Replant diseases are a common occurrence in perennial cropping systems. In apple, progress toward the development of a universally effective disease management strategy, beyond the use of broad-spectrum soil fumigants, is impeded by inconsistencies in defining replant disease etiology. A preponderance of evidence attributes apple replant disease to plant-induced changes in the soil microbiome including the proliferation of soilborne plant pathogens. Findings from alternative studies suggest that the contribution of abiotic factors, such as the accumulation of phenolic detritus from previous orchard plantings, may play a part as well. Engineering of the resident soil microbiome using resource-based strategies is demonstrating potential to limit activity of replant pathogens and improve productivity in newly established orchards. An understanding of factors promoting the assembly of a disease-suppressive soil microbiome along with consideration of host factors that confer disease tolerance or resistance is imperative to the developing a more holistic view of orchard ecosystem dynamics. Here, we review the literature concerning the transition of orchard soil from a healthy state to a replant disease-conducive state. Included in the scope of this review are studies on the influence of soil type and geography on the apple replant pathogen complex. Furthermore, several tolerance and innate resistance mechanisms that have been described in apple to date, including the role of root chemistry/exudates are discussed. Finally, the interplay between apple rootstock genotype and key resource-based strategies which have been shown to “reshape” the plant holobiont in favor of a more prophylactic or disease-suppressive state is highlighted.

The effect of plant cultivar on the degree of mycorrhization and the benefits mediated by arbuscular mycorrhizal fungi (AMF) have been documented in many crops. In apple, a wide variety of rootstocks are commercially available; however, it is not clear whether some rootstock genotypes are more susceptible to mycorrhization than others and/or whether AMF species identity influences rootstock compatibility. This study addresses these questions by directly testing the ability/efficacy of four different AMF species (Rhizophagus irregularis, Septoglomus deserticola, Claroideoglomus claroideum or Claroideoglomus etunicatum) to colonize a variety of commercially available Geneva apple rootstock genotypes (G.11, G.41, G.210, G.969, and G.890). Briefly, micropropagated plantlets were inoculated with individual species of AMF or were not inoculated. The effects of the rootstock genotype/AMF interaction on mycorrhization, plant growth, and/or leaf nutrient concentrations were assessed. We found that both rootstock genotype and the identity of the AMF are significant sources of variation affecting the percentage of colonization. However, these factors largely operate independently in terms of the extent of root colonization. Among the AMF tested, C. etunicatum and R. irregularis represented the most compatible fungal partners, regardless of apple rootstock genotype. Among the rootstocks tested, semi-dwarfing rootstocks appeared to have an advantage over dwarfing rootstocks in regard to establishing and maintaining associations with AMF. Nutrient uptake and plant growth outcomes were also influenced in a rootstock genotype/AMF species-specific manner. Our findings suggest that matching host genetics with compatible AMF species has the potential to enhance agricultural practices in nursery and orchard systems.

The exchange of metabolites (i.e., metabolic interactions) between bacteria in the rhizosphere determines various plant-associated functions. Systematically understanding the metabolic interactions in the rhizosphere, as well as in other types of microbial communities, would open the door to the optimization of specific predefined functions of interest, and therefore to the harnessing of the functionality of various types of microbiomes. However, mechanistic knowledge regarding the gathering and interpretation of these interactions is limited. Here, we present a framework utilizing genomics and constraint-based modeling approaches, aiming to interpret the hierarchical trophic interactions in the soil environment. 243 genome scale metabolic models of bacteria associated with a specific disease-suppressive vs disease-conducive apple rhizospheres were drafted based on genome-resolved metagenomes, comprising an in silico native microbial community. Iteratively simulating microbial community members’ growth in a metabolomics-based apple root-like environment produced novel data on potential trophic successions, used to form a network of communal trophic dependencies. Network-based analyses have characterized interactions associated with beneficial vs non-beneficial microbiome functioning, pinpointing specific compounds and microbial species as potential disease supporting and suppressing agents. This framework provides a means for capturing trophic interactions and formulating a range of testable hypotheses regarding the metabolic capabilities of microbial communities within their natural environment. Essentially, it can be applied to different environments and biological landscapes, elucidating the conditions for the targeted manipulation of various microbiomes, and the execution of countless predefined functions.

Arbuscular mycorrhizal fungi (AMF) are promoted as commercial bioinoculants for sustainable agriculture. Little is known, however, about the survival of AMF inoculants in soil and their impacts on native or pre-established AMF communities in root tissue. The current study was designed to assess the stability of pre-existing/nursery-derived AMF in apple rootstocks after being planted into soil containing a known community of AMF with a limited number of species. Root-associated endophytic communities (bacteria and fungi) are known to differ depending on apple rootstock genotype. Thus, an additional aim of this study was to explore the effect of apple rootstock genotype on AMF community structure. A greenhouse experiment was conducted in which a variety of apple rootstock genotypes (G.890, G.935, M.26, and M.7) were inoculated with a commercially available, multi-species AMF consortium. Nursery-derived AMF communities were sequenced, and changes to AMF community structure following cultivation in pasteurized soil (inoculated and non-inoculated) were assessed using a Glomeromycota-specific phylogenetic tree, which included 91 different AMF species from 24 genera. Results show that inoculant colonization potential was limited and that apple rootstocks serve as a significant source of inoculum from the nursery where they are produced. Rootstocks established relationships with introduced AMF in a genotype-specific manner. Regardless of colonization success, however, the inoculant caused alterations to the resident AMF communities of both Geneva and Malling rootstocks, particularly low abundance taxa. In addition, phylogeny-based analysis revealed a unique, well-supported clade of unknown taxonomy, highlighting the importance of using phylogenetic-based classification for accurate characterization of AMF communities. IMPORTANCE: Understanding the impacts of introduced AMF on residential AMF communities is essential to improving plant productivity in nursery and orchard systems. In general, there is a dearth of data on the interactions of commercial AMF inoculants with pre-established AMF communities living in symbiosis with the host plant. The interplay between apple rootstock genotype and the endophytic root microbiome is also an area where more research is needed. This study demonstrates the potential for nursery-established AMF associations to be maintained when transplanted into the field. In addition to providing insight into rootstock/AMF associations, our study calls attention to the current issues attendant with relying on web-based databases for determining AMF identity. The use of phylogenetic tools represents one possible solution and may be of value to industry practitioners in terms of improving product composition and consistency.

Brassicaceae seed meal (SM) soil amendment has been utilized as an effective strategy to control the biological complex of organisms, which includes oomycetes, fungi, and parasitic nematodes, that incites the phenomenon termed apple replant disease. Soil-borne disease control attained in response to Brassicaceae SM amendment is reliant on multiple chemical and biological attributes, including specific SM-generated modifications to the soil/rhizosphere microbiome. In this study, we conducted a comparative analyses of apple root gene expression as influenced by rootstock genotype combined with a seed meal (SM) soil amendment. Apple replant disease (ARD) susceptible (M.26) and tolerant (G.210) rootstocks cultivated in SM-amended soil exhibited differential gene expression relative to corresponding non-treated control (NTC) orchard soil. The temporal dynamics of gene expression indicated that the SM-amended soil system altered the trajectory of the root transcriptome in a genotype-specific manner. In both genotypes, the expression of genes related to plant defense and hormone signaling were altered in SM-amended soil, suggesting SM-responsive phytohormone regulation. Altered gene expression was temporally associated with changes in rhizosphere microbiome density and composition in the SM-treated soil. Gene expression analysis across the two rootstocks cultivated in the pathogen-infested NTC soil showed genotype-specific responses indicative of different defensive strategies. These results are consistent with previously described resistance mechanisms of ARD “tolerant” rootstock cultivars and also add to our understanding of the multiple mechanisms by which SM soil amendment and the resulting rhizosphere microbiome affect apple rootstock physiology. Future studies which assess transcriptomic and metagenomic data in parallel will be important for illuminating important connections between specific rhizosphere microbiota, gene-regulation, and plant health.

Currently, there are no standard management practices to counteract the adverse effects of fumigation on the soil microbiome. In this study, a variety of pre-plant soil amendments were examined for their ability to recruit and maintain apple rhizosphere microbiomes that are suppressive to pathogen re-infestation of fumigated orchard soils. The capacity of these amendments to improve other characteristics of soil productivity was also evaluated. Results suggest that composted chicken manure and liquid chitin are likely to be detrimental to plant and soil health when used as a post-fumigation soil amendment. In comparison, insect frass (IF) resulted in a significant increase in tree trunk diameter relative to the fumigated control. Following pathogen re-infestation of fumigated soil, however, IF induced a significant increase in Pythium ultimum in the rhizosphere. Therefore, IF can benefit the growth of young apple trees in fumigated soil but may stimulate pathogen activity upon re-infestation. To date, the possibility of using soil amendments to suppress pathogen re-infestation of fumigated soils has not been tested. Results from this study ground support the use of soil amendments as an intervention strategy for “steering” the soil and rhizosphere microbiome in more beneficial and/or prophylactic directions following fumigation.