Holo-omics for deciphering plant-microbiome interactions

Abstract

Host-microbiome interactions are recognized for their importance to host health. An improved understanding of the molecular underpinnings of host-microbiome relationships will advance our capacity to accurately predict host fitness and manipulate interaction outcomes. Within the plant microbiome research field, unlocking the functional relationships between plants and their microbial partners is the next step to effectively using the microbiome to improve plant fitness. We propose that strategies that pair host and microbial datasets—referred to here as holo-omics—provide a powerful approach for hypothesis development and advancement in this area. We discuss several experimental design considerations and present a case study to highlight the potential for holo-omics to generate a more holistic perspective of molecular networks within the plant microbiome system. In addition, we discuss the biggest challenges for conducting holo-omics studies; specifically, the lack of vetted analytical frameworks, publicly available tools, and required technical expertise to process and integrate heterogeneous data. Finally, we conclude with a perspective on appropriate use-cases for holo-omics studies, the need for downstream validation, and new experimental techniques that hold promise for the plant microbiome research field. We argue that utilizing a holo-omics approach to characterize host-microbiome interactions can provide important opportunities for broadening system-level understandings and significantly inform microbial approaches to improving host health and fitness.

Transcriptomic and Metabolomic Approaches Deepen Our Knowledge of Plant–Endophyte Interactions

“…Early research on plant-endophyte interactions relied on host agronomic characteristics, composition determination, and strains' isolation, cultivation, and characterization when speculating about the interaction mechanism involved. Nowadays, with the rapid development in high-throughput sequencing, the omics technologies (at the genome, transcriptome, and proteome levels) can provide new insights to elucidate the mechanism of interaction in a given system (Xu et al, 2021). Moreover, when coupled to metabolomic studies, omics-type investigations can gradually resolve aspects of the relationships between endophyte infection, metabolite accumulation, and stress mitigation in host plants.…”

Nutrient and moisture limitation reveal keystone metabolites that link switchgrass rhizosphere metabolome and microbiome dynamics

“…A limited number of studies have used this approach-notably in human gut, lung, urinary tract, wastewater, and biological soil crust systems (22,(32)(33)(34)(35)(36) -but it has not been applied within rhizosphere soils. Linking exometabolite chemistry, microbiome assembly and plant phenotypes under abiotic stress is needed to identify functional links between specific metabolites and microbial lineages (37). These metabolite-driven changes in plant microbiomes will enable us to manipulate microbial communities and optimize plant-microbe interactions in the rhizosphere for better crop health and productivity, particularly in resource limited environments such as marginal soils.…”

Rhizosphere Microbiome: The Emerging Barrier in Plant-Pathogen Interactions

“…Recently, one new experimental technique, the holo-omics strategy, that pairs host and microbial datasets was proposed (Nyholm et al, 2020). The experimental designs pair host-centered omic strategies, such as transcriptomics, metabolomics, epigenomics, and proteomics, with the more commonly used microbial-focused techniques, such as amplicon sequencing, shotgun meta-genomic, meta transcriptomics, and exometabolomics (Xu et al, 2021). Such holo-omic studies have the power to resolve the functionality of a plant microbiome ecosystem and provide significant information about microbial approach to improving host health and fitness, which will only increase in the near future.…”