A 7-year path towards exploring a disease-suppressive arsenal

Cooperation between host plants and microbiota is important for the defence against pathogen infection but remains largely elusive in how it works on the above ground. Recently, we discovered a metabolic defence induced by the rice panicle microbiome to defend against fungal disease.
Published in Microbiology
A 7-year path towards exploring a disease-suppressive arsenal
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False smut balls—typical symptoms of Ustilaginoidea virens
successful infection on the rice panicles (Credits: Xiaoyu Liu)

Ustilaginoidea virens is a biotrophic fungal pathogen that initiates infection at the flowering stage of rice plants through the gap between the lemma and palea of flower1. Successful establishment of infection by this pathogen results in rice false smut (RFS) disease, and this disease has already spread across all rice production regions worldwide2. Some synthetic chemical fungicides have been developed to control RFS, but large input of chemical fungicides has been criticized due to the ecological risks towards non-target organisms in field.

To find out a more environmentally friendly solution, we have implemented not only the studies in lab but also sought for the hidden clues in field since 7 years ago. It came to our attention that resistance to U. virens infection emerged in a susceptible rice cultivar, whereas the companion plants grown in a neighboring paddy field at the same site were seriously diseased. It was exciting because the inconsistence with the classical ‘disease triangle’ occasionally implied some unidentified disease-suppressive action, which is involved with the native microbiota, the hidden subcomponents in plant defense system3.

Field sampling in Dai Village, Xiaoshan District, Hangzhou, Zhejiang Province, China (Credits: Haruna Matsumoto)
Morphology of partial microbial isolates obtained from the panicles
of the disease-suppressive plants (Credits: Mengcen Wang)

Although most of previous works have characterized association of the rhizosphere microbiota with disease suppression in various host plants, we found that the rhizosphere microbial community was not distinguishable between diseased and disease-suppressive plants in either diversity or composition. Instead, it was remarkable that the disease-suppressive plants harbored a distinctive microbial community in the panicles. We further screened a total of 2,357 panicle microbial isolates for the disease-suppressive capacity and found 31 isolates could suppress disease in vivo, despite that most of them could not directly antagonize U. virens. These results led us to a hypothesis that the disease-suppressive action by the native microbiota is not only attributed to the pathogen-antagonizing microbial interaction but a more complex pattern involving the interactions among U. virens, rice and the native microbiota.

Substantial progresses were not made until the role of branched-chain amino acids (BCAAs) was successfully re-defined in the disease-suppressive panicles through integration of metabolic profiling, host genome editing and microbial isolate transplantation experiments together with multiple lines of biochemical and genetic evidences. Interestingly, BCAAs were recently found to play a role in activating salicylic acid-mediated defence responses to promote resistance against fungal disease in wheat4, but it remained elusive whether/how they directly interfere the fungal infection. We further showed that the keystone taxa of panicle microbiota promoted BCAAs accumulation by suppressing expression of a BCAA aminotransferase gene in rice, and the BCAAs accumulated could induce apoptosis-like cell death in U. virens, leading to impaired infection. Moreover, mutation of the BCAA aminotransferase gene also led to BCAAs accumulation and conferred the RFS resistance, even without inoculation of any keystone microbial taxa. In the subsequent 2-year field trials, BCAAs was applied in combination with chemical fungicides with a 50% reduction in dose and showed similar efficacy to higher fungicide concentrations. The overall findings not only decipher the mechanism by which the panicle microbiota facilitate host plants to defeat pathogen attack, but also offer a promising path to breeding of resistance against the RFS by modulation of BCAAs level. More relevant 

Last but not least, we have been curious why the assembly of the panicle microbioal community was different between the disease-suppressive and diseased plants, which belonged to the same rice cultivar. We have noticed that different seed treatments had been implemented on the rice plants from this study (with or without fungicidal seed coating), but we are still not sure whether this widespread Anthropocene activity drives the variance in the assembly of the phyllosphere microbiota in the same cultivar and Anthropocene activities is really an overlooked factor that could determine the outcome of plant-microbiome interactions. We believe that the future work would uncover not only the specific impact but also the underlying mechanism in terms of plant health and disease.

Co-evolution of host plants and the phyllosphere microbiome is sophisticated, which always involves with a crosstalk network composed by an array of signaling molecules and transduction pathways5,6,7. This study identifies a piece of the mechanistics underlying the phyllosphere microbiome-mediated disease resistance8, whilst we are still standing at the dawn of the phyllosphere microbiome studies. 

Proposed model for the phyllosphere microbiome-coordinated crosstalk in disease resistance (Credits: Nat Food 3, 997–1004, https://doi.org/10.1038/s43016-022-00636-2)

References
1. Zhang, Y. et al. Specific adaptation of Ustilaginoidea virens in occupying host florets revealed by comparative and functional genomics. Nat Commun 5, 3849, doi:10.1038/ncomms4849 (2014).

2. Sun, W. et al. Ustilaginoidea virens: Insights into an Emerging Rice Pathogen. Annual Review of Phytopathology 58, doi:10.1146/annurev-phyto-010820-012908 (2020).

3. Matsumoto, H. et al. Bacterial seed endophyte shapes disease resistance in rice. Nat Plants 7, 60–72, doi:10.1038/s41477-020-00826-5 (2021).

4. Corredor-Moreno, P. et al. The branched-chain amino acid aminotransferase TaBCAT1 modulates amino acid metabolism and positively regulates wheat rust susceptibility. Plant Cell 33, 1728-1747, doi:10.1093/plcell/koab049 (2021).

5. Ma, KW., Niu, Y., Jia, Y. et al. Coordination of microbe–host homeostasis by crosstalk with plant innate immunity. Nat. Plants 7, 814–825 (2021).

6. Trivedi, P., Leach, J.E., Tringe, S.G. et al. Plant–microbiome interactions: from community assembly to plant health. Nat Rev Microbiol 18, 607–621 (2020).

7. Zhan, C., Matsumoto, H., Liu, Y. & Wang, M. Pathways to engineering the phyllosphere microbiome for sustainable crop production. Nat Food 3, 997–1004, (2022).

8. Liu, X., Matsumoto, H., Lv, T. et al. Phyllosphere microbiome induces host metabolic defence against rice false-smut disease. Nat Microbiol (2023). https://doi.org/10.1038/s41564-023-01379-x

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