Microbiome Signature of Endophytes in Wheat Seed Response to Wheat Dwarf Bunt Caused by Tilletia controversa Kühn

ABSTRACT Wheat dwarf bunt leads to the replacement of seeds with fungal galls containing millions of teliospores of the pathogen Tilletia controversa Kühn. As one of the most devastating internationally quarantined wheat diseases, wheat dwarf bunt spreads to cause distant outbreaks by seeds containi...

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Main Authors: Zhaoyu Ren, Amanda Juan Chen, Qianqian Zong, Zhenzhen Du, Qingyuan Guo, Taiguo Liu, Wanquan Chen, Li Gao
Format: Article
Language:English
Published: American Society for Microbiology 2023-02-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.00390-22
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author Zhaoyu Ren
Amanda Juan Chen
Qianqian Zong
Zhenzhen Du
Qingyuan Guo
Taiguo Liu
Wanquan Chen
Li Gao
author_facet Zhaoyu Ren
Amanda Juan Chen
Qianqian Zong
Zhenzhen Du
Qingyuan Guo
Taiguo Liu
Wanquan Chen
Li Gao
author_sort Zhaoyu Ren
collection DOAJ
description ABSTRACT Wheat dwarf bunt leads to the replacement of seeds with fungal galls containing millions of teliospores of the pathogen Tilletia controversa Kühn. As one of the most devastating internationally quarantined wheat diseases, wheat dwarf bunt spreads to cause distant outbreaks by seeds containing teliospores. In this study, based on a combination of amplicon sequencing and isolation approaches, we analyzed the seed microbiome signatures of endophytes between resistant and susceptible cultivars after infection with T. controversa. Among 310 bacterial species obtained only by amplicon sequencing and 51 species obtained only by isolation, we found 14 overlapping species by both methods; we detected 128 fungal species only by amplicon sequencing, 56 only by isolation, and 5 species by both methods. The results indicated that resistant uninfected cultivars hosted endophytic communities that were much more stable and beneficial to plant health than those in susceptible infected cultivars. The susceptible group showed higher diversity than the resistant group, the infected group showed more diversity than the uninfected group, and the microbial communities in seeds were related to infection or resistance to the pathogen. Some antagonistic microbes significantly suppressed the germination rate of the pathogen’s teliospores, providing clues for future studies aimed at developing strategies against wheat dwarf bunt. Collectively, this research advances the understanding of the microbial assembly of wheat seeds upon exposure to fungal pathogen (T. controversa) infection. IMPORTANCE This is the first study on the microbiome signature of endophytes in wheat seed response to wheat dwarf bunt caused by Tilletia controversa Kühn. Some antagonistic microbes suppressed the germination of teliospores of the pathogen significantly, which will provide clues for future studies against wheat dwarf bunt. Collectively, this research first advances the understanding of the microbial assembly of wheat seed upon exposure to the fungal pathogen (T. controversa) infection.
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spelling doaj.art-bbd64838207e49d78ac7b28a1d097be42023-02-14T14:15:49ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-02-0111110.1128/spectrum.00390-22Microbiome Signature of Endophytes in Wheat Seed Response to Wheat Dwarf Bunt Caused by Tilletia controversa KühnZhaoyu Ren0Amanda Juan Chen1Qianqian Zong2Zhenzhen Du3Qingyuan Guo4Taiguo Liu5Wanquan Chen6Li Gao7State Key Laboratory for Biology of Plant Disease and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of ChinaMicrobiome Research Center, Moon (Guangzhou) Biotech Ltd., Guangzhou, People’s Republic of ChinaState Key Laboratory for Biology of Plant Disease and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of ChinaState Key Laboratory for Biology of Plant Disease and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of ChinaXinjiang Agricultural University, Urumqi, Xinjiang, People’s Republic of ChinaState Key Laboratory for Biology of Plant Disease and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of ChinaState Key Laboratory for Biology of Plant Disease and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of ChinaState Key Laboratory for Biology of Plant Disease and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of ChinaABSTRACT Wheat dwarf bunt leads to the replacement of seeds with fungal galls containing millions of teliospores of the pathogen Tilletia controversa Kühn. As one of the most devastating internationally quarantined wheat diseases, wheat dwarf bunt spreads to cause distant outbreaks by seeds containing teliospores. In this study, based on a combination of amplicon sequencing and isolation approaches, we analyzed the seed microbiome signatures of endophytes between resistant and susceptible cultivars after infection with T. controversa. Among 310 bacterial species obtained only by amplicon sequencing and 51 species obtained only by isolation, we found 14 overlapping species by both methods; we detected 128 fungal species only by amplicon sequencing, 56 only by isolation, and 5 species by both methods. The results indicated that resistant uninfected cultivars hosted endophytic communities that were much more stable and beneficial to plant health than those in susceptible infected cultivars. The susceptible group showed higher diversity than the resistant group, the infected group showed more diversity than the uninfected group, and the microbial communities in seeds were related to infection or resistance to the pathogen. Some antagonistic microbes significantly suppressed the germination rate of the pathogen’s teliospores, providing clues for future studies aimed at developing strategies against wheat dwarf bunt. Collectively, this research advances the understanding of the microbial assembly of wheat seeds upon exposure to fungal pathogen (T. controversa) infection. IMPORTANCE This is the first study on the microbiome signature of endophytes in wheat seed response to wheat dwarf bunt caused by Tilletia controversa Kühn. Some antagonistic microbes suppressed the germination of teliospores of the pathogen significantly, which will provide clues for future studies against wheat dwarf bunt. Collectively, this research first advances the understanding of the microbial assembly of wheat seed upon exposure to the fungal pathogen (T. controversa) infection.https://journals.asm.org/doi/10.1128/spectrum.00390-22wheat seedTilletia controversa Kühnwheat dwarf buntamplicon sequencingisolationendophytes
spellingShingle Zhaoyu Ren
Amanda Juan Chen
Qianqian Zong
Zhenzhen Du
Qingyuan Guo
Taiguo Liu
Wanquan Chen
Li Gao
Microbiome Signature of Endophytes in Wheat Seed Response to Wheat Dwarf Bunt Caused by Tilletia controversa Kühn
Microbiology Spectrum
wheat seed
Tilletia controversa Kühn
wheat dwarf bunt
amplicon sequencing
isolation
endophytes
title Microbiome Signature of Endophytes in Wheat Seed Response to Wheat Dwarf Bunt Caused by Tilletia controversa Kühn
title_full Microbiome Signature of Endophytes in Wheat Seed Response to Wheat Dwarf Bunt Caused by Tilletia controversa Kühn
title_fullStr Microbiome Signature of Endophytes in Wheat Seed Response to Wheat Dwarf Bunt Caused by Tilletia controversa Kühn
title_full_unstemmed Microbiome Signature of Endophytes in Wheat Seed Response to Wheat Dwarf Bunt Caused by Tilletia controversa Kühn
title_short Microbiome Signature of Endophytes in Wheat Seed Response to Wheat Dwarf Bunt Caused by Tilletia controversa Kühn
title_sort microbiome signature of endophytes in wheat seed response to wheat dwarf bunt caused by tilletia controversa kuhn
topic wheat seed
Tilletia controversa Kühn
wheat dwarf bunt
amplicon sequencing
isolation
endophytes
url https://journals.asm.org/doi/10.1128/spectrum.00390-22
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