Toward a holistic view of orchard ecosystem dynamics: A comprehensive review of the multiple factors governing development or suppression of apple replant disease

Somera, Tracey S.; Mazzola, Mark

doi:10.3389/fmicb.2022.949404

Cited by 15 publications

(11 citation statements)

References 138 publications

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“…However, no significant differences in oomycetes alpha diversity metrics were identified between matrices, except that the healthy rhizosphere had a reduced number of observed features relative to the diseased rhizosphere. This trend was also observed for fungal and bacterial communities and may suggest a dramatic shift in the way microbial communities interact with each other and with the host ( Somera and Mazzola, 2022 ).…”

Section: Discussionmentioning

confidence: 65%

Soil, rhizosphere, and root microbiome in kiwifruit vine decline, an emerging multifactorial disease

Guaschino,

Garello,

Nari

et al. 2024

Front. Microbiol.

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Kiwifruit vine decline syndrome (KVDS) is characterized by severe root system impairment, which leads to irreversible wilting of the canopy. Plants usually collapse rapidly from the appearance of the first aboveground symptoms, without recovery even in the following seasons. The syndrome has been negatively impacting kiwifruit yield in different areas of Italy, the main producing European country, since its first outbreak in 2012. To date, a unique, common causal factor has yet to be found, and the syndrome is referred to as multifactorial. In this article, we investigated the whole biotic community (fungi, bacteria, and oomycetes) associated with the development of KVDS in three different belowground matrices/compartments (soil, rhizosphere, and root). Sampling was performed at both healthy and affected sites located in the main kiwifruit-producing area of Northwestern Italy. To address the multifactorial nature of the syndrome and to investigate the potential roles of abiotic factors in shaping these communities, a physicochemical analysis of soils was also performed. This study investigates the associations among taxonomic groups composing the microbiome and also between biotic and abiotic factors. Dysbiosis was considered as a driving event in shaping KVDS microbial communities. The results obtained from this study highlight the role of the oomycete genus Phytopythium, which resulted predominantly in the oomycete community composition of diseased matrices, though it was also present in healthy ones. Both bacterial and fungal communities resulted in a high richness of genera and were highly correlated to the sampling site and matrix, underlining the importance of multiple location sampling both geographically and spatially. The rhizosphere community associated with KVDS was driven by a dysbiotic process. In addition, analysis of the association network in the diseased rhizosphere revealed the presence of potential cross-kingdom competition for plant-derived carbon between saprobes, oomycetes, and bacteria.

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Section: Discussionmentioning

confidence: 65%

Soil, rhizosphere, and root microbiome in kiwifruit vine decline, an emerging multifactorial disease

Guaschino,

Garello,

Nari

et al. 2024

Front. Microbiol.

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“…Several studies claimed that Fusarium was one of the primary causal pathogens of ARD in China (Wang et al 2018 ; Jiang et al 2022 ). However, there are no studies so far providing clear evidence for the contribution of Fusarium to ARD as discussed by Somera and Mazzola ( 2022 ). Our study revealed two ASVs assigned to Fusarium to occur in significantly higher relative abundance in ARD than grass soil.…”

Section: Discussionmentioning

confidence: 99%

“…Apple replant disease (ARD) is a phenomenon occurring in tree nurseries and apple orchards worldwide. Replanting apples on the same soil as previous apple cultures leads to severe disease symptoms, resulting in reduced plant growth and yield losses (Mazzola and Manici 2012 ; Winkelmann et al 2019 ; Somera and Mazzola 2022 ). Despite decades of research trying to elucidate the etiology of ARD, the disease is still not fully understood.…”

Section: Introductionmentioning

confidence: 99%

“…Over the past years, alternatives to soil fumigation like spatial reorganization of planting in the orchards, biofumigation, or breeding of tolerant rootstocks have been evaluated (Leinfelder and Merwin 2006 ; Rumberger et al 2007 ; Yim et al 2016 , 2017 ). Surprisingly, reports on the effects of microbial inoculants on the rhizosphere microbiome and the response of the plant in ARD-affected soils are rare (Somera and Mazzola 2022 ). Only a few studies investigated the effect of beneficial bacteria, mainly members of the genus Bacillus , with regard to ARD, focusing on plant growth but typically not considering effects on the microbiome (Utkhede et al 2001 ; Karlidag et al 2007 ; Duan et al 2021 , 2022a , 2022b ).…”

Section: Introductionmentioning

confidence: 99%

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Rhizosphere competent inoculants modulate the apple root–associated microbiome and plant phytoalexins

Hauschild,

Orth,

Liu

et al. 2024

Appl Microbiol Biotechnol

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Modulating the soil microbiome by applying microbial inoculants has gained increasing attention as eco-friendly option to improve soil disease suppressiveness. Currently, studies unraveling the interplay of inoculants, root-associated microbiome, and plant response are lacking for apple trees. Here, we provide insights into the ability of Bacillus velezensis FZB42 or Pseudomonas sp. RU47 to colonize apple root-associated microhabitats and to modulate their microbiome. We applied the two strains to apple plants grown in soils from the same site either affected by apple replant disease (ARD) or not (grass), screened their establishment by selective plating, and measured phytoalexins in roots 3, 16, and 28 days post inoculation (dpi). Sequencing of 16S rRNA gene and ITS fragments amplified from DNA extracted 28 dpi from different microhabitat samples revealed significant inoculation effects on fungal β-diversity in root-affected soil and rhizoplane. Interestingly, only in ARD soil, most abundant bacterial amplicon sequence variants (ASVs) changed significantly in relative abundance. Relative abundances of ASVs affiliated with Enterobacteriaceae were higher in rhizoplane of apple grown in ARD soil and reduced by both inoculants. Bacterial communities in the root endosphere were not affected by the inoculants but their presence was indicated. Interestingly and previously unobserved, apple plants responded to the inoculants with increased phytoalexin content in roots, more pronounced in grass than ARD soil. Altogether, our results indicate that FZB42 and RU47 were rhizosphere competent, modulated the root-associated microbiome, and were perceived by the apple plants, which could make them interesting candidates for an eco-friendly mitigation strategy of ARD. Key points • Rhizosphere competent inoculants modulated the microbiome (mainly fungi) • Inoculants reduced relative abundance of Enterobacteriaceae in the ARD rhizoplane • Inoculants increased phytoalexin content in roots, stronger in grass than ARD soil

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“…Furthermore, such dominant players may vary amongst replant sites and soil types [ 4 ]. Moreover, like other plant diseases, ARD disease occurrence is often associated with changes in microbiome structure, diversity, and function [ 9 , 10 , 11 ], which can influence microbial domination.…”

Section: Introductionmentioning

confidence: 99%

Apple Root Microbiome as Indicator of Plant Adaptation to Apple Replant Diseased Soils

et al. 2023

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The tree fruit industry in Nova Scotia, Canada, is dominated by the apple (Malus domestica) sector. However, the sector is faced with numerous challenges, including apple replant disease (ARD), which is a well-known problem in areas with intensive apple cultivation. A study was performed using 16S rRNA/18S rRNA and 16S rRNA/ITS2 amplicon sequencing to assess soil- and root-associated microbiomes, respectively, from mature apple orchards and soil microbiomes alone from uncultivated soil. The results indicated significant (p < 0.05) differences in soil microbial community structure and composition between uncultivated soil and cultivated apple orchard soil. We identified an increase in the number of potential pathogens in the orchard soil compared to uncultivated soil. At the same time, we detected a significant (p < 0.05) increase in relative abundances of several potential plant-growth-promoting or biocontrol microorganisms and non-fungal eukaryotes capable of promoting the proliferation of bacterial biocontrol agents in orchard soils. Additionally, the apple roots accumulated several potential PGP bacteria from Proteobacteria and Actinobacteria phyla, while the relative abundances of fungal taxa with the potential to contribute to ARD, such as Nectriaceae and plant pathogenic Fusarium spp., were decreased in the apple root microbiome compared to the soil microbiome. The results suggest that the health of a mature apple tree can be ascribed to a complex interaction between potential pathogenic and plant growth-promoting microorganisms in the soil and on apple roots.

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Toward a holistic view of orchard ecosystem dynamics: A comprehensive review of the multiple factors governing development or suppression of apple replant disease

Cited by 15 publications

References 138 publications

Soil, rhizosphere, and root microbiome in kiwifruit vine decline, an emerging multifactorial disease

Soil, rhizosphere, and root microbiome in kiwifruit vine decline, an emerging multifactorial disease

Rhizosphere competent inoculants modulate the apple root–associated microbiome and plant phytoalexins

Apple Root Microbiome as Indicator of Plant Adaptation to Apple Replant Diseased Soils

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