Insights to Gossypium defense response against Verticillium dahliae: the Cotton Cancer.


Journal

Functional & integrative genomics
ISSN: 1438-7948
Titre abrégé: Funct Integr Genomics
Pays: Germany
ID NLM: 100939343

Informations de publication

Date de publication:
01 May 2023
Historique:
received: 16 01 2023
accepted: 19 04 2023
revised: 15 04 2023
medline: 2 5 2023
pubmed: 1 5 2023
entrez: 30 4 2023
Statut: epublish

Résumé

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.

Identifiants

pubmed: 37121989
doi: 10.1007/s10142-023-01065-5
pii: 10.1007/s10142-023-01065-5
doi:

Substances chimiques

Plant Proteins 0

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

142

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

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
pubmed: 18801424
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
pubmed: 21029325 pmcid: 6640509
Akiyama K, Matsuzaki KI, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435(7043):824–827
pubmed: 15944706
Andersen EJ, Ali S, Byamukama E, Yen Y, Nepal MP (2018) Disease resistance mechanisms in plants. Genes 9(7):339
pubmed: 29973557 pmcid: 6071103
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
pubmed: 16665597 pmcid: 1056764
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
pubmed: 33562629 pmcid: 7916069
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
pubmed: 17022171
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
pubmed: 12060224
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
pubmed: 29177423
Bhat R, Subbarao K (1999) Host range specificity in Verticillium dahliae. Phytopathology 89(12):1218–1225
pubmed: 18944648
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
pubmed: 24329768
Boch J, Bonas U (2010) Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annual review of phytopathology 48:419–436
pubmed: 19400638
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
pubmed: 19933107
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
pubmed: 36012499 pmcid: 9409477
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
pubmed: 19448638 pmcid: 2891026
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
pubmed: 19400727
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
pubmed: 19423812 pmcid: 2729760
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
doi: 10.1104/pp.17.00426 pubmed: 28584067 pmcid: 5462057
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
doi: 10.1104/pp.114.247577 pubmed: 25225186 pmcid: 4226363
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
pubmed: 24337817
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
pubmed: 31479566
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
doi: 10.1111/pbi.12758 pubmed: 28509421
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
doi: 10.3390/plants11141828 pubmed: 35890462 pmcid: 9316592
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
doi: 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
doi: 10.3390/ijms22147328 pubmed: 34298948 pmcid: 8306359
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
pubmed: 26873979 pmcid: 4783372
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
pubmed: 20660643 pmcid: 2942870
Coego A, Ramirez V, Gil MJ, Flors V, Mauch-Mani B, Vera P (2005) An Arabidopsis homeodomain transcription factor, overexpressor of cationic peroxidase
pubmed: 15923348 pmcid: 1167556
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
pubmed: 15272302 pmcid: 514913
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
pubmed: 26670613 pmcid: 4682923
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
pubmed: 32343491
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
doi: 10.3390/plants11202758 pubmed: 36297782 pmcid: 9611673
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
pubmed: 14973158 pmcid: 385286
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
pubmed: 19197359 pmcid: 2631132
Dong X (2004) NPR1, all things considered. Current Opinion in Plant Biology 7(5):547–552
pubmed: 15337097
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
pubmed: 27088499 pmcid: 4835097
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
pubmed: 20674465
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
pubmed: 22981427
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
doi: 10.1038/cr.2013.114 pubmed: 23958582 pmcid: 3790235
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
doi: 10.1073/pnas.1400822111 pubmed: 24550464 pmcid: 3970504
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
doi: 10.1016/j.ijbiomac.2020.11.191 pubmed: 33275973
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
pubmed: 12848825
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
pubmed: 15987996 pmcid: 1167537
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
pubmed: 20507429
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
pubmed: 21617027 pmcid: 3149960
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
pubmed: 21803860 pmcid: 3192574
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
pubmed: 21151869 pmcid: 2998422
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
pubmed: 21219508
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
pubmed: 23675706 pmcid: 4395461
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
pubmed: 26407676
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
pubmed: 31636399
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
pubmed: 24502957 pmcid: 3967090
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
pubmed: 20870416
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
pubmed: 24558350 pmcid: 3928049
Göhre V, Robatzek S (2008) Breaking the barriers: microbial effector molecules subvert plant immunity. Annual review of phytopathology 46:189–215
pubmed: 18422429
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
doi: 10.3389/fpls.2017.02133 pubmed: 29326741 pmcid: 5733346
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
pubmed: 26971283
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
doi: 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
doi: 10.1126/science.286.5441.950 pubmed: 10542148
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
pubmed: 25332864 pmcid: 4190182
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
pubmed: 27432176
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
doi: 10.3390/ijms19123997 pubmed: 30545043 pmcid: 6321269
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
pubmed: 28665036
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
pubmed: 10069832 pmcid: 32108
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
doi: 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
doi: 10.1094/Mpmi-10-19-0302-R pubmed: 31868566
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
doi: 10.1016/j.plantsci.2021.110833 pubmed: 33691967
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
doi: 10.3390/ijms222313041 pubmed: 34884844 pmcid: 8657740
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
doi: 10.3390/ijms23158437 pubmed: 35955570 pmcid: 9368853
Ingle RA, Carstens M, Denby KJ (2006) PAMP recognition and the plant–pathogen arms race. Bioessays 28(9):880–889
pubmed: 16937346
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
doi: 10.1007/s11103-017-0599-3 pubmed: 28258551
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
doi: 10.1186/s12870-022-03774-8 pubmed: 35918649 pmcid: 9347136
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
doi: 10.3389/fpls.2022.870882 pubmed: 35668804 pmcid: 9164164
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
doi: 10.1093/nar/gkt780 pubmed: 23999092 pmcid: 3814374
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
pubmed: 11080161 pmcid: 305818
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
pubmed: 16941900
Jones JD, Dangl JL (2006a) The plant immune system. Nature 444(7117):323–329
pubmed: 17108957
Jones JDG, Dangl JL (2006b) The plant immune system. Nature 444(7117):323–329. https://doi.org/10.1038/nature05286
doi: 10.1038/nature05286 pubmed: 17108957
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
pubmed: 30861483 pmcid: 6731392
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
pubmed: 30531948 pmcid: 6381595
Klosterman SJ, Atallah ZK, Vallad GE, Subbarao KV (2009) Diversity, pathogenicity, and management of Verticillium species. Annual review of phytopathology 47:39–62
pubmed: 19385730
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
pubmed: 21829347 pmcid: 3145793
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
pubmed: 22155845
Koornneef A, Pieterse CM (2008) Cross talk in defense signaling. Plant Physiology 146(3):839–844
pubmed: 18316638 pmcid: 2259093
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
pubmed: 29048113
Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Current Opinion in Plant Biology 5(4):325–331
pubmed: 12179966
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
pubmed: 1731993
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
pubmed: 26248304
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
pubmed: 14742872 pmcid: 341906
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
pubmed: 8580966
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
pubmed: 26869704 pmcid: 4825149
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
pubmed: 28501625
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
pubmed: 28602397
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
pubmed: 29052967 pmcid: 6638185
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
doi: 10.3389/fpls.2018.00119 pubmed: 29467784 pmcid: 5808209
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
doi: 10.1111/pbi.12781 pubmed: 28640983
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
doi: 10.3389/fpls.2018.00642 pubmed: 29881391 pmcid: 5976743
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
pubmed: 30720746 pmcid: 6387439
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
doi: 10.1186/s12870-019-1888-6 pubmed: 31455203 pmcid: 6712776
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
doi: 10.1016/j.plantsci.2019.04.013 pubmed: 31084865
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
doi: 10.3389/fpls.2020.575015 pubmed: 33193513 pmcid: 7606878
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
doi: 10.3389/fpls.2021.695691 pubmed: 34567025 pmcid: 8456104
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
doi: 10.3389/fpls.2022.840397 pubmed: 35574065 pmcid: 9096875
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
doi: 10.1016/j.jgg.2013.12.001 pubmed: 24576457
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
pubmed: 26484653
Lipka U, Fuchs R, Lipka V (2008) Arabidopsis non-host resistance to powdery mildews. Current Opinion in Plant Biology 11(4):404–411
pubmed: 18499508
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
doi: 10.3389/fpls.2022.1050216 pubmed: 36407619 pmcid: 9669655
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
doi: 10.3390/genes11101134 pubmed: 32992523 pmcid: 7600627
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
pubmed: 25156390
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
pubmed: 23340743
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
pubmed: 10557251 pmcid: 59466
Liu J, Osbourn A, Ma P (2015a) MYB transcription factors as regulators of phenylpropanoid metabolism in plants. Molecular plant 8(5):689–708
pubmed: 25840349
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
doi: 10.1111/pbi.13751 pubmed: 34812570
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
doi: 10.1016/j.plantsci.2019.110374 pubmed: 32005380
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
pubmed: 12509529 pmcid: 143489
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
pubmed: 3753013
Lund ST, Stall RE, Klee HJ (1998) Ethylene regulates the susceptible response to pathogen infection in tomato. The Plant Cell 10(3):371–382
pubmed: 9501111 pmcid: 144005
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
pubmed: 11696190
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
pubmed: 24928658
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
doi: 10.1016/j.plantsci.2020.110724 pubmed: 33288028
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
pubmed: 28630893 pmcid: 5457145
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
pubmed: 29736016
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
doi: 10.3390/ijms21197126 pubmed: 32992496 pmcid: 7582620
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
pubmed: 34980143 pmcid: 8722193
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
pubmed: 12239383 pmcid: 161092
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
pubmed: 19808805
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
pubmed: 21049563
Meng X, Zhang S (2013) MAPK cascades in plant disease resistance signaling. Annual review of phytopathology 51(1):245–266
pubmed: 23663002
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
pubmed: 29807597
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
pubmed: 26757733
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
doi: 10.1111/mpp.13093 pubmed: 34169624 pmcid: 8358998
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
pubmed: 33692545
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
pubmed: 19079047
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
pubmed: 7954830
Oh C-S, Martin GB (2011) Effector-triggered immunity mediated by the Pto kinase. Trends in plant science 16(3):132–140
pubmed: 21112235
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
pubmed: 17114278 pmcid: 1761963
Pabo CO, Sauer RT (1992) Transcription factors: structural families and principles of DNA recognition. Annual review of biochemistry 61(1):1053–1095
pubmed: 1497306
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
pubmed: 20447269
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
pubmed: 32284014
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
pubmed: 15584962
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
pubmed: 21255281 pmcid: 3815910
Pritchard L, Birch PR (2014) The zigzag model of plant–microbe interactions: is it time to move on? Molecular plant pathology 15(9):865
pubmed: 25382065 pmcid: 6638871
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
pubmed: 29660240
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
pubmed: 29757140 pmcid: 5993538
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
doi: 10.1007/s11103-019-00824-y pubmed: 30671725
Rajamuthiah R, Mylonakis E (2014) Effector triggered immunity: activation of innate immunity in metazoans by bacterial effectors. Virulence 5(7):697–702
pubmed: 25513770 pmcid: 4189875
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
doi: 10.3389/fpls.2014.00323 pubmed: 25071806 pmcid: 4085877
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
doi: 10.3389/fpls.2021.760520 pubmed: 34777442 pmcid: 8586545
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
pubmed: 11118137
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
pubmed: 20573001
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
pubmed: 15149103
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
pubmed: 22970788
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
pubmed: 25923844
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
pubmed: 20149112
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
pubmed: 29462745
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
doi: 10.1016/j.gene.2021.145797 pubmed: 34175389
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
doi: 10.1038/nbt.2650 pubmed: 23929338
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
pubmed: 17616629 pmcid: 2043372
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
pubmed: 32046212 pmcid: 7037454
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
doi: 10.1111/pbi.13640 pubmed: 34036698 pmcid: 8486250
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
pubmed: 24856287 pmcid: 4123193
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
doi: 10.1016/j.plantsci.2021.111126 pubmed: 34895552
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
doi: 10.3389/fpls.2021.690754 pubmed: 34386026 pmcid: 8353158
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
doi: 10.1111/mpp.13137 pubmed: 34515397 pmcid: 8578822
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
doi: 10.3389/fpls.2019.00526 pubmed: 31105726 pmcid: 6499033
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
pubmed: 15133157 pmcid: 429405
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
pubmed: 19220788
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
pubmed: 10594097 pmcid: 59477
Thomma BP, Penninckx IA, Cammue BP, Broekaert WF (2001) The complexity of disease signaling in Arabidopsis. Current opinion in immunology 13(1):63–68
pubmed: 11154919
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
pubmed: 15986925
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
pubmed: 20144723
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
pubmed: 22387367
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
doi: 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
pubmed: 20921160 pmcid: 2948990
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
pubmed: 12940951
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
pubmed: 25977940 pmcid: 4428347
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
pubmed: 21928292
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
doi: 10.1038/nbt.2969 pubmed: 25038773
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
pubmed: 27784753
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
pubmed: 28086169
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
pubmed: 28741129
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
doi: 10.3389/fpls.2018.00896 pubmed: 30018623 pmcid: 6038728
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
doi: 10.1111/pbi.12755 pubmed: 28499063
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
doi: 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
pubmed: 32093336 pmcid: 7073113
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
pubmed: 31846204
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
pubmed: 33185953
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
pubmed: 36509244
Wasternack C (2014) Action of jasmonates in plant stress responses and development—applied aspects. Biotechnology advances 32(1):31–39
pubmed: 24095665
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
pubmed: 23558912 pmcid: 3662512
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
pubmed: 30150593 pmcid: 6164985
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
pubmed: 26167868 pmcid: 4500557
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
doi: 10.3389/fpls.2021.743795 pubmed: 34868127 pmcid: 8636836
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
doi: 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
pubmed: 22813739
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
doi: 10.3389/fpls.2021.772649 pubmed: 34975954 pmcid: 8715758
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
doi: 10.3390/genes13050765 pubmed: 35627150 pmcid: 9141244
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
pubmed: 29576969 pmcid: 5858604
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
pubmed: 33638657
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
doi: 10.1007/s00299-021-02672-x pubmed: 33638657
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
doi: 10.3389/fpls.2020.00069 pubmed: 32158454 pmcid: 7052014
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
doi: 10.1094/Mpmi-03-20-0071-R pubmed: 33507814
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
doi: 10.3389/fpls.2021.654676 pubmed: 34177978 pmcid: 8226099
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
pubmed: 15133151 pmcid: 429402
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
pubmed: 21862479 pmcid: 3223054
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
pubmed: 25326626 pmcid: 4246195
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
pubmed: 29431919 pmcid: 6096726
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
pubmed: 24015279 pmcid: 3754920
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
pubmed: 25704161
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
pubmed: 25732590
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
doi: 10.1186/s12870-018-1565-1 pubmed: 30526498 pmcid: 6286592
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
doi: 10.3389/fpls.2017.02272 pubmed: 29387078 pmcid: 5776133
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
pubmed: 32449805 pmcid: 7687085
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
doi: 10.1186/s12870-021-02992-w pubmed: 33992078 pmcid: 8122570
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
pubmed: 36833403 pmcid: 9957175
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
pubmed: 16463103
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
pubmed: 22558219 pmcid: 3338460
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
pubmed: 33692546 pmcid: 8016741
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
pubmed: 33684883
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
pubmed: 24946686
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
doi: 10.1016/j.jare.2020.10.003 pubmed: 33842017
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
pubmed: 22733494
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
pubmed: 26925819
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
pubmed: 26908252
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
doi: 10.1371/journal.pone.0166000 pubmed: 27846253 pmcid: 5112940
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
doi: 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
doi: 10.3389/fpls.2019.00134 pubmed: 30842780 pmcid: 6391353
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
pubmed: 30267563
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
doi: 10.1111/mpp.12755 pubmed: 30267563
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
pubmed: 27463643 pmcid: 4962994
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
pubmed: 33438060
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
doi: 10.3390/ijms22179115 pubmed: 34502024 pmcid: 8431740
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
doi: 10.3390/biom11081145 pubmed: 34439811 pmcid: 8392396
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
doi: 10.3390/plants11182342 pubmed: 36145743 pmcid: 9505811
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
pubmed: 15658807
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
pubmed: 17890373 pmcid: 2048704
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
doi: 10.1016/j.cell.2020.04.028 pubmed: 32442407
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
doi: 10.1016/j.ijbiomac.2021.12.037 pubmed: 34920061
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
doi: 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
pubmed: 24391949 pmcid: 3877274
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
pubmed: 33670294 pmcid: 7918698
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
doi: 10.3390/ijms22041795 pubmed: 33670294 pmcid: 7918698
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
pubmed: 34831184 pmcid: 8616101
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
doi: 10.1016/j.ijbiomac.2022.01.120 pubmed: 35074330
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
pubmed: 17321073

Auteurs

Muhammad Jawad Umer (MJ)

State Key Laboratory of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, China.

Jie Zheng (J)

State Key Laboratory of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, China.
Hainan Yazhou Bay Seed Laboratory, China/National Nanfan, Research Institute of Chinese Academy of Agricultural Sciences, Sanya, 572025, China.

Mengying Yang (M)

State Key Laboratory of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, China.
School of Agricultural Sciences, Zhengzhou University, Zhengzhou, China.

Raufa Batool (R)

State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China.

Aamir Ali Abro (AA)

State Key Laboratory of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, China.

Yuqing Hou (Y)

State Key Laboratory of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, China.

Yanchao Xu (Y)

State Key Laboratory of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, China.

Haileslassie Gebremeskel (H)

Mehoni Agricultural Research Center, Ethiopian Institute of Agricultural Research, Addis Ababa, Ethiopia.

Yuhong Wang (Y)

State Key Laboratory of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, China.

ZhongLi Zhou (Z)

State Key Laboratory of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, China.

Xiaoyan Cai (X)

State Key Laboratory of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, China.
Hainan Yazhou Bay Seed Laboratory, China/National Nanfan, Research Institute of Chinese Academy of Agricultural Sciences, Sanya, 572025, China.
Zhengzhou Research Base, State Key Laboratory of Cotton Biology, Zhengzhou University/Institute of Cotton Research, Chinese Academy of Agricultural Science, Anyang, China.

Fang Liu (F)

State Key Laboratory of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, China. liufcri@163.com.
Hainan Yazhou Bay Seed Laboratory, China/National Nanfan, Research Institute of Chinese Academy of Agricultural Sciences, Sanya, 572025, China. liufcri@163.com.
School of Agricultural Sciences, Zhengzhou University, Zhengzhou, China. liufcri@163.com.
Zhengzhou Research Base, State Key Laboratory of Cotton Biology, Zhengzhou University/Institute of Cotton Research, Chinese Academy of Agricultural Science, Anyang, China. liufcri@163.com.

Baohong Zhang (B)

State Key Laboratory of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, China. zhangb@ecu.edu.
Department of Biology, East Carolina University, Greenville, NC, 27858, USA. zhangb@ecu.edu.

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