The Impact of Beneficial Plant-Associated Microbes on Plant Phenotypic Plasticity
rather than as discrete relationships between hosts and microbes, as they have been Mycorrhizas are examples of a mutualism that occurs between plant roots and fungi . this in spite of the fact that the leaf surface is a hostile environment. PDF | Plant community dynamics are driven by the microbial mediation of soil by the impact of the symbiotic microbes on the environment and competition for soil the relationship between the host and its symbiotic microbial community and. plant-microbe ecology; symbiotic microbial communities; interactions of host and They also assist and enhance plant resistance to adverse environmental the relationships between plant hosts and their symbiotic microbial communities.
To absorb phosphate, mycorrhiza-induced phosphate transporter genes, such as MtPT4, are predominantly or exclusively up-regulated in plant root cells containing arbuscules. Nitrogen sources such as ammonium and amino acids are translocated to the plant via fungal hyphae.
Several ammonium transporters AMTs have been identified in plants, and it will be interesting to determine their precise expression patterns and subcellular location. Moreover, they show that GmAMT4. Plant factors in RN symbiosis RN symbiosis in legumes involves host-specific recognition and post-embryonic development of a nitrogen-fixing organ, the root nodule. Among these phenomena, nodule senescence, namely regulation of nodule lifespan, is uncharted territory but would gain in importance when our aim is to achieve long-term nitrogen-fixing activity in legumes.
The MtATB2 gene encodes a bZIP transcription factor and is regulated by sucrose and light conditions as well as during nodule senescence. For nodule function, carbon is provided mainly as sucrose derived from photosynthesis and transported via the phloem.
Leguminous plants strictly control nodule numbers, because nodulation and nitrogen fixation are an energy drain on the host. To maintain the symbiotic balance with rhizobia, plants have evolved negative feedback systems known as autoregulation of nodulation AON.
Thus, plenty is invaluable for dissecting the complex web of negative regulatory systems in nodulation. The homologs are widely conserved in non-leguminous plants but their functions are unknown.
Transformation with OsNSP1 and OsNSP2 fully rescued the mutant phenotypes such as nodule development and nitrogenase activity, indicating that these rice transcription factors can potentially mediate Nod factor signaling in L. Bacterial factors in RN symbiosis In response to stimulation by flavonoids exuded from legume roots into soil, rhizobia synthesize signaling molecules that are responsible for nodule formation.
These signaling molecules, named Nod factors, have been identified as lipochito- oligosaccharides decorated with diverse chemical substitutions Spaink In this special issue, Maruya and Saeki examine the physiological functions of the BacA homolog in Mesorhizobium loti.
From study of a bacA mutant, they found that BacA is dispensable for M. These results raise the question of why BacA is not absolutely required for symbiosis with M. One fascinating explanation is that BacA is exclusively required in galegoid legumes producing defensin-type antimicrobial peptides NCR peptides.
Soil resources and microbial interactions Soil resources can govern the coexistence of plant species by resource partitioning and sharing. Studies have found root symbionts that increase the efficiency of nutrient uptake and allow the host to persist in a low nutrient environment, thereby directly contributing to the competitive exclusion of other plants [ 55 ].
Rhizosphere microbes can alter the availability of different forms of nitrogen or phosphorus in the soil and affect plant-plant interactions via the mediation of resource partitioning [ 56 ].
Soil resources can also be transferred by shared symbiotic fungi called common mycorrhizal networks CMNs [ 57 ]. In nature, different plant species commonly share the broadly specific mycorrhizal fungi.
Simard and Durall demonstrated the direct transfer of resources from one plant to another via CMNs with labeled carbon, nitrogen, and phosphorus [ 57 ]. Plant community dynamics are driven by the microbial mediation of soil resource partitioning and sharing. Host response to microbes and soil community feedback The dynamic density and composition of the rhizospheric microbes can affect the coexistence of plant species via indirect feedback i.
Ecologists have proposed three hypotheses to explain the mechanism that produces low diversity plant communities. The empty niche hypothesis suggests that novel symbionts inhabit the areas invaded by invasive plants [ 59 ]. These symbionts are more efficient at resource acquisition and preferentially associated with invasive plants than with other plants.
Positive feedback might be exemplified by the enhanced growth and survival of exotic seedlings near native established symbionts [ 6263 ]. Plant monodominance, coexistence, and invasion ecology have high relation to symbiotic microbial interactions.
Plant soil community feedback in low diversity communities modified after Bever et al. Plants shape the microbial community Microbial interactions play a crucial role in plant community ecology and performance. How do plants harbor unique microbial communities? How do plants shape a unique rhizosphere microbial community? These are the questions that must be addressed. Modern genomic technologies e.
They collected more than A. They observed that the root microbial communities of plants are sufficiently dependent on the host genotype to vary between inbred A. However, the mechanisms were not clear but included differences in the host physiology and immune responses.
Plant genes responsible for defense affect the variation of the microbial community Several studies showed that plant genotype has a small but significant effect on the composition of the endophytic, rhizosphere, or phyllosphere microbial communities [ 1764 — 67 ]. A quantitative trait locus QTL analysis and a genome-wide association study GWAS were used to identify taxa linked to host genes in humans, mice, plants, and flies [ 1768 — 70 ].
Furthermore, host genetic variation shaped species richness in the bacterial community. In Matthew's study, accessions of A. The field experiment data suggested that the plant tissue structure i. To understand the plant host genetic factors that affect the associated microbial population, Bodenhausen et al.Symbiosis: Mutualism, Commensalism, and Parasitism
A panel of 55 A. The results showed that lacs and pec1 mutants affected cuticle formation, which led to an increased bacterial abundance and community composition.
The Impact of Beneficial Plant-Associated Microbes on Plant Phenotypic Plasticity
Moreover, the ethylene signaling gene ein2 was observed to be a host factor that modulated the community composition. Soil microbes are chemotactically attracted to plant root exudates, volatile organic carbon, and rhizodeposition, and then proliferate in this carbon-rich environment [ 72 ]. Plant root exudates differ between plant species, so differences in rhizosphere microbiomes of different plant species are expected [ 73 ]. More recent studies have provided strong evidence for plant species-specific microbiomes [ 7475 ].
Plants can also shape the microbial community via root exudates. Root exudates can be categorized as sugars, amino acids, organic acids, nucleotides, flavonoids, antimicrobial compounds, and enzymes [ 473 ]. The types of root exudate 3. Organic acids and amino acids The composition of root exudates from different cultivars affects the growth of soil-borne pathogens. The susceptible peanut cultivar Ganhua-5 GH and the mid-resistant cultivar Quanhua-7 QH were chosen for a root exudate analysis and evaluated for the responses of the soil-borne pathogens Fusarium oxysporum and Fusarium solani [ 76 ].
The contents of total amino acids, alanine, and sugars in the root exudate of susceptible cultivars were significantly higher than in the mid-resistant cultivar, whereas the contents of total phenolic acids, p-hydroxybenzoic acid, benzoic acid, and p-coumaric acid were significantly lower than in mid-resistant cultivars. These differences in the root exudate composition of susceptible and resistant cultivars might be assumed to regulate the resistance mechanism in the peanut rhizosphere.
Plant–Microbe Communications for Symbiosis | Plant and Cell Physiology | Oxford Academic
However, the spore germination and mycelial growth of the soil-borne pathogens F. If root exudates do not directly inhibit the growth of pathogens, the effects of other factors must be considered.
A previous report showed that organic acids modulated the colonization and enhanced the biofilm formation of the root microbiome. Fumaric acid significantly induced biofilm formation, whereas malic acid evoked the greatest chemotactic response.
The results showed that organic acids from banana root exudates played a crucial role in attracting and initiating PGPR colonization on the plant roots. Rice exudates that primarily contained the amino acid residues of histidine, proline, valine, alanine, and glycine, and the carbohydrates glucose, arabinose, mannose, galactose, and glucuronic acid may induce a higher chemotactic response by the endophytic bacteria Corynebacterium flavescens and Bacillus pumilus [ 78 ].
Sugars The amount of sugar secretion might affect infection by plant pathogens. They proposed that the expression of SWEET2 modulated sugar secretion, limiting the carbon loss to the rhizosphere.
The reduction of available substrates in the rhizosphere contributed to the resistance to Pythium. Antimicrobial compounds Root exudates can also participate in belowground plant defense.
Phytoanticipins are defensive compounds that are constitutively produced and released by the plant root prior to a biotic stress such as pathogen infection. In a recent study, Arabidopsis roots deficient in diterpene rhizathalene A production were found to be more susceptible to insect herbivory [ 81 ]. Therefore, rhizathalene A was considered as a part of a constitutive direct defense system of the roots. Phytoalexins were defined as inducible defensive compounds that are not detected in healthy plants [ 80 ].
Five phenylpropanoid root-derived aromatic root exudates were induced by the attack of the soil-borne pathogen Fusarium graminearum and exhibited antifungal activity [ 82 ]. In general, root-secreted terpenoid and phenolic defensive compounds have strong antibacterial and antifungal activity [ 8384 ]. The largest class of plant defensive chemicals above- and below ground is terpenoids.
Nonvolatile terpenoids can be secreted into the rhizosphere [ 85 ], and volatile organic compounds VOCs can be emitted from the roots as plant defensive compounds. Phenylpropanoids are a group of plant defensive phenolic root exudates. After a Fusarium graminearum infection, barley rapidly accumulated and secreted phenylpropanoids, which are cinnamic acid derivatives to resist a fungal attack [ 82 ].
Phenolic root exudates not only have antimicrobial activity but also beneficially attract soil-borne microorganisms that affect the native soil microbial community [ 86 ]. Plants can shape the specific rhizosphere microbial community via root exudates. Environmental factors effects on root exudates Plants with different genotypes produce root exudates with different compositions. Abiotic and biotic factors also affect root exudates. Physico-chemical soil properties such as nutrient availability, organic matter content, pH, structure, and texture can affect the availability of root exudates and microbial recruitment by the plant roots.
Some biotic factors such as soil microbial secondary metabolism can also affect the exudates. Temperature Since the onset of climate change and global warming, the resultant extreme heat and cold have affected the harvest of several crops.
They found more amino acids in exudates in plants grown at a low soil temperature that markedly affected the pathogenicity of Rhizoctonia fragariae [ 87 ]. Soil moisture Flood and drought have reduced global cereal harvests. Several reports have demonstrated that the soil moisture affects the release of root exudates. The temporarily wilting of plants increased the release of amino acids from the plant roots, which might be related to the incidence of pathogens in the rhizosphere [ 88 ]. Plants such as peas, soybeans, wheat, barley, and tomatoes were grown in normal moist sand and dried, remoistened sand for the liberation of amino acids.
The total amount of amino nitrogen in the temporarily dried sand was many times higher than in the normal moist sand. Soil pH and nutrition The soil pH status and the availability of nutrients such as carbon, nitrogen, and phosphate have been found to affect the release of plant root exudates and the creation of specific chemical niches in the soil, as well as the abundance of plant pathogens and beneficial microbes [ 89 — 91 ]. Bowen first demonstrated a marked effect of nutrient status on the exudation of amides and amino acids from roots of Pinus radiate seedlings [ 89 ].
The results showed the strong support for the hypothesis that niche differentiation was based on the structuring of the AM fungal community by soil pH [ 91 ]. Root secretion of phenolics was induced in Fe-deficient soil and altered the microbial community in the rhizosphere [ 92 ].
Microorganisms Soil microorganisms play a crucial role in plant growth and plant exudates. Microorganisms can affect exudation by affecting the permeability of root cells and root metabolism. Microorganisms can also absorb certain compounds in root exudates and excrete other compounds. Some microbes and also some antibiotics e.
Soil microbes can also induce the exudation of phenolic compounds for enhancing plant Fe absorption in low-Fe availability soil [ 96 ]. Microbial community diversity and plant performances 4. Variation of microbial community in plant life cycle Plant and rhizosphere microbial diversity varies throughout the plant life cycle. The factors influencing the composition and diversity of the microbial community can be classified as four processes: For seed plants, the life cycle begins with a seed.
Seed dispersal is an important ecological process. Seeds carry associated microbes that originate from their parent and the environment, thereby increasing the microbial diversity in a new environment. Recent studies have suggested that bacterial seed coatings can protect against pathogens [ 98 ].
Microbial seed epiphytes have an advantage over soil bacteria during plant colonization. Seed coating methods are a major area of research, and numerous patents have been filed i. After seed dispersal, during seed germination, seed-bone microbes might gain a competitive advantage over other microbes to colonize after germination, and opportunistic microbes from the surrounding soil might have access to a novel niche as the plant develops.
Microbial diversity and the community dynamically change throughout the plant life cycle. Networking of plant-microbes hub and edge microbes Plant microbiota forms a complex network. A wide range of studies has demonstrated that plant-associated microbes live either inside plant tissue or on the surface of plant organs such as the leaves and roots .
Plant-Microbe Ecology: Interactions of Plants and Symbiotic Microbial Communities
Field experiments showed that both plant genotype and abiotic factors affected the microbiome composition. In addition, they observed that specific species e.
Microbial hubs might be responsible for mediating defense signals among plants and the effectiveness of biological control agents [ 19 ]. These microbial hubs and keystone species have a large impact on plant performance. A number of hypothetical relationships between plant performance and microbial diversity and composition have been proposed [ 19 ]. Microbial hubs might indirectly affect other taxa by changing host performance, response, or metabolites without directly interacting with other microbes.
How can the microbial hubs be identified and how can the interaction of plants and microbes be understood? The requirement of new techniques to analyze whether a microbe has successfully entered a plant, and the observation of changes in the genotypic and phenotypic expression will be an added advantage in the study of plant-microbe interactions.
Plant growth—promoting microbes The soil constitutes a pool of microscopic life forms including bacteria, fungi, actinomycetes, protozoa, and algae, and of these, bacteria are by far the most common. The highest numbers of bacteria are found in the rhizosphere, the region around the plant roots, as differentiated from the bulk soil [ ].
Regardless of the concentration of bacteria in the soil, the bacteria may affect a plant in one of three ways. From the perspective of the plant, the interaction between the soil bacteria and a plant may be beneficial, harmful, or neutral [ ]. Plant growth-promoting bacteria PGPB include those that are free living, those that form specific symbiotic relationships with plants e. PGPB can promote plant growth directly by facilitating the acquisition of compounds or modulating plant hormone levels and indirectly by reducing the inhibitory effect of pathogenicity and plant growth by acting as biocontrol agents [ ].
PGPB and abiotic stress In nature, all living organisms are affected by environmental factors such as abiotic stress. Some plants have internal mechanisms to cope up with such stress, while others overcome.
Abiotic stress factors include water deficit, excessive water, extreme temperatures, and salinity. The association of PGPB with certain plants can help the plants combat certain abiotic stresses and prevent the plants from dying.