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A Cotton Gbvdr5 Gene Encoding a Leucine-Rich-Repeat Receptor-Like Protein Confers Resistance to Verticillium dahliae in Transgenic Arabidopsis and Upland Cotton

Abstract

Leucine-rich-repeat receptor-like proteins (eLRR-RLPs) play significant roles in plant defense against pathogens and in plant development. Several eLRR-RLP genes such as Ve1, Gbve, and Gbve1 have been reported to confer resistance to Verticillium dahliae. Gbvdr5, a newly discovered RLP gene from V. dahliae-resistant island cotton cultivar H7124, has a short tail as Ve1. There is a cytosine deletion in Gbvdr5 homologous genes at nucleotide position 2765, which is downstream from the initiation codon in all susceptible upland cotton cultivars analyzed. This deletion was found to cause premature termination of the protein, creating a 937 aa product, but the Gbvdr5 protein had the full 1,077 aa. Transient expression analyses indicated that Gbvdr5 is localized on the plasma membrane. Quantitative polymerase chain reaction analysis revealed that the Gbvdr5 gene was activated by SA, MeJA, ABA, and ETH, and it was induced by V. dahliae isolates V991 and DF-CQ-2 in H7124, whereas was unchanged or repressed in susceptible upland cotton Simian 3. Gbvdr5-promoter-driven GUS activity was found mostly in the root tips and stem growing points of transgenic Arabidopsis. Silencing of Gbvdr5 in Verticillium-wilt-resistant cotton H7124 compromised cotton resistance to V. dahliae isolates V991 and BP2. The resistance was verified by transforming the Gbvdr5 gene into Arabidopsis and upland cotton through Agrobacterium-mediated transformation. Overexpression of the Gbvdr5 gene endowed transgenic Arabidopsis with resistance to defoliating isolate V991 and non-defoliating isolate BP2, but it had no effect on either DF-CQ-2 or JR2 of V. dahliae. The transformed cotton also had confirmed resistance to V991 and BP2. More callose deposition, more expression of the defense-related genes PR1 and PR5, and HR-mimic cell death were observed in the transgenic Arabidopsis when inoculated with V. dahliae. This demonstrated that Verticillium–plant interactions may involve some specific ways of recognizing V. dahliae and Gbvdr5 may be a suitable candidate gene for breeding Verticillium-wilt-resistant cotton lines.

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Abbreviations

SA:

Salicylic acid

MeJA:

Methyl jasmonate

ETH:

Ethylene

ABA:

Abscise acid

GUS:

Beta-glucuronidase

RLP:

Receptor-like proteins

HR:

Hypersensitive response

PR:

Pathogen-related

LRR:

Leucine-rich-repeat

Ve:

Verticillium genus

References

  1. Amyotte SG, Tan X, Pennerman K, Jimenez-Gasco Mdel M, Klosterman SJ, Ma LJ, Dobinson KF, Veronese P (2012) Transposable elements in phytopathogenic Verticillium spp.: insights into genome evolution and inter- and intra-specific diversification. BMC Genomics 13:314

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  2. Beckman C, Mueller W, Tessier B, Harrison N (1982) Recognition and callose deposition in response to vascular infection in Fusarium wilt-resistant or susceptible tomato plants. Physiol Plant Pathol 20:1–10

    Article  Google Scholar 

  3. Bollig K, Specht A, Zahn M, Horst WJ (2013) Sulphur supply impairs spread of Verticillium dahliae in tomato. Eur J Plant Pathol 135:81–96

    CAS  Article  Google Scholar 

  4. Chai Y, Zhao L, Liao Z, Sun X, Zuo K, Zhang L, Wang S, Tang K (2003) Molecular cloning of a potential Verticillium dahliae resistance gene SlVe1 with multi-site polyadenylation from Solanum licopersicoides. DNA Seq 14:375–384

  5. Chakrabarti A, Panter SN, Harrison K, Jones JD, Jones DA (2009) Regions of the Cf-9B disease resistance protein able to cause spontaneous necrosis in Nicotiana benthamia lie within the region controlling pathogen recognition in tomato. Mol Plant Microbe Interact 22:1214–1226

    CAS  PubMed  Article  Google Scholar 

  6. Daayf F, Nicole M, Boher B, Pando A, Geiger JP (1997) Early vascular defense reactions of cotton roots infected with a defoliating mutant strain of Verticillium dahliae. Eur J Plant Pathol 103:125–136

    CAS  Article  Google Scholar 

  7. de Jonge R, van Esse HP, 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. Proc Natl Acad Sci U S A 109:5110–5115

    PubMed Central  PubMed  Article  Google Scholar 

  8. Denance N, Ranocha P, Oria N, Barlet X, Riviere MP, Yadeta KA, Hoffmann L, Perreau F, Clement G, Maia-Grondard A, van den Berg GC, Savelli B, Fournier S, Aubert Y, Pelletier S, Thomma BP, Molina A, Jouanin L, Marco Y, Goffner D (2013) Arabidopsis wat1 (walls are thin1)-mediated resistance to the bacterial vascular pathogen, Ralstonia solanacearum, is accompanied by cross-regulation of salicylic acid and tryptophan metabolism. Plant J 73:225–239

    CAS  PubMed  Article  Google Scholar 

  9. Diaz I, Vicente-Carbajosa J, Abraham Z, Martínez M, Moneda IL, Carbonero P (2002) The GAMYB protein from barley interacts with the DOF transcription factor BPBF and activates endosperm-specific genes during seed development. Plant J 29:453–464

    CAS  PubMed  Article  Google Scholar 

  10. Dixon MS, Hatzixanthis K, Jones DA, Harrison K, Jones JD (1998) The tomato Cf-5 disease resistance gene and six homologs show pronounced allelic variation in leucine-rich repeat copy number. Plant Cell Online 10:1915–1925

    CAS  Article  Google Scholar 

  11. Dixon MS, Jones DA, Keddie JS, Thomas CM, Harrison K, Jones JD (1996) The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84:451–459

    CAS  PubMed  Article  Google Scholar 

  12. Durel C, Parisi L, Laurens F, Van de Weg W, Liebhard R, Jourjon M (2003) Genetic dissection of partial resistance to race 6 of Venturia inaequalis in apple. Genome 46:224–234

    CAS  PubMed  Article  Google Scholar 

  13. Ellinger D, Naumann M, Falter C, Zwikowics C, Jamrow T, Manisseri C, Somerville SC, Voigt CA (2013) Elevated early callose deposition results in complete penetration resistance to powdery mildew in Arabidopsis. Plant Physiol 161:1433–1444

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  14. 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 Physiol 156:2255–2265

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  15. Fradin EF, Zhang Z, Juarez Ayala JC, Castroverde CD, Nazar RN, Robb J, Liu CM, Thomma BP (2009) Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiol 150:320–332

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  16. Fritz-Laylin LK, Krishnamurthy N, Tör M, Sjölander KV, Jones JD (2005) Phylogenomic analysis of the receptor-like proteins of rice and Arabidopsis. Plant Physiol 138:611–623

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  17. Guérin F, Gladieux P, Cam BL (2007) Origin and colonization history of newly virulent strains of the phytopathogenic fungus Venturia inaequalis. Fungal Genet Biol 44:284–292

    PubMed  Article  Google Scholar 

  18. Guo WZ, Cai CP, Wang CB, Han ZG, Song XL, Wang K, Niu XW, Wang C, Lu KY, Shi B, Zhang TZ (2007) A microsatellite-based, gene-rich linkage map reveals genome structure, function and evolution in Gossypium. Genetics 176(1):527–541

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  19. Hartmann U, Sagasser M, Mehrtens F, Stracke R, Weisshaar B (2005) Differential combinatorial interactions of cis-acting elements recognized by R2R3-MYB, BZIP, and BHLH factors control light-responsive and tissue-specific activation of phenylpropanoid biosynthesis genes. Plant Mol Biol 57:155–171

    CAS  PubMed  Article  Google Scholar 

  20. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    CAS  PubMed Central  PubMed  Google Scholar 

  21. Jian GL, Ma C, Zheng CL, Zou YF (2003) Advances in cotton breeding for resistance to Fusarium and Verticillium wilt in the last fifty years in China. Agric Sci China 2:280–288

    Google Scholar 

  22. Jones DA, Jones J (1997) The role of leucine-rich repeat proteins in plant defences. Adv Bot Res 24:89–167

    Article  Google Scholar 

  23. Jones DA, Thomas CM, Hammond-Kosack KE, Balint-Kurti PJ, Jones J (1994) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266:789–793

    CAS  PubMed  Article  Google Scholar 

  24. Joosten M, De Wit P (1999) The tomato-Cladosporium fulvum interaction: a versatile experimental system to study plant–pathogen interactions. Annu Rev Phytopathol 37:335–367

    CAS  PubMed  Article  Google Scholar 

  25. Kamiya N, Nagasaki H, Morikami A, Sato Y, Matsuoka M (2003) Isolation and characterization of a rice WUSCHEL‐type homeobox gene that is specifically expressed in the central cells of a quiescent center in the root apical meristem. Plant J 35:429–441

    CAS  PubMed  Article  Google Scholar 

  26. Kawchuk LM, Hachey J, Lynch DR, Kulcsar F, van Rooijen G, Waterer DR, Robertson A, Kokko E, Byers R, Howard RJ, Fischer R, Prufer D (2001) Tomato Ve disease resistance genes encode cell surface-like receptors. Proc Natl Acad Sci U S A 98:6511–6515

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  27. Kruijt M, Brandwagt BF, de Wit PJ (2004) Rearrangements in the Cf-9 disease resistance gene cluster of wild tomato have resulted in three genes that mediate Avr9 responsiveness. Genetics 168:1655–1663

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  28. Kruijt M, De Kock MJ, De Wit PJ (2005) Receptor-like proteins involved in plant disease resistance. Mol Plant Pathol 6:85–97

    CAS  PubMed  Article  Google Scholar 

  29. Laloi C, Mestres-Ortega D, Marco Y, Meyer Y, Reichheld JP (2004) The Arabidopsis cytosolic thioredoxin h5 gene induction by oxidative stress and its W-box-mediated response to pathogen elicitor. Plant Physiol 134:1006–1016

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  30. Luo H, Song F, Goodman R, Zheng Z (2005) Up-regulation of OsBIHD1, a rice gene encoding BELL homeodomain transcriptional factor, in disease resistance responses. Plant Biol 7:459–468

    CAS  PubMed  Article  Google Scholar 

  31. Maruyama-Nakashita A, Nakamura Y, Watanabe-Takahashi A, Inoue E, Yamaya T, Takahashi H (2005) Identification of a novel cis-acting element conferring sulfur deficiency response in Arabidopsis roots. Plant J 42:305–314

    CAS  PubMed  Article  Google Scholar 

  32. Nakamura M, Tsunoda T, Obokata J (2002) Photosynthesis nuclear genes generally lack TATA-boxes: a tobacco photosystem I gene responds to light through an initiator. Plant J 29:1–10

    CAS  PubMed  Article  Google Scholar 

  33. Ochsenbein C, Przybyla D, Danon A, Landgraf F, Göbel C, Imboden A, Feussner I, Apel K (2006) The role of EDS1 (enhanced disease susceptibility) during singlet oxygen-mediated stress responses of Arabidopsis. Plant J 47:445–456

    CAS  PubMed  Article  Google Scholar 

  34. Oldroyd GE, Staskawicz BJ (1998) Genetically engineered broad-spectrum disease resistance in tomato. Proc Natl Acad Sci U S A 95:10300–10305

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  35. Pantelides IS, Tjamos SE, Paplomatas EJ (2010) Ethylene perception via ETR1 is required in Arabidopsis infection by Verticillium dahliae. Mol Plant Pathol 11:191–202

    CAS  PubMed  Article  Google Scholar 

  36. Park CJ, Ronald PC (2012) Cleavage and nuclear localization of the rice XA21 immune receptor. Nat Commun 3:920

    PubMed Central  PubMed  Article  Google Scholar 

  37. Porebski S, Bailey LG, Baum BR (1997) Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Mol Biol Report 15:8–15

    CAS  Article  Google Scholar 

  38. Qi JS, Li HF (2006) A new detection method of wilting induction by phytotoxin from V. dahliae on cotton through leaf pricking and spreading. Cotton Sci 18(4):228–232

    Google Scholar 

  39. Rechsteiner M, Rogers SW (1996) PEST sequences and regulation by proteolysis. Trends Biochem Sci 21:267–271

    CAS  PubMed  Article  Google Scholar 

  40. Robatzek S, Chinchilla D, Boller T (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev 20:537–542

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  41. Ron M, Avni A (2004) The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell Online 16:1604–1615

    CAS  Article  Google Scholar 

  42. Ruthardt N, Fischer R, Emans N, Kawchuk LM (2007) Tomato protein of the resistance gene Ve2 to Verticillium wilt [Verticillium spp.] is located in the endoplasmic reticulum. Can J Plant Pathol 29:3–8

    CAS  Article  Google Scholar 

  43. Stokes TL, Kunkel BN, Richards EJ (2002) Epigenetic variation in Arabidopsis disease resistance. Genes Dev 16:171–182

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  44. Sutoh K, Yamauchi D (2003) Two cis-acting elements necessary and sufficient for gibberellin-upregulated proteinase expression in rice seeds. Plant J 34:635–645

    CAS  PubMed  Article  Google Scholar 

  45. Takken FL, Thomas CM, Joosten MH, Golstein C, Westerink N, Hille J, Nijkamp HJJ, De Wit PJ, Jones JD (1999) A second gene at the tomato Cf-4 locus confers resistance to Cladosporium fulvum through recognition of a novel avirulence determinant. Plant J 20:279–288

    CAS  PubMed  Article  Google Scholar 

  46. Tang X, Xie M, Kim YJ, Zhou J, Klessig DF, Martin GB (1999) Overexpression of Pto activates defense responses and confers broad resistance. Plant Cell 11:15–29

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  47. Terzaghi WB, Cashmore AR (1995) Light-regulated transcription. Annu Rev Plant Biol 46:445–474

    CAS  Article  Google Scholar 

  48. Thomas CM, Jones DA, Parniske M, Harrison K, Balint-Kurti PJ, Hatzixanthis K, Jones J (1997) Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell Online 9:2209–2224

    CAS  Article  Google Scholar 

  49. 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. Mol Plant-Microbe Interact 18:555–561

    CAS  PubMed  Article  Google Scholar 

  50. Torres MA, Jones JD, Dangl JL (2005) Pathogen-induced, NADPH oxidase–derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat Genet 37:1130–1134

    CAS  PubMed  Article  Google Scholar 

  51. Umbeck P, Johnson G, Barton K, Swain W (1987) Genetically transformed cotton (Gossypium hirsutum L.) plants. Nat Biotechnol 5:263–266

    CAS  Article  Google Scholar 

  52. Van der Hoorn RA, Roth R, De Wit PJ (2001) Identification of distinct specificity determinants in resistance protein Cf-4 allows construction of a Cf-9 mutant that confers recognition of avirulence protein AVR4. Plant Cell Online 13:273–285

    Article  Google Scholar 

  53. Vining K, Davis T (2009) Isolation of a Ve homolog, mVe1, and its relationship to Verticillium wilt resistance in Mentha longifolia (L.) Huds. Mol Gen Genomics 282:173–184

    CAS  Article  Google Scholar 

  54. Wang D, Weaver ND, Kesarwani M, Dong X (2005) Induction of protein secretory pathway is required for systemic acquired resistance. Science 308:1036–1040

    CAS  PubMed  Article  Google Scholar 

  55. 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 11:4296–4309

    CAS  PubMed  Article  Google Scholar 

  56. Wang G, Ellendorff U, Kemp B, Mansfield JW, Forsyth A, Mitchell K, Bastas K, Liu CM, Woods-Tör A, Zipfel C (2008) A genome-wide functional investigation into the roles of receptor-like proteins in Arabidopsis. Plant Physiol 147:503–517

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  57. Wang G, Fiers M, Ellendorff U, Wang Z, de Wit PJ, Angenent GC, Thomma BP (2010) The diverse roles of extracellular leucine-rich repeat-containing receptor-like proteins in plants. Crit Rev Plant Sci 29:285–299

    CAS  Article  Google Scholar 

  58. Wang, P., Ning, Z.Y., Lin, L., Chen, H., Mei, H.X., Zhao, J., Liu, B.L., Zhang, X., Guo, W.Z. and Zhang, T.Z. Genetic dissection of tetraploid cotton resistant to Verticillium wilt using interspecific chromosome segment introgression lines. The Crop Journal (2014) (in press)

  59. Xu L, Zhu LF, Tu LL, Liu LL, Yuan DJ, Jin L, Long L, Zhang XL (2011) 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. J Exp Bot 62:5607–5621

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  60. Yu DQ, Chen CH, Chen ZX (2001) Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression. Plant Cell Online 13:1527–1540

    CAS  Article  Google Scholar 

  61. Zhang BL, Yang YW, Chen TZ, Yu WG, Liu TL, Li HJ, Fan XH, Ren YZ, Shen DY, Liu L, Dou DL, Chang YH (2012a) Island cotton Gbve1 gene encoding a receptor-like protein confers resistance to both defoliating and non-defoliating isolates of Verticillium dahliae. PLoS One 7:e51091

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  62. Zhang TZ, Zhou ZH, Min LF (2000) Inheritance of cotton resistance to Verticillium dahliae and strategies to develop resistant or tolerant cultivars. Acta Agron Sin 26:673–680

    Google Scholar 

  63. Zhang WW, Jiang TF, Cui X, Qi FJ, Jian GL (2012b) Colonization in cotton plants by a green fluorescent protein labelled strain of Verticillium dahliae. Eur J Plant Pathol 135:867–876

    Article  Google Scholar 

  64. Zhang Y, Wang XF, Yang S, Chi J, Zhang GY, Ma ZY (2011) Cloning and characterization of a Verticillium wilt resistance gene from Gossypium barbadense and functional analysis in Arabidopsis thaliana. Plant Cell Rep 30:2085–2096

    CAS  PubMed  Article  Google Scholar 

  65. Zhang Z, Fradin E, de Jonge R, van Esse HP, Smit P, Liu C-M, Thomma BP (2013a) Optimized agroinfiltration and virus-induced gene silencing to study Ve1-mediated Verticillium resistance in tobacco. Mol Plant-Microbe Interact 26:182–190

    CAS  PubMed  Article  Google Scholar 

  66. Zhang, Z., van Esse, H.P., van Damme, M., Fradin, E.F., Liu, C.M. and Thomma, B.P. Ve1-mediated resistance against Verticillium does not involve a hypersensitive response in Arabidopsis. Mol Plant Pathol (2013b)

  67. Zhao YL, Wang HM, Chen W, Li YH (2014) Genetic structure, linkage disequilibrium and association mapping of Verticillium wilt resistance in elite cotton (Gossypium hirsutum L.) germplasm population. PLoS One 9(1):e86308

    PubMed Central  PubMed  Article  Google Scholar 

  68. Zhu HQ, Feng ZL, Li ZF, Zhao LH, Shi YQ (2010) Verticillium wilt identification of cotton varieties (lines) root dipped with quantitatived microbial in bottomless paper pot filled with vermiculite. China Cotton 37(12):15–17

    Google Scholar 

  69. Zuo KJ, Qin J, Zhao JY, Ling H, Zhang LD, Cao YF, Tang KX (2007) Over-expression GbERF2 transcription factor in tobacco enhances brown spots disease resistance by activating expression of downstream genes. Gene 391:80–90

    CAS  PubMed  Article  Google Scholar 

  70. 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. Mol Biol 39:191–199

    CAS  Article  Google Scholar 

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Acknowledgments

This work was supported by the Natural Science Foundation of Jiangsu Province (BK20131336), National Natural Science Foundation of China (no. 31371930), Independent Innovation of Agricultural Sciences in Jiangsu Province (no. cx (12) 5022), and National Science and Technology Major Project for Transgenic Breeding (no. 2014ZX08005-001B).

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Correspondence to Baolong Zhang or Din-Pow Ma.

Additional information

Yuwen Yang and Xitie Ling have equal contribution.

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Figure S1
figure10

Primary structures of Gbvdr5 compared with Gbve1, Gbve, ve1, and ve2. (JPEG 6735 kb)

Figure S2
figure11

The promoter sequence of Gbvdr5 and Ghvdr5. A; the promoter sequence of Gbvdr5. The box indicated the start codon. B, Alignment of Gbvdr5 with Ghvdr5 derived from Yumian 1. (GIF 107 kb)

Figure S3
figure12

The transformation of cotton hypocotyls with Agrobacterium. (A) Cotton hypocotyl explants for Agrobacterium transformation (B). Kanamycin-resistant calli on kanamycin-containing selective culture medium (C). Kanamycin-resistant calli on proliferation medium without kanamycin (D). Embryogenesis: embryogenic calli and globular embryos (E). Embryogenesis: embryogenic calli, globular embryos, and torpedo embryos (F). Embryogenesis: globular embryos and cotyledonary embryos (G). Regenerated plantlets in medium (H). Transgenic plants transferred in pots (I). Transgenic plants in greenhouse (JPEG 309 kb)

Figure S4
figure13

Standard curve and PCR efficiency of real-time PCR primers. A: Standard curve of Gbvdr5 real-time PCR primer; B: standard curve of internal gene UBQ14. (GIF 29 kb)

High-resolution image (TIFF 9093 kb)

High-resolution image (TIFF 2823 kb)

Table S1

The characterized domains in the promoter of Gbvdr5 gene (DOC 55 kb)

Table S2

The primers used in this study (DOC 67 kb)

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Yang, Y., Ling, X., Chen, T. et al. A Cotton Gbvdr5 Gene Encoding a Leucine-Rich-Repeat Receptor-Like Protein Confers Resistance to Verticillium dahliae in Transgenic Arabidopsis and Upland Cotton. Plant Mol Biol Rep 33, 987–1001 (2015). https://doi.org/10.1007/s11105-014-0810-5

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Keywords

  • Gossypium
  • Gbvdr5
  • Verticillium dahliae
  • Resistance
  • Genetic transformation