Root growth, function and rhizosphere microbiome analyses show local rather than systemic effects in apple plant response to replant disease soil.

Maik Lucas,Doris Vetterlein,Kornelia Smalla,Alicia Balbín-Suárez,Francisco Martinez-Abarca

doi:10.1371/journal.pone.0204922

Abstract

Apple replant disease (ARD) is the phenomenon of soil decline occurring after repeated planting of apple trees at the same site. This study aimed to elucidate whether ARD is systemic, i.e. whether the contact of parts of the root system with ARD soil causes the whole plant to show poor shoot and root growth. A split-root experiment was conducted with seedlings of ‘M26’, offering the same plant for its root system the choice between the substrates ARD soil (+ARD), γ-sterilized ARD soil (-ARD) or soil from a grass parcel (Control) with the following combinations: +ARD/+ARD, -ARD/-ARD; +ARD/-ARD; +ARD/Control. Root growth was analysed throughout the 34-day growing period. Samples from bulk, rhizosphere and rhizoplane soil were collected separately for each compartment, and analysed by fingerprints of 16S rRNA gene or ITS fragments amplified from total community (TC) DNA. The response of the plant to +ARD was not systemic as root growth in -ARD compartment was always superior to root growth in +ARD soil. Crosswise 15N-labelling of the N-fertilizer applied to the split-root compartments showed that nitrate-N uptake efficiency was higher for roots in -ARD soil compared to those in +ARD. Bacterial and fungal community composition in the rhizoplane and rhizosphere of the same plants differed significantly between the compartments containing +ARD/-ARD or +ARD/Control. The strongest differences between the bacterial fingerprints were observed in the rhizoplane and rhizosphere. Bacterial genera with increased abundance in response to ARD were mainly Streptomyces but also Sphingobium, Novosphingobium, Rhizobium, Lysobacter and Variovorax. The strongest differences between the fungal fingerprints were observed in bulk soil. Our data showed that the response of the apple plant to ARD soil is local and not systemic.

Highlights

Apple replant disease (ARD) in generalThe phenomenon of apple replant disease (ARD), i.e. the reduction of crop productivity in field systems repeatedly planted with apple trees, has been recently reviewed by Mazzola & Manici [1]
In the present experiment plants grown in +ARD/-ARD soil showed shoot growth comparable to plants grown in -ARD/-ARD only, while those from +ARD/+ARD rhizoboxes showed poor shoot growth
For root growth, compensation was observed in -ARD/+ARD or control/+ARD treatment, i.e. if one of the compartments was filled with -ARD soil or control soil, root growth in the +ARD compartment was enhanced compared to +ARD/+ARD

Summary

Introduction

The phenomenon of apple replant disease (ARD), i.e. the reduction of crop productivity in field systems repeatedly planted with apple trees, has been recently reviewed by Mazzola & Manici [1]. It is common to all major apple growing areas of the world, in contrast to other replant diseases, the causal agents are still not known. Replant disease is persistent in soils for many years, while polyphenols are degraded within months [6]. Treating soil with fumigants or sterilizing it alleviates the problem, while diluting pasteurized soil with only 10% ARD soil is sufficient to reduce apple tree growth. Mazzola & Manici [1] concluded that biotic components should be the causal agents. Cylindrocarpon spp., Rhizoctonia solani (Kuhn), Pythium, Phytophthora, and nematodes (Pratylenchus spp.) are assumed to contribute to the disease [4]

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Results

Conclusion