Root exposure to apple replant disease soil triggers local defense response and rhizoplane microbiome dysbiosis

Abstract

A soil column split-root experiment was designed to investigate the ability of apple replant disease (ARD) causing agents to spread in soil. ‘M26’ apple rootstocks grew into a top layer of Control soil, followed by a barrier-free split-soil layer (Control soil/ARD soil). We observed a severely reduced root growth, concomitant with enhanced gene expression of phytoalexin biosynthetic genes and phytoalexin content in roots from ARD soil, indicating a pronounced local plant defense response. Amplicon sequencing (bacteria, archaea, fungi) revealed local shifts in diversity and composition of microorganisms in the rhizoplane of roots from ARD soil. An enrichment of OTUs affiliated to potential ARD fungal pathogens (Ilyonectria and Nectria sp.) and bacteria frequently associated with ARD (Streptomyces, Variovorax) was noted. In conclusion, our integrated study supports the idea of ARD being local and not spreading into surrounding soil, as only the roots in ARD soil were affected in terms of growth, phytoalexin biosynthetic gene expression, phytoalexin production, and altered microbiome structure. This study further reinforces the microbiological nature of ARD, being likely triggered by a disturbed soil microbiome enriched with low mobility ARD-causing agents that induce a strong plant defense and rhizoplane microbiome dysbiosis, concurring with root damage.

Comprehensive Analysis of the Influence of Fulvic Acid from Paper Mill Effluent on Soil Properties, Soil Microbiome, and Growth of Malus hupehensis Rehd. Seedlings under Replant Conditions

“…ARD is a soil-borne disease caused by a complex of the imbalance of nutrient elements, soil property deterioration, allelopathy accumulation, and shifts in bacterial and fungal communities . Biotic factors, including explosive reproduction of harmful fungi and the deterioration of the microbial community structure after long-term planting of fruit trees, are recognized as the dominant factor resulting in ARD. , In recent years, broad-spectrum fumigants, such as methyl bromide, which indiscriminately kill most soil microorganisms, have favorable effects in controlling ARD.…”

Identification of Candidate Genes Associated With Tolerance to Apple Replant Disease by Genome-Wide Transcriptome Analysis

“…However, a relationship between ARD severity and the production of terpenoid phytoalexins in the plant has not been observed to date. Several studies on ARD demonstrated remarkably higher contents of biphenyl and dibenzofuran phytoalexins in plants cultivated in ARD soils compared to disinfected ARD soils ( Winkelmann et al, 2019 ; Reim et al, 2020 ; Rohr et al, 2020b ; Balbin-Suarez et al, 2021 ; Busnena et al, 2021 ). However, Reim et al (2020) showed that the genes coding for biosynthesis of these phytoalexins were more strongly induced in the susceptible rootstock ‘M9’ than in the ARD tolerant genotype Mr5, indicating that these phytoalexin compounds do not help against ARD.…”

The Phlorizin-Degrading Bacillus licheniformis XNRB-3 Mediates Soil Microorganisms to Alleviate Apple Replant Disease

“…This disease is most harmful to young replanted trees, and it can reduce the growth of trees, increase the susceptibility of trees to diseases, discolor roots, result in root tip necrosis, and reduce root biomass, which can ultimately lead to plant death within the first growing season. Furthermore, the yield and quality of fruit trees more than 20 years old is decreased in plants with ARD, and death can occur in severe cases ( Mazzola and Manici, 2012 ; Yim et al, 2020 ; Balbín-Suárez et al, 2021 ). An increasing number of studies have shown that biotic factors are the main factors that cause ARD, including nematodes ( Pratylenchus spp.…”