The Arabidopsis holobiont: a (re)source of insights to understand the amazing world of plant–microbe interactions

Environmental Microbiome (2023) 18:9 Poupin et al. Environmental Microbiome https://doi.org/10.1186/s40793-023-00466-0 Open Access REVIEW The Arabidopsis holobiont: a (re)source of insights to understand the amazing world of plant–microbe interactions M. J. Poupin1,2,3, T. Ledger1,2,3, R. Roselló‑Móra4 and B. González1,2,3* Abstract As holobiont, a plant is intrinsically connected to its microbiomes. However, some characteristics of these microbi‑ omes, such as their taxonomic composition, biological and evolutionary role, and especially the drivers that shape them, are not entirely elucidated. Reports on the microbiota of Arabidopsis thaliana first appeared more than ten years ago. However, there is still a lack of a comprehensive understanding of the vast amount of information that has been generated using this holobiont. The main goal of this review was to perform an in-depth, exhaustive, and systematic analysis of the literature regarding the Arabidopsis–microbiome interaction. A core microbiota was identified as com‑ posed of a few bacterial and non-bacterial taxa. The soil (and, to a lesser degree, air) were detected as primary micro‑ organism sources. From the plant perspective, the species, ecotype, circadian cycle, developmental stage, environ‑ mental responses, and the exudation of metabolites were crucial factors shaping the plant–microbe interaction. From the microbial perspective, the microbe-microbe interactions, the type of microorganisms belonging to the microbiota (i.e., beneficial or detrimental), and the microbial metabolic responses were also key drivers. The underlying mecha‑ nisms are just beginning to be unveiled, but relevant future research needs were identified. Thus, this review provides valuable information and novel analyses that will shed light to deepen our understanding of this plant holobiont and its interaction with the environment. Keywords Arabidopsis, Bacteria, Community, Fungi, Microbiota, Plant, Plant-growth-promotion-rhizobacteria, Plantroot-exudates, Rhizosphere *Correspondence: B. González 1 Laboratorio de Bioingeniería, Facultad de Ingeniería y Ciencias, Universidad Adolfo Ibáñez, 7941169 Santiago, Chile 2 Center of Applied Ecology and Sustainability (CAPES), Santiago, Chile 3 Millennium Nucleus for the Development of Super Adaptable Plants (MN-SAP), Santiago, Chile 4 Marine Microbiology Group, Department of Animal and Microbial Biodiversity, Mediterranean Institute for Advanced Studies (IMEDEA UIBCSIC), Illes Balears, Majorca, Spain Introduction The realization that all animal and plant species harbor complex associated microbial communities (the microbiota) in their surfaces as well as and inner parts is relatively recent in Biology [17]. Furthermore, the holistic view of the holobiont represented by the conjunction of a macro-organism and its microbiome (the associated microorganisms and their collective genomes) is even newer [26]. For decades, our understanding of these inter-kingdom interactions increased thanks to studies of plant or animal models interacting with single microbial species, such as pathogens and, to a lesser degree, beneficial microorganisms. However, the characteristics of the microbiome in experimental model © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativeco mmons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Poupin et al. Environmental Microbiome (2023) 18:9 species regarding their taxonomic composition, biological role, and especially the drivers that shape those microbiomes are far from being completely understood. Plants are holobiont harboring microorganisms in their internal and external tissues [43, 65, 72, 192] (Fig. 1A). Therefore, plant fitness, environmental responses, adaptation, and evolution should be addressed, considering plants as complex dynamic entities controlled by the hologenome: the host genome plus all the genomes of the microbiome. Page 2 of 26 After rice (Oryza sativa), Arabidopsis thaliana is the second most studied plant species and has proven to be a valuable model in plant sciences [37, 144, 185], specifically to get insights into plant development and responses to the environment [92, 144]. As with other well-studied biological models, a few studies targeting A. thaliana interactions with bacterial populations were available at the beginning of this century, mainly using culture-dependent molecular approaches (e.g., [63, 91]. Since then, a great deal of information has been obtained Fig. 1 Features and connections in the Arabidopsis microbiota. A The distribution of the main microbial taxa among different plant compartments is represented by symbols explained in the boxes at the bottom of the figure; light blue for bacterial phyla and light orange for fungal phyla, while relative abundances of the major phyla are represented next to each compartment [20, 22, 23, 30, 60, 85, 191]. B Connections among the microbiota of compartments and their different sources (inputs) of inoculation. The arrow width represents the relative contributions of the sources based on the percentage of each source input with respect to the total input. Dashed lines represent minor influences. Roots comprise endorhizosphere plus rhizoplane. Leaves comprise the endophyllosphere plus the epiphyllosphere. Names of the taxa are Pseudomonadota, Actinomycetota, Bacillota, Bacteroidota, Acidobacteriota, Chloroflexota, Cyanobacteriota, Planctomycetota, Basidiomycota, Ascomycota, Zygomycota, and Mucoromycota, formerly Proteobacteria, Actinobacteria, Firmicutes, Bacteroidetes, Acidobacteria, Chloroflexi, Cyanobacteria, Planctomycetes, Basidiomycetes, Ascomycetes, Zygomycetes, and Mucoromycetes, respectively Poupin et al. Environmental Microbiome (2023) 18:9 with culture-independent molecular techniques and, more recently, with omics approaches. Massive sequencing allows statistically significant comparisons among plant compartments using Operational Taxonomic Units (OTUs) or a more accurate manually supervised clustering of O (...truncated)