Endophytic <italic toggle="yes">Streptomyces hygroscopicus</italic> OsiSh-2-Mediated Balancing between Growth and Disease Resistance in Host Rice
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
Affiliations
Yan Gao
State Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Province Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, Hunan, China
Qing Ning
State Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Province Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, Hunan, China
Yuanzhu Yang
State Key Laboratory of Hybrid Rice, Yahua Seeds Science Academy of Hunan, Changsha, Hunan, China
Ying Liu
State Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Province Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, Hunan, China
Shuqi Niu
State Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Province Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, Hunan, China
Xiaochun Hu
State Key Laboratory of Hybrid Rice, Yahua Seeds Science Academy of Hunan, Changsha, Hunan, China
Huairong Pan
State Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Province Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, Hunan, China
Zhigang Bu
State Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Province Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, Hunan, China
Ning Chen
State Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Province Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, Hunan, China
Jinyou Guo
State Key Laboratory of Hybrid Rice, Yahua Seeds Science Academy of Hunan, Changsha, Hunan, China
Jinlan Yu
State Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Province Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, Hunan, China
Lidan Cao
State Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Province Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, Hunan, China
Peng Qin
State Key Laboratory of Hybrid Rice, Yahua Seeds Science Academy of Hunan, Changsha, Hunan, China
Junjie Xing
State Key Laboratory of Hybrid Rice, Hunan Hybrid Rice Research Center, Changsha, Hunan, China
Bin Liu
State Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Province Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, Hunan, China
Xuanming Liu
State Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Province Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, Hunan, China
Yonghua Zhu
State Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Province Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, Hunan, China
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.”