Temporal and spatial dynamics in the apple flower microbiome in the presence of the phytopathogen Erwinia amylovora

Abstract

Plant microbiomes have important roles in plant health and productivity. However, despite flowers being directly linked to reproductive outcomes, little is known about the microbiomes of flowers and their potential interaction with pathogen infection. Here, we investigated the temporal spatial dynamics of the apple stigma microbiome when challenged with a phytopathogen Erwinia amylovora, the causal agent of fire blight disease. We profiled the microbiome from the stigmas of individual flowers, greatly increasing the resolution at which we can characterize shifts in the composition of the microbiome. Individual flowers harbored unique microbiomes at the operational taxonomic unit level. However, taxonomic analysis of community succession showed a population gradually dominated by bacteria within the families Enterobacteriaceae and Pseudomonadaceae. Flowers inoculated with E. amylovora established large populations of the phytopathogen, with pathogen-specific gene counts of >3.0 × 107 in 90% of the flowers. Yet, only 42% of inoculated flowers later developed fire blight symptoms. This reveals that pathogen abundance on the stigma is not sufficient to predict disease outcome. Our data demonstrate that apple flowers represent an excellent model in which to characterize how plant microbiomes establish, develop, and correlate with biological processes such as disease progression in an experimentally tractable plant organ.

Plant Genotype Shapes the Bacterial Microbiome of Fruits, Leaves, and Soil in Olive Plants

“…For example, the abiotic environment has been reported to strongly drive the composition of the plant microbiome, including soil [ 1 , 2 , 3 ], atmosphere [ 4 ], geography [ 5 , 6 ], and many others. In addition, the plant microbiome is under the influence of many biotic factors, some of them exogenous like herbivory [ 1 , 7 ] or plant diseases [ 8 , 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 , 17 ], some others are instead driven by the plant itself. Indeed, previous studies reported variation in the structure of plant microbiomes according to compartment (e.g., root, leaf, fruit, flower) [ 18 ], but also within the same compartment, for example between different parts of flowers and fruits, or between internal and external tissues [ 18 , 19 ].…”

Complete Genome Sequences of Curtobacterium , Pantoea , Erwinia , and Two Pseudomonas sp. Strains, Isolated from Apple Flower Stigmas from Connecticut, USA

“…1079, were isolated from apple flower stigma samples collected on the apple cultivar ‘Early Macoun’ ( Malus x domestica NY75414-1) planted at Lockwood Farm in Hamden, CT (41.406°N, 72.906°W) ( 1 ). Our previous data showed that Enterobacteriaceae and Pseudomonadaceae are the two predominant families of bacteria on apple stigma ( 2 , 3 ). Within the Enterobacteriaceae , the genera Pantoea and Erwinia were predominant, and within the Pseudomonadaceae , Pseudomonas was the principal genus ( 3 ).…”

“…Our previous data showed that Enterobacteriaceae and Pseudomonadaceae are the two predominant families of bacteria on apple stigma ( 2 , 3 ). Within the Enterobacteriaceae , the genera Pantoea and Erwinia were predominant, and within the Pseudomonadaceae , Pseudomonas was the principal genus ( 3 ). The genus Curtobacterium , belonging to the phylum Actinobacteria , was much less abundant in the microbiome and was investigated as a representative of the apple stigma “rare biosphere” ( 3 ).…”

“…Within the Enterobacteriaceae , the genera Pantoea and Erwinia were predominant, and within the Pseudomonadaceae , Pseudomonas was the principal genus ( 3 ). The genus Curtobacterium , belonging to the phylum Actinobacteria , was much less abundant in the microbiome and was investigated as a representative of the apple stigma “rare biosphere” ( 3 ). These four strains were identified in our previous study by 16S rRNA gene comparisons ( 1 ).…”

Bacterial Quorum-Quenching Lactonase Hydrolyzes Fungal Mycotoxin and Reduces Pathogenicity of Penicillium expansum—Suggesting a Mechanism of Bacterial Antagonism

“…The apple microbiome depends on many factors such as genotype, management practices, and more [1,[47][48][49][50][51]. A recent study indicated that the abundance and distribution of bacterial phyla in the "Royal Gala" apple fruit were consistent in most examined countries [1].…”