coating response in Craigella tomatoes infected with Verticillium dahliae, races 1 and 2. Physiological and Molecular Plant Pathology 47(3):141–157
Gong Q, Yang Z, Wang X, Butt HI, Chen E, He S, Zhang C, Zhang X, Li F (2017) Salicylic acid-related cotton (Gossypium arboreum) ribosomal protein GaRPL18 contributes to resistance to Verticillium dahliae. BMC plant biology 17(1):1–15
Grayston S, Vaughan D, Jones D (1997) Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. Applied soil ecology 5(1):29–56
Gu Z, Liu T, Ding B, Li F, Wang Q, Qian S, Ye F, Chen T, Yang Y, Wang J, Wang G (2017) Two lysin-motif receptor kinases, Gh-LYK1 and Gh-LYK2, contribute to resistance against Verticillium wilt in upland cotton. Frontiers in Plant Science 8:2133. https://doi.org/10.3389/fpls.2017.02133
Guo W, Jin L, Miao Y, He X, Hu Q, Guo K, Zhu L, Zhang X (2016) An ethylene response-related factor, GbERF1-like, from Gossypium barbadense improves resistance to Verticillium dahliae via activating lignin synthesis. Plant molecular biology 91(3):305–318
Guo J, Cao PH, Yuan LT, Xia GX, Zhang HY, Li J, Wang FX (2022) Revealing the contribution of GbPR10.5D1 to resistance against Verticillium dahliae and its regulation for structural defense and immune signaling. Plant Genome 1:e20271. https://doi.org/10.1002/tpg2.20271
Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286(5441):950–952. https://doi.org/10.1126/science.286.5441.950
He Q, Zhu S, Zhang B (2014a) MicroRNA–target gene responses to lead-induced stress in cotton (Gossypium hirsutum L.). Functional & integrative genomics 14:507–515
He X, Sun Q, Jiang H, Zhu X, Mo J, Long L, Xiang L, Xie Y, Shi Y, Yuan Y, Cai Y (2014b) Identification of novel microRNAs in the Verticillium wilt-resistant upland cotton variety KV-1 by high-throughput sequencing. Springerplus 3:564
He X, Zhu L, Xu L, Guo W, Zhang X (2016) GhATAF1, a NAC transcription factor, confers abiotic and biotic stress responses by regulating phytohormonal signaling networks. Plant Cell Reports 35(10):2167–2179
He X, Wang TY, Zhu W, Wang YJ, Zhu LF (2018a) GhHB12, a HD-ZIP I transcription factor, negatively regulates the cotton resistance to Verticillium dahliae. International Journal of Molecular Sciences 19(12):3997. https://doi.org/10.3390/ijms19123997
He X, Zhu L, Wassan GM, Wang Y, Miao Y, Shaban M, Hu H, Sun H, Zhang X (2018b) GhJAZ2 attenuates cotton resistance to biotic stresses via the inhibition of the transcriptional activity of GhbHLH171. Molecular plant pathology 19(4):896–908
Hoffman T, Schmidt JS, Zheng X, Bent AF (1999) Isolation of ethylene-insensitive soybean mutants that are altered in pathogen susceptibility and gene-for-gene disease resistance. Plant Physiology 119(3):935–950
Horner C (1954) Pathogenicity of Verticillium isolates to peppermint. Phytopathology 44:239–242
Hu Q, Zhu L, Zhang X, Guan Q, Xiao S, Min L, Zhang X (2019) GhCPK33 negatively regulates defense against Verticillium dahliae by phosphorylating GhOPR3 (vol 178, pg 876, 2018). Plant Physiology 180(2):1241–1241. https://doi.org/10.1104/pp.19.00423
Hu G, Hao M, Wang L, Liu J, Zhang Z, Tang Y, Peng Q, Yang Z, Wu J (2020) The cotton miR477-CBP60A module participates in plant defense against Verticillium dahlia. Molecular Plant-Microbe Interactions 33(4):624–636. https://doi.org/10.1094/Mpmi-10-19-0302-R
Hu Q, Xiao SH, Wang XR, Ao CW, Zhang XL, Zhu LF (2021) GhWRKY1-like enhances cotton resistance to Verticillium dahliae via an increase in defense-induced lignification and S monolignol content. Plant Science 305:110833. https://doi.org/10.1016/j.plantsci.2021.110833
Huang W, Zhang Y, Zhou J, Wei F, Feng Z, Zhao L, Shi Y, Feng H, Zhu H (2021) The respiratory burst oxidase homolog protein D (GhRbohD) positively regulates the cotton resistance to Verticillium dahliae. International Journal of Molecular Sciences 22(23):13041. https://doi.org/10.3390/ijms222313041
Huang L, Li G, Wang Q, Meng Q, Xu F, Chen Q, Liu F, Hu Y, Luo M (2022) GhCYP710A1 participates in cotton resistance to Verticillium wilt by regulating stigmasterol synthesis and plasma membrane stability. International Journal of Molecular Sciences 23(15):8437. https://doi.org/10.3390/ijms23158437
Ingle RA, Carstens M, Denby KJ (2006) PAMP recognition and the plant–pathogen arms race. Bioessays 28(9):880–889
Isaac I, Keyworth W (1948) Verticillium wilt of the hop (Humulus lupulus) a study of the pathogenicity of isolates from fluctuating and from progressive outbreaks. Annals of Applied Biology 35(2):243–249
Jalali B, Bhargava S, Kamble A (2006) Signal transduction and transcriptional regulation of plant defence responses. Journal of Phytopathology 154(2):65–74
Janga MR, Campbell LM, Rathore KS (2017) CRISPR/Cas9-mediated targeted mutagenesis in upland cotton (Gossypium hirsutum L.). Plant molecular biology 94(4-5):349–360. https://doi.org/10.1007/s11103-017-0599-3
Jia MZ, Li ZF, Han S, Wang S, Jiang J (2022a) Effect of 1-aminocyclopropane-1-carboxylic acid accumulation on Verticillium dahliae infection of upland cotton. Bmc Plant Biology 22(1):386. https://doi.org/10.1186/s12870-022-03774-8
Jia P, Tang Y, Hu G, Quan Y, Chen A, Zhong N, Peng Q, Wu J (2022b) Cotton miR319b-targeted TCP4-like enhances plant defense against Verticillium dahliae by activating GhICS1 transcription expression. Frontiers in Plant Science 13:870882. https://doi.org/10.3389/fpls.2022.870882
Jian G, Lu M, Xiu J, Wang F, Zhang H (2004) Control strategy of Verticillium dahliae in cotton. China Plant Protection 24(4):30–31
Jiang WZ, Zhou HB, Bi HH, Fromm M, Yang B, Weeks DP (2013) Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic acids research 41(20):e188. https://doi.org/10.1093/nar/gkt780
Jin H, Cominelli E, Bailey P, Parr A, Mehrtens F, Jones J, Tonelli C, Weisshaar B, Martin C (2000) Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. The EMBO journal 19(22):6150–6161
Johansson A, Staal J, Dixelius C (2006) Early responses in the Arabidopsis-Verticillium longisporum pathosystem are dependent on NDR1, JA-and ET-associated signals via cytosolic NPR1 and RFO1. Molecular Plant-Microbe Interactions 19(9):958–969
Jones JD, Dangl JL (2006a) The plant immune system. Nature 444(7117):323–329
Jones JDG, Dangl JL (2006b) The plant immune system. Nature 444(7117):323–329. https://doi.org/10.1038/nature05286
Kalwan G, Gill SS, Priyadarshini P, Gill R, Yadava YK, Yadav S, Baruah PM, Agarwala N, Gaikwad K, Jain PK (2022) Approaches for identification and analysis of plant circular RNAs and their role in stress responses. Environmental and experimental botany 205:105099
Kanyuka K, Rudd JJ (2019) Cell surface immune receptors: the guardians of the plant’s extracellular spaces. Current Opinion in Plant Biology 50:1–8
Katiyar A, Smita S, Lenka SK, Rajwanshi R, Chinnusamy V, Bansal KC (2012) Genome-wide classification and expression analysis of MYB transcription factor families in rice and Arabidopsis. BMC genomics 13(1):1–19
Katsantonis D, Hillocks RJ, Gowen S (2005) Enhancement of germination of spores of Verticillium dahliae and Fusarium oxysporum f. sp. vasinfectum in vascular fluid from cotton plants infected with the root-knot nematode. Phytoparasitica 33(3):215–224
Kawchuk LM, Hachey J, Lynch DR, Kulcsar F, Van Rooijen G, Waterer DR, Robertson A, Kokko E, Byers R, Howard RJ, Fischer R (2001) Tomato Ve disease resistance genes encode cell surface-like receptors. Proceedings of the National Academy of Sciences 98(11):6511–6515
Keller NP (2019) Fungal secondary metabolism: regulation, function and drug discovery. Nature Reviews Microbiology 17(3):167–180
Klosterman SJ, Atallah ZK, Vallad GE, Subbarao KV (2009) Diversity, pathogenicity, and management of Verticillium species. Annual review of phytopathology 47:39–62
Klosterman SJ, Subbarao KV, Kang S, Veronese P, Gold SE, Thomma BP, Chen Z, Henrissat B, Lee YH, Park J, Garcia-Pedrajas MD (2011) Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. PLoS pathogens 7(7):e1002137
Knoester M, Van Loon LC, Van Den Heuvel J, Hennig J, Bol JF, Linthorst HJ (1998) Ethylene-insensitive tobacco lacks nonhost resistance against soil-borne fungi. Proceedings of the National Academy of Sciences 95(4):1933–1937
Kohorn BD, Kohorn SL, Todorova T, Baptiste G, Stansky K, McCullough M (2012) A dominant allele of Arabidopsis pectin-binding wall-associated kinase induces a stress response suppressed by MPK6 but not MPK3 mutations. Molecular plant 5(4):841–851
Koornneef A, Pieterse CM (2008) Cross talk in defense signaling. Plant Physiology 146(3):839–844
Kouzai Y, Kimura M, Watanabe M, Kusunoki K, Osaka D, Suzuki T, Matsui H, Yamamoto M, Ichinose Y, Toyoda K, Matsuura T (2018) Salicylic acid-dependent immunity contributes to resistance against Rhizoctonia solani, a necrotrophic fungal agent of sheath blight, in rice and Brachypodium distachyon. New phytologist 217(2):771–783
Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Current Opinion in Plant Biology 5(4):325–331
Lee S-W, Nazar RN, Powell DA, Robb J (1992) Reduced PAL gene suppression in Verticillium-infected resistant tomatoes. Plant molecular biology 18(2):345–352
Li C, Brant E, Budak H, Zhang BH (2021) CRISPR/Cas: a Nobel Prize award-winning precise genome editing technology for gene therapy and crop improvement. Journal of Zhejiang University-SCIENCE B 22(4):253–284 https://doi.org/10.1631/jzus.B2100009
Li C, Chu W, AliGill R, Sang SF, Shi YQ, Hu XZ, Yang YT, Zaman QU, Zhang BH (2023) Computational tools and resources for CRISPR/Cas genome editing. Genomics Proteomics & Bioinformatics https://doi.org/10.1016/j.gpb.2022.02.006
Li C, Unver T, Zhang BH (2017) A high-efficiency CRISPR/Cas9 system for targeted mutagenesis in Cotton (Gossypium hirsutum L.). Scientific Reports 7(1) https://doi.org/10.1038/srep43902
Li C, Zhang B (2016) MicroRNAs in control of plant development. Journal of cellular physiology 231(2):303–313
Li J, Brader G, Palva ET (2004) The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. The Plant Cell 16(2):319–331
Li SF, Parish RW (1995) Isolation of two novel myb-like genes from Arabidopsis and studies on the DNA-binding properties of their products. The Plant Journal 8(6):963–972
Li YB, Han LB, Wang HY, Zhang J, Sun ST, Feng DQ, Yang CL, Sun YD, Zhong NQ, Xia GX (2016) The thioredoxin GbNRX1 plays a crucial role in homeostasis of apoplastic reactive oxygen species in response to Verticillium dahliae infection in cotton. Plant Physiology 170(4):2392–2406
Li Q-F, Zhang Y-C, Chen Y-Q, Yu Y (2017a) Circular RNAs roll into the regulatory network of plants. Biochemical and biophysical research communications 488(2):382–386
Li X-L, Ojaghian MR, Zhang J-Z, Zhu S-J (2017b) A new species of Scopulariopsis and its synergistic effect on pathogenicity of Verticillium dahliae on cotton plants. Microbiological research 201:12–20
Li NY, Ma XF, Short DP, Li TG, Zhou L, Gui YJ, Kong ZQ, Zhang DD, Zhang WQ, Li JJ, Subbarao KV (2018a) The island cotton NBS-LRR gene GbaNA1 confers resistance to the non-race 1 Verticillium dahliae isolate Vd991. Molecular plant pathology 19(6):1466–1479
Li NY, Zhou L, Zhang DD, Klosterman SJ, Li TG, Gui YJ, Kong ZQ, Ma XF, Short DP, Zhang WQ, Li JJ (2018b) Heterologous expression of the cotton NBS-LRR gene GbaNA1 enhances Verticillium wilt resistance in Arabidopsis. Frontiers in Plant Science 9:119. https://doi.org/10.3389/fpls.2018.00119
Li R, Li R, Li X, Fu D, Zhu B, Tian H, Luo Y, Zhu H (2018c) Multiplexed CRISPR/Cas9-mediated metabolic engineering of gamma-aminobutyric acid levels in Solanum lycopersicum. Plant Biotechnology Journal 16(2):415–427. https://doi.org/10.1111/pbi.12781
Li X, Pei Y, Sun Y, Liu N, Wang P, Liu D, Ge X, Li F, Hou Y (2018d) A cotton cyclin-dependent kinase E confers resistance to Verticillium dahliae mediated by jasmonate-responsive pathway. Frontiers in Plant Science 9:642. https://doi.org/10.3389/fpls.2018.00642
Li N, Han X, Feng D, Yuan D, Huang L-J (2019a) Signaling crosstalk between salicylic acid and ethylene/jasmonate in plant defense: do we understand what they are whispering? International journal of molecular sciences 20(3):671
Li X, Liu N, Sun Y, Wang P, Ge X, Pei Y, Liu D, Ma X, Li F, Hou Y (2019b) The cotton GhWIN2 gene activates the cuticle biosynthesis pathway and influences the salicylic and jasmonic acid biosynthesis pathways. Bmc Plant Biology 19(1):379. https://doi.org/10.1186/s12870-019-1888-6
Li X, Sun Y, Liu N, Wang P, Pei Y, Liu D, Ma X, Ge X, Li F, Hou Y (2019c) Enhanced resistance to Verticillium dahliae mediated by an F-box protein GhACIF1 from Gossypium hirsutum. Plant Science 284:127–134. https://doi.org/10.1016/j.plantsci.2019.04.013
Li ZS, Wang XY, Cui YP, Qiao KK, Zhu LF, Fan SL, Ma QF (2020) Comprehensive genome-wide analysis of thaumatin-like gene family in four cotton species and functional identification of GhTLP19 involved in regulating tolerance to Verticillium dahlia and drought. Frontiers in Plant Science 11:575015. https://doi.org/10.3389/fpls.2020.575015
Li TG, Zhang QQ, Jiang XL, Li R, Dhar N (2021) Cotton CC-NBS-LRR gene GbCNL130 confers resistance to Verticillium wilt across different species. Frontiers in Plant Science 12:695691. https://doi.org/10.3389/fpls.2021.695691
Li H, Zhang S, Zhao Y, Zhao X, Xie W, Guo Y, Wang Y, Li K, Guo J, Zhu QH, Zhang X (2022) Identification and characterization of cinnamyl alcohol dehydrogenase encoding genes involved in lignin biosynthesis and resistance to Verticillium dahliae in upland cotton (Gossypium hirsutum L.). Frontiers in Plant Science 13:840397. https://doi.org/10.3389/fpls.2022.840397
Liang Z, Zhang K, Chen KL, Gao CX (2014) Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system. Journal of Genetics and Genomics 41(2):63–68. https://doi.org/10.1016/j.jgg.2013.12.001
Ligoxigakis E, Vakalounakis D, Thanassoulopoulos C (2002) Weed hosts of Verticillium dahliae in Crete: susceptibility, symptomatology and significance. Phytoparasitica 30(5):511–518
Lin B, Zhuo K, Chen S, Hu L, Sun L, Wang X, Zhang LH, Liao J (2016) A novel nematode effector suppresses plant immunity by activating host reactive oxygen species-scavenging system. New phytologist 209(3):1159–1173
Lipka U, Fuchs R, Lipka V (2008) Arabidopsis non-host resistance to powdery mildews. Current Opinion in Plant Biology 11(4):404–411
Liu L, Wang D, Zhang C, Liu H, Guo H, Cheng H, Liu E, Su X (2022a) The heat shock factor GhHSFA4a positively regulates cotton resistance to Verticillium dahliae. Frontiers in Plant Science 13:1050216. https://doi.org/10.3389/fpls.2022.1050216
Liu S, Sun R, Zhang X, Feng Z, Wei F, Zhao L, Zhang Y, Zhu L, Feng H, Zhu H (2020) Genome-wide analysis of OPR family genes in cotton identified a role for GhOPR9 in resistance. Genes 11(10):1134. https://doi.org/10.3390/genes11101134
Liu T, Song T, Zhang X, Yuan H, Su L, Li W, Xu J, Liu S, Chen L, Chen T, Zhang M (2014a) Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis. Nature communications 5(1):1–10
Liu T, Song T, Zhang X, Yuan H, Su L, Li W, Xu J, Liu S, Chen L, Chen T, Zhang M (2014b) Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis. Nature communications 5:4686
Liu W, Zhang BH (2022) The landscape of genome sequencing and assembling in plants. Funct Integr Genomics 22, 1147–1152. https://doi.org/10.1007/s10142-022-00916-x
Liu W, Liu J, Ning Y, Ding B, Wang X, Wang Z, Wang G-L (2013) Recent progress in understanding PAMP-and effector-triggered immunity against the rice blast fungus Magnaporthe oryzae. Molecular plant 6(3):605–620
Liu X, Hao L, Li D, Zhu L, Hu S (2015b) Long non-coding RNAs and their biological roles in plants. Genomics, proteomics & bioinformatics 13(3):137–147
Liu J, Benedict CR, Stipanovic RD, Bell AA (1999) Purification and characterization of S-adenosyl-L-methionine: desoxyhemigossypol-6-O-methyltransferase from cotton plants. An enzyme capable of methylating the defense terpenoids of cotton. Plant Physiology 121(3):1017–1024
Liu J, Osbourn A, Ma P (2015a) MYB transcription factors as regulators of phenylpropanoid metabolism in plants. Molecular plant 8(5):689–708
Liu T, Chen T, Kan J, Yao Y, Guo D, Yang Y, Ling X, Wang J, Zhang B (2022b) The GhMYB36 transcription factor confers resistance to biotic and abiotic stress by enhancing PR1 gene expression in plants. Plant Biotechnology Journal 20(4):722–735. https://doi.org/10.1111/pbi.13751
Long L, Xu FC, Zhao JR, Li B, Xu L, Gao W (2020) GbMPK3 overexpression increases cotton sensitivity to Verticillium dahliae by regulating salicylic acid signaling. Plant Science 292:110374. https://doi.org/10.1016/j.plantsci.2019.110374
Lorenzo O, Piqueras R, Sánchez-Serrano JJ, Solano R (2003) Ethylene response factor1 integrates signals from ethylene and jasmonate pathways in plant defense. The Plant Cell 15(1):165–178
Low PS, Heinstein PF (1986) Elicitor stimulation of the defense response in cultured plant cells monitored by fluorescent dyes. Archives of Biochemistry and Biophysics 249(2):472–479
Lund ST, Stall RE, Klee HJ (1998) Ethylene regulates the susceptible response to pathogen infection in tomato. The Plant Cell 10(3):371–382
Luo P, Wang YH, Wang GD, Essenberg M, Chen XY (2001) Molecular cloning and functional identification of (+)-δ-cadinene-8-hydroxylase, a cytochrome P450 mono-oxygenase (CYP706B1) of cotton sesquiterpene biosynthesis. The Plant Journal 28(1):95–104
Luo X, Xie C, Dong J, Yang X, Sui A (2014) Interactions between Verticillium dahliae and its host: vegetative growth, pathogenicity, plant immunity. Applied microbiology and biotechnology 98(16):6921–6932
Luo X, Li Z, Xiao S, Ye Z, Nie X, Zhang X, Kong J, Zhu L (2021) Phosphate deficiency enhances cotton resistance to Verticillium dahliae through activating jasmonic acid biosynthesis and phenylpropanoid pathway. Plant Science 302:110724. https://doi.org/10.1016/j.plantsci.2020.110724
Ma H, Duan J, Ke J, He Y, Gu X, Xu TH, Yu H, Wang Y, Brunzelle JS, Jiang Y, Rothbart SB (2017) A D53 repression motif induces oligomerization of TOPLESS corepressors and promotes assembly of a corepressor-nucleosome complex. Science advances 3(6):e1601217
Ma Z, He S, Wang X, Sun J, Zhang Y, Zhang G, Wu L, Li Z, Liu Z, Sun G, Yan Y (2018) Resequencing a core collection of upland cotton identifies genomic variation and loci influencing fiber quality and yield. Nature genetics 50(6):803–813
Ma Q, Wang N, Ma L, Lu J, Wang H, Wang C, Yu S, Wei H (2020) The cotton BEL1-like transcription factor GhBLH7-D06 negatively regulates the defense response against Verticillium dahliae. International Journal of Molecular Sciences 21(19):7126. https://doi.org/10.3390/ijms21197126
Ma Z, Zheng Y, Chao Z, Chen H, Zhang Y, Yin M, Shen J, Yan S (2022) Visualization of the process of a nanocarrier-mediated gene delivery: stabilization, endocytosis and endosomal escape of genes for intracellular spreading. Journal of Nanobiotechnology 20(1):1–12
Mansoori B, Smith C (2005) Elicitation of ethylene by Verticillium albo-atrum phytotoxins in potato. Journal of Phytopathology 153(3):143–149
Marino D, Froidure S, Canonne J, Ben Khaled S, Khafif M, Pouzet C, Jauneau A, Roby D, Rivas S (2013) Arabidopsis ubiquitin ligase MIEL1 mediates degradation of the transcription factor MYB30 weakening plant defence. Nature communications 4(1):1–9
Mauch-Mani B, Slusarenko AJ (1996) Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance of Arabidopsis to Peronospora parasitica. The Plant Cell 8(2):203–212
McCarthy RL, Zhong R, Ye Z-H (2009) MYB83 is a direct target of SND1 and acts redundantly with MYB46 in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant and Cell Physiology 50(11):1950–1964
Melech-Bonfil S, Sessa G (2010) Tomato MAPKKKε is a positive regulator of cell-death signaling networks associated with plant immunity. The Plant Journal 64(3):379–391
Meng X, Zhang S (2013) MAPK cascades in plant disease resistance signaling. Annual review of phytopathology 51(1):245–266
Meng X, Li F, Liu C, Zhang C, Wu Z, Chen Y (2010) Isolation and characterization of an ERF transcription factor gene from cotton (Gossypium barbadense L.). Plant molecular biology reporter 28(1):176–183
Meng J, Gao H, Zhai W, Shi J, Zhang M, Zhang W, Jian G, Zhang M, Qi F (2018) Subtle regulation of cotton resistance to Verticillium wilt mediated by MAPKK family members. Plant Science 272:235–242
Meyer R, Slater V, Dubery IA (1994) A phytotoxic protein-lipopolysaccharide complex produced by Verticillium dahliae. Phytochemistry 35(6):1449–1453
Miao W, Wang X, Li M, Song C, Wang Y, Hu D, Wang J (2010) Genetic transformation of cotton with a harpin-encoding gene hpa Xoo confers an enhanced defense response against different pathogens through a priming mechanism. BMC plant biology 10(1):1–14
Michelmore RW, Paran I, Kesseli R (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proceedings of the National Academy of Sciences 88(21):9828–9832
Mitter N, Worrall EA, Robinson KE, Li P, Jain RG, Taochy C, Fletcher SJ, Carroll BJ, Lu GQ, Xu ZP (2017) Clay nanosheets for topical delivery of RNAi for sustained protection against plant viruses. Nature Plants 3(2):1–10
Mo HJ, Sun YX, Zhu XL, Wang XF, Zhang Y, Yang J, Yan GJ, Ma ZY (2016) Cotton S-adenosylmethionine decarboxylase-mediated spermine biosynthesis is required for salicylic acid-and leucine-correlated signaling in the defense response to Verticillium dahliae. Planta 243(4):1023–1039
Mo S, Zhang Y, Wang X, Yang J, Sun Z, Zhang D, Chen B, Wang G, Ke H, Liu Z, Meng C (2021) Cotton GhSSI2 isoforms from the stearoyl acyl carrier protein fatty acid desaturase family regulate Verticillium wilt resistance. Molecular Plant Pathology 22(9):1041–1056. https://doi.org/10.1111/mpp.13093
Nachmias A, Buchner V, Burstein Y (1985) Biological and immunochemical characterization of a low molecular weight phytotoxin isolated from a protein—lipopolysaccharide complex produced by a potato isolate of Verticillium dahliae Kleb. Physiological Plant Pathology 26(1):43–55
Ngou BPM, Ahn H-K, Ding P, Jones JD (2021) Mutual potentiation of plant immunity by cell-surface and intracellular receptors. Nature 592(7852):110–115
Nie H, Wang Y, Su Y, Hua J (2018) Exploration of miRNAs and target genes of cytoplasmic male sterility line in cotton during flower bud development. Functional & integrative genomics 18:457–476
Nordborg M, Weigel D (2008) Next-generation genetics in plants. Nature 456(7223):720–723
Nürnberger T, Kemmerling B (2009) Pathogen-associated molecular patterns (PAMP) and PAMP-triggered immunity. Annual review of plant biology 34:16–47
Ogata K, Morikawa S, Nakamura H, Sekikawa A, Inoue T, Kanai H, Sarai A, Ishii S, Nishimura Y (1994) Solution structure of a specific DNA complex of the Myb DNA-binding domain with cooperative recognition helices. Cell 79(4):639–648
Oh C-S, Martin GB (2011) Effector-triggered immunity mediated by the Pto kinase. Trends in plant science 16(3):132–140
Oñate-Sánchez L, Anderson JP, Young J, Singh KB (2007) AtERF14, a member of the ERF family of transcription factors, plays a nonredundant role in plant defense. Plant Physiology 143(1):400–409
Pabo CO, Sauer RT (1992) Transcription factors: structural families and principles of DNA recognition. Annual review of biochemistry 61(1):1053–1095
Panigrahi GK, Sahoo A, Satapathy KB (2021) Insights to plant immunity: defense signaling to epigenetics. Physiological and Molecular Plant Pathology 113:101568
Pantelides IS, Tjamos SE, Paplomatas EJ (2010) Ethylene perception via ETR1 is required in Arabidopsis infection by Verticillium dahliae. Molecular plant pathology 11(2):191–202
Parkhi V, Kumar V, Campbell LAM, Bell AA, Rathore KS (2010) Expression of arabidopsis NPR1 in transgenic cotton confers resistance to non-defoliating isolates of Verticillium dahliae but not the defoliating isolates. Journal of Phytopathology 158(11-12):822–825
Pegg G (1965) Phytotoxin production by Verticillium albo-atrum Reinke et Berthold. Nature 208(5016):1228–1229
Pegg GF, Brady BL (2002) Verticillium wilts. CABI
Pegg G, Gull K, Newsam R (1976) Transmission electron microscopy of Verticillium albo-atrum hyphae in xylem vessels of tomato plants. Physiological Plant Pathology 8(3):221–224
Peng RH, Jones DC, Liu F, Zhang BH (2021) From Sequencing to Genome Editing for Cotton Improvement. Trends in Biotechnology 39(3):221–224 https://doi.org/10.1016/j.tibtech.2020.09.001
Polychronopoulos A, Houston B, Lownsbery B (1969) Penetration and development of Rhizoctonia solani in sugar beet seedlings infected with Heterodera schachtii. Phytopathology 59(4):482
Porter C, Green R (1952) Production of exotoxin in the genus Verticillium. Phytopathology 42:472
Postel, S., Kemmerling, B. (2009). Plant systems for recognition of pathogen-associated molecular patternsSeminars in cell & developmental biology. 20. 9. Academic Press.
Pottinger SE, Innes RW (2020) RPS5-mediated disease resistance: fundamental insights and translational applications. Annual review of phytopathology 58:139–160
Preston J, Wheeler J, Heazlewood J, Li SF, Parish RW (2004) AtMYB32 is required for normal pollen development in Arabidopsis thaliana. The Plant Journal 40(6):979–995
Prieto P, Navarro-Raya C, Valverde-Corredor A, Amyotte SG, Dobinson KF, Mercado-Blanco J (2009) Colonization process of olive tissues by Verticillium dahliae and its in planta interaction with the biocontrol root endophyte Pseudomonas fluorescens PICF7. Microbial Biotechnology 2(4):499–511
Pritchard L, Birch PR (2014) The zigzag model of plant–microbe interactions: is it time to move on? Molecular plant pathology 15(9):865
Qi J, Song CP, Wang B, Zhou J, Kangasjärvi J, Zhu JK, Gong Z (2018) Reactive oxygen species signaling and stomatal movement in plant responses to drought stress and pathogen attack. Journal of integrative plant biology 60(9):805–826
Qin J, Wang K, Sun L, Xing H, Wang S, Li L, Chen S, Guo HS, Zhang J (2018) The plant-specific transcription factors CBP60g and SARD1 are targeted by a Verticillium secretory protein VdSCP41 to modulate immunity. Elife 7:e34902
Qin T, Liu S, Zhang Z, Sun L, He X, Lindsey K, Zhu L, Zhang X (2019) GhCyP3 improves the resistance of cotton to Verticillium dahliae by inhibiting the E3 ubiquitin ligase activity of GhPUB17. Plant Molecular Biology 99(4-5):379–393. https://doi.org/10.1007/s11103-019-00824-y
Rajamuthiah R, Mylonakis E (2014) Effector triggered immunity: activation of innate immunity in metazoans by bacterial effectors. Virulence 5(7):697–702
Ramegowda V, Mysore KS, Senthil-Kumar M (2014) Virus-induced gene silencing is a versatile tool for unraveling the functional relevance of multiple abiotic-stress-responsive genes in crop plants. Frontiers in Plant Science 5:323. https://doi.org/10.3389/fpls.2014.00323
Ren Z, Liu W, Wang X, Chen M, Zhao J, Zhang F, Feng H, Liu J, Yang D, Ma X, Li W (2021) Seven in absentia ubiquitin ligases positively regulate defense against Verticillium dahliae in Gossypium hirsutum. Frontiers in Plant Science 12:760520. https://doi.org/10.3389/fpls.2021.760520
Resende M, Flood J, Cooper RM (1994) Host specialization of Verticillium dahliae, with emphasis on isolates from cocoa (Theobroma cacao). Plant Pathology 43(1):104–111
Riechmann JL, Heard J, Martin G, Reuber L, Jiang CZ, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290(5499):2105–2110
Robb J, Powell D, Street P (1989) Vascular coating: a barrier to colonization by the pathogen in Verticillium wilt of tomato. Canadian Journal of Botany 67(2):600–607
Robison MM, Shah S, Tamot B, Pauls KP, Moffatt BA, Glick BR (2001) Reduced symptoms of Verticillium wilt in transgenic tomato expressing a bacterial ACC deaminase. Molecular plant pathology 2(3):135–145
Saeedizadeh A, Kheiri A, Okhovat M, Hoseininejad A (2003) Study on interaction between root-knot nematode Meloidogyne javanica and wilt fungus Verticillium dahliae on olive seedlings in greenhouse. Communications in Agricultural and Applied Biological Sciences 68(4 Pt A):139–143
Sanju S, Siddappa S, Thakur A, Shukla PK, Srivastava N, Pattanayak D, Sharma S, Singh BP (2015) Host-mediated gene silencing of a single effector gene from the potato pathogen Phytophthora infestans imparts partial resistance to late blight disease. Functional & integrative genomics 15:697–706
Santhanam P, Thomma B (2013) Verticillium dahliae Sge1 differentially regulates expression of candidate effector genes. Molecular Plant-microbe Interactions:MPMI 26(2):249–256
Schenke D, Boettcher C, Scheel D (2011) Crosstalk between abiotic ultraviolet-B stress and biotic (flg22) stress signalling in Arabidopsis prevents flavonol accumulation in favor of pathogen defence compound production. Plant, cell & environment 34(11):1849–1864
Schweizer LPLLD, Tollot GTSLL, Kahmann MZARSR (2015) Fungal effectors and plant susceptibility. Annual review of plant biology 66:513–545
Seo PJ, Park CM (2010) MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis. New phytologist 186(2):471–483
Shaban M, Miao Y, Ullah A, Khan AQ, Menghwar H, Khan AH, Ahmed MM, Tabassum MA, Zhu L (2018) Physiological and molecular mechanism of defense in cotton against Verticillium dahliae. Plant Physiology and Biochemistry 125:193–204
Shaban M, Khan AH, Noor E, Malik W, Ali HMW, Shehzad M, Akram U, Qayyum A (2021) A 13-lipoxygenase, GhLOX2, positively regulates cotton tolerance against Verticillium dahliae through JA-mediated pathway. Gene 796:145797. https://doi.org/10.1016/j.gene.2021.145797
Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z, Zhang K, Liu J, Xi JJ, Qiu JL, Gao C (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nature biotechnology 31(8):686–688. https://doi.org/10.1038/nbt.2650
Shwab EK, Bok JW, Tribus M, Galehr J, Graessle S, Keller NP (2007) Histone deacetylase activity regulates chemical diversity in Aspergillus. Eukaryotic cell 6(9):1656–1664
Song R, Li J, Xie C, Jian W, Yang X (2020) An overview of the molecular genetics of plant resistance to the Verticillium wilt pathogen Verticillium dahliae. International journal of molecular sciences 21(3):1120
Song Y, Zhai Y, Li L, Yang Z, Ge X, Yang Z, Zhang C, Li F, Ren M (2021) BIN2 negatively regulates plant defence against Verticillium dahliae in Arabidopsis and cotton. Plant Biotechnology Journal 19(10):2097–2112. https://doi.org/10.1111/pbi.13640
Storey G, Evans K (1987) Interactions between Globodera pallida juveniles, Verticillium dahliae and three potato cultivars, with descriptions of associated histopathologies. Plant Pathology 36(2):192–200
Stotz HU, Mitrousia GK, de Wit PJ, Fitt BD (2014) Effector-triggered defence against apoplastic fungal pathogens. Trends in plant science 19(8):491–500
Su YX, Wang GL, Huang ZY, Hu LL, Fu T, Wang XY (2022) Silencing GhIAA43, a member of cotton AUX/IAA genes, enhances wilt resistance via activation of salicylic acid-mediated defenses. Plant Science 314:111126. https://doi.org/10.1016/j.plantsci.2021.111126
Subbarao KV, Chassot A, Gordon TR, Hubbard JC, Bonello P, Mullin R, Okamoto D, Davis RM, Koike ST (1995) Genetic relationships and cross pathogenicities of Verticillium dahliae isolates from cauliflower and other crops. Phytopathology 85(10):1105–1112
Sufyan M, Daraz U, Hyder S, Zulfiqar U, Iqbal R, Eldin SM, Rafiq F, Mahmood N, Shahzad K, Uzair M, Fiaz S (2023) An overview of genome engineering in plants, including its scope, technologies, progress and grand challenges. Functional & integrative genomics 23(2):119
Sun L, Zhu L, Xu L, Yuan D, Min L, Zhang X (2014) Cotton cytochrome P450 CYP82D regulates systemic cell death by modulating the octadecanoid pathway. Nature communications 5(1):1–12
Sun M, Zhang Z, Ren Z, Wang X, Sun W, Feng H, Zhao J, Zhang F, Li W, Ma X, Yang D (2021a) The GhSWEET42 glucose transporter participates in Verticillium dahliae infection in cotton. Frontiers in Plant Science 12:690754. https://doi.org/10.3389/fpls.2021.690754
Sun YD, Zhong MM, Li YB, Zhang RH, Su L, Xia GX, Wang HY (2021b) GhADF6-mediated actin reorganization is associated with defence against Verticillium dahliae infection in cotton. Molecular Plant Pathology 22(12):1656–1667. https://doi.org/10.1111/mpp.13137
Tai HH, Goyer C, Platt H, De Koeyer D, Murphy A, Uribe P, Halterman D (2013) Decreased defense gene expression in tolerance versus resistance to Verticillium dahliae in potato. Functional & integrative genomics 13:367–378
Talboys P (1958) Association of tylosis and hyperplasia of the xylem with vascular invasion of the hop by Verticillium albo-atrum. Transactions of the British Mycological Society 41(2):249-IN248
Tang Y, Zhang Z, Lei Y, Hu G, Liu J, Hao M, Chen A, Peng Q, Wu J (2019) Cotton WATs modulate SA biosynthesis and local lignin deposition participating in plant resistance against Verticillium dahliae. Frontiers in Plant Science 10:526. https://doi.org/10.3389/fpls.2019.00526
Temple SH, DeVay J, Forrester LL (1973) Temperature effects upon development and pathogenicity of defoliating and nondefoliating pathotypes of Verticillium dahliae in leaves of cotton plants. Phytopathology 63:953–958
Thaler JS, Owen B, Higgins VJ (2004) The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles. Plant Physiology 135(1):530–538
Thatcher LF, Manners JM, Kazan K (2009) Fusarium oxysporum hijacks COI1-mediated jasmonate signaling to promote disease development in Arabidopsis. The Plant Journal 58(6):927–939
Thomma BP, Eggermont K, Tierens KF-J, Broekaert WF (1999) Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. Plant Physiology 121(4):1093–1101
Thomma BP, Penninckx IA, Cammue BP, Broekaert WF (2001) The complexity of disease signaling in Arabidopsis. Current opinion in immunology 13(1):63–68
Tjamos SE, Flemetakis E, Paplomatas EJ, Katinakis P (2005) Induction of resistance to Verticillium dahliae in Arabidopsis thaliana by the biocontrol agent K-165 and pathogenesis-related proteins gene expression. Molecular Plant-Microbe Interactions 18(6):555–561
Tripathy BC, Oelmüller R (2012) Reactive oxygen species generation and signaling in plants. Plant signaling & behavior 7(12):1621–1633
Tzima A, Paplomatas EJ, Rauyaree P, Kang S (2010) Roles of the catalytic subunit of cAMP-dependent protein kinase A in virulence and development of the soilborne plant pathogen Verticillium dahliae. Fungal Genetics and Biology 47(5):406–415
Tzima AK, Paplomatas EJ, Tsitsigiannis DI, Kang S (2012) The G protein β subunit controls virulence and multiple growth-and development-related traits in Verticillium dahliae. Fungal Genetics and Biology 49(4):271–283
Upadhyay SK, Kumar J, Alok A, Tuli R (2013) RNA-guided genome editing for target gene mutations in wheat. G3-Genes Genomes. Genetics 3(12):2233–2238. https://doi.org/10.1534/g3.113.008847
Vellosillo T, Vicente J, Kulasekaran S, Hamberg M, Castresana C (2010) Emerging complexity in reactive oxygen species production and signaling during the response of plants to pathogens. Plant Physiology 154(2):444–448
Veronese P, Narasimhan ML, Stevenson RA, Zhu JK, Weller SC, Subbarao KV, Bressan RA (2003) Identification of a locus controlling Verticillium disease symptom response in Arabidopsis thaliana. The Plant Journal 35(5):574–587
Vyas VK, Barrasa MI, Fink GR (2015) A Candida albicans CRISPR system permits genetic engineering of essential genes and gene families. Science advances 1(3):e1500248
Wang FX, Ma YP, Yang CL, Zhao PM, Yao Y, Jian GL, Luo YM, Xia GX (2011) Proteomic analysis of the sea-island cotton roots infected by wilt pathogen Verticillium dahliae. Proteomics 11(22):4296–4309
Wang X, Wang C, Xie C, Yang X (2014a) Advances in molecular mechanisms of Verticillium pathogenicity and plant resistance to Verticillium wilt. Journal of Henan Agricultural Sciences 43(1):1–6
Wang YP, Cheng X, Shan QW, Zhang Y, Liu JX, Gao CX, Qiu JL (2014b) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nature biotechnology 32(9):947–951. https://doi.org/10.1038/nbt.2969
Wang H, Wang W, Zhan J, Huang W, Xu H (2015) An efficient PEG-mediated transient gene expression system in grape protoplasts and its application in subcellular localization studies of flavonoids biosynthesis enzymes. Scientia Horticulturae 191:82–89
Wang W, Yuan Y, Yang C, Geng S, Sun Q, Long L, Cai C, Chu Z, Liu X, Wang G, Du X (2016) Characterization, expression, and functional analysis of a novel NAC gene associated with resistance to verticillium wilt and abiotic stress in cotton. G3: Genes, Genomes, Genetics 6(12):3951–3961
Wang L, Wu SM, Zhu Y, Fan Q, Zhang ZN, Hu G, Peng QZ, Wu JH (2017a) Functional characterization of a novel jasmonate ZIM-domain interactor (NINJA) from upland cotton (Gossypium hirsutum). Plant Physiology and Biochemistry 112:152–160
Wang W, Sun Y, Han L, Su L, Xia G, Wang H (2017b) Overexpression of GhPFN2 enhances protection against Verticillium dahliae invasion in cotton. Science China Life Sciences 60(8):861–867
Wang P, Sun Y, Pei YK, Li XC, Zhang XY, Li FG, Hou YX (2018a) GhSNAP33, a t-SNARE protein from Gossypium hirsutum, mediates resistance to Verticillium dahliae infection and tolerance to drought stress. Frontiers in Plant Science 9:896. https://doi.org/10.3389/fpls.2018.00896
Wang P, Zhang J, Sun L, Ma Y, Xu J, Liang S, Deng J, Tan J, Zhang Q, Tu L, Daniell H (2018b) High efficient multisites genome editing in allotetraploid cotton (Gossypium hirsutum) using CRISPR/Cas9 system. Plant Biotechnology Journal 16(1):137–150. https://doi.org/10.1111/pbi.12755
Wang H, Sun S, Ge W, Zhao L, Hou B, Wang K, Lyu Z, Chen L, Xu S, Guo J, Li M (2020a) Horizontal gene transfer of Fhb7 from fungus underlies Fusarium head blight resistance in wheat. Science 368(6493):844. https://doi.org/10.1126/science.aba5435
Wang J, Song L, Gong X, Xu J, Li M (2020b) Functions of jasmonic acid in plant regulation and response to abiotic stress. International journal of molecular sciences 21(4):1446
Wang W, Feng B, Zhou JM, Tang D (2020c) Plant immune signaling: advancing on two frontiers. Journal of integrative plant biology 62(1):2–24
Wang G, Wang X, Zhang Y, Yang J, Li Z, Wu L, Wu J, Wu N, Liu L, Liu Z, Zhang M (2021a) Dynamic characteristics and functional analysis provide new insights into long non-coding RNA responsive to Verticillium dahliae infection in Gossypium hirsutum. BMC plant biology 21:1–13
Wang H, Chen B, Tian J, Kong Z (2021b) Verticillium dahliae VdBre1 is required for cotton infection by modulating lipid metabolism and secondary metabolites. Environmental Microbiology 23(4):1991–2003
Wang G, Wang X, Zhang Y, Yang J, Li Z, Wu L, Wu J, Wu N, Liu L, Liu Z, Zhang M (2021c) Dynamic characteristics and functional analysis provide new insights into long non-coding RNA responsive to Verticillium dahliae infection in Gossypium hirsutum. BMC Plant Biology 21:1–3
Wang Y, Zhao J, Chen Q, Zheng K, Deng X, Gao W, Pei W, Geng S, Deng Y, Li C, Chen Q (2023) Quantitative trait locus mapping and identification of candidate genes for resistance to Verticillium wilt in four recombinant inbred line populations of Gossypium hirsutum. Plant Science 327:111562
Wasternack C (2014) Action of jasmonates in plant stress responses and development—applied aspects. Biotechnology advances 32(1):31–39
Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Annals of Botany 111(6):1021–1058
Wasternack C, Strnad M (2018) Jasmonates: news on occurrence, biosynthesis, metabolism and action of an ancient group of signaling compounds. International journal of molecular sciences 19(9):2539
Wei F, Shang W, Yang J, Hu X, Xu X (2015) Spatial pattern of Verticillium dahliae microsclerotia and cotton plants with wilt symptoms in commercial plantations. PloS one 10(7):e0132812
Wei T, Tang Y, Jia P, Zeng Y, Wang B, Wu P, Quan Y, Chen A, Li Y, Wu J (2021) A cotton lignin biosynthesis gene, GhLAC4, fine-tuned by ghr-miR397 modulates plant resistance against Verticillium dahliae. Frontiers in Plant Science 12:743795. https://doi.org/10.3389/fpls.2021.743795
Wen-Jie L, Na W, Chen C, Zhao YP, Hou YX (2022) Identification and expression analysis of arabinogalactan protein genes in cotton reveal the function of GhAGP15 in Verticillium dahliae resistance. Gene 822:146336. https://doi.org/10.1016/j.gene.2022.146336
Wood R (1982) Fungal wilt diseases of plants. JSTOR
Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, Brindle ID, De Luca V, Després C (2012) The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Reports 1(6):639–647
Wu Y, Zhang L, Zhou J, Zhang X, Feng Z, Wei F, Zhao L, Zhang Y, Feng H, Zhu H (2021) Calcium-dependent protein kinase GhCDPK28 was dentified and involved in Verticillium wilt resistance in cotton. Frontiers in Plant Science 12:772649. https://doi.org/10.3389/fpls.2021.772649
Wu N, Li WJ, Chen C, Zhao YP, Hou YX (2022) Analysis of the PRA1 genes in cotton identifies the role of GhPRA1.B1-1A in Verticillium dahliae resistance. Genes 13(5):765. https://doi.org/10.3390/genes13050765
Xiang L, Cai C, Cheng J, Wang L, Wu C, Shi Y, Luo J, He L, Deng Y, Zhang X, Yuan Y (2018) Identification of circularRNAs and their targets in Gossypium under Verticillium wilt stress based on RNA-seq. PeerJ 6:e4500
Xiao S, Hu Q, Shen J, Liu S, Yang Z, Chen K, Klosterman SJ, Javornik B, Zhang X, Zhu L (2021a) GhMYB4 downregulates lignin biosynthesis and enhances cotton resistance to Verticillium dahliae. Plant Cell Reports 40:735–751
Xiao S, Hu Q, Shen J, Liu S, Yang Z, Chen K, Klosterman SJ, Javornik B, Zhang X, Zhu L (2021b) GhMYB4 downregulates lignin biosynthesis and enhances cotton resistance to Verticillium dahliae. Plant Cell Reports 40(4):735–751. https://doi.org/10.1007/s00299-021-02672-x
Xiao S, Ming Y, Hu Q, Ye Z, Si H, Liu S, Zhang X, Wang W, Yu Y, Kong J, Klosterman SJ (2023) GhWRKY41 forms a positive feedback regulation loop and increases cotton defense response against Verticillium dahliae by regulating phenylpropanoid metabolism. Plant Biotechnology Journal 2023:1
Xie FL, Jones DC, Wang QL, Sun RR, Zhang BH (2015) Small RNA sequencing identifies miRNA roles in ovule and fibre development. Plant Biotechnology Journal 13(3):355–369 https://doi.org/10.1111/pbi.12296
Xing J, Chin C-K (2000) Modification of fatty acids in eggplant affects its resistance to Verticilliumdahliae. Physiological and Molecular Plant Pathology 56(5):217–225
Xiong X, Sun S, Li Y, Zhang X, Sun J, Xue F (2019) The cotton WRKY transcription factor GhWRKY70 negatively regulates the defense response against Verticillium dahliae. The Crop Journal 7(3):393–402
Xiong XP, Sun SC, Zhang XY, Li YJ, Liu F, Zhu QH, Xue F, Sun J (2020) GhWRKY70D13 regulates resistance to Verticillium dahliae in cotton through the ethylene and jasmonic acid signaling pathways. Frontiers in Plant Science 11:69. https://doi.org/10.3389/fpls.2020.00069
Xiong XP, Sun SC, Zhu QH, Zhang XY, Li YJ, Liu F, Xue F, Sun J (2021a) The cotton lignin biosynthetic gene Gh4CL30 regulates lignification and phenolic content and contributes to Verticillium wilt resistance. Molecular Plant-Microbe Interactions 34(3):240–254. https://doi.org/10.1094/Mpmi-03-20-0071-R
Xiong XP, Sun SC, Zhu QH, Zhang XY, Liu F, Li YJ, Xue F, Sun J (2021b) Transcriptome analysis and RNA interference reveal GhGDH2 regulating cotton resistance to Verticillium wilt by JA and SA signaling pathways. Frontiers in Plant Science 12:654676. https://doi.org/10.3389/fpls.2021.654676
Xu Y-H, Wang J-W, Wang S, Wang J-Y, Chen X-Y (2004) Characterization of GaWRKY1, a cotton transcription factor that regulates the sesquiterpene synthase gene (+)-δ-cadinene synthase-A. Plant Physiology 135(1):507–515
Xu L, Zhu L, Tu L, Guo X, Long L, Sun L, Gao W, Zhang X (2011a) Differential gene expression in cotton defence response to Verticillium dahliae by SSH. Journal of Phytopathology 159(9):606–615
Xu L, Zhu L, Tu L, Liu L, Yuan D, Jin L, Long L, Zhang X (2011b) Lignin metabolism has a central role in the resistance of cotton to the wilt fungus Verticillium dahliae as revealed by RNA-Seq-dependent transcriptional analysis and histochemistry. Journal of experimental botany 62(15):5607–5621
Xu L, Zhu LF, Zhang XL (2013) Research on resistance mechanism of cotton to Verticillium wilt. Acta Agronomica Sinica 38(9):1553–1560
Xu L, Zhang W, He X, Liu M, Zhang K, Shaban M, Sun L, Zhu J, Luo Y, Yuan D, Zhang X (2014) Functional characterization of cotton genes responsive to Verticillium dahliae through bioinformatics and reverse genetics strategies. Journal of experimental botany 65(22):6679–6692
Xu J, Wang X, Li Y, Zeng J, Wang G, Deng C, Guo W (2018) Host-induced gene silencing of a regulator of G protein signalling gene (Vd RGS 1) confers resistance to Verticillium wilt in cotton. Plant Biotechnology Journal 16(9):1629–1643
Yang L, Jue D, Li W, Zhang R, Chen M, Yang Q (2013) Identification of MiRNA from eggplant (Solanum melongena L.) by small RNA deep sequencing and their response to Verticillium dahliae infection. PloS one 8(8):e72840
Yang CL, Liang S, Wang HY, Han LB, Wang FX, Cheng HQ, Wu XM, Qu ZL, Wu JH, Xia GX (2015a) Cotton major latex protein 28 functions as a positive regulator of the ethylene responsive factor 6 in defense against Verticillium dahliae. Molecular plant 8(3):399–411
Yang C, Lu X, Ma B, Chen S-Y, Zhang J-S (2015b) Ethylene signaling in rice and Arabidopsis: conserved and diverged aspects. Molecular plant 8(4):495–505
Yang J, Zhang Y, Wang X, Wang W, Li Z, Wu J, Wang G, Wu L, Zhang G, Ma Z (2018a) HyPRP1 performs a role in negatively regulating cotton resistance to V-dahliae via the thickening of cell walls and ROS accumulation. Bmc Plant Biology 18:339. https://doi.org/10.1186/s12870-018-1565-1
Yang YW, Chen TZ, Ling XT, Ma ZQ (2018b) Gbvdr6, a gene encoding a receptor-like protein of cotton (Gossypium barbadense), confers resistance to Verticillium wilt in Arabidopsis and upland cotton. Frontiers in Plant Science 8:2272. https://doi.org/10.3389/fpls.2017.02272
Yang L, Zhang Y, Guan R, Li S, Xu X, Zhang S, Xu J (2020) Co-regulation of indole glucosinolates and camalexin biosynthesis by CPK5/CPK6 and MPK3/MPK6 signaling pathways. Journal of integrative plant biology 62(11):1780–1796
Yang J, Xie MX, Wang XF, Wang GN, Zhang Y, Li ZK, Ma ZY (2021) Identification of cell wall-associated kinases as important regulators involved in Gossypium hirsutum resistance to Verticillium dahliae. Bmc Plant Biology 21(1):220. https://doi.org/10.1186/s12870-021-02992-w
Yang S, Ge Q, Wan S, Sun Z, Chen Y, Li Y, Liu Q, Gong J, Xiao X, Lu Q, Shi Y (2023) Genome-wide identification and characterization of the PPO gene family in cotton (Gossypium) and their expression variations responding to Verticillium wilt infection. Genes 14(2):477
Yanhui C, Xiaoyuan Y, Kun H, Meihua L, Jigang L, Zhaofeng G, Zhiqiang L, Yunfei Z, Xiaoxiao W, Xiaoming Q, Yunping S (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant molecular biology 60(1):107–124
Yi F, An G, Song A, Cheng K, Liu J, Wang C, Wu S, Wang P, Zhu J, Liang Z, Chang Y (2023) Strigolactones positively regulate Verticillium wilt resistance in cotton via crosstalk with other hormones. Plant Physiology 2023:kiad053
Yin Z, Li Y, Han X, Shen F (2012) Genome-wide profiling of miRNAs and other small non-coding RNAs in the Verticillium dahliae–inoculated cotton roots. PloS one 7(4):e35765
Yinhua J, Xiwen W, Junling S, Zhongli Z, Zaoe P, Shoupu H, Baoyin P, Liru W, Xiongming D (2014) Association mapping of resistance to Verticillium wilt in Gossypium hirsutum L. germplasm. African journal of Biotechnology 13:31
Yuan M, Jiang Z, Bi G, Nomura K, Liu M, Wang Y, Cai B, Zhou JM, He SY, Xin XF (2021a) Pattern-recognition receptors are required for NLR-mediated plant immunity. Nature 592(7852):105–109
Yuan M, Ngou BPM, Ding P, Xin X-F (2021b) PTI-ETI crosstalk: an integrative view of plant immunity. Current Opinion in Plant Biology 62:102030
Zeng H, Chen R, Luo X, Tian J (2016) Isolation and anti-Verticillium dahliae activity from Bacillus axarquiensis TUBP1 protein. Process Biochemistry 51(10):1691–1698
Zipfel C (2014) Plant pattern-recognition receptors. Trends in immunology 35(7):345–351
Zhang BH (2015) MicroRNA: a new target for improving plant tolerance to abiotic stress. Journal of Experimental Botany 66(7):1749–1761 https://doi.org/10.1093/jxb/erv013
Zhang DQ, Zhang ZY, Unver T, Zhang BH (2021) CRISPR/Cas: A powerful tool for gene function study and crop improvement. Journal of Advanced Research 29:207–221. https://doi.org/10.1016/j.jare.2020.10.003
Zhang J, Shao F, Li Y, Cui H, Chen L, Li H, Zou Y, Long C, Lan L, Chai J, Chen S (2007) A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell host & microbe 1(3):175–185
Zhang W-W, Jian G-L, Jiang T-F, Wang S-Z, Qi F-J, Xu S-C (2012) Cotton gene expression profiles in resistant Gossypium hirsutum cv. Zhongzhimian KV1 responding to Verticillium dahliae strain V991 infection. Molecular biology reports 39:9765–9774
Zhang Y, Wang XF, Ding ZG, Ma Q, Zhang GR, Zhang SL, Li ZK, Wu LQ, Zhang GY, Ma ZY (2013) Transcriptome profiling of Gossypium barbadense inoculated with Verticillium dahliae provides a resource for cotton improvement. BMC genomics 14(1):1–18
Zhang T, Jin Y, Zhao J-H, Gao F, Zhou B-J, Fang Y-Y, Guo H-S (2016a) Host-induced gene silencing of the target gene in fungal cells confers effective resistance to the cotton wilt disease pathogen Verticillium dahliae. Molecular plant 9(6):939–942
Zhang X, Zhou G, Shabala S, Koutoulis A, Shabala L, Johnson P, Li C, Zhou M (2016b) Identification of aerenchyma formation-related QTL in barley that can be effective in breeding for waterlogging tolerance. Theoretical and Applied Genetics 129(6):1167–1177
Zhang YL, Li ZF, Feng ZL, Feng HJ, Shi YQ, Zhao LH, Zhang XL, Zhu HQ (2016c) Functional analysis of the pathogenicity-related gene VdPR1 in the vascular wilt fungus Verticillium dahliae. Plos One 11(11):e0166000. https://doi.org/10.1371/journal.pone.0166000
Zhang YW, Bai Y, Wu GH, Zou SH, Chen YF, Gao CX, Tang DZ (2017) Simultaneous modification of three homoeologs of TaEDR1 by genome editing enhances powdery mildew resistance in wheat. Plant Journal 91(4):714–724. https://doi.org/10.1111/tpj.13599
Zhang SQ, Xu ZP, Sun H, Sun LQ, Shaban M, Yang XY, Zhu LF (2019a) Genome-wide identification of papain-like cysteine proteases in Gossypium hirsutum and functional characterization in response to Verticillium dahliae. Frontiers in Plant Science 10:134. https://doi.org/10.3389/fpls.2019.00134
Zhang Y, Wu L, Wang X, Chen B, Zhao J, Cui J, Li Z, Yang J, Wu L, Wu J, Zhang G (2019b) The cotton laccase gene GhLAC15 enhances Verticillium wilt resistance via an increase in defence-induced lignification and lignin components in the cell walls of plants. Molecular plant pathology 20(3):309–322
Zhang Y, Wu L, Wang X, Chen B, Zhao J, Cui J, Li Z, Yang J, Wu L, Wu J, Zhang G (2019c) The cotton laccase gene GhLAC15 enhances Verticillium wilt resistance via an increase in defence-induced lignification and lignin components in the cell walls of plants. Molecular Plant Pathology 20(3):309–322. https://doi.org/10.1111/mpp.12755
Zhao P, Zhao Y-L, Jin Y, Zhang T, Guo H-S (2014) Colonization process of Arabidopsis thaliana roots by a green fluorescent protein-tagged isolate of Verticillium dahliae. Protein & cell 5(2):94–98
Zhao Y-L, Zhou T-T, Guo H-S (2016) Hyphopodium-specific VdNoxB/VdPls1-dependent ROS-Ca2+ signaling is required for plant infection by Verticillium dahliae. PLoS pathogens 12(7):e1005793
Zhao Y, Chen W, Cui Y, Sang X, Lu J, Jing H, Wang W, Zhao P, Wang H (2021a) Detection of candidate genes and development of KASP markers for Verticillium wilt resistance by combining genome-wide association study, QTL-seq and transcriptome sequencing in cotton. Theoretical and Applied Genetics 134(4):1063–1081
Zhao Y, Jing H, Zhao P, Chen W, Li X, Sang X, Lu J, Wang H (2021b) GhTBL34 is associated with Verticillium wilt resistance in cotton. International Journal of Molecular Sciences 22(17):9115. https://doi.org/10.3390/ijms22179115
Zhao YP, Shen JL, Li WJ, Wu N, Chen C, Hou YX (2021c) Evolutionary and characteristic analysis of RING-DUF1117 E3 ubiquitin ligase genes in Gossypium discerning the role of GhRDUF4D in Verticillium dahliae resistance. Biomolecules 11(8):1145. https://doi.org/10.3390/biom11081145
Zhao J, Xu J, Wang Y, Liu J, Dong C, Zhao L, Ai N, Xu Z, Guo Q, Feng G, Xu P (2022) Membrane localized GbTMEM214s participate in modulating cotton resistance to Verticillium wilt. Plants-Basel 11(18):2342. https://doi.org/10.3390/plants11182342
Zhen X-H, Li Y-Z (2004) Ultrastructural changes and location of β-1, 3-glucanase in resistant and susceptible cotton callus cells in response to treatment with toxin of Verticillium dahliae and salicylic acid. Journal of plant physiology 161(12):1367–1377
Zhong R, Richardson EA, Ye Z-H (2007) The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. The Plant Cell 19(9):2776–2792
Zhou JM, Zhang YL (2020) Plant immunity: danger perception and signaling. Cell 181(5):978–989. https://doi.org/10.1016/j.cell.2020.04.028
Zhou J, Wu Y, Zhang X, Zhao L, Feng Z, Wei F, Zhang Y, Feng H, Zhou Y, Zhu H (2022a) MPK homolog GhNTF6 was involved in cotton against Verticillium wilt by interacted with VdEPG1. International Journal of Biological Macromolecules 195:456–465. https://doi.org/10.1016/j.ijbiomac.2021.12.037
Zhou J, Zhao L, Wu Y, Zhang X, Cheng S, Wei F, Zhang Y, Zhu H, Zhou Y, Feng Z, Feng H (2022b) A DEK domain-containing protein GhDEK2D mediated Gossypium hirsutum enhanced resistance to Verticillium dahliae. Plant Signaling & Behavior 17:1. https://doi.org/10.1080/15592324.2021.2024738
Zhu KY, Palli SR (2020) Mechanisms, applications, and challenges of insect RNA interference. Annual review of entomology 65:1
Zhu Q-H, Fan L, Liu Y, Xu H, Llewellyn D, Wilson I (2013) miR482 regulation of NBS-LRR defense genes during fungal pathogen infection in cotton. PloS one 8(12):e84390
Zhu D, Zhang X, Zhou J, Wu Y, Zhang X, Feng Z, Wei F, Zhao L, Zhang Y, Shi Y, Feng H (2021a) Genome-wide analysis of ribosomal protein GhRPS6 and its role in cotton Verticillium wilt resistance. International journal of molecular sciences 22(4):1795
Zhu D, Zhang X, Zhou J, Wu Y, Zhang X, Feng Z, Wei F, Zhao L, Zhang Y, Shi Y, Feng H (2021b) Genome-wide analysis of ribosomal protein GhRPS6 and its role in cotton Verticillium wilt resistance. International Journal of Molecular Sciences 22(4):1795. https://doi.org/10.3390/ijms22041795
Zhu H, Song J, Dhar N, Shan Y, Ma XY, Wang XL, Chen JY, Dai XF, Li R, Wang ZS (2021c) Transcriptome analysis of a cotton cultivar provides insights into the differentially expressed genes underlying heightened resistance to the devastating Verticillium wilt. Cells 10(11):2961
Zhu YT, Hu XQ, Wang P, Wang HW, Ge XY, Li FG, Hou YX (2022) GhODO1, an R2R3-type MYB transcription factor, positively regulates cotton resistance to Verticillium dahliae via the lignin biosynthesis and jasmonic acid signaling pathway. International Journal of Biological Macromolecules 201:580–591. https://doi.org/10.1016/j.ijbiomac.2022.01.120
Zuo K, Wang J, Wu W, Chai Y, Sun X, Tang K (2005) Identification and characterization of differentially expressed ESTs of Gossypium barbadense infected by Verticillium dahliae with suppression subtractive hybridization. Molecular Biology 39(2):191–199
Zuo K-J, Qin J, Zhao J-Y, Ling H, Zhang L-D, Cao Y-F, Tang K-X (2007) Over-expression GbERF2 transcription factor in tobacco enhances brown spots disease resistance by activating expression of downstream genes. Gene 391(1-2):80–90
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We are thankful to the Institute of Cotton Research, CAAS, Anyang.
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This work was supported by the National Key R&D Program of China (2021YFE0101200) and the National Natural Science Foundation of China (32272090, 32072023, 32171994).
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FL, BH, and MJU devised the idea. MJU and ZJ wrote the main manuscript text. YM, RB, AAA, YH, HG, and YX prepared figures. YW, ZZ, and XC prepared tables. All authors reviewed the manuscript.
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Umer, M.J., Zheng, J., Yang, M. et al. Insights to Gossypium defense response against Verticillium dahliae: the Cotton Cancer. Funct Integr Genomics 23, 142 (2023). https://doi.org/10.1007/s10142-023-01065-5
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DOI: https://doi.org/10.1007/s10142-023-01065-5