Trichomes form genotype-specific microbial hotspots in the phyllosphere of tomato

Abstract

Background The plant phyllosphere is a well-studied habitat characterized by low nutrient availability and high community dynamics. In contrast, plant trichomes, known for their production of a large number of metabolites, are a yet unexplored habitat for microbes. We analyzed the phyllosphere as well as trichomes of two tomato genotypes (Solanum lycopersicum LA4024, S. habrochaites LA1777) by targeting bacterial 16S rRNA gene fragments. Results Leaves, leaves without trichomes, and trichomes alone harbored similar abundances of bacteria (108–109 16S rRNA gene copy numbers per gram of sample). In contrast, bacterial diversity was found significantly increased in trichome samples (Shannon index: 4.4 vs. 2.5). Moreover, the community composition was significantly different when assessed with beta diversity analysis and corresponding statistical tests. At the bacterial class level, Alphaproteobacteria (23.6%) were significantly increased, whereas Bacilli (8.6%) were decreased in trichomes. The bacterial family Sphingomonadacea (8.4%) was identified as the most prominent, trichome-specific feature; Burkholderiaceae and Actinobacteriaceae showed similar patterns. Moreover, Sphingomonas was identified as a central element in the core microbiome of trichome samples, while distinct low-abundant bacterial families including Hymenobacteraceae and Alicyclobacillaceae were exclusively found in trichome samples. Niche preferences were statistically significant for both genotypes and genotype-specific enrichments were further observed. Conclusion Our results provide first evidence of a highly specific trichome microbiome in tomato and show the importance of micro-niches for the structure of bacterial communities on leaves. These findings provide further clues for breeding, plant pathology and protection as well as so far unexplored natural pathogen defense strategies.

Histochemical Evidence for Nitrogen-Transfer Endosymbiosis in Non-Photosynthetic Cells of Leaves and Inflorescence Bracts of Angiosperms

“…Secondly, when we removed or reduced bacteria in our seed disinfection and elevated CO 2 experiments, we found that trichomes no longer stained for nitrate ( Figure 12 , Figure 13 and Figure 14 ). Kusstatscher et al [ 90 ] found that tomato leaf trichomes are “hot-spots” for alpha-Proteobacteria (many of which are diazotrophic). Blaskovich et al [ 91 ] showed that cannabinoids in Cannabis sativa trichomes may inhibit some bacteria, but many Gram-negative potential nitrogen fixers were not inhibited.…”

Functions and biosynthesis of plant signaling metabolites mediating plant–microbe interactions

“…Plant-microbe interactions are reciprocal 5,9,262 —plants feed legions of microbes at their own cost, 263 in exchange for other benefits from microbes. 5,7,74,264 Understanding the general principles of how plant metabolites mediate plant–microbe interactions is important for designing strategies for purposely directing plant–microbe interactions toward an outcome benefiting plant health and performance.…”

Distinct Phyllosphere Microbiome of Wild Tomato Species in Central Peru Upon Dysbiosis

“…A spatial niche within the phyllosphere, the trichome microbiome of S. lycopersicum and S. habrochaites, has been described by (Kusstatscher et al, 2020). While they observed similar bacteria richness on leaves of domesticated and wild tomato species, beta diversities were significantly different between leaves and trichomes of tested tomato genotypes in a glass house study (Kusstatscher et al 2020).…”

“…Interestingly, the yeast genus Hannaella was frequently found on the tomato cultivar 'Ganbarune', which suggests that host genotypes impact particular microbes on the phyllosphere of tomatoes (Toju, Okayasu, and Notaguchi 2019). A spatial niche within the phyllosphere, the trichome microbiome of S. lycopersicum and S. habrochaites, has been described by (Kusstatscher et al, 2020). While they observed similar bacteria richness on leaves of domesticated and wild tomato species, beta diversities were significantly different between leaves and trichomes of tested tomato genotypes in a glass house study (Kusstatscher et al 2020).…”