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Link to original content: https://pubmed.ncbi.nlm.nih.gov/34823272
Evidence for host-microbiome co-evolution in apple - PubMed Skip to main page content
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. 2022 Jun;234(6):2088-2100.
doi: 10.1111/nph.17820. Epub 2021 Nov 25.

Evidence for host-microbiome co-evolution in apple

Ahmed Abdelfattah  1   2 , Ayco J M Tack  3 , Birgit Wasserman  1 , Jia Liu  4 , Gabriele Berg  1   2   5 , John Norelli  6 , Samir Droby  7 , Michael Wisniewski  8
Affiliations

Evidence for host-microbiome co-evolution in apple

Ahmed Abdelfattah et al. New Phytol. 2022 Jun.

Abstract

Plants evolved in association with a diverse community of microorganisms. The effect of plant phylogeny and domestication on host-microbiome co-evolutionary dynamics are poorly understood. Here we examined the effect of domestication and plant lineage on the composition of the endophytic microbiome of 11 Malus species, representing three major groups: domesticated apple (M. domestica), wild apple progenitors, and wild Malus species. The endophytic community of M. domestica and its wild progenitors showed higher microbial diversity and abundance than wild Malus species. Heirloom and modern cultivars harbored a distinct community composition, though the difference was not significant. A community-wide Bayesian model revealed that the endophytic microbiome of domesticated apple is an admixture of its wild progenitors, with clear evidence for microbiome introgression, especially for the bacterial community. We observed a significant correlation between the evolutionary distance of Malus species and their microbiome. This study supports co-evolution between Malus species and their microbiome during domestication. This finding has major implications for future breeding programs and our understanding of the evolution of plants and their microbiomes.

Keywords: bacterial community; endophytes; fungal community; microbial introgression; microbiota; phylosymbiosis.

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Figures

Fig. 1
Fig. 1
A conceptual figure on the impact of domestication on the plant endophytic microbiome. (a) A phylogenetic distance among Malus species which contains wild species (black branches) and progenitor wild species (blue branches). The extended green branch represents Malus domestica with its close affiliation its main ancestor (M. sieversii). Dashed lines indicate introgression events between Malus progenitors which contributed to the formation of M. domestica. (b) The predicted three scenarios: Scenario 1, reduction in species diversity due to loss in microbial species; Scenario 2, increase in microbial diversity due to introgressive hybridization during the apple domestication; Scenario 3, diversity was not affected by domestication.
Fig. 2
Fig. 2
Box plots showing fungal (a–c) and bacterial (d–f) richness, Shannon diversity and community composition. The presented species were grouped into three groups from left to right: heirloom and modern cultivars of domesticated apple (Malus × domestica), wild progenitors (M. orientalis, M. prunifolia, M. sieversii, and M. sylvestris), and nonprogenitor Malus species (M. angustifolia, M. coronaria, M. ioensis, M. kansuensis, M. prattii, and M. yunnanensis). Superimposed on the box plots are the horizontally jittered raw data points combined for each domestication group. Box plots show the median (horizontal line), the lower and upper bounds of each box plot denote the first and third quartiles, and whiskers above and below the box plot show 1.5 times the interquartile range. The points located outside of the whiskers of the box plot represent the outliers. Ordination plots of fungal (c) and bacterial (f) community composition of Malus × domestica, wild progenitors and wild Malus species, based Bray–Curtis dissimilarity index. Results of the global statistical analyses are reported at the top of each panel and pairwise comparisons for alpha diversity are added onto the box plots.
Fig. 3
Fig. 3
Dendrogram based on the similarity of the core fungal (a) and bacterial (b) community composition, according to Bray–Curtis index among Malus domestica cultivars, highlighting the difference between heirloom and modern cultivars. The dendrograms were visualized using the fviz_dend function in the R package factoextra v.1.0.7. Results of the global statistical analyses are reported at the top of each panel. (c) Network analysis showing the core microbiome distribution from wild Malus species, to progenitors, to domesticated apple. Blue and red circles (nodes) represent fungal and bacterial taxa, respectively. The core microbiome was calculated for each Malus group separately as amplicon sequence variants present in at least 70% of the samples. Node size corresponds to bacterial and fungal abundance, i.e. gene copy numbers measured by qPCR, as indicated in the legend on the lower left.
Fig. 4
Fig. 4
Results of hierarchical clustering based on Bray–Curtis dissimilarity distances of the fungal (a) and bacterial (b) community composition using clustering method ‘average’. (c) Shows the phylogenetic tree based on Malus ITS gene. Malus phylogenetic distance was inferred by using the neighbor‐joining tree estimation in R package phangorn. The leaf color indicates Malus groups: green = Malus × domestica and its wild progenitors (M. sieversii, M. orientalis, M. prunifolia, and M. sylvestris), blue = North American species (M. angustifolia, M. coronaria, and M. ioensis), and red = Asian species (M. kansuensis, M. yunnanensis, and M. prattii). The phylogenic plots were visualized using the fviz_dend function in the R package factoextra v.1.0.7.
Fig. 5
Fig. 5
Treemap charts showing the estimated sources of the fungal (a) and bacterial (b) communities in Malus domestica. The estimates were calculated using Bayesian approach as implemented in SourceTracker2 by setting M. domestica as the sole sink and all the other Malus species (M. sieversii, M. orientalis, M. prunifolia, M. sylvestris, M. kansuensis, M. yunnanensis, M. angustifolia, M. coronaria, M. ioensis, and M. prattii) as potential sources. An unknown source was added automatically by the algorithm to allocate taxa in M. domestica with low probability to have originated from any of the assigned sources. The fungal and bacterial communities were rarefied to 1500 reads per sample in both the sink and sources.
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