MPMI PhytoFrontiers Phytobiomes all journals
RESEARCH

DNA-Based Quantification of Fusarium oxysporum f. sp. vasinfectum in Environmental Soils to Describe Spatial Variation in Inoculum Density

    Affiliations
    Authors and Affiliations
    • Roy L. Davis II
    • Thomas Isakeit
    • Thomas M. Chappell
    1. Department of Plant Pathology and Microbiology, Texas A&M University, College Station, TX 77843

    Fusarium wilt of cotton, caused by the soilborne fungal pathogen Fusarium oxysporum f. sp. vasinfectum (FOV), occurs in regions of the United States where cotton (Gossypium spp.) is grown. Race 4 of this pathogen (FOV4) is especially aggressive, and does not require the co-occurrence of the root knot nematode (Meloidogyne incognita) to infect cotton. Its sudden appearance in far-west Texas in 2016 after many years of being restricted to California is of great concern, as is the threat of its continued spread through the cotton-producing regions of the United States. The aim of this research was to analyze the spatial variability of FOV4 inoculum density in the location where FOV4 is locally emerging, using quantitative and droplet digital PCR methods. Soil samples collected from a field with known FOV4 incidence in Fabens, Texas, were analyzed. Appreciable variation in inoculum density was found to occur at spatial scales smaller than the size of plots involved in cultivar trial research, and was spatially autocorrelated (Moran’s I, Z = 17.73, P < 0.0001). These findings indicate that, for cultivar trials, accounting for the spatial distribution of inoculum, either by directly quantifying it or through the use of densely distributed calibration checks, is important to the interpretation of results.

    Literature Cited

    • Armstrong, G. M., and Armstrong, J. K. 1960. American, Egyptian, and Indian cotton-wilt Fusaria: Their pathogenicity and relationship to other wilt Fusaria. U.S. Dep. Agric. Tech. Bull. 1219:1-19. Google Scholar
    • Bell, A. A., Gu, A., Olvey, J., Wagner, T. A., Tashpulatov, J. J., Prom, S., Quintana, J., Nichols, R. L., and Liu, J. 2019. Detection and characterization of Fusarium oxysporum f. sp. vasinfectum VCG0114 (race 4) isolates of diverse geographical origin. Plant Dis. 103:1998-2009. https://doi.org/10.1094/PDIS-09-18-1624-RE Link, ISIGoogle Scholar
    • Bennett, R. S. 2012. Survival of Fusarium oxysporum f. sp. vasinfectum chlamydospores under solarization temperatures. Plant Dis. 96:1564-1568. https://doi.org/10.1094/PDIS-09-11-0812-RE Link, ISIGoogle Scholar
    • Bennett, R. S., and Colyer, P. D. 2010. Dry heat and hot water treatments for disinfesting cottonseed of Fusarium oxysporum f. sp. vasinfectum. Plant Dis. 94:1469-1475. https://doi.org/10.1094/PDIS-01-10-0052 Link, ISIGoogle Scholar
    • Bennett, R. S., Hutmacher, R. B., and Davis, R. M. 2008. Seed transmission of Fusarium oxysporum f. sp. vasinfectum race 4 in California. J. Cotton Sci. 12:160-164. Google Scholar
    • Bennett, R. S., Spurgeon, D. W., DeTar, W. R., Gerik, J. S., Hutmacher, R. B., and Hanson, B. D. 2011. Efficacy of four soil treatments against Fusarium oxysporum f. sp. vasinfectum race 4 on cotton. Plant Dis. 95:967-976. https://doi.org/10.1094/PDIS-09-10-0696 Link, ISIGoogle Scholar
    • Chawla, S., Woodward, J. E., Wheeler, T. A., and Wright, R. J. 2012. Effect of Fusarium oxysporum f. sp. vasinfectum inoculum density, Meloidogyne incognita and cotton cultivar on Fusarium wilt development. Tex. J. Agric. Nat. Resour. 25:45-56. Google Scholar
    • Cianchetta, A. N., Allen, T. W., Hutmacher, R. B., Kemerait, R. C., Kirkpatrick, T. L., Lawrence, G. W., Lawrence, K. S., Mueller, J. D., Nichols, R. L., Olsen, M. W., Overstreet, C., Woodward, J. E., and Davis, R. M. 2015. Survey of Fusarium oxysporum f. sp. vasinfectum in the United States. J. Cotton Sci. 19:328-336. ISIGoogle Scholar
    • Cox, K. L., Jr., Babilonia, K., Wheeler, T. A., He, P., and Shan, L. 2019. Return of old foes – Recurrence of bacterial blight and Fusarium wilt of cotton. Curr. Opin. Plant Biol. 50:95-103. https://doi.org/10.1016/j.pbi.2019.03.012 Crossref, ISIGoogle Scholar
    • Crutcher, F. K., Doan, H. K., Bell, A. A., Davis, R. M., Stipanovic, R. D., Nichols, R. L., and Liu, J. 2016. Evaluation of methods to detect the cotton wilt pathogen Fusarium oxysporum f. sp. vasinfectum race 4. Eur. J. Plant Pathol. 144:225-230. https://doi.org/10.1007/s10658-015-0763-z Crossref, ISIGoogle Scholar
    • Davis, R. M., Colyer, P. D., Rothrock, C. S., and Kochman, J. K. 2006. Fusarium wilt of cotton: Population diversity and implication for management. Plant Dis. 90:692-703. https://doi.org/10.1094/PD-90-0692 Link, ISIGoogle Scholar
    • DeVay, J. E., Gutierrez, A. P., Pullman, G. S., Wakeman, R. J., Garber, R. H., Jeffers, D. P., Smith, S. N., Goodell, P. B., and Roberts, P. A. 1997. Inoculum densities of Fusarium oxysporum f. sp. vasinfectum and Meloidogyne incognita in relation to the development of Fusarium wilt and the phenology of cotton plants (Gossypium hirsutum). Phytopathology 87:341-346. https://doi.org/10.1094/PHYTO.1997.87.3.341 Link, ISIGoogle Scholar
    • Diaz, J., Garcia, J., Lara, C., Hutmacher, R. B., Ulloa, M., Nichols, R. L., and Ellis, M. 2021. Characterization of current Fusarium oxysporum f. sp. vasinfectum isolates from cotton in the San Joaquin Valley of California and Lower Valley El Paso Texas. Plant Dis. 105:1898-1911. https://doi.org/10.1094/PDIS-05-20-1038-RE Link, ISIGoogle Scholar
    • Doan, H. K., Zhang, S., and Davis, R. M. 2014. Development and evaluation of AmplifyRP Accerer8 diagnostic assay for the detection of Fusarium oxysporum f. sp. vasinfectum race 4 in cotton. Plant Health Prog. 15:48-52. https://doi.org/10.1094/PHP-RS-13-0115 LinkGoogle Scholar
    • Gordon, T. R. 2017. Fusarium oxysporum and the Fusarium wilt syndrome. Annu. Rev. Phytopathol. 55:23-39. https://doi.org/10.1146/annurev-phyto-080615-095919 Crossref, ISIGoogle Scholar
    • Halpern, H. C., Bell, A. A., Wagner, T. A., Liu, J., Nichols, R. L., Olvey, J., Woodward, J. E., Sanogo, S., Jones, C. A., Chan, C. T., and Brewer, M. T. 2017. First report of Fusarium wilt of cotton caused by Fusarium oxysporum f. sp. vasinfectum race 4 in Texas, U.S.A. Plant Dis. 102:446. https://doi.org/10.1094/PDIS-07-17-1084-PDN LinkGoogle Scholar
    • Hao, J. J., Yang, M. E., and Davis, R. M. 2009. Effect of soil inoculum density of Fusarium oxysporum f. sp. vasinfectum race 4 on disease development in cotton. Plant Dis. 93:1324-1328. https://doi.org/10.1094/PDIS-93-12-1324 Link, ISIGoogle Scholar
    • Hindson, B. J., Ness, K. D., Masquelier, D. A., Belgrader, P., Heredia, N. J., Makarewicz, A. J., Bright, I. J., Lucero, M. Y., Hiddessen, A. L., Legler, T. C., Kitano, T. K., Hodel, M. R., Petersen, J. F., Wyatt, P. W., Steenblock, E. R., Shah, P. H., Bousse, L. J., Troup, C. B., Mellen, J. C., Wittmann, D. K., Erndt, N. G., Cauley, T. H., Koehler, R. T., So, A. P., Dube, S., Rose, K. A., Montesclaros, L., Wang, S.-L., Stumbo, D. P., Hodges, S. P., Romine, S., Milanovich, F. P., White, H. E., Regan, J. F., Karlin-Neumann, G. A., Hindson, C. M., Saxonov, S., and Colston, B. W. 2011. High-throughput droplet digital PCR system for absolute quantitation of DNA copy number. Anal. Chem. 83:8604-8610. https://doi.org/10.1021/ac202028g Crossref, ISIGoogle Scholar
    • Hutmacher, R. B., Ulloa, M., Wright, S. D., Hutmacher, R. B., Ulloa, M., Wright, S. D., Campbell, B. T., Percy, R., Wallace, T., Myers, G., Bourland, F., Weaver, D., Chee, P., Thaxton, P., Zhang, J.-F., Smith, W., Dever, J., Kuraparthy, V., Bowman, D., Jones, D., and Burke, J. 2013. Elite upland cotton germplasm-pool assessment of Fusarium wilt resistance in California. Agronomy 105:1635-1644. https://doi.org/10.2134/agronj2013.0264 Crossref, ISIGoogle Scholar
    • Isakeit, T., and Arce, J. 2021. Evaluation of commercial Upland cotton varieties for reaction to Fusarium oxysporum f. sp. vasinfectum race 4 in Texas. 2021 Proceedings of the Beltwide Cotton Conference, pp. 488-491. The Cotton Foundation, National Cotton Council of America, Cordova, TN. Google Scholar
    • Kim, Y., Hutmacher, R. B., and Davis, R. M. 2005. Characterization of California isolates of Fusarium oxysporum f. sp. vasinfectum. Plant Dis. 89:366-372. https://doi.org/10.1094/PD-89-0366 Link, ISIGoogle Scholar
    • Ortiz, C. S., Bell, A. A., Magill, C. W., and Liu, J. 2017. Specific PCR detection of Fusarium oxysporum f. sp. vasinfectum California race 4 based on a unique Tfo1 insertion event in the PHO gene. Plant Dis. 101:34-44. https://doi.org/10.1094/PDIS-03-16-0332-RE Link, ISIGoogle Scholar
    • Rački, N., Dreo, T., Gutierrez-Aguirre, I., Blejec, A., and Ravnikar, M. 2014. Reverse transcriptase droplet digital PCR shows high resilience to PCR inhibition from plant, soil, and water samples. Plant Methods 10:42. https://doi.org/10.1186/s13007-014-0042-6 Crossref, ISIGoogle Scholar
    • Sanogo, S., and Zhang, J. 2016. Resistance sources, resistance screening techniques and disease management for Fusarium wilt in cotton. Euphytica 207:255-271. https://doi.org/10.1007/s10681-015-1532-y Crossref, ISIGoogle Scholar
    • SAS Institute Inc. 2014. SAS 9.4 Help and Documentation. SAS Institute Inc., Cary, NC. Google Scholar
    • Starr, J. L., Jeger, M. J., Martyn, R. D., and Schilling, K. 1989. Effects of Meloidogyne incognita and Fusarium oxysporum f. sp. vasinfectum on plant mortality and yield of cotton. Phytopathology 79:640-646. https://doi.org/10.1094/Phyto-79-640 Crossref, ISIGoogle Scholar
    • Ulloa, M., Hutmacher, R. B., Davis, R. M., Wright, S. D., Percy, R., and Marsh, B. 2006. Breeding for Fusarium wilt race 4 resistance in cotton under field and greenhouse conditions. J. Cotton Sci. 10:114-127. Google Scholar
    • Ulloa, M., Hutmacher, R. B., Roberts, P. A., Wright, S. D., Nichols R. L., and Davis, R. M. 2013. Inheritance and QTL mapping of Fusarium wilt race 4 resistance in cotton. Theor. Appl. Genet. 126:1405-1418. https://doi.org/10.1007/s00122-013-2061-5 Crossref, ISIGoogle Scholar
    • Ulloa, M., Hutmacher, R. B., Schramm, T., Ellis, M. L., Nichols, R., Roberts, P. A., and Wright, S. D. 2020. Sources, selection and breeding of Fusarium wilt (Fusarium oxysporum f. sp. vasinfectum) race 4 (FOV4) resistance in Upland (Gossypium hirsutum L.) cotton. Euphytica 216:109. https://doi.org/10.1007/s10681-020-02643-5 Crossref, ISIGoogle Scholar
    • U.S. Department of Agriculture’s National Agricultural Statistics Service. 2020. Southern Plains Region. In: Annual Cotton Review. U.S. Department of Agriculture’s National Agricultural Statistics Service, Washington, DC and the Oklahoma Department of Agriculture, Food, and Forestry, Oklahoma City, OK. https://www.nass.usda.gov/Statistics_by_State/Texas/Publications/Current_News_Release/2020_Rls/tx-cotton-review-2020.pdf Google Scholar
    • Wang, C., Ulloa, M., Duong, T., and Roberts, P. A. 2018. Quantitative trait loci mapping of multiple independent loci for resistance to Fusarium oxysporum f. sp. vasinfectum race 1 and 4 in an interspecific cotton population. Phytopathology 108:759-767. https://doi.org/10.1094/PHYTO-06-17-0208-R Link, ISIGoogle Scholar
    • Wen, R., Lee, J., Chu, M., Tonu, N., Dumonceaux, T., Gossen, B. D., Yu, F., and Peng, G. 2020. Quantification of Plasmodiophora brassicae resting spores in soils using droplet digital PCR (ddPCR). Plant Dis. 104:1188-1194. https://doi.org/10.1094/PDIS-03-19-0584-RE Link, ISIGoogle Scholar
    • Zhang, J., Abdelraheem, A., Zhu, Y., Wheeler, T. A., Dever, J. K., Frelichowski, J., Love, J., Ulloa, M., Jenkins, J. N., McCarty, J. C., Jr., Nichols, R., and Wedegaertner, T. 2020. Assessing genetic variation for Fusarium wilt race 4 resistance in tetraploid cotton by screening over three thousand germplasm lines under greenhouse or controlled conditions. Euphytica 216:108. https://doi.org/10.1007/s10681-020-02646-2 Crossref, ISIGoogle Scholar
    • Zhu, Y., Lujan, P. A., Wedegaertner, T., Nichols, R. L., Abdelraheem, A., Zhang, J. F., and Sanogo, S. 2020. First report of Fusarium oxysporum f. sp. vasinfectum race 4 causing Fusarium wilt of cotton in New Mexico, U.S.A. Plant Dis. 104:588. https://doi.org/10.1094/PDIS-06-19-1170-PDN Link, ISIGoogle Scholar