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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. Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License.
The plant holobiont is relatively well-studied, with particular focus on agricultural species such as and . 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 Ergoline, 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 Commensalism plant-protist associations, such as Phytomonas ().
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.
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.
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.
The phytomicrobiome is composed of a community of microorganisms that associate and interact with a host plant including bacteria, archaea, fungi, , , protozoa, , and . Collectively, the plant and its phytomicrobiome are a holobiont, a term originally coined by Adolf Meyer-Abich but most frequently associated with and popularized by Lynn Margulis and rigorously explored by Bordenstein and Theis. While the phytomicrobiome includes parasitic and commensal microbes, it also includes mutualists, or beneficial microbes, such as mycorrhizal fungi (MF) and plant growth-promoting bacteria (PGPB) that enable the plant holobiont to survive within a wide range of environments. Beneficial microbes mediate plant holobiont responses to abiotic and biotic stresses and allow the plant holobiont to adapt to environmental variations. The plant host can then modify the abundance and composition of beneficial microbial species within the phytomicrobiome, at least in part, by secreting biochemical compounds. This selection occurs most strongly in the endosphere, followed by the rhizoplane, and finally the rhizosphere. For example, root exudates can select for and promote the growth of certain beneficial microbes by serving as carbon and/or energy sources for microbial metabolism.
The earliest and arguably most essential example of a specific symbiotic function within the plant holobiome arose from the endosymbiosis of an alphaproteobacterium and a cyanobacterium. These microbes are now the mitochondrion and chloroplast, respectively, and are microbes that have been fully integrated into plant cells (see diagram). These did not replace particular functions of the ancestral organism, but rather provided new functions, giving an evolutionarily competitive edge to the newly evolving plants.
In this paper, we focus on how beneficial bacteria and fungi, a relatively small fraction of the phytomicrobiome, have had a disproportionately large influence on plant holobiont evolution. We also review the fundamental roles that the phytomicrobiome plays in plant holobiont development and survival. Finally, we propose that a greater integration of holobiont theory should be incorporated into the plant sciences.
Approximately half of a billion years later, eukaryotic cells containing mitochondria engulfed cyanobacteria (photosynthetic prokaryotes), which like the alphaproteobacteria became fully incorporated into and dependent on plant cells, resulting in the chloroplast (diagram). Chloroplasts convert energy from the sun into carbohydrates, using water as the electron donor. However, large-scale gene loss from plastids has occurred during the course of evolution, and higher plant chloroplasts now contain only 120–130 genes compared with the 1700 to 7500 genes contained in cyanobacterial genomes. In spite of their reduced genome size, chloroplasts and cyanobacteria still carry out some of the same functions, ranging from gene expression to metabolism.
Organisms have been described as entities evolved from constituent elements that are highly cooperative and minimally conflicting; however, there is ongoing debate regarding the levels of cooperation and conflict within holobionts. In plants, chloroplasts and mitochondria are highly cooperative with plant cells while relationships between the plant and the phytomicrobiome are more varied including the mutualistic and parasitic interactions. For example, relationships between plants and PGPB are organismal given that they are highly cooperative and low conflict in nature. On the other hand, some plant-microbe interactions are more opportunistic for one member and therefore are not organismal. The plant is therefore a eukaryotic organism, with prokaryotic constituents (entrained microbes), that interacts with its phytomicrobiome to form the plant holobiont. As a result, the difference between the plant and the phytomicrobiome blurs and the concept of the holobiont becomes pre-eminent. It can then be argued that the influence of microbes on the evolution of plants is so profound that without microbes, the concept of the “plant” fails.
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