Plant and Soil

, Volume 304, Issue 1–2, pp 209–225 | Cite as

Long-term orchard groundcover management systems affect soil microbial communities and apple replant disease severity

  • Angelika St. Laurent
  • Ian A. Merwin
  • Janice E. Thies
Regular Article

Abstract

Apple replant disease (ARD) is a soil-disease syndrome of complex etiology that affects apple tree roots in replanted orchards, resulting in stunted tree growth and reduced yields. To investigate whether different groundcover management systems (GMSs) influence subsequent ARD severity, we grew apple seedlings in an outdoor nursery in pots containing orchard soil from field plots where four GMSs had been maintained for 14 years in an orchard near Ithaca, NY, USA. The GMS treatments were: (1) pre-emergence herbicide (Pre-H), bare soil strips maintained by applying tank-mixed glyphosate, norflurazon and diuron herbicides annually; (2) post-emergence herbicide (Post-H), sparse weed cover maintained by applying glyphosate in May and July each year; (3) mowed sod grass (Mowed Sod); and (4) bark mulch (Mulch). Soils were also sampled from the grass drive lane maintained between the trees in the orchard (Grass Lane). Sampled soils (Orchard soil) were either pasteurized or left untreated, placed into 4-L pots, and planted with one apple seedling per pot. After 3 months of growth, soil (Bioassay soil) and apple tree roots (Bioassay roots) were sampled from each pot and microbial populations colonizing samples were characterized. Seedling growth was reduced in soils sampled from all four GMS treatments compared to the Grass Lane soils. Among the GMS treatments, seedling biomass was greater in Pre-H than in the Post-H soil. Soil microbial communities and nutrient availability differed among all four GMS treatments and the Grass Lane. Root-lesion (Pratylenchus sp.) nematode populations were higher in the Mowed Sod than in the other GMS treatments. Soil bacterial and fungal community composition was assessed in Orchard and Bioassay soils and Bioassay roots with a DNA fingerprinting method (T-RFLP). Redundancy analysis indicated that soils sampled from the different GMS treatments differentially influenced seedling biomass. A clone library of 267 soil bacteria was developed from sampled Orchard soils and Bioassay roots. These communities were dominated by Acidobacteria (25% of sequences), Actinobacteria (19%), δ-Proteobacteria (12%), β-Proteobacteria (10%), and these ratios differed among the GMS soils. Members of the family Comamonadaceae were detected only in tree-row soil, not in the Grass Lanes. The dominant sequences among 145 cloned fungi associated with apple seedling roots were Fusarium oxysporum (16% of sequences), an uncultured soil fungus submitted under DQ420986 (12%), and Rhodotorula mucilaginosa (9%). In a redundancy analysis, factors including fungal and oomycete community compositions, soil respiration rates, population sizes of culturable bacteria and fungi, soil organic matter content, and nutrient availability, were not significant predictors of apple seedling biomass in these soils. Different GMS treatments used by apple growers may influence subsequent ARD severity in replanted trees, but edaphic factors commonly associated with soil fertility may not reliably predict tree-root health and successful establishment of replanted orchards.

Keywords

Apple replant disease Glyphosate Norflurazon Diuron Herbicides Mulch Orchard floor management Soil microbial communities 

Abbreviations

AMMI

Additive Main effects with Multiplicative Interaction

ARD

Apple Replant Disease

DGGE

Denaturing Gradient Gel Electrophoresis

GMS

Groundcover Management Systems

ITS

Internal Transcribed Spacer

OTU

Operational Taxonomic Unit

PCA

Principal Component Analysis

RDA

Redundancy Analysis

T-RFLP

Terminal Restriction Fragment Length Polymorphism

References

  1. Arcate JM, Karp MA, Nelson EB (2006) Diversity of Peronosporomycete communities associated with the rhizosphere of different plant species. Microb Ecol 51:36–50PubMedCrossRefGoogle Scholar
  2. Arroyo-García R, Cenis JL, Tello J, Martiez-Zapater JM, Cifuentes D (2003) Genetic relationships among seven specialized forms of Fusarium oxysporum determined by DNA sequencing of the ITS region and AFLPs. Span J Agric Res 1:55–63Google Scholar
  3. Atkinson D (1980) The distribution and effectiveness of the roots of tree crops. Hort Rev 2:424–490Google Scholar
  4. Benizri E, Piutti S, Verger S, Pagès L, Vercambre G, Poessel JL, Michelot P (2005) Replant diseases: bacterial community structure and diversity in peach rhizosphere as determined by metabolic and genetic fingerprinting. Soil Biol Biochem 37:1738–1746CrossRefGoogle Scholar
  5. Boehm MJ, Wu T, Stone A, Kraakman B, Iannotti DA, Wilson GE, Madden LV, Hoitink HA (1997) Cross-polarized magic angle spinning 13C nuclear magnetic resonance spectroscopic characterization of soil organic matter relative to culturable bacterial species composition and sustained biological control of Pythium root rot. Appl Environ Microb 63:162–168Google Scholar
  6. Brown MW, Tworkoski T (2004) Pest management benefits of compost mulch in apple orchards. Agr Ecosyst Environ 103:465–472CrossRefGoogle Scholar
  7. Bruns TD, White TJ, Taylor JW (1991) Fungal molecular systematics. In: Johnston RF (ed) Annual review of ecology and systematics. Annual Reviews Inc., Palo Alto, CA, USA, pp 525–564Google Scholar
  8. Buszard DJ, Jensen P (1986) A note on the incidence of apple replant disease in Quebec Canada orchards. Phytoprotection 67:133–136Google Scholar
  9. Časka V, Vančura V, Hudská G, Přikryl Z (1982) Rhizosphere microorganisms in relation to apple replant problem. Plant Soil 69:187–197CrossRefGoogle Scholar
  10. Ceasar AJ, Burr TJ (1987) Growth promotion of apple seedlings and rootstocks by specific strains of bacteria. Phytopathology 77:1583–1588CrossRefGoogle Scholar
  11. Chung YR, Hoitink HAH, Lipps PE (1988) Interactions between organic matter decomposition level and soilborne disease severity. Agr Ecosyst Environ 24:183–193CrossRefGoogle Scholar
  12. Cole JR, Chai B, Marsh TL, Farris RJ, Wang Q, Kulam SA, Chandra S, McGarrell DM, Schmidt TM, Garrity GM, Tiedje JM (2003) The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res 31:442–443PubMedCrossRefGoogle Scholar
  13. Culman SW, Duxbury JM, Lauren JG, Thies JE (2006) Microbial community response to soil solarization in Nepal’s rice–wheat cropping system. Soil Biol Biochem 38:3359–3371CrossRefGoogle Scholar
  14. DeFigueiredo DR, Pereira MJ, Moura A, Silva L, Bárrios S, Fonseca F, Henriques I, Correia A (2007) Bacterial community composition over a dry winter in meso- and eutrophic Portuguese water bodies. FEMS Microbiol Ecol 59:638–650CrossRefGoogle Scholar
  15. Dullahide SR, Stirling GR, Nikulin A, Stirling AM (1994) The role of nematodes, fungi, bacteria and abiotic factors in the etiology of apple replant problems in the Granite Belt of Queensland. Aust J Exp Agr 34:1177–1182CrossRefGoogle Scholar
  16. Facteau TJ, Chestnut NE, Rowe KE (1996) Tree, fruit size and yield of ‘ Bing’ sweet cherry as influenced by rootstock, replant area, and training system. Sci Hortic-Amsterdam 67:13–26CrossRefGoogle Scholar
  17. Foy CL, Drake CR, Pirkey CL (1996) Impact of herbicides applied annually for twenty-three years in a deciduous orchard. Weed Technol 10:587–591Google Scholar
  18. Fracchia S, Godeas A, Scervino JM, Sampredo I, Ocampo JA, García-Romera I (2003) Interaction between the soil yeast Rhodotorula mucilaginosa and the arbuscular mycorrhizal fungi Glomus mosseae and Gigaspora rosea. Soil Biol Biochem 35:701–707CrossRefGoogle Scholar
  19. Gauch HG, Furnas RE (1991) Statistical analysis of yield trials with MATMODEL. Argon J 83:916–920Google Scholar
  20. Grosch R, Schwerwinsky K, Lottmann J, Berg G (2007) Fungal antagonists of the plant pathogen Rhizoctonia solani: selection, control efficacy and influence on the indigenous microbial community. Mycol Res 110:1464–1474CrossRefGoogle Scholar
  21. Gure A, Wahlström K, Stenlid J (2005) Pathogenicity of seed-associated fungi to Podocarpus falcatus in vitro. Forest Pathol 35:23–35CrossRefGoogle Scholar
  22. Heuer H, Krsek M, Baker P, Smalla K, Wellington EMH (1997) Analysis of Actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denatureing gradients. Appl Environ Microb 63:3233–3241Google Scholar
  23. Hipps NA, Davies MJ, Johnson DS (2004) Effect of different ground vegetation management systems on soil quality, growth and fruit quality of culinary apple trees. J Hortic Sci Biotech 79:610–618Google Scholar
  24. Kable PF, Mai WF (1968) Influence of soil moisture on Pratylenchus penetrans. Nematologica 14:101–122CrossRefGoogle Scholar
  25. Leinfelder MM, Merwin IA (2006) Rootstock selection, preplant soil treatments, and tree planting positions as factors in managing apple replant disease. Hort Sci 41:394–401Google Scholar
  26. Mai WF, Abawi GS (1978) Determining the cause and extent of apple, cherry, and pear replant diseases under controlled conditions. Phytopathology 68:1540–1544CrossRefGoogle Scholar
  27. Mai WF, Abawi GS (1981) Controlling replant diseases of pome and stone fruits in Northeastern United-States by preplant fumigation. Plant Dis 65:859–864CrossRefGoogle Scholar
  28. Mai WF, Merwin IA, Abawi GS (1994) Diagnosis, etiology, and management of replant problems in New York cherry and apple orchards. Acta Hort 363:33–41Google Scholar
  29. Mali VR, Bojnansky V (1979) Occurrence of Olpidium brassicae on Euonymus europaea in Czechoslovakia. Biologia 34:47–54Google Scholar
  30. Manici LM, Ciavatta C, Kelderer M, Erschbaumer G (2003) Replant problems in South Tyrol: role of fungal pathogens and microbial population in conventional and organic apple orchards. Plant Soil 256:315–324CrossRefGoogle Scholar
  31. Mazzola M (1997) Identification and pathogenicity of Rhizoctonia spp. isolated from apple roots and orchard soils. Phytopathology 88:930–938CrossRefGoogle Scholar
  32. Mazzola M (1998) Elucidation of the microbial complex having a causal role in the development of apple replant disease in Washington. Phytopathology 88:930–938CrossRefPubMedGoogle Scholar
  33. Mazzola M (1999) Transformation of soil microbial community structure and Rhizoctonia-suppressive potential in response to apple roots. Phytopathology 89:920–927CrossRefPubMedGoogle Scholar
  34. Merwin IA (2003) Orchard floor management systems. In: Ferree DC (ed) Apples: botany, production and uses. CABI Publ., Wallingford, EnglandGoogle Scholar
  35. Merwin IA, Ray JA (1997) Spatial and temporal factors in weed interference with newly planted apple trees. HortScience 32:633–637Google Scholar
  36. Merwin IA, Stiles WC (1989) Root-lesion nematodes, potassium deficiency, and prior cover crops as factors in apple replant disease. J Am Soc Hortic Sci 114:724–728Google Scholar
  37. Merwin IA, Stiles WC (1994) Orchard groundcover management impacts on apple tree growth and yield, and nutrient availability and uptake. J Am Soc Hortic Sci 199:209–215Google Scholar
  38. Merwin IA, Wilcox WF, Stiles WC (1992) Influence of orchard ground cover management on development of Phytophthora crown and root rots of apple. Plant Dis 76:199–205CrossRefGoogle Scholar
  39. Merwin IA, Stiles WC, van Es HM (1994) Orchard groundcover management impacts on soil physical properties. J Am Soc Hortic Sci 119:216–222Google Scholar
  40. Merwin IA, Ray JA, Steenhuis TS, Boll J (1996) Groundcover management systems influence fungicide and nitrate-N concentrations in leachate and runoff from a New York apple orchard. J Amer Soc Hort Sci 121:249–257Google Scholar
  41. Moeseneder M-M, Arrieta J-M, Muyzer G, Winter C, Herndl G-J (1999) Optimization of terminal-restriction fragment length polymorphism analysis for complex marine bacterioplankton communities and comparison with denaturing gradient gel electrophoresis. Appl Environ Microbiol 65:3518–3525PubMedGoogle Scholar
  42. Mulder D (ed) (1978) Soil disinfestations. Elsevier, Amsterdam, p 369Google Scholar
  43. Muyzer G, Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie van Leeuwenhoek 73:127–141PubMedCrossRefGoogle Scholar
  44. Oliveira MT, Merwin IA (2001) Soil physical conditions in a New York orchard after eight years under different groundcover management systems. Plant Soil 234:233–237CrossRefGoogle Scholar
  45. Rodella AA, Saboya LV (1999) Calibration for conductimetric determination of carbon dioxide. Soil Biol Biochem 32:2059–2060CrossRefGoogle Scholar
  46. Rumberger A, Yao S, Merwin IA, Nelson EB, Thies JE (2004) Rootstock genotype and orchard replant position rather than soil fumigation or compost amendment determine tree growth and rhizosphere bacterial community composition in an apple replant soil. Plant Soil 264:247–260CrossRefGoogle Scholar
  47. Rumberger A, Merwin IA, Thies JE (2007) Microbial community development in the rhizosphere of apple trees at a replant site. Soil Biol Biochem 39:1645–1654CrossRefGoogle Scholar
  48. Sampredo I, Aranda E, Scervoni JM, Fracchia S, García-Romera I, Ocampo JA, Godeas A (2004) Improvement by soil yeasts of arbuscular mycorrhizal symbiosis of soybean (Glycine max) colonized by Glomus mosseae. Mycorrhiza 14:229–234CrossRefGoogle Scholar
  49. Storer DA (1984) A simple high sample volume ashing procedure for determination of soil organic matter. Soil Sci Plant Anal 15:759–772Google Scholar
  50. Termorshuizen AJ, Lotz LAP (2002) Does large-scale cropping of herbicide-resistant cultivars increase the incidence of polyphagous soil-borne plant pathogens? Outlook Agr 31:51–54Google Scholar
  51. Thies JE, Grossman JM (2006) The soil habitat and soil ecology. In: Biological strategies for sustainable soil systems. Publisher: Marcel Dekker/CRC Press, p 59–78Google Scholar
  52. Tworkoski T, Miller S (2001) Apple and peach orchard establishment following multi-year use of diuron, simazine and terbacil. HortScience 36:1211–1213Google Scholar
  53. Urbach E, Vergin KL, Larson GL, Giovanni SJ (2002) Dynamic bacterioplankton populations in ultraoligotrophic Crater Lake. Abstr Gen Meet Am Soc Microbiol 102:343–344Google Scholar
  54. Utkhede RS, Hogue EJ (1998) Effect of herbicides, plastic mulch, and hand weed on development of phytophthora crown and root rot of apple trees. Can J Plant Pathol 20:81–86CrossRefGoogle Scholar
  55. 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 115:105–122CrossRefGoogle Scholar
  56. Wallace RB, Johnson MJ, Suggs SV, Ken-ichi M, Bhatt R, Keiichi I (1981) A set of synthetic oligodeoxyribonucleotide primers for DNA sequencing in the plasmid vector pBR322. Gene 16:21–26PubMedCrossRefGoogle Scholar
  57. Walsh BD, Salmins S, Buszard DJ, Mackenzie A (1996) Impact of soil management systems on organic dwarf apple orchards and soil aggregate stability, bulk density, temperature and water content. Can J Soil Sci 76:203–209Google Scholar
  58. Yao S, Merwin IA, Bird GW, Abawi GS, Thies JE (2005) Orchard floor management practices that maintain vegetative or biomass groundcover stimulate soil microbial activity and alter soil microbial community composition. Plant Soil 271:377–389CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Angelika St. Laurent
    • 1
  • Ian A. Merwin
    • 2
  • Janice E. Thies
    • 1
  1. 1.Department of Crop and Soil ScienceCornell UniversityIthacaUSA
  2. 2.Department of HorticultureCornell UniversityIthacaUSA

Personalised recommendations