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

Abstract

Plants are colonized by myriads of microbes across kingdoms, which affect host development, fitness, and reproduction. Hence, plant microbiomes have been explored across a broad range of host species, including model organisms, crops, and trees under controlled and natural conditions. Tomato is one of the world’s most important vegetable crops; however, little is known about the microbiota of wild tomato species. To obtain insights into the tomato microbiota occurring in natural environments, we sampled epiphytic microbes from leaves of four tomato species, Solanum habrochaites, S. corneliomulleri, S. peruvianum, and S. pimpinellifolium, from two geographical locations within the Lima region of Peru over 2 consecutive years. Here, a high-throughput sequencing approach was applied to investigate microbial compositions including bacteria, fungi, and eukaryotes across tomato species and geographical locations. The phyllosphere microbiome composition varies between hosts and location. Yet, we identified persistent microbes across tomato species that form the tomato microbial core community. In addition, we phenotypically defined healthy and dysbiotic samples and performed a downstream analysis to reveal the impact on microbial community structures. To do so, we compared microbial diversities, unique OTUs, relative abundances of core taxa, and microbial hub taxa, as well as co-occurrence network characteristics in healthy and dysbiotic tomato leaves and found that dysbiosis affects the phyllosphere microbial composition in a host species-dependent manner. Yet, overall, the present data suggests an enrichment of plant-promoting microbial taxa in healthy leaves, whereas numerous microbial taxa containing plant pathogens occurred in dysbiotic leaves.Concluding, we identify the core phyllosphere microbiome of wild tomato species, and show that the overall phyllosphere microbiome can be impacted by sampling time point, geographical location, host genotype, and plant health. Future studies in these components will help understand the microbial contribution to plant health in natural systems and can be of use in cultivated tomatoes.

Biotic and abiotic stress distinctly drive the phyllosphere microbial community structure

“…Inoculation with the Xanthomonas resulted in fewer Firmicutes and Actinobacteria in both cultivars at the end season. Similar findings of disrupting the abundance of Firmicutes and Actinobacteria upon dysbiosis have been reported both in the phyllosphere and rhizosphere (71,78,79). Inoculation also significantly negatively affected the relative abundance of various genera, including Pseudomonas, Pantoea , and Methylobacterium .…”

Microbial communities living inside plant leaves or on the leaf surface are differently shaped by environmental cues

“…Geographical locations, plant compartment and growing season are among the main ecological factors that shape the microbial communities in natural plants. Despite some research has been conducted on the impact of geographical locations, compartment and short period of time on the formation of microbial communities in natural plants [13,[41][42][43][44], there is still a lack of studies exploring the role of abiotic factors in shaping microbial communities throughout the plants growing seasons over several plant generations. A further question not studied so far is to what extent does the stability of biotic interaction networks are susceptible to abiotic factors?…”

“…The second critical process is deterministic, which includes environmental factors and biotic interactions [9]. Apart from these factors, the microbiome can be impacted by sampling time point, geographical location and host genotype [13]. A comparison of root microbiota in various plants (maize, sorghum, and wheat) revealed that these plants had distinct community compositions.…”

Small‐spored Alternaria spp. (section Alternaria) are common pathogens on wild tomato species

“…Specifically targeting leaves with infection symptoms throughout these regions, we found that Alternaria spp. are omnipresent on the leaves but that P. infestans was rare or absent (Runge et al, 2022). Taking into account that we and other studies previously found clearly quantifiable differences in resistance against A. solani between and within wild tomato populations (Chaerani & Voorrips, 2006; Stam et al, 2017) we focused specifically on the diversity of Alternaria and closely related fungal genera.…”