Plants and bacteria battle for control of water during leaf infection, as is demonstrated by a bacterial species that manipulates plant cells to create a water-rich environment that promotes bacterial growth. See Article p.524
Invading bacterial leaf pathogens disarm a plant's defence mechanisms by injecting what are known as effector proteins directly into plant cells. In addition to the plant's defence mechanisms, invading bacteria might encounter another obstacle — a severe shortage of water in the leaf intercellular space (apoplast) that limits bacterial growth. On page 524, Xin et al.1 report that Pseudomonas syringae bacteria inject effector proteins that specifically target plant-cell processes to promote apoplast hydration, thereby creating an environment suitable for bacterial growth.
High humidity favours the development of bacterial leaf diseases that are associated with the formation of leaf spots. An early symptom of leaf-spot diseases is water soaking2, a localized abundance of water in the apoplast. Extensive water soaking of plants is associated with epidemics and severe disease symptoms3.
To investigate the relationship between the water soaking of leaves and bacterial growth, Xin and colleagues used microscopy to analyse the thale cress plant Arabidopsis thaliana. They observed that water soaking occurred only transiently during the start of leaf-spot development. The leaf sites that exhibited this transient water soaking were also the sites of early bacterial replication, and ultimately became the locations of disease lesions. These results provide direct visual evidence that links water soaking to bacterial growth and leaf-spot development.
The WstE and AvrE effector-protein family can promote water soaking in some plant species4,5, although the mechanism involved and the role of water soaking in plant infection had not been identified for these proteins. Xin et al. found that the P. syringae effector proteins AvrE and HopM1 can each promote water soaking in A. thaliana, and that this soaking occurs regardless of whether the proteins are expressed by the bacteria or expressed in the plant cell by genetic engineering. The authors demonstrated that HopM1 induces soaking though a pathway that involves degradation of the plant protein MIN7. This discovery indicates that a bacterial pathogen can actively promote hydration of the apoplast by modifying a plant-cell target.
How water accumulates in the apoplast after MIN7 is destroyed is not known. Possible mechanisms include changes in cell-membrane function and stability, changes to the aquaporins — water-transport proteins — in cell membranes, or alterations to ion-transport activity across the membrane. A role for the cell membrane as a target for pathogen-mediated effects on water movement is supported by the facts that MIN7 is involved in maintaining a normal cell membrane6 and that AvrE moves to the cell membrane after injection7.
Xin et al. found that only two plant functions must be altered to enable bacterial infection: a plant immune-defence system known as pattern-triggered immunity and water limitation in the apoplast. A plant mutant lacking both MIN7 and pattern-triggered immunity enabled strong growth, not only of a non-pathogenic P. syringae strain, but also of other bacterial communities normally resident at low levels on leaves. The growth of these resident communities in the apoplast correlated with the appearance of leaf yellowing and small regions of plant-cell death, revealing that even bacteria not known to be pathogenic can exact a detectable toll on plant health if the conditions arise to enable excessive bacterial proliferation.
The humidity in the air outside the leaf can influence a plant's ability to maintain a water-limited apoplast, because this ambient air connects directly to the apoplast through pores called stomata. Low-humidity air should help to limit the water in the apoplast and aid in antibacterial defence. This is consistent with the low levels of leaf-spot disease observed in arid conditions. By contrast, continuous water soaking should negate a defence strategy of maintaining low apoplast hydration, and this is consistent with the abundant growth of non-pathogenic bacteria in the apoplast of persistently water-soaked leaves5.
Xin and colleagues tested different ambient humidity conditions, and demonstrated that the humidity must be high to enable the pathogen to induce water soaking that is dependent on the injection of AvrE or HopM1 (Fig. 1). This strong requirement for humidity reflects a fundamental tenet of plant pathology: disease depends on the host, the pathogen and the environment.
Plants and pathogens battle for water during the initial pathogenic attack, and also later, after the plants have been infected. Xin and colleagues found that MIN7 is stabilized by a type of plant immune response known as effector-triggered immunity. This indicates that the plants have evolved mechanisms to counteract the bacterially induced destruction of MIN7 that enables apoplast hydration. The ability of plants to affect such hydration is consistent with the low apoplast hydration observed in A. thaliana plants that can resist an attack by P. syringae8. Reduced fluid movement into the apoplast during effector-triggered resistance of A. thaliana to P. syringae attack suggests that, as well as preventing apoplast hydration, plants might also actively promote drying of the apoplast9.
The authors' study supports a model in which plants maintain a water-limited apoplast as a barrier against bacterial growth, and in which pathogen effectors disarm this barrier, leading to water soaking in conditions of high humidity. A key next step in understanding this fascinating plant–pathogen battle for control of water will be to identify the nature of the 'flood gates' to the apoplast and the molecular mechanisms by which pathogens open them.Footnote 1
Xin, X. F. et al. Nature 539, 524–529 (2016).
Davis, K. R., Schott, E. & Ausubel, F. M. Mol. Plant-Microb. Interact. 4, 477–488 (1991).
Beattie, G. A. Annu. Rev. Phytopathol. 49, 533–555 (2011).
Asselin, J. E. et al. Plant Physiol. 167, 1117–1135 (2015).
Ham, J. H., Majerczak, D. R., Arroyo-Rodriguez, A. S., Mackey, D. M. & Coplin, D. L. Mol. Plant-Microb. Interact. 19, 1092–1102 (2006).
Tanaka, H., Kitakura, S., De Rycke, R., De Groodt, R. & Friml, J. Curr. Biol. 19, 391–397 (2009).
Xin, X.-F. et al. Plant Physiol. 169, 793–802 (2015).
Wright, C. A. & Beattie, G. A. Proc. Natl Acad. Sci. USA 101, 3269–3274 (2004).
Freeman, B. C. & Beattie, G. A. Mol. Plant-Microb. Interact. 22, 857–867 (2009).
Jin, L. et al. PLoS Pathog. 12, e1005609 (2016).
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Molecular Plant (2020)
Molecular Plant-Microbe Interactions (2018)