Dysbiosis discovered in plants

Most of us are familiar with the term “Inflammatory Bowel Disease (IBD)”. However, you likely have not heard about “Inflammatory Phyllosphere Disease (IPD)”. This is because I have just made it up to draw your attention, and to describe a form of dysbiosis in plants that we have just reported.

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Background

As some of you may know, my lab has been studying bacterial pathogenesis in plants for many years. We typically use the Arabidopsis-Pseudomonas syringae pathosystem as a model. After more than two decades of studies, we and other researchers have begun to understand how P. syringae infects susceptible host plants. To make a long story short, we found that (i) suppression of host innate immunity and (ii) induction of an aqueous environment in the intercellular spaces (in which bacteria live) are two main virulence activities of P. syringae.  Arabidopsis polymutants (e.g., the mfec quadruple mutant), which are simultaneously defective in these two pathways, allow uncontrolled proliferation of nonpathogenic mutants of P. syringae that otherwise do not infect wild-type plants1, 2.

What does this have to do with dysbiosis?

Well, in the previous study we noticed a puzzling result with the Arabidopsis mfec quadruple mutant: leaves of the Arabidopsis mfec mutant sometimes exhibited disease-like symptoms, including leaf chlorosis and necrosis, even without bacterial inoculation (Fig. 1)!  Furthermore, mfec leaves had an abnormally high level of endophytic microbiome1. However, at that time we did not know whether the abnormal microbiome level was the cause of the disease-like symptoms in the mfec mutant plants or merely a consequence of some unknown developmental abnormality of the mfec mutant, independent of the microbiome. 

Fig. 1. Arabidopsis leaves from wild-type and mfec mutant plants. Please note chlorosis and necrosis symptoms in mfec leaves.

In the current study1, we designed experiments to resolve the cause vs. effect relationship with respect to the observed abnormal microbiome in the induction of disease-like symptoms in the mfec mutant. We conducted a variety of experiments, including 16S rDNA profiling, development of gnotobiotic plant growth systems, construction of synthetic bacterial communities, thousands of microbe-microbe interaction assays, and identification of additional Arabidopsis mutants that show dysbiotic symptoms. These experiments led to a number of interesting findings.  It appears that plants have evolved an ancient genetic network, involving components of innate immunity, to properly assemble a diverse and health-promoting endophytic leaf microbiome. Without this network, the endophytic leaf microbiome becomes abnormal and plants develop IPD. This is noteworthy, as a defect in innate immunity is associated with IBD in humans – an interesting conceptual parallel between humans and plants in the development of dysbiosis.

What’s next?

We are excited about our finding of a genetic network used by plants to prevent dysbiosis. Much is to be discovered about dysbiosis and its prevention mechanisms in plants as well as in humans and animals. In this respect, the advanced genetic tractability of Arabidopsis may be well suited to further identify common and unique eukaryotic genes that are causally involved in the prevention of dysbiosis.

Leaves and other aboveground parts of terrestrial plants (collectively called the phyllosphere) make up one of Earth’s most abundant biospheres. The phyllosphere takes up carbon dioxide for photosynthesis (producing food, fuel, fiber and medicines) and releases oxygen for animals and humans to breathe. By discovering plant genes behind dysbiosis prevention, we can start thinking about ways to configure a better plant microbiome as a new tool to increase plant health and productivity as part of a global solution to feed the raising world population in the face of climate change. 

References:

1. Xin XF, Nomura K, Aung K, Velásquez AC, Yao J, Boutrot F, Chang JH, Zipfel C, He SY (2016) Establishment of an aqueous host apoplast is a critical step in bacterial pathogenesis in plants. Nature, 539:524-529. 

2. Xin XF, Kvitko B, He SY (2018) Pseudomonas syringae: What does it take to become a pathogen. Nature Rev Microbiol 16:316-328 

3. Chen T, Nomura K, Sohrabi R, Wang X, Xu J, Yao L, Paasch B, Ma L, Kremer J, Cheng Y, Zhang L, Wang, E, Wang N, Xin X, He SY (2020) A plant genetic network for preventing dysbiosis in the phyllosphere. Nature https://www.nature.com/article...


 

 

 

 

 

 

Go to the profile of Sheng-Yang He

Sheng-Yang He

University Distinguished Professor, HHMI, Michigan State University

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