Abstract
Nonpathogenic strain ARK-1 of Rhizobium vitis has antagonistic activity against a tumorigenic (Ti) strain of R. vitis and works as a biocontrol agent, but the temporal dynamics of the bacterial colonization in plants needs to be understood. Here we showed that the incidence of galls induced by Ti strain was reduced to about 60% when both upper and lower positions on the grapevine stem were inoculated with ARK-1 3 cm from the site that was inoculated with Ti 5 days later. A bacterial cell detection assay in the grapevine tissue revealed that ARK-1 moved at least 3 cm in 5 days.
References
Burr TJ, Otten L (1999) Crown gall of grape: biology and disease management. Annu Rev Phytopathol 37:53–80
Burr TJ, Reid CL (1994) Biological control of grape crown gall with non-tumorigenic Agrobacterium vitis strain F2/5. Am J Enol Vitic 45:213–219
Burr TJ, Bazzi C, Süle S, Otten L (1998) Crown gall of grape: biology of Agrobacterium vitis and the development of disease control strategies. Plant Dis 82:1288–1297
Chen F, Guo YB, Wang JH, Li JY, Wang HM (2007) Biological control of grape crown gall by Rahnella aquatilis HX2. Plant Dis 91:957–963
Chilton MD, Drummond MH, Merlo DJ, Sciaky D, Montoya AL, Gordon MP, Nester EW (1977) Stable incorporation of plasmid DNA into higher plant cells: the molecular basis of crown gall tumorigenesis. Cell 11:263–271
Gelvin SB (2012) Traversing the cell: Agrobacterium T-DNA’s journey to the host genome. Front Plant Sci 3:52
Gohlke J, Deeken R (2014) Plant responses to Agrobacterium tumefaciens and crown gall development. Front Plant Sci 5:155
Htay K, Kerr A (1974) Biological control of crown gall: seed and root inoculation. J Appl Bacteriol 37:525–530
Johnson KL, Cronin H, Reid CL, Burr TJ (2016) Distribution of Agrobacterium vitis in grapevines and its relevance to pathogen elimination. Plant Dis 100:791–796
Kawaguchi A (2013) Biological control of crown gall on grapevine and root colonization by nonpathogenic Rhizobium vitis strain ARK-1. Microbes Environ 28:306–311
Kawaguchi A (2014) Reduction in pathogen populations at grapevine wound sites is associated with the mechanism underlying the biological control of crown gall by Rhizobium vitis strain ARK-1. Microbes Environ 29:296–302
Kawaguchi A (2015) Biological control agent Agrobacterium vitis strain ARK-1 suppresses expression of the virD2 and virE2 genes in tumorigenic A. vitis. Euro J Plant Pathol 143:789–799
Kawaguchi A, Inoue K (2012) New antagonistic strains of non-pathogenic Agrobacterium vitis to control grapevine crown gall. J Phytopathol 160:509–518
Kawaguchi A, Inoue K, Nasu H (2005) Inhibition of crown gall formation by Agrobacterium radiobacter biovar 3 strains isolated from grapevine. J Gen Plant Pathol 71:422–430
Kawaguchi A, Inoue K, Nasu H (2007) Biological control of grapevine crown gall by nonpathogenic Agrobacterium vitis strain VAR03-1. J Gen Plant Pathol 73:133–138
Kawaguchi A, Inoue K, Ichinose Y (2008) Biological control of crown gall of grapevine, rose, and tomato by nonpathogenic Agrobacterium vitis strain VAR03-1. Phytopathology 98:1218–1225
Kawaguchi A, Kondo K, Inoue K (2012) Biological control of apple crown gall by nonpathogenic Rhizobium vitis strain VAR03-1. J Gen Plant Pathol 78:287–293
Kawaguchi A, Inoue K, Tanina K (2015) Evaluation of the nonpathogenic Agrobacterium vitis strain ARK-1 for crown gall control in diverse plant species. Plant Dis 99:409–414
Kawaguchi A, Inoue K, Tanina K, Nita M (2017) Biological control for grapevine crown gall using nonpathogenic Rhizobium vitis strain ARK-1. Proc Jpn Acad Ser. B Phys Biol Sci 93:547–560
Kawaguchi A, Nita M, Ishii T, Watanabe M, Noutoshi Y (2019) Biological control agent Rhizobium (=Agrobacterium) vitis strain ARK-1 suppresses expression of the essential and non-essential vir genes of tumorigenic R. vitis. BMC Res Notes 12:1–6
Kerr A (1980) Biological control of crown gall through production of agrocin 84. Plant Dis 64:24–30
Kerr A, Bullard G (2020) Biocontrol of crown gall by Rhizobium rhizogenes: challenges in biopesticide commercialisation. Agronomy 10:1126
Kerr A, Htay K (1974) Biological control of crown gall through bacteriocin production. Physiol Plant Pathol 4:37–44
New PB, Kerr A (1972) Biological control of grown gall: field measurements and glasshouse experiments. J Appl Bacteriol 35:279–287
Pitzschke A, Hirt H (2010) New insights into an old story: Agrobacterium-induced tumour formation in plants by plant transformation. EMBO J 29:1021–1032
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Website www.R-project.org
Reader JS, Ordoukhanian PT, Kim JG, de Crécy-Lagard V, Hwang I, Farrand S, Schimmel P (2005) Major biocontrol of plant tumors targets tRNA synthetase. Science 309:1533
Saito K, Watanabe M, Matsui H, Yamamoto M, Y. Ichinose Y, Toyoda K, Kawaguchi A, Noutoshi Y, (2018) Characterization of the suppressive effects of the biological control strain VAR03-1 of Rhizobium vitis on the virulence of tumorigenic R. vitis. J Gen Plant Pathol 84:58–64
Staphorst JL, van Zyl FGH, Strijdom BW, Groenewold ZE (1985) Agrocin-producing pathogenic and nonpathogenic biotype-3 strains of Agrobacterium tumefaciens active against biotype-3 pathogens. Curr Microbiol 12:45–52
Tarbah F, Goodman RN (1987) Systemic spread of Agrobacterium tumefaciens biovar 3 in the vascular system of grapes. Phytopathology 77:915–920
Wächter R, Langhans M, Aloni R, Götz S, Weilmünster A, Koops A, Temguia L, Mistrik I, Pavlovkin J, Rascher U, Schwalm K, Koch KE, Ullrich CI (2003) Vascularization, high-volume solution flow, and localized roles for enzymes of sucrose metabolism during tumorigenesis by Agrobacterium tumefaciens. Plant Physiol 133:1024–1037
Wang HM, Wang HX, Ng TB, Li JY (2003) Purification and characterization of an antibacterial compound produced by Agrobacterium vitis strain E26 with activity against A. tumefaciens. Plant Pathol 52:134–139
Young JM, Kuykendall LD, Martínez-Romero E, Kerr A, Sawada H (2001) A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and Allorhizobium undicola de Lajudie et al. 1998 as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis. Int J Syst Evol Microbiol 51:89–103
Acknowledgements
This research was supported by KAKENHI Grant 17H03778 and 20K20572 from the Ministry of Education, Culture, Sports, Science and Technology of Japan to A. Kawaguchi and Y. Noutoshi. We are grateful to Dr. K. Inoue (Research Institute for Agriculture, Okayama Prefectural Technology Center for Agriculture, Forestry and Fisheries) who gave us much useful advice.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing financial interests.
Ethical standards
This article does not contain any studies with human participants or animals performed by the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
10327_2021_1043_MOESM3_ESM.pptx
Supplementary Fig. S1. The four treatments (i ii, iii, and iv) used to investigate gall suppression activity of ARK-1 at a distance from the inoculation site. (i) Sterile distilled water was pipetted into both upper and lower sites, and Ti strain was pipetted into the middle site. (ii) ARK-1 was pipetted into both upper and lower sites, and Ti strain was pipetted into the middle site. (iii) Sterile distilled water was pipetted into the upper and lower sites, and 5 days later (5 dai), Ti strain was pipetted into the middle site. (iv) ARK-1 was pipetted into the upper and lower sites, and 5 days later, Ti strain was pipetted into the middle site. Galls were counted and measured 5 months later. (PPTX 82 KB)
Rights and permissions
About this article
Cite this article
Kawaguchi, A., Noutoshi, Y. Migration of biological control agent Rhizobium vitis strain ARK-1 in grapevine stems and inhibition of galls caused by tumorigenic strain of R. vitis. J Gen Plant Pathol 88, 63–68 (2022). https://doi.org/10.1007/s10327-021-01043-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10327-021-01043-4