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.
Introduction
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.