Aspergillus cvjetkovicii protects against phytopathogens through interspecies chemical signalling in the phyllosphere

Xiaoyan Fan^{1

2

3

4

5}, Haruna Matsumoto^{1

2

3}, Haorong Xu^{1

2

3}, Hongda Fang^{1

2

3}, Qianqian Pan^{1

2

3}, Tianxing Lv^{1

2

3}, Chengfang Zhan^{1

2

3}, Xiaoxiao Feng⁶, Xiaoyu Liu^{1

2

3

7}, Danrui Su^{1

2

3}, Mengyuan Fan^{1

2}, Zhonghua Ma^{1

2}, Gabriele Berg^{4

8

9}, Shaojia Li¹⁰, Tomislav Cernava^{11

12}, Mengcen Wang^{13

14

15

16}

Affiliations

¹ College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China.
² State Key Laboratory of Rice Biology and Breeding, Ministry of Agricultural and Rural Affairs Laboratory of Molecular Biology of Crop Pathogens and Insects, Zhejiang University, Hangzhou, China.
³ Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Institute of Pesticide and Environmental Toxicology, Zhejiang University, Hangzhou, China.
⁴ Institute of Environmental Biotechnology, Graz University of Technology, Graz, Austria.
⁵ National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, China.
⁶ Agricultural Experiment Station, Zhejiang University, Hangzhou, China.
⁷ Australian Research Council Centre of Excellence in Plant Energy Biology, The University of Western Australia, Perth, Western Australia, Australia.
⁸ Leibniz Institute for Agricultural Engineering and Bioeconomy (ATB), Potsdam, Germany.
⁹ Institute for Biochemistry and Biology, University of Potsdam, Potsdam, Germany.
¹⁰ College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China. shaojiali@zju.edu.cn.
¹¹ Institute of Environmental Biotechnology, Graz University of Technology, Graz, Austria. t.cernava@soton.ac.uk.
¹² School of Biological Sciences, Faculty of Environmental and Life Sciences, University of Southampton, Southampton, UK. t.cernava@soton.ac.uk.
¹³ College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China. wmctz@zju.edu.cn.
¹⁴ State Key Laboratory of Rice Biology and Breeding, Ministry of Agricultural and Rural Affairs Laboratory of Molecular Biology of Crop Pathogens and Insects, Zhejiang University, Hangzhou, China. wmctz@zju.edu.cn.
¹⁵ Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Institute of Pesticide and Environmental Toxicology, Zhejiang University, Hangzhou, China. wmctz@zju.edu.cn.
¹⁶ Global Education Program for AgriScience Frontiers, Graduate School of Agriculture, Hokkaido University, Sapporo, Japan. wmctz@zju.edu.cn.

PMID: 39103572
DOI: 10.1038/s41564-024-01781-z

Aspergillus cvjetkovicii protects against phytopathogens through interspecies chemical signalling in the phyllosphere

Xiaoyan Fan et al. Nat Microbiol. 2024 Nov.

. 2024 Nov;9(11):2862-2876.

doi: 10.1038/s41564-024-01781-z. Epub 2024 Aug 5.

Authors

Affiliations

¹ College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China.
² State Key Laboratory of Rice Biology and Breeding, Ministry of Agricultural and Rural Affairs Laboratory of Molecular Biology of Crop Pathogens and Insects, Zhejiang University, Hangzhou, China.
³ Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Institute of Pesticide and Environmental Toxicology, Zhejiang University, Hangzhou, China.
⁴ Institute of Environmental Biotechnology, Graz University of Technology, Graz, Austria.
⁵ National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, China.
⁶ Agricultural Experiment Station, Zhejiang University, Hangzhou, China.
⁷ Australian Research Council Centre of Excellence in Plant Energy Biology, The University of Western Australia, Perth, Western Australia, Australia.
⁸ Leibniz Institute for Agricultural Engineering and Bioeconomy (ATB), Potsdam, Germany.
⁹ Institute for Biochemistry and Biology, University of Potsdam, Potsdam, Germany.
¹⁰ College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China. shaojiali@zju.edu.cn.
¹¹ Institute of Environmental Biotechnology, Graz University of Technology, Graz, Austria. t.cernava@soton.ac.uk.
¹² School of Biological Sciences, Faculty of Environmental and Life Sciences, University of Southampton, Southampton, UK. t.cernava@soton.ac.uk.
¹³ College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China. wmctz@zju.edu.cn.
¹⁴ State Key Laboratory of Rice Biology and Breeding, Ministry of Agricultural and Rural Affairs Laboratory of Molecular Biology of Crop Pathogens and Insects, Zhejiang University, Hangzhou, China. wmctz@zju.edu.cn.
¹⁵ Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Institute of Pesticide and Environmental Toxicology, Zhejiang University, Hangzhou, China. wmctz@zju.edu.cn.
¹⁶ Global Education Program for AgriScience Frontiers, Graduate School of Agriculture, Hokkaido University, Sapporo, Japan. wmctz@zju.edu.cn.

PMID: 39103572
DOI: 10.1038/s41564-024-01781-z

Erratum in

Author Correction: Aspergillus cvjetkovicii protects against phytopathogens through interspecies chemical signalling in the phyllosphere.
Fan X, Matsumoto H, Xu H, Fang H, Pan Q, Lv T, Zhan C, Feng X, Liu X, Su D, Fan M, Ma Z, Berg G, Li S, Cernava T, Wang M. Fan X, et al. Nat Microbiol. 2025 Mar;10(3):809. doi: 10.1038/s41564-025-01942-8. Nat Microbiol. 2025. PMID: 39891013 No abstract available.

Abstract

Resident microbiota produces small molecules that influence the chemical microenvironments on leaves, but its signalling roles in pathogen defence are not yet well understood. Here we show that Aspergillus cvjetkovicii, enriched in rice leaf microbiota, subverts Rhizoctonia solani infections via small-molecule-mediated interspecies signalling. 2,4-Di-tert-butylphenol (2,4-DTBP), identified as a key signalling molecule within the Aspergillus-enriched microbiota, effectively neutralizes reactive oxygen species-dependent pathogenicity by switching off bZIP-activated AMT1 transcription in R. solani. Exogenous application of A. cvjetkovicii and 2,4-DTBP demonstrated varying degrees of protective effects against R. solani infection in diverse crops, including cucumber, maize, soybean and tomato. In rice field experiments, they reduced the R. solani-caused disease index to 19.7-32.2%, compared with 67.2-82.6% in the control group. Moreover, 2,4-DTBP showed activity against other rice phytopathogens, such as Fusarium fujikuroi. These findings reveal a defensive strategy against phytopathogens in the phyllosphere, highlighting the potential of symbiotic microbiota-driven neutralization of pathogenicity.

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References

1. Mendes, R. et al. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332, 1097–1100 (2011). - PubMed
1. Senapati, M. et al. Rhizoctonia solani Kühn pathophysiology: status and prospects of sheath blight disease management in rice. Front. Plant Sci. 3, 881116 (2022).
1. Ajayi-Oyetunde, O. O. & Bradley, C. A. Rhizoctonia solani: taxonomy, population biology and management of rhizoctonia seedling disease of soybean. J. Plant Pathol. 67, 3–17 (2018).
1. Stephens, P. M. et al. Reduced severity of Rhizoctonia solani disease on wheat seedlings associated with the presence of the earthworm Aporrectodea trapezoides (lumbricidae). Soil Biol. Biochem. 25, 1477–1484 (1993).
1. Pascual, C. B. et al. Characterization by conventional techniques and PCR of Rhizoctonia solani isolates causing banded leaf sheath blight in maize. J. Plant Pathol. 49, 108–118 (2000).

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Aspergillus cvjetkovicii protects against phytopathogens through interspecies chemical signalling in the phyllosphere

Affiliations

Aspergillus cvjetkovicii protects against phytopathogens through interspecies chemical signalling in the phyllosphere

Authors

Affiliations

Erratum in

Abstract

References

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Full Text Sources