Endophytic <italic toggle="yes">Streptomyces hygroscopicus</italic> OsiSh-2-Mediated Balancing between Growth and Disease Resistance in Host Rice
ABSTRACT Plants fine-tune the growth-defense trade-off to survive when facing pathogens. Meanwhile, plant-associated microbes, such as the endophytes inside plant tissues, can benefit plant growth and stress resilience. However, the mechanisms for the beneficial microbes to increase stress resistanc...
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American Society for Microbiology
2021
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oai:doaj.org-article:e880dc7b1e06437892e93c48270840282021-11-10T18:37:51ZEndophytic <italic toggle="yes">Streptomyces hygroscopicus</italic> OsiSh-2-Mediated Balancing between Growth and Disease Resistance in Host Rice10.1128/mBio.01566-212150-7511https://doaj.org/article/e880dc7b1e06437892e93c48270840282021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01566-21https://doaj.org/toc/2150-7511ABSTRACT Plants fine-tune the growth-defense trade-off to survive when facing pathogens. Meanwhile, plant-associated microbes, such as the endophytes inside plant tissues, can benefit plant growth and stress resilience. However, the mechanisms for the beneficial microbes to increase stress resistance with little yield penalty in host plants remain poorly understood. In the present study, we report that endophytic Streptomyces hygroscopicus OsiSh-2 can form a sophisticated interaction with host rice, maintaining cellular homeostasis under pathogen-infection stress, and optimize plant growth and disease resistance in rice. Four-year field trials consistently showed that OsiSh-2 could boost host resistance to rice blast pathogen Magnaporthe oryzae while still maintaining a high yield. The integration of the proteomic, physiological, and transcriptional profiling analysis revealed that OsiSh-2 induced rice defense priming and controlled the expression of energy-consuming defense-related proteins, thus increasing the defense capability with the minimized costs of plant immunity. Meanwhile, OsiSh-2 improved the chloroplast development and optimally maintained the expression of proteins related to plant growth under pathogen stress, thus promoting the crop yield. Our results provided a representative example of an endophyte-mediated modulation of disease resistance and fitness in the host plant. The multilayer effects of OsiSh-2 implicate a promising future of using endophytic actinobacteria for disease control and crop yield promotion. IMPORTANCE Under disease stress, activation of defense response in plants often comes with the cost of a reduction in growth and yield, which is referred as the growth-defense trade-off. The microorganisms which can be recruited by plants to mitigate the growth-defense trade-off are of great value in crop breeding. Here, we reported a rice endophytic actinomycetes Streptomyces hygroscopicus OsiSh-2, which can improve host performances on resistance to rice blast while still sustaining high yield in the 4-year field trials. The proteomic, physiological, and transcriptional profiling data offer insights into the molecular basis underlying the balancing between defense and growth in OsiSh-2-rice symbiont. The findings provide an example for the endophyte-mediated modulation of growth-defense trade-offs in plants and indicated the promising application of endophytic actinobacterial strains in agriculture to breed “microbe-optimized crops.”Yan GaoQing NingYuanzhu YangYing LiuShuqi NiuXiaochun HuHuairong PanZhigang BuNing ChenJinyou GuoJinlan YuLidan CaoPeng QinJunjie XingBin LiuXuanming LiuYonghua ZhuAmerican Society for Microbiologyarticleendophytic actinobacteriadisease resistancedefense primingfitnessproteomic analysisphotosynthetic efficiencyMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021) |
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endophytic actinobacteria disease resistance defense priming fitness proteomic analysis photosynthetic efficiency Microbiology QR1-502 |
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endophytic actinobacteria disease resistance defense priming fitness proteomic analysis photosynthetic efficiency Microbiology QR1-502 Yan Gao Qing Ning Yuanzhu Yang Ying Liu Shuqi Niu Xiaochun Hu Huairong Pan Zhigang Bu Ning Chen Jinyou Guo Jinlan Yu Lidan Cao Peng Qin Junjie Xing Bin Liu Xuanming Liu Yonghua Zhu Endophytic <italic toggle="yes">Streptomyces hygroscopicus</italic> OsiSh-2-Mediated Balancing between Growth and Disease Resistance in Host Rice |
| description |
ABSTRACT Plants fine-tune the growth-defense trade-off to survive when facing pathogens. Meanwhile, plant-associated microbes, such as the endophytes inside plant tissues, can benefit plant growth and stress resilience. However, the mechanisms for the beneficial microbes to increase stress resistance with little yield penalty in host plants remain poorly understood. In the present study, we report that endophytic Streptomyces hygroscopicus OsiSh-2 can form a sophisticated interaction with host rice, maintaining cellular homeostasis under pathogen-infection stress, and optimize plant growth and disease resistance in rice. Four-year field trials consistently showed that OsiSh-2 could boost host resistance to rice blast pathogen Magnaporthe oryzae while still maintaining a high yield. The integration of the proteomic, physiological, and transcriptional profiling analysis revealed that OsiSh-2 induced rice defense priming and controlled the expression of energy-consuming defense-related proteins, thus increasing the defense capability with the minimized costs of plant immunity. Meanwhile, OsiSh-2 improved the chloroplast development and optimally maintained the expression of proteins related to plant growth under pathogen stress, thus promoting the crop yield. Our results provided a representative example of an endophyte-mediated modulation of disease resistance and fitness in the host plant. The multilayer effects of OsiSh-2 implicate a promising future of using endophytic actinobacteria for disease control and crop yield promotion. IMPORTANCE Under disease stress, activation of defense response in plants often comes with the cost of a reduction in growth and yield, which is referred as the growth-defense trade-off. The microorganisms which can be recruited by plants to mitigate the growth-defense trade-off are of great value in crop breeding. Here, we reported a rice endophytic actinomycetes Streptomyces hygroscopicus OsiSh-2, which can improve host performances on resistance to rice blast while still sustaining high yield in the 4-year field trials. The proteomic, physiological, and transcriptional profiling data offer insights into the molecular basis underlying the balancing between defense and growth in OsiSh-2-rice symbiont. The findings provide an example for the endophyte-mediated modulation of growth-defense trade-offs in plants and indicated the promising application of endophytic actinobacterial strains in agriculture to breed “microbe-optimized crops.” |
| format |
article |
| author |
Yan Gao Qing Ning Yuanzhu Yang Ying Liu Shuqi Niu Xiaochun Hu Huairong Pan Zhigang Bu Ning Chen Jinyou Guo Jinlan Yu Lidan Cao Peng Qin Junjie Xing Bin Liu Xuanming Liu Yonghua Zhu |
| author_facet |
Yan Gao Qing Ning Yuanzhu Yang Ying Liu Shuqi Niu Xiaochun Hu Huairong Pan Zhigang Bu Ning Chen Jinyou Guo Jinlan Yu Lidan Cao Peng Qin Junjie Xing Bin Liu Xuanming Liu Yonghua Zhu |
| author_sort |
Yan Gao |
| title |
Endophytic <italic toggle="yes">Streptomyces hygroscopicus</italic> OsiSh-2-Mediated Balancing between Growth and Disease Resistance in Host Rice |
| title_short |
Endophytic <italic toggle="yes">Streptomyces hygroscopicus</italic> OsiSh-2-Mediated Balancing between Growth and Disease Resistance in Host Rice |
| title_full |
Endophytic <italic toggle="yes">Streptomyces hygroscopicus</italic> OsiSh-2-Mediated Balancing between Growth and Disease Resistance in Host Rice |
| title_fullStr |
Endophytic <italic toggle="yes">Streptomyces hygroscopicus</italic> OsiSh-2-Mediated Balancing between Growth and Disease Resistance in Host Rice |
| title_full_unstemmed |
Endophytic <italic toggle="yes">Streptomyces hygroscopicus</italic> OsiSh-2-Mediated Balancing between Growth and Disease Resistance in Host Rice |
| title_sort |
endophytic <italic toggle="yes">streptomyces hygroscopicus</italic> osish-2-mediated balancing between growth and disease resistance in host rice |
| publisher |
American Society for Microbiology |
| publishDate |
2021 |
| url |
https://doaj.org/article/e880dc7b1e06437892e93c4827084028 |
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