Plant microbiome

Microbiome in plant ecosystem

Schematic plant and plant-associated microbiota colonizing different niches on and inside the plant tissue. All the above-ground plant parts together, called the phyllosphere, are a continuously evolving habitat due to ultraviolet (UV) radiation and altering climatic conditions. It is primarily composed of leaves. Below-ground plant parts, mainly roots, are generally influenced by soil properties. Harmful interactions affect the plant growth through pathogenic activities of some microbiota members (left side). On the other hand, beneficial microbial interactions promote plant growth (right side).[10]

The study of the association of plants with microorganisms precedes that of the animal and human microbiomes, notably the roles of microbes in nitrogen and phosphorus uptake. The most notable examples are plant root-arbuscular mycorrhizal (AM) and legume-rhizobial symbioses, both of which greatly influence the ability of roots to uptake various nutrients from the soil. Some of these microbes cannot survive in the absence of the plant host (obligate symbionts include viruses and some bacteria and fungi), which provides space, oxygen, proteins, and carbohydrates to the microorganisms. The association of AM fungi with plants has been known since 1842, and over 80% of land plants are found associated with them.[11] It is thought AM fungi helped in the domestication of plants.[12][5]

In this animation a root tuber is being colonized by an arbuscular mycorrhizal fungus (AMF)

Traditionally, plant-microbe interaction studies have been confined to culturable microbes. The numerous microbes that couldn't be cultured have remained uninvestigated, so knowledge of their roles is largely unknown.[5] The possibilities of unraveling the types and outcomes of these plant-microbe interactions has generated considerable interest among ecologists, evolutionary biologists, plant biologists, and agronomists.[13][14][1] Recent developments in multiomics and the establishment of large collections of microorganisms have dramatically increased knowledge of the plant microbiome composition and diversity. The sequencing of marker genes of entire microbial communities, referred to as metagenomics, sheds light on the phylogenetic diversity of the microbiomes of plants. It also adds to the knowledge of the major biotic and abiotic factors responsible for shaping plant microbiome community assemblages.[14][5]

The focus of plant microbiome studies has been directed at model plants, such as Arabidopsis thaliana, as well as important economic crop species including barley (Hordeum vulgare), corn (Zea mays), rice (Oryza sativa), soybean (Glycine max), wheat (Triticum aestivum), whereas less attention has been given to fruit crops and tree species.[15][2]

Microbial consortia naturally formed
on the roots of Arabidopsis thaliana

Scanning electron microscopy pictures of root surfaces from natural A. thaliana populations showing the complex microbial networks formed on roots.
a) Overview of an A. thaliana root (primary root) with numerous root hairs. b) Biofilm-forming bacteria. c) Fungal or oomycete hyphae surrounding the root surface. d) Primary root densely covered by spores and protists. e, f) Protists, most likely belonging to the Bacillariophyceae class. g) Bacteria and bacterial filaments. h, i) Different bacterial individuals showing great varieties of shapes and morphological features.[16]

The rhizosphere comprises the 1–10 mm zone of soil immediately surrounding the roots that is under the influence of the plant through its deposition of root exudates, mucilage and dead plant cells.[17] A diverse array of organisms specialize in living in the rhizosphere, including bacteria, fungi, oomycetes, nematodes, algae, protozoa, viruses, and archaea.[18]

The most frequently studied beneficial rhizosphere organisms are mycorrhizae, rhizobium bacteria, plant-growth promoting rhizobacteria (PGPR), and biocontrol microbes. It has been projected that one gram of soil could contain more than one million distinct bacterial genomes,[19] and over 50,000 OTUs (operational taxonomic units) have been found within the potato rhizosphere.[20] Among the prokaryotes in the rhizosphere, the most frequent bacteria are within the Acidobacteria, Proteobacteria, Planctomycetes, Actinobacteria, Bacteroidetes, and Firmicutes.[21][22] In some studies, no significant differences were reported in the microbial community composition between the bulk soil (soil not attached to the plant root) and rhizosphere soil.[23][24] Certain bacterial groups (e. g. Actinobacteria, Xanthomonadaceae) are less abundant in the rhizosphere than in nearby bulk soil .[21][5]

Mycorrhizal fungi are abundant members of the rhizosphere community, and have been found in over 200,000 plant species, and are estimated to associate with over 80% of all plants.[25] Mycorrhizae–root associations play profound roles in land ecosystems by regulating nutrient and carbon cycles. Mycorrhizae are integral to plant health because they provide up to 80% of the nitrogen and phosphorus requirements. In return, the fungi obtain carbohydrates and lipids from host plants.[26] Recent studies of arbuscular mycorrhizal fungi using sequencing technologies show greater between-species and within-species diversity than previously known.[27][5]

A leaf from a healthy Arabidopsis plant (left) and a leaf from a dysbiosis mutant plant (right)[29]

The aerial surface of a plant (stem, leaf, flower, fruit) is called the phyllosphere and is considered comparatively nutrient poor when compared to the rhizosphere and endosphere. The environment in the phyllosphere is more dynamic than the rhizosphere and endosphere environments. Microbial colonizers are subjected to diurnal and seasonal fluctuations of heat, moisture, and radiation. In addition, these environmental elements affect plant physiology (such as photosynthesis, respiration, water uptake etc.) and indirectly influence microbiome composition.[5] Rain and wind also cause temporal variation to the phyllosphere microbiome.[30]

Overall, there remains high species richness in phyllosphere communities. Fungal communities are highly variable in the phyllosphere of temperate regions and are more diverse than in tropical regions.[31] There can be up to 107 microbes per square centimetre present on the leaf surfaces of plants, and the bacterial population of the phyllosphere on a global scale is estimated to be 10²⁶ cells.[32] The population size of the fungal phyllosphere is likely to be smaller.[33]

Phyllosphere microbes from different plants appear to be somewhat similar at high levels of taxa, but at the lower levels taxa there remain significant differences. This indicates microorganisms may need finely tuned metabolic adjustment to survive in phyllosphere environment.[31] Proteobacteria seems to be the dominant colonizers, with Bacteroidetes and Actinobacteria also predominant in phyllospheres.[34] Although there are similarities between the rhizosphere and soil microbial communities, very little similarity has been found between phyllosphere communities and microorganisms floating in open air (aeroplankton).[35][5]

Some microorganisms, such as endophytes, penetrate and occupy the plant internal tissues, forming the endospheric microbiome. The arbuscular mycorrhizal and other endophytic fungi are the dominant colonizers of the endosphere.[36] Bacteria, and to some degree archaea, are important members of endosphere communities. Some of these endophytic microbes interact with their host and provide obvious benefits to plants.[21][37][38] Unlike the rhizosphere and the rhizoplane, the endospheres harbor highly specific microbial communities. The root endophytic community can be very distinct from that of the adjacent soil community. In general, diversity of the endophytic community is lower than the diversity of the microbial community outside the plant.[24] The identity and diversity of the endophytic microbiome of above-and below-ground tissues may also differ within the plant.[39][36][5]

Individual seeds possessed high microbial diversity, that was higher in the embryo than in the pericarp. Plant seeds can serve as natural vectors for vertical transmission of beneficial endophytes that confer disease resistance.[40] Evidence showing the transmission of microorganisms from seeds to the developing seedling, was found to occur in experimental and natural conditions.[41] It also seems that the transmission to new plant happens through specific mechanisms where certain microorganisms migrate from seed to plant leaves and other to plant roots.[42]