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Growth rate of fine root systems influences rootstock tolerance to replant disease

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Abstract

Aims

Plant tolerance to herbivory has often been linked to plant growth rate, with faster growing plants that present high tissue turnover rates expected to be more tolerant than slower-growing plants. We tested whether this relationship also holds for rootstock growth rate and tolerance to apple replant disease (ARD).

Methods

An ARD susceptible rootstock, M.26 and ARD tolerant rootstock, CG.6210 were grown in soil from an apple replant site (FS) and in pasteurized soil (PS) from the same site. Total below ground biomass production was determined by harvesting a subset of plants per soil treatment and rootstock at 11, 17, and 23 weeks after planting. Root samples were collected prior to each harvesting date to determine root respiration and total carbon (C) and nitrogen (N) content. Root dynamics were tracked during the growing season by digitally photographing root observation windows.

Results

Total root biomass, first and second order roots, and second-to-first order root ratio were higher in CG.6210 than in M.26 in both soil treatments. Roots of CG.6210 were thinner and had lower N concentration than those of M.26. Roots of M.26 had longer lifespans than those of CG.6210, and the mortality risk of M.26 roots was 56 % that of CG.6210 roots.

Conclusion

Our study indicates that rootstocks with faster growing root systems can tolerate ARD infection by investing fewer resources in individual root construction that can be shed more readily.

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References

  • Allen MF, Allen EB, Friese CF (1989) Responses of the non-mycotrophic plant Salsola kali to invasion by vesicular–arbuscular mycorrhizal fungi. New Phytol 111:45–49

    Article  Google Scholar 

  • Anderson LJ, Comas LH, Lakso AN, Eissenstat DM (2003) Multiple risk factors in root survivorship: a 4-year study in Concord grape. New Phytol 158:489–501

    Article  Google Scholar 

  • Auvil TD, Schmidt TR, Hanrahan I, Castillo F, McFerson JR, Fazio G (2011) Evaluation of dwarfing rootstocks in Washington apple replant sites. Acta Horticult (ISHS) 903:265–271

    Google Scholar 

  • Bartsch N (1987) Responses of root systems of young Pinus sylvestris and Picea abies plants to water deficits and soil acidity. Can J For Res 17:805–812

    Article  Google Scholar 

  • Bauerle TL, Eissenstat DM, Granett J, Gardner DM, Smart DR (2007) Consequences of insect herbivory on grape fine root systems with different growth rates. Plant Cell Environ 30:786–795

    Article  CAS  PubMed  Google Scholar 

  • Blaker NS, MacDonald JD (1986) The role of salinity in the development of Phytophthora root rot of citrus. Phytopathology 76:970–975

    Article  Google Scholar 

  • Braun PG (1991) The combination of Cylindrocarpon lucidum and Pythium irregulare as a possible cause of apple replant disease in Nova Scotia. Can J Plant Pathol 13:291–297

    Article  Google Scholar 

  • Caruso FL, Neubauer BF, Begin MD (1989) A histological study of apple roots affected by replant disease. Can J Bot 67:742–749

    Article  Google Scholar 

  • Coley PD (1988) Effects of plant growth rate and leaf lifetime on the amount of anti-herbivore defense. Oecologia 74:531–536

    Article  Google Scholar 

  • Comas LH, Eissenstat DM, Lakso AN (2000) Assessing root death and root system dynamics in a study of grape canopy pruning. New Phytol 147:171–178

    Article  CAS  Google Scholar 

  • Cox DR (1972) Regression Models and Life-Tables. J R Stat Soc Series B Stat Methodol 34:187–220

  • Dunn R (1979) Effect of Xiphinema americanum and Rhizoctonia solani on browning of apple roots. Fungic Nematic Tests 35:214

    Google Scholar 

  • Édin M, Guignebault P, Lavoisier C, Warot C (2004) Adaptation and renewal of apple orchards: how to replant successfully. Infos-Ctifl 201:32–36

    Google Scholar 

  • Eissenstat DM, Wells CE, Yanai RD, Whitbeck JL (2000) Building roots in a changing environment: implications for root longevity. New Phytol 147:33–42

    Article  CAS  Google Scholar 

  • Fan H, Zhao Z, Liu H, Zhao G, Zhang X, Zhang Z (2008) Changes of soil nutrition in root zone and their effects on growth of the replanted apple. Acta Hort Sin 35:1727–1734

    CAS  Google Scholar 

  • Feeny P (1976) Plant apparency and chemical defense. Recent Adv Phytochem 10:1–40

    CAS  Google Scholar 

  • Graham JH (1990) Evaluation of tolerance of citrus rootstocks to Phytophthora root rot in chlamydospore-infested soil. Plant Dis 74:743–746

    Article  Google Scholar 

  • Graham JH (1995) Root regeneration and tolerance of citrus rootstocks to root-rot caused by Phytophthora nicotianae. Phytopathology 85:111–117

    Article  Google Scholar 

  • Guo D, Mitchell RJ, Withington JM, Fan P, Hendricks JJ (2008) Endogenous and exogenous controls of root life span, mortality and nitrogen flux in a longleaf pine forest: root branch order predominates. J Ecol 96:737–745

    Article  CAS  Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Hishi T (2007) Heterogeneity of individual roots within the fine root architecture: causal links between physiological and ecosystem functions. J For Res 12:126–133

    Article  Google Scholar 

  • Hoffland E, Niemann GJ, van Pelt JA, Pureveen JBM, Eijkel GB, Boon JJ, Lambers HL (1996) Relative growth rate correlates negatively with pathogen resistance in radish: the role of plant chemistry. Plant Cell Environ 19:1281–1290

    Article  Google Scholar 

  • Isutsa DK, Merwin IA (2000) Malus germplasm varies in resistance or tolerance to apple replant disease in a mixture of New York orchard soils. HortSci 35:262–268

    Google Scholar 

  • Jaffee BA, Abawi GS, Mai WF (1981) Etiology of an apple replant disease. Phytopathology 71:228

    Google Scholar 

  • Kandula DRW, Jones EE, Horner IJ, Stewart A (2010) The effect of Trichoderma bio-inoculants on specific apple replant disease (SARD) symptoms in apple rootstocks in New Zealand. Australas Plant Pathol 39:312–318

    Article  CAS  Google Scholar 

  • Kaplan EL, Meier P (1958) Nonparametric Estimation from Incomplete Observations. J Am Statist Assoc 53:457–481

    Google Scholar 

  • Kimberling DN, Scott ER, Price PW (1990) Testing a new hypothesis: plant vigor and phylloxera distribution on wild grape in Arizona. Oecologia 84:1–8

    Article  Google Scholar 

  • Kosola KR, Eissenstat DM, Graham JH (1995) Root demography of mature citrus trees: the influence of Phytophthora nicotianae. Plant Soil 171:283–288

    Article  CAS  Google Scholar 

  • Leinfelder MM, Merwin IA (2006) Rootstock selection, preplant soil treatments, and tree planting positions as factors in managing apple replant disease. HortSci 41:394–401

    Google Scholar 

  • Liljeroth E (1995) Comparisons of early root cortical senescence between barley cultivars, Triticum species and other cereals. New Phytol 130:495–501

    Article  Google Scholar 

  • Mai WF, Abawi GS (1981) Controlling replant diseases of pome and stone fruits in northeastern United States by preplant fumigation. Plant Dis 65:859–864

    Article  Google Scholar 

  • Mai WF, Merwin IA, Abawi GS (1994) Diagnosis, etiology and management of replant disorders in New York cherry and apple orchards. Acta Horticult (ISHS) 363:33–41

    Google Scholar 

  • Mazzola M (1998) Elucidation of the microbial complex having a causal role in the development of apple replant disease in Washington. Phytopathology 88:930–938

    Article  CAS  PubMed  Google Scholar 

  • Mazzola M, Manici LM (2012) Apple replant disease: role of microbial ecology in cause and control. Annu Rev Phytopathol 50:45–65

    Article  CAS  PubMed  Google Scholar 

  • Mazzola M, Brown J, Zhao XW, Izzo AD, Fazio G (2009) Interaction of brassicaceous seed meal and apple rootstock on recovery of Pythium spp. and Pratylenchus penetrans from roots grown in replant soils. Plant Dis 93:51–57

    Article  Google Scholar 

  • Merwin IA, Byard R, Robinson TL, Carpenter S, Hoying SA, Iungerman KA, Fargione M (2001) Developing an integrated program for diagnosis and control of replant problems in New York apple orchards. N Y Fruit Q 9:11–15

    Google Scholar 

  • Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos 62:244–251

    Article  Google Scholar 

  • Rhoades DF, Cates RG (1976) Toward a general theory of plant antiherbivore chemistry. Recent Adv Phytochem 10:168–213

    CAS  Google Scholar 

  • Robinson TL, Hoying SA, Fargione M, Iungerman KA (2002) On-farm trials of the Cornell Geneva apple rootstocks in NY. N Y Fruit Q 10:22–26

    Google Scholar 

  • Robinson TL, Fazio G, Aldwinckle HS, Hoying SA, Russo N (2006) Field performance of Geneva® apple rootstocks in the Eastern USA. Sodinink Darzinink 25:181–191

    Google Scholar 

  • Rogers WS (1939) Root studies VIII. Apple root growth in relation to rootstock, soil, seasonal and climatic factors. J Pomol Hortic Sci 17:99–130

    Google Scholar 

  • Rookes JE, Wright ML, Cahill DM (2008) Elucidation of defence responses and signalling pathways induced in Arabidopsis thaliana following challenge with Phytophthora cinnamomi. Physiol Mol Plant Pathol 72:151–161

    Article  CAS  Google Scholar 

  • Rumberger A, Yao SR, 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 264:247–260

    Article  CAS  Google Scholar 

  • St. Laurent A, Merwin IA, Thies JE (2008) Long-term orchard groundcover management systems affect soil microbial communities and apple replant disease severity. Plant Soil 304:209–225

    Article  CAS  Google Scholar 

  • Tewoldemedhin YT, Mazzola M, Mostert L, McLeod A (2011) Cylindrocarpon species associated with apple tree roots in South Africa and their quantification using real-time PCR. Eur J Plant Pathol 129:637–651

    Article  Google Scholar 

  • van Schoor L, Denman S, Cook NC (2009) Characterisation of apple replant disease under South African conditions and potential biological management strategies. Sci Hortic 119:153–162

    Article  Google Scholar 

  • Watt M, Silk WK, Passioura JB (2006) Rates of root and organism growth, soil conditions, and temporal and spatial development of the rhizosphere. Ann Bot 97:839–855

    Article  PubMed  Google Scholar 

  • Wells CE, Eissenstat DM (2001) Marked differences in survivorship among apple roots of different diameters. Ecology 82:882–892

    Article  Google Scholar 

  • Wells CE, Eissenstat DM (2002) Beyond the roots of young seedlings: the influence of age and order on fine root physiology. J Plant Growth Regul 21:324–334

    Article  CAS  Google Scholar 

  • Woods JO, Carr TG, Price PW, Stevens LE, Cobb NS (1996) Growth of coyote willow and the attack and survival of a mid-rib galling sawfly, Euura sp. Oecologia 108:714–722

    Article  Google Scholar 

  • Yao SR, Merwin IA, Brown MG (2006) Root dynamics of apple rootstocks in a replanted orchard. HortSci 41:1149–1155

    Google Scholar 

  • Yim B, Smalla K, Winkelmann T (2013) Evaluation of apple replant problems based on different soil disinfection treatments—links to soil microbial community structure? Plant Soil 366:617–631

    Article  CAS  Google Scholar 

Download references

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Correspondence to Taryn L. Bauerle.

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Responsible Editor: Alain Pierret.

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Atucha, A., Emmett, B. & Bauerle, T.L. Growth rate of fine root systems influences rootstock tolerance to replant disease. Plant Soil 376, 337–346 (2014). https://doi.org/10.1007/s11104-013-1977-5

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  • DOI: https://doi.org/10.1007/s11104-013-1977-5

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