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The vicious cycle of lettuce corky root disease: effects of farming system, nitrogen fertilizer and herbicide

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Abstract

Aims

This study was aimed at testing the hypothesis that lettuce corky root (CR) disease caused by Rhizorhapis suberifaciens was less severe in organic than conventional farms, due to the absence of herbicide and fertilizer, and greater soil microbial activity in organic farms.

Methods

CR severity and soil quality were assessed in pairs of conventional and organic farms in California. To determine factors contributing to CR, effects of N fertilizer and pronamide herbicide were assessed on CR severity and plant weight in separate field experiments.

Results

CR was significantly more severe in conventional than organic farms, and there was a negative exponential relationship between CR severity and microbial activity. Split applications of soluble N fertilizer enhanced susceptibility to CR compared to pre-plant application of slow release N fertilizer. Pronamide increased disease severity on seedlings compared to untreated controls and reduced the dry weights of seedlings and mature heads.

Conclusions

Conventional practices, like fertilizer and herbicide use, increase plant susceptibility to and reduce microbial competition or antibiosis against R. suberifaciens in conventional lettuce production farms, potentially leading to enhanced environmental pollution due to a decrease in nutrient use efficiency and an increased need for fertilizer and water for diseased plants.

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References

  • Al-Khatib K (1996) Tulip (Tulipa spp.) daffodil (Narcissus spp.) and iris (Iris spp.) response to preemergence herbicides. Weed Technol 10:710–715

    CAS  Google Scholar 

  • Alvarez J, Datnoff LE, Nagata RT (1992) Crop rotation minimizes losses from corky root in Florida lettuce. HortSci 27:66–68

    Google Scholar 

  • Anonymous (1986) Crop Protection Chemicals Reference, 2nd edn. Chem and Pharmac Press, J Wiley and Sons, and Chem Pharmac Publ Corp: New York

  • Bottoms TG, Smith RF, Cahn MD, Hartz TK (2012) Nitrogen requirements and N status determination of lettuce. HortSci 47:1768–1774

    CAS  Google Scholar 

  • Brown PR, Michelmore RW (1988) The genetics of corky root resistance in lettuce. Phytopathology 78:1145–1150

    Article  Google Scholar 

  • Clark MS, Ferris H, Klonsky K, Lanini WT, van Bruggen AHC, Zalom FG (1998) Agronomic, economic, and environmental comparison of pest management in conventional and alternative tomato and corn systems in Northern California. Agric Ecosyst Environ 68:51–71

    Article  Google Scholar 

  • Daamen RA, Wijnands FG, van der Vliet G (1989) Epidemics of diseases and pests of winter wheat at different levels of agrochemical input. A study on the possibilities for designing an integrated cropping system. J Phytopathol 125:305–319

    Article  Google Scholar 

  • Drinkwater LE, Workneh F, Letourneau DK, van Bruggen AHC, Shennan C (1995) Fundamental differences between conventional and organic tomato agroecosystems in California. Ecol Applic 5:1098–1112

    Article  Google Scholar 

  • Francis IM, Jochimsen KN, de Vos P, van Bruggen AHC (2014) Reclassification of rhizosphere bacteria including strains causing corky root of lettuce as Rhizorhapis suberifaciens gen. nov., Sphingobium mellinum sp. nov., Sphingobium xanthum sp. nov., Sphingopyxis sp., and Rhizorhabdus argenteus gen. nov., sp. nov. Int J Syst Evol Microbiol 64:1340–1350

    Article  CAS  PubMed  Google Scholar 

  • Gattinger A, Mueller A, Haeni M, Skinner C, Fliessbach A, Buchmann N, Mäder P, Stolze M, Smith P, El-Hage Scialabba N, Niggli U (2012) Enhanced top soil carbon stocks under organic farming. Proc Natl Acad Sci 109:18226–18231

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Geisseler D, Horwath WR (2013) Lettuce Production in California. Fertilizer Research and Education Program. http://apps.cdfa.ca.gov/frep/docs/Lettuce_Production_CA.pdf. Accessed 1 May 2014

  • Haas G, Berg M, Koepke U (2002) Nitrate leaching: comparing conventional, integrated and organic agricultural production systems. In: Steenvorden J, Claessen F, Willems J (eds) Agricultural effects on ground and surface waters. Intern Association of Hydrological Sciences, IAHS Publ 273, Oxfordshire, pp 131–136

    Google Scholar 

  • Hager AG, Nordby D (2007) Herbicide persistence and how to test for residues in soils. Illinois Agricultural Pest Management Handbook. IPM program, University of Illinois Extension, Urabana-Champaign, Illinois. http://ipm.illinois.edu/pubs/iapmh/15chapter.pdf. Accessed 1 May 2014

  • Harter T, Lund JR (2012) Addressing Nitrate in California’s Drinking Water with a Focus on Tulare Lake Basin and Salinas Valley Groundwater. Report for the State Water Resources Control Board Report to the Legislature. Center for Watershed Sciences, University of California, Davis, p 78

  • He M, Ma W, Tian G, Blok W, Khodzaeva A, Zelenev VV, Semenov AM, van Bruggen AHC (2010) Daily changes of infections by Pythium ultimum after a nutrient impulse in organic versus conventional soils. Phytopathology 100:593–600

    Article  CAS  PubMed  Google Scholar 

  • Hiddink GA, van Bruggen AHC, Termorshuizen AJ, Raaijmakers JM, Semenov AV (2005) Effect of organic management of soils on suppressiveness to Gaeumannomyces graminis var. tritici and its antagonist, Pseudomonas fluorescens. Eur J Plant Pathol 113:417–435

    Article  Google Scholar 

  • Jackson LE, Ramirez IR, Yokota R, Fennimore SA, Koike ST, Henderson DM, Chaney WE, Klonsky KM (2003) Scientists, growers assess trade-offs in use of tillage, cover crops and compost. Calif Agric 57:48–54

    Article  Google Scholar 

  • Jackson LE, Ramirez I, Yokota R, Fennimore SA, Koike ST, Henderson DM, Chaney WE, Calderon FJ, Klonsky K (2004) On-farm assessment of organic matter and tillage management on vegetable yield, soil, weeds, pests, and economics in California. Agric Ecosyst Environ 103:443–463

    Article  Google Scholar 

  • Kerns DL, Matheron ME, Palumbo JC, Sanchez CA, Still DW, Tickes BR, Umeda K, Wilcox MA (1999) Guidelines for Head Lettuce Production in Arizona. IPM Series Number 12. Publication number az1099. Cooperative Extension, College of Agriculture and Life Sciences, University of Arizona, Tucson, Arizona. http://cals.arizona.edu/crops/vegetables/cropmgt/az1099.html. Accessed 1 May 2014

  • Klonsky K (2010) A Look at California’s Organic Agriculture Production. University of California Giannini Foundation of Agricultural Economics. ARE Update 14: 8–11

  • Klonsky KM (2012) Comparison of production costs and resource use for organic and conventional production systems. Am J Agric Econ 94:314–321

    Article  Google Scholar 

  • Kramer SB, Reganold JP, Glover JD, Bohannan BJM, Mooney HA (2006) Reduced nitrate leaching and enhanced denitrifier activity and efficiency in organically fertilized soils. Proc Natl Acad Sci 103:4522–4527

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Levesque CA, Rahe JE (1992) Herbicide interactions with fungal root pathogens, with special reference to glyphosate. Annu Rev Phytopathol 30:579–602

    Article  CAS  PubMed  Google Scholar 

  • Mäder P, Fliessbach A, Dubois D, Gunst L, Fried P, Niggli U (2002) Soil fertility and biodiversity in organic farming. Science 296:1694–1697

    Article  PubMed  Google Scholar 

  • Mersie W, Elliott J (1993) Selectivity of pronamide and trifluralin in Belgian endive Cichorium entybus. Weed Technol 7:226–229

    CAS  Google Scholar 

  • Messiha NAS, van Bruggen AHC, van Diepeningen AD, de Vos OJ, Termorshuizen AJ, Tjou-Tam-Sin NNA, Janse JD (2007) Potato brown rot incidence and severity under different management and amendment regimes in different soil types. Eur J Plant Pathol 119:367–381

    Article  Google Scholar 

  • Messiha NAS, van Bruggen AHC, Franz E, Janse JD, Schoeman-Weerdesteijn ME, Termorshuizen AJ, van Diepeningen AD (2009) Effects of soil type, management type and soil amendments on the survival of the potato brown rot bacterium Ralstonia solanacearum. Appl Soil Ecol 43:206–215

    Article  Google Scholar 

  • Muramoto J (1999) Comparison of Nitrate Content in Leafy Vegetables from Organic and Conventional Farms in California. Center for Agroecology and sustainable Food Systems, University of California. http://www.agroecology.org/documents/Joji/leafnitrate.pdf. Accessed 1 May 2014

  • National Research Council (2010) Towards sustainable agricultural systems in the 21st century. The National Academies, Washington

    Google Scholar 

  • O’Brien RD, van Bruggen AHC (1992a) Accuracy, precision, and correlation to yield loss of disease severity scales for corky root of lettuce. Phytopathology 82:91–96

    Article  Google Scholar 

  • O’Brien RD, van Bruggen AHC (1992b) Yield losses to iceberg lettuce due to corky root caused by Rhizomonas suberifaciens. Phytopathology 82:154–159

    Article  Google Scholar 

  • O’Brien RD, van Bruggen AHC (1993) Effect of temperature on corky root of lettuce and growth of the pathogen Rhizomonas suberifaciens. Can J Plant Pathol 15:85–90

    Article  Google Scholar 

  • Ogbuchiekwe EJ, McGiffen ME Jr, Ngouajio M (2004) Economic return in production of lettuce and cantaloupe is affected by cropping system and management practice. HortSci 39:1321–1325

    Google Scholar 

  • Potter TL, Truman CC, Strickland TC, Bosch DD, Webster TM, Franklin DH, Bednarz CW (2006) Combined effects of constant versus variable intensity simulated rainfall and reduced tillage management on cotton preemergence herbicide runoff. J Environ Qual 35:1894–1902

    Article  CAS  PubMed  Google Scholar 

  • Poudel DD, Horwath WR, Lanini WT, Temple SR, van Bruggen AHC (2002) Comparison of soil N availability and leaching potential, crop yields and weeds in organic, low-input and conventional farming systems in northern California. Agric Ecosyst Environ 90:125–137

    Article  CAS  Google Scholar 

  • Purea M, Sutton BG (1989) Application of propyzamide Kerb to lettuce via trickle irrigation. Acta Hortic 247:257–261

    Google Scholar 

  • Reichard SL, Sulc RM, Rhodes LH, Loux MM (1997) Effects of herbicides on Sclerotinia crown and stem rot of alfalfa. Plant Dis 81:787–790

    Article  CAS  Google Scholar 

  • Rouchaud J, Moons C, Benoit F, Ceustermans N, Maraite H (1987) Metabolism of 14-C-pronamide in the soil and in lettuce (Lactuca sativa) under field conditions. Weed Sci 35:469–475

    CAS  Google Scholar 

  • Sanyal D, Shrestha A (2008) Direct effect of herbicides on plant pathogens and disease development in various cropping systems. Weed Sci 56:155–160

    Article  CAS  Google Scholar 

  • Senechkin IV, Speksnijder AGCL, Semenov AM, van Bruggen AHC, van Overbeek LS (2010) Isolation and partial characterization of bacterial strains on low organic carbon medium from soils fertilized with different organic amendments. Microb Ecol 60:829–839

    Article  PubMed  Google Scholar 

  • Senechkin IV, van Overbeek L, van Bruggen AHC (2014) Greater Fusarium wilt suppression after complex than after simple organic amendments as affected by soil pH, total carbon and ammonia-oxidizing bacteria. Appl Soil Ecol 73:148–155

    Article  Google Scholar 

  • Smith RF, Klonsky KM, De Moura RL (2009) Sample Costs to Produce Iceberg Lettuce Head Lettuce, Central Coast Region, Monterey & Santa Cruz Counties. University of California Cooperative Extension. Publ. lt-cc-09-2. Oakland, CA

  • Smith R, Cahn M, Daugovish O, Koike ST, Natwick E, Smith H, Subbarao K, Takele E, Turini T (2011) Leaf Lettuce Production in California. University of California Vegetable Research and Information Center. Publ 7216. http://anrcatalog.ucdavis.edu/pdf/7216.pdf. Accessed 1 May 2014

  • Stopes C, Lord EI, Philipps L, Woodward L (2002) Nitrate leaching from organic farms and conventional farms following best practice. Soil Use Manag 18:256–263

    Article  Google Scholar 

  • Subbarao KV, Hubbard JC, Schulbach KF (1997) Comparison of lettuce diseases and yield under subsurface drip and furrow irrigation. Phytopathology 87:877–883

    Article  CAS  PubMed  Google Scholar 

  • Tourte L, Smith R F, Klonsky KM, De Moura RL (2009) Sample Costs to Produce Organic Leaf Lettuce. University of California Cooperative Extension. LT-CC-09-O, Oakland, CA

  • Turini T, Cahn M, Cantwell M, Jackson L, Koike S, Natwick E, Smith R, Subbarao K, Takele E (2011) Iceberg Lettuce Production in California. University of California Vegetable Research and Information Center. Publ 7215. http://anrcatalog.ucdavis.edu/pdf/7215.pdf . Accessed 1 May 2014

  • van Bruggen AHC, Jochimsen KN (1993) First report of Rhizomonas suberifaciens causing corky root of lettuce in Australia. Australas. Plant Pathol 22:14–19

    Google Scholar 

  • van Bruggen AHC, Rubatzky VE (1992) Use of transplants instead of direct seeding to reduce corky root severity and losses due to corky root in iceberg lettuce. Plant Dis 76:703–708

    Article  Google Scholar 

  • van Bruggen AHC, Semenov AM (1999) A new approach to the search for indicators of root disease suppression. Australas Plant Pathol 28:4–10

    Article  Google Scholar 

  • van Bruggen AHC, Termorshuizen AJ (2003) Integrated approaches to root disease management in organic farming systems. Australas Plant Pathol 32:141–156

    Article  Google Scholar 

  • van Bruggen AHC, Grogan RG, Bogdanoff CP, Waters CM (1988) Corky root of lettuce in California caused by a gram‑negative bacterium. Phytopathology 78:1139–1145

    Article  Google Scholar 

  • van Bruggen AHC, Brown PR, Jochimsen KN (1989) Corky root of lettuce caused by strains of a gram‑negative bacterium from muck soils of Florida, New York, and Wisconsin. Appl Environ Microbiol 55:2635–2640

    PubMed Central  PubMed  Google Scholar 

  • van Bruggen AHC, Brown PR, Greathead AS (1990a) Distinction between infectious and non-infectious corky root of lettuce in relation to nitrogen fertilizer. J Am Soc Hortic Sci 115:762–770

    Google Scholar 

  • van Bruggen AHC, Brown PR, Shennan C, Greathead AS (1990b) The effect of cover crops and fertilization with ammonium nitrate on corky root of lettuce. Plant Dis 74:584–589

    Article  Google Scholar 

  • van Bruggen AHC, Jochimsen KN, Brown PR (1990c) Rhizomonas suberifaciens gen. nov., sp. nov., the causal agent of corky root of lettuce. Int J Syst Bacteriol 40:175–188

    Article  Google Scholar 

  • van Bruggen AHC, Jochimsen KN, Steinberger EM, Segers P, Gillis M (1993) Classification of Rhizomonas suberifaciens, an unnamed Rhizomonas species, and Sphingomonas spp. in rRNA superfamily IV. Int J Syst Bacteriol 43:1–7

    Article  PubMed  Google Scholar 

  • van Bruggen AHC, Semenov AM, van Diepeningen AD, de Vos OJ, Blok WJ (2006) Relation between soil health, wave-like fluctuations in microbial populations, and soil-borne plant disease management. Eur J Plant Pathol 115:105–122

    Article  Google Scholar 

  • van Bruggen AHC, Francis IM, Jochimsen KN (2014a) Non-pathogenic rhizosphere bacteria belonging to the genera Rhizorhapis and Sphingobium provide specific control of lettuce corky root disease caused by the same but not different genera. Plant Pathol. doi:10.1111/ppa.12212

    Google Scholar 

  • van Bruggen AHC, Ochoa O, Francis IM, Michelmore RW (2014b) Differential interactions between strains of Rhizorhapis, Sphingobium, Sphingopyxis or Rhizorhabdus and accessions of Lactuca spp. with respect to severity of corky root disease. Plant Pathol. doi:10.1111/ppa.12188

    Google Scholar 

  • van Diepeningen AD, de Vos OJ, Zelenev VV, Semenov AM, van Bruggen AHC (2005) DGGE fragments oscillate with or counter to fluctuations of cultivable bacteria along wheat roots. Microb Ecol 50:506–517

    Article  PubMed  Google Scholar 

  • van Diepeningen AD, de Vos OJ, Korthals GW, van Bruggen AHC (2006) Effects of organic versus conventional management on chemical and biological parameters in agricultural soils. Appl Soil Ecol 31:120–135

    Article  Google Scholar 

  • Vaughan MA, Vaughn KC (1987) Pronamide disrupts mitosis in a unique manner. Pesticide Biochem Physiol 28:182–193

    Article  CAS  Google Scholar 

  • Workneh F, van Bruggen AHC (1994a) Suppression of corky root of tomatoes in soils from organic farms associated with soil microbial activity and nitrogen status of soil and tomato tissue. Phytopathology 84:688–694

    Article  Google Scholar 

  • Workneh F, van Bruggen AHC (1994b) Microbial density, composition, and diversity in organically and conventionally managed rhizosphere soil in relation to suppression of corky root of tomatoes. Appl Soil Ecol 1:219–230

    Article  Google Scholar 

  • Workneh F, van Bruggen AHC, Drinkwater LE, Shennan C (1993) Variables associated with corky root and Phytophthora root rot of tomatoes in organic and conventional farms. Phytopathology 83:581–589

    Article  Google Scholar 

  • Zelenev VV, van Bruggen AHC, Semenov AM (2000) “BACWAVE”, a spatial-temporal model for traveling waves of bacterial populations in response to a moving carbon source in soil. Microb Ecol 40:260–272

    CAS  PubMed  Google Scholar 

  • Zelenev VV, van Bruggen AHC, Semenov AM (2005) Short-term wavelike dynamics of bacterial populations in response to nutrient input from fresh plant residues. Microb Ecol 49:83–93

    Article  CAS  PubMed  Google Scholar 

  • Zelenev VV, van Bruggen AHC, Leffelaar PA, Bloem J, Semenov AM (2006) Oscillating dynamics of bacterial populations and their predators in response to fresh organic matter added to soil: the simulation model ‘BACWAVE-WEB’. Soil Biol Biochem 38:1690–1711

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Niklaus J. Grünwald for assistance with the surveys in conventional and organic lettuce farms in California. We are grateful to Art Greathead, Phil Brown, Jonathan Becker, Mark Bergtholdt and Pauline Sanders for their help with the nitrogen and herbicide experiments. This research was partially funded by the California Iceberg Lettuce Research and Advisory Board. Additional funding came from several USDA-NRICGP grants (‘Decomposition of plant residues and suppression of root diseases’, ‘Oligotrophic bacteria and root disease suppression’, and ‘Transition from conventional to low-input or organic farming systems: Soil biology and soil fertility’).

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Authors and Affiliations

  1. Department of Plant Pathology, University of Florida, Gainesville, FL, 32611, USA

    Ariena H. C. van Bruggen & Isolde M. Francis

  2. Department of Plant Pathology, University of California, Davis, CA, 95616, USA

    Ariena H. C. van Bruggen & Randy Krag

  3. Emerging Pathogens Institute, University of Florida, Gainesville, FL, 32611, USA

    Ariena H. C. van Bruggen

  4. Beckstoffer Vineyards, Red Hills, Kelseyville, CA, 95451, USA

    Randy Krag

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  1. Ariena H. C. van Bruggen
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  2. Isolde M. Francis
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Correspondence to Ariena H. C. van Bruggen.

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van Bruggen, A.H.C., Francis, I.M. & Krag, R. The vicious cycle of lettuce corky root disease: effects of farming system, nitrogen fertilizer and herbicide. Plant Soil 388, 119–132 (2015). https://doi.org/10.1007/s11104-014-2312-5

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