In this case, the EVs were found to contain proteins including cell wall-remodelling enzymes and defence proteins that affect fungal viability. Plant—microbe interactions are not simply differentiated by whether the microbes are friend or foe—the molecular and phenotypic outcome depends on which microbial strain is present. Liang et al. Once microbes enter, the level of colonization and host physiological changes can vary, for example in the well-known pathway of autoregulation of nodulation AON that modulates rhizobial colonization of legumes.
The plant microbiome
In addition to strain-specific differences, legumes vary in how they regulate AON. Regulation of plant—microbe interactions occurs with a high degree of spatial resolution, as has been found for many biotic and abiotic encounters Walker et al. This is also the case at the molecular level where modulation of spatio-temporal patterns and gene expression levels can fine-tune the production of reactive oxygen species ROS , a central element of the plant immune response.
RbohD and RbohF were found to be exquisitely regulated during Arabidopsis responses to both the hemibiotrophic bacterial pathogen Pseudomonas syringae pv. As the plant—microbe interaction progresses to resistance, susceptibility, or mutualism, changes come with either a net cost or benefit that can tip the balance in one direction or the other.
Plant-Microbe Ecology: Interactions of Plants and Symbiotic Microbial Communities
Some of these immune responses can directly change homeostasis. For example, production of ROS at the plasma membrane PM has been found to increase membrane order in response to a wide range of elicitors Sandor et al. This seems to be part of a general stimulation of defence response, with alterations of lateral membrane fluidity found in more specific cases Sandor et al. Autophagy is a general process controlling abiotic and biotic stress responses but is also key for maintaining cellular homeostasis and, when plant—pathogen interactions regulate autophagy, the balance between resistance and susceptibilty becomes complicated, as reviewed in Leary et al.
Even more fundamental to the cell are transcriptional and translational mechanisms.
Genes Involved in Microbe-Plant Interactions | D.P.S. Verma | Springer
Meteignier et al. They identified genes that have uncoupled transcription and translation during plant—pathogen interactions, specifically during the effector-triggered immunity ETI response Meteignier et al. Crosstalk is found in plant-directed processes but also in microbe-directed processes. The phenotypic outcome depends on whether a particular balance is reached and held, or tipped in one direction or the other.
The ubiquitin—proteasome system UPS has been found to be key for this balance since it brings together stress responses mediated by the phytohormones salicylic acid SA and jasmonic acid JA , to control growth and immunity reviewed in Adams and Spoel, Similarly, histone acetylation and deacetylation have been identified as key regulators of immunity Ramirez-Prado et al.
Recently, Liu et al. Crosstalk is also found to impact plant processes indirectly. For example, at a structural level, cell wall organization is affected during plant defence responses reviewed in Castilleux et al. Multiple developmental pathways are affected during plant symbiosis and it has been found that different symbiotic nodule types indeterminate and determinate produce auxin maxima in different mechanistic ways as part of the regulation of microbial housing reviewed in Kohlen et al.
Plant-derived auxin can antagonize plant defences, virulence gene expression, and stress responses. Microbe-produced auxins have been found to regulate plant cellular processes both indirectly and directly reviewed in Kunkel and Harper, It has long been known that different hormone pathways can act antagonistically during plant growth versus immunity responses, as a mechanism of crosstalk.
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Some organisms can directly modulate these pathways; for example, it has been found that infestation of rice by the phloem-feeding brownhopper results in suppression of the brassinosteroid BR pathway while simultaneously activating the SA and JA pathways Pan et al. Brownhopper susceptibility is altered in BR signalling mutants and increased following treatment with high levels of BR that promote JA synthesis and signalling and reduce SA levels Pan et al. Crosstalk also occurs during mutualism; for example, strigolactones are key regulators of plant arbuscular mycorrhizal fungi AMF interactions and they are part of crosstalk with auxin, abscisic acid ABA , and gibberelic acid GA pathways reviewed in Lanfranco et al.
Strigolactones can also influence the AMF directly, resulting in changes in fungal gene expression and also microbial secretion of small proteins that could act as host non-specific effector proteins to modulate the outcome of AMF interactions reviewed in Lanfranco et al. The balance of disease versus resistance can be further tipped depending on environmental factors, something of clear importance as we look to develop plants for a future of climate change.
Identifying target genes that could be modulated in order to mitigate enhanced climate effects could be key for this.
Tomato resistance to Frankliniella occidentalis thrips is modulated depending on UV levels, and Escobar-Bravo et al. Interestingly this seems to be an indirect effect, again highlighting the high degree of crosstalk between abiotic and biotic responses. The mitogen-activated protein kinase gene MPK4 has found to be CO 2 responsive and to affect plant responses to aphids by regulating both stomatal aperture and JA-dependent resistance Guo et al. This is certainly a checkpoint that could be manipulated, alongside the use of classical approaches to enhance resilience of crops Piquerez et al.
Finally, we must look both underground and overground for regulators.
Plant—microbe interactions are mediated by other microbes in the environment, in both the rhizosphere and phyllosphere. Understanding root exudation to potentially encourage particular communities to develop, and investigating the bacterial genes that affect colonization are promising directions. We can exploit new advances in the methods to study plant—microbe interactions across chemical, molecular, metagenomic, and exometabolomic scales, as reviewed in Jacoby and Kopriva Resistance, susceptibility, or mutualism—the outcome is finely balanced and comes with costs to plant and microbe.
The latest research in plant—microbe interactions must take this into account, but could also exploit it to develop high-yielding and resistant new crop varieties. The key information that will enable us to realize food security comes from study of plant—microbe interactions at a fundamental level and its implementation through traditional breeding and plant engineering.
Oxford University Press is a department of the University of Oxford. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide. Sign In or Create an Account. Sign In. Advanced Search. Article Navigation. Close mobile search navigation Article Navigation. Article Contents. Facilitating host—microbe interactions: making a connection. Taking advantage of the situation: tipping the balance.
Crosstalk of immunity and plant homeostasis: nothing is for free.
Environmental input: we are not alone. Corrected proof. Plant—microbe interactions: tipping the balance Vardis Ntoukakis. Oxford Academic. Google Scholar. Miriam L Gifford. Correspondence: miriam. Cite Citation. Permissions Icon Permissions. Food security , hormones , immunity , plant defence , plant—microbe , plant—mutualist , resistance , symbiosis , transcriptional regulation.
The ubiquitin-proteasome system as a transcriptional regulator of plant immunity. Search ADS. Gou et al. 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. 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.
Taking advantage of the situation: tipping the balance
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 [ 83 , 84 ]. The largest class of plant defensive chemicals above- and below ground is terpenoids.
Related Genes Involved in Microbe-Plant Interactions
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