plant holobiont plant holobiont since the colonization of land by ancestral plant lineages 450 million years ago, plants and their associated microbes have been interacting with each other, forming an assemblage of species that is often referred to as a holobiont. selective pressure acting on holobiont components has likely shaped plant-associated microbial communities and selected for host-adapted microorganisms that impact plant fitness. however, the high microbial densities detected on plant tissues, together with the fast generation time of microbes and their more ancient origin compared to their host, suggest that microbe-microbe interactions are also important selective forces sculpting complex microbial assemblages in the phyllosphere, rhizosphere, and plant endosphere compartments. part of a series onmicrobiomes plant microbiomes endosphere phyllosphere rhizosphere laimosphere root microbiome soil microbiome spermosphere marine microbiomes seagrass coral cetacean marine microbial symbiosis human microbiomes human milk fecal transplant gut–brain axis placental salivary uterine necrobiome other microbiomes mycobiome phycosphere built environment drosophila gut microbiota plant endophyte epiphyte rhizobacteria human gut lung oral skin vaginal marine microbial community initial acquisition accessible carbohydrates flora (microbiology) holobionts plant holobiont marine holobiont coral crab seagrass sponge rhodolith hologenomics hologenome evolution viromes bat human mangrove viriome virosphere related biomass partitioning dysbiosis gnotobiosis phytobiome quorum sensing biological dark matter microbial population biology microbial cooperation metagenomics viral metatranscriptomics metabolomics pan-genome superorganism symbiogenesis projects human microbiome project earth microbiome project category introduction plant–microbe partnership (a) plants are colonized initially by microbes originating from the seed. this seed-derived microbiota is complemented and partly substituted gradually by rhizosphere microorganisms migrating into the plant via roots. plant–microbe partnerships occur at different levels of complexity.(b) the plant interacts with single organisms. it responds to the presence of a microbe and its metabolites and vice versa the microbe is affected by the plant environment and reacts to plant metabolism and physiology.(c) the plant interacts with the microbiota in the soil and rhizosphere. plant exudates attract microbes in the soil thereby directing a subset of them to the root zone. in turn, the activity of the microbiota in the root zone has strong impact on plant growth and health.(d) the microorganisms within the root and rhizosphere microbiota dynamically interact with each other and the microbiota in the root. although most work on host-microbe interactions has been focused on animal systems such as corals, sponges, or humans, there is a substantial body of literature on plant holobionts. plant-associated microbial communities impact both key components of the fitness of plants, growth and survival, and are shaped by nutrient availability and plant defense mechanisms. several habitats have been investigated as harbouring plant-associated microbes, including the rhizoplane (surface of root tissue), the rhizosphere (periphery of the roots), the endosphere (inside plant tissue), and the phyllosphere (total above-ground surface area). the holobiont concept originally suggested a significant fraction of the microbiome genome together with the host genome is transmitted from one generation to the next and thus can propagate unique properties of the holobiont. in this regard, studies have shown that seeds can play such a role. evidence of this process have been recently proven showing that the majority, up to 95%, of the seed microbiome is mistranslated across generations. the plant holobiont is relatively well-studied, with particular focus on agricultural species such as legumes and grains. bacteria, fungi, archaea, protists, and viruses are all members of the plant holobiont. the bacteria phyla known to be part of the plant holobiont are actinomycetota, bacteroidota, bacillota, and pseudomonadota. for example, nitrogen-fixers such as azotobacter (proteobacteria) and bacillus (firmicutes) greatly improve plant performance. fungi of the phyla ascomycota, basidiomycota, and glomeromycota colonize plant tissues and provide a variety of functions for the plant host. arbuscular mycorrhizal fungi (glomeromycota), for instance, are common across plant groups and provide improved nutrient acquisition, temperature and drought resistance, and reduced pathogen load. epichloë species (ascomycota) are part of the meadow fescue holobiont and provide herbivore resistance by producing ergot alkaloids, which cause ergotism in mammals. protist members of the plant holobiont are less well-studied, with most knowledge oriented towards pathogens. however, there are examples of commensalistic plant-protist associations, such as phytomonas (trypanosomatidae). like all other organisms, plants do not lead solitary lives, as there are myriads of microbes and viruses living around and within them. some microbes, whether endophytic or epiphytic, play diverse roles in supporting healthy plant growth, whereas others are pathogenic, which can become dominant over the beneficial ones to cause disease. in recent years, various cutting-edge tools developed for studying the associations between microbes and plants and extensive modern research on plant microbiomes have dramatically furthered knowledge on ecological functions and key roles of the plant microbiome in supporting plant adaptability to dynamic environments. currently, plant-associated microorganisms are considered reservoirs of additional genes and traits, which are critical to the growth and development of the host. furthermore, the plant pathobiome—which represents the disease-causing agents in the context of the interaction between the microbial communities and plant host in its biotic environment—is another important component of the plant microbiome that remains relatively understudied. research focussing on the widely accepted one pathogen–one disease hypothesis has led to many breakthroughs, such as the identification of diseases and novel disease-causing organisms, as well as the development of control strategies using effective compounds against individual pathogens, which have proven successful in controlling several diseases. however, this came at the cost of neglect of plant pathology in a holistic approach—or systems-based plant pathology—in which communities and their interactions are considered rather than individual organisms. this reductionist scheme has limited our ability to overcome certain important challenges, such as the emergence of novel and severe diseases, with little that could be done to counter these diseases without considering the associated biotic factors. the plant holobiont plant holobiont as a complex system this includes beneficial plant-associated microbes—the symbiome—and the collective pathogenic microbes—the pathobiome. the beneficial and pathogenic microbes are in continuous antagonism and competition for space and nutrients. when pathogenic microbes prevail, they interfere with normal plant functions, leading to disease development. co-operative interactions amongst pathogenic microbes may result in more severe disease and multiple infections. the stable, beneficial plant microbiome may be altered to facilitate the development of certain diseases, as observed in the olive knot disease. as functional macrobes living in a close association with diverse communities of microbes and viruses, plants should be considered a "holobiont", viewed as a complex system in continuous interaction with the resident microbes and the surrounding environment. the microbes with their functional genes represent the plant microbiome, or the phytobiome, and their composition may differ among individual plants, as well as across various stages of growth or sites and tissues of the same plant. despite the extensive taxonomic overlap between the microbiomes of different plant tissues, each compartment exhibits a unique composition of strains and species, as evidenced from the specificity of different operational taxonomic units (otus) in various tissues of plants within the same genus. the beneficial roles of microbes associated with plants include, but are not limited to, supporting plant growth at different stages starting from seed germination, promoting plant resistance to biotic and abiotic stresses, and assisting plants in nutrient uptake. the plant growth-promoting bacteria and the arbuscular mycorrhiza represent the beneficial microbes that are mostly involved in supporting plant growth and nutrition by facilitating nutrients mobilisation. the mycorrhizae were even reported to manipulate plant hormonal signalling to facilitate their colonisation of the root surface in a way similar to the mechanisms of some pathogenic microbes, while in this case, the hijacking is beneficial for the host plant. alternatively, pathogenic microbes are also a part of the phytobiome, although this concept has been partly overlooked in most studies on this topic. despite their presence within the microbial communities, pathogenic microbes are differentiated from the rest of the phytobiome based on their ability to damage the plant tissues through transient blooming under specific conditions, which is consistent with the core concept of the disease triangle in epidemiology. defining specific taxonomic groups as pathogenic or beneficial could be misleading, as some microbial genera might include beneficial members that support growth at certain stages of a plant species, but are pathogenic at another stage or to other plant species. for instance, while some members of the genus rhizoctonia are essential for promoting seed germination and supporting the growth of certain orchid species, others are devastating pathogens causing seedling damping-off, root rot, stem rot, and canker in several plants and even post-harvest rot in some crops. therefore, studying the types and taxonomic composition of plant microbiomes might not be sufficient to completely understand the roles of the plant microbiome, and the functional potential of the characterised microbial structure must be investigated within their communities. studies have shown that under specific conditions, the stable, beneficial plant microbiome may be altered to facilitate the development and establishment of certain diseases. a model representing this phenomenon is the olive knot disease caused by pseudomonas savastanoi pv. savastanoi. the knots formed by pseudomonas savastanoi pv. savastanoi in the aerial parts of olive trees harbour a specific multi-species community of endophytic non-pathogenic bacteria, which cooperate with the main causative bacteria to enhance disease severity. the well-documented co-existence and shared quorum-sensing signals of specific bacterial communities of pantoea and erwinia in the olive knots and the causative agent pseudomonas savastanoi pv. savastanoi in different olive-growing regions of the world suggests the co-evolution and conserved roles of this bacterial consortium in promoting disease development. co-inoculation of pantoea and erwinia species with pseudomonas savastanoi pv. savastanoi facilitated bacterial colonisation, nutrient exploitation, plant defence disruption, and knot enlargement. in this context, plant pathogenic microbes may specifically manipulate the structure of the plant microbiome to generate conditions conducive to their own survival and colonisation. kim et al. demonstrated that the plant pathogen burkholderia glumae employs the specific type-6 secretion system (t6ss) for interaction with rice endophytic microbes, thereby reducing the populations of specific bacterial genera, such as luteibacter and dyella, which promote plant growth and contribute to protection against pathogenic bacteria. metagenomic analysis in their study also revealed significant changes in the community structure of endophytic microbiota in infected rice plants compared with non-infected plants or plants infected with a t6ss-defective b. glumae mutant. specifically, these changes facilitated the colonisation and establishment of b. glumae at the early stages of infection. another example in which the plant-associated beneficial bacteria turn harmful under specific conditions to support the development of the disease is the root-knot caused by the nematode meloidogyne incognita. nematode infection is associated with the presence of specific microbes harbouring abundant genes involved in pathogenesis, such as genes encoding plant polysaccharide-degrading enzymes. hence, assessments of the taxonomic composition should always be aligned to functional analyses of the existing microbial communities, and the plant holobiont should be separated into the symbiome or pathobiome under specific conditions based on function rather than taxonomy. overall, the plant holobiont could be represented as a never-ending war between the allies of pathogenic microbes, as the pathobiome, and the key beneficial microbes, as the symbiome. symbiotic relationships under natural conditions, plants are always associated with a well-orchestrated community of microbes — the phytomicrobiome. the nature and degree of microbial effect on the plant host can be positive, neutral, or negative, and depends largely on the environment. the phytomicrobiome is integral for plant growth and function; microbes play a key role in plant nutrient acquisition, biotic and abiotic stress management, physiology regulation through microbe-to-plant signals, and growth regulation via the production of phytohormones. relationships between the plant and phytomicrobiome members vary in intimacy, ranging from casual associations between roots and the rhizosphere microbial community, to endophytes that live between plant cells, to the endosymbiosis of microbes by the plant cell resulting in mitochondria and chloroplasts. if we consider these key organelles to also be members of the phytomicrobiome, how do we distinguish between the two? if we accept the mitochondria and chloroplasts as both members of the phytomicrobiome and the plant (entrained microbes), the influence of microbes on the evolution of plants becomes so profound that without microbes, the concept of the "plant" is not viable. the phytomicrobiome is composed of a community of microorganisms that associate and interact with a host plant including bacteria, archaea, fungi, oomycetes, viruses, protozoa, algae, and nematodes. collectively, the plant and its phytomicrobiome are a holobiont, a term originally coined by