Xuexia Miao

Personal Profile

Working experiences:

2020.05 – Present Principal Investigator CAS Center for Excellence in Molecular Plant Sciences/Shanghai Institute of Plant Physiology and Ecology, CAS

2013.05 – 2020.04 Principal Investigator CAS Key Laboratory of Insect Developmental and Evolutionary Biology, Shanghai Institute of Plant Physiology and Ecology, SIBS, CAS

2007.01 - 2013.04 Professor Shanghai Institute of Plant Physiology and Ecology, CAS

2006.01 - 2006.12 Postdoctoral Research Fellow, University of Paris Sud

2002.09 - 2005.12 Associate Professor Shanghai Institute of Plant Physiology and Ecology, SIBS, CAS

1998.09 - 1999.09 Assistant Professor Shanghai Institute of Entomology, CAS

1995.08 - 1998.08 Lecturer Henan Agricultural University

1988.07 - 1992.08 Assistant Engineer Henan Jinxing Brewery

Education experiences:

1999.09 - 2002.06 Graduate University of Chinese Academy of Sciences Ph.D, Biological Control

1992.09 - 1998.06 Henan Agricultural University M.S, Applied Microbiology

1984.09 - 1988.06 Henan Agricultural University B.S, Plant Protection

Research Work

  Our major research interest focuses on plant-insect interactions. Two main areas of research are currently being pursued:

 

  (1) Exploration of resistance genes in rice and their mechanism. To identify endogenous insect-resistance genes from rice, taking advantage of forward and reverse genetics approaches, we have cloned some resistance genes. And then the gene function, metabolic pathways and resistance mechanisms will be analyzed through biochemical and molecular biology approaches. Our ultimate research goal is to supply some new gene loci for breeding insect-resistant rice.

 

  (2) R&D of new type biological insecticides. Since 2015, the output and dosage of chemical pesticides in China have continued to fall, and there is an urgent need for green and environment friendly new biopesticides to be iteratively supplemented. Nucleic acid biopesticide is known as the third revolution in the history of pesticides, which is a new type of biopesticide with biological safety and ecological safety. Our research group has developed species-specific nucleic acid biopesticides for important pests on major food and vegetable crops in China to minimize the impact of pesticides on other organisms and the environment.

Main Achievements

(1) Discovery and verification of dual resistance genes to brown planthopper and rice blast fungus

  The plant hormone jasmonic acid (JA) regulates a wide range of developmental processes and plays a central role in regulating plant defenses against biotic and abiotic stresses (Creelman and Mullet, 1995). The main products of the JA synthetic pathway are OPDA (cis-12–oxo-phytodienoic acid), JA, and JA-Ile (the bioactive form of JA conjugated with isoleucine), which serve as signaling compounds regulating multiple defense responses to both microbial pathogens and herbivore attack (Lyons et al., 2013). Allene oxide cyclase (AOC) produces the JA precursor OPDA, which is reduced by OPDA reductase (OPR) and then yields JA by three rounds of β-oxidation (Schaller, 2001; Wasternack & Strnad, 2018). Only one rice chloroplast gene encodes AOC (Riemann et al., 2013) and rice OPR3 is functionally equivalent to Arabidopsis OPR3 (Yara et al., 2008). Previous studies indicated that JA signaling was involved in rice resistance to chewing insect caterpillars of Spodoptera litura, while the phloem-sap feeding insect of BPH probably induces the salicylic acid (SA) pathway (Zhang et al., 2004; Karban and Chen, 2007). However, how the JA and SA pathways regulate the responses to piercing-sucking and/or chewing herbivorous insects is still unclear.

  To study the exact role of OPDA in plant resistance and whether OPDA is involved in rice resistance against BPH, rice AOC (which produces OPDA) and OPR3 (which reduces OPDA) when they were overexpressed. Results showed that enhanced expression of AOC led to the increased resistance to both SSB and BPH, while OPR3 overexpression increased resistance to SSB only. Further studies revealed that rice resistance to BPH under AOC overexpression may be due to the increased level of OPDA, which functions independently of the JA pathway and serves as an important signaling molecule to improve plant resistance to phloem-sap feeding insects (Guo et al., 2014).

 

(2) MYB22–TOPLESS–HDAC1 is a novel transcriptional repressor complex in plant resistance to planthopper

  The MYB family is one of the biggest TF families and is involved in regulating diverse biological processes ranging from plant development to defense (Ambawat et al., 2013). In rice, OsMYB30 directly activates the expression of Os4CL3/5 in the phenylpropanoid pathway, which leads to the accumulation of lignin in sclerenchyma cells, thereby protecting plants from Magnaporthe oryzae (Li et al., 2020). Another OsMYB30 TF also enhances plant resistance to BPH by binding directly to the PAL6/PAL8 promoters to activate their expression and increase salicylic acid and lignin levels (He et al., 2020). However, all above mentioned TFs are transcriptional activators.

  Our study indicated that MYB22 regulates rice resistance to BPH via its EAR motif. Several biochemical experiments indicated that MYB22 is a transcriptional repressor that interacts with the corepressor TOPLESS via its EAR motif and recruits HDAC1 to form a tripartite complex. However, whether MYB22 functions as a transcriptional repressor influencing the rice–BPH interaction is unclear. OsF3′H is a flavonoid biosynthesis pathway-related gene that negatively regulates rice resistance to BPH. Based on a bioinformatics analysis and the results of EMSA and transient transcription assays, MYB22 can bind directly to the OsF3′H promoter and repress gene expression along with TOPLESS and HDAC1. Our results revealed a novel transcriptional regulatory mechanism influencing the rice–BPH interaction. MYB22–TOPLESS–HDAC1 is a novel transcriptional repressor complex with components that synergistically and positively regulate rice resistance to BPH through the transcriptional repression of OsF3′H (Sun et al., 2023).

 

(3) The OsmiR396–OsGRF8–OsF3H-flavonoid pathway mediates resistance to the brown planthopper in rice

  The functions of miR396 in plant development have largely been revealed (Hewezi et al., 2012). However, whether and how miR396 functions in insect resistance is largely unknown. Flavonoids are a representative group of secondary metabolites that are widespread in plants and have protective functions against environmental stresses (Bharti et al., 2015; Pourcel et al., 2007). To investigate the possible involvement of miRNAs in rice–BPH interactions, we performed miRNA sequencing analyses before and after BPH infestation and identified BPH-induced OsmiR396. Through the functional analysis of OsmiR396, one target gene, OsGRF8, and one gene in flavonoid biosynthesis, OsF3H, were identified. A biochemical analysis of the direct regulation of OsGRF8 on OsF3H and a genetic correlation analysis between OsmiR396 and OsF3H, showed that OsmiR396–OsGRF8 modulated BPH resistance by directly regulating OsF3H. Thus, we revealed a new BPH resistance mechanism mediated by the OsmiR396–OsGRF8–OsF3H–flavonoid pathway (Dai et al., 2019). During the study, we also found that OsmiR396 has a major role related to the regulation of rice grain size. Further studies confirmed that the OsmiR396/GRF meditated rice grain size regulation (Yang et al., 2021).

 

(4) Confirmation of a dual resistance gene to piercing-sucking and chewing insects in rice

  Plant mitochondria play an important role in the response to biotic stress and are deeply involved in the signaling networks related to plant innate immune responses, which usually impact the ability to generate changes in respiration, membrane potential and ROS production (Colombatti et al. 2014). Mitochondrial outer membrane protein 64 is suggested to interact dynamically with the TOM complex (Chew et al.2004; Schweiger et al, 2013). A research result indicated that OM64 is phosphorylated within its TPR domain and reduces the binding affinity of OM64 to Hsp90 and impairs the import efficiency of the mitochondrial preprotein (Nickel et al. 2019). So, we want to know whether OM64 is involved in plant immune responses.

  Using a rice OM64 gene loss-of function mutant from a rice T-DNA insertion mutant library that showed a significantly increased level of resistance to BPH. The om64 mutant also showed enhanced resistance to SSB, a chewing insect, which was due to promotion of Jasmonic acid biosynthesis and related responses. Importantly, om64 plants presented no significant changes in rice yield-related characters. Our results indicated that the lack of OM64 stimulated rice can defense against piercing-sucking and chewing insects simultaneously. Further study indicated that deletion of OM64 in rice led to the enhanced production of hydrogen peroxide (H2O2), hence conferred rice resistant to BPH. In addition, OM64 involved in rice defense against the chewing insect SSB, this mainly through SSB induced Jasmonic acid (JA) biosynthesis and responses (Guo et al., 2020).

 

(5) R&D of RNAi-based insecticides and its industrialization

  RNAi has not only provided a novel and powerful reverse genetics tool for gene functional study, but also showed great potential in pest management (Baum et al., 2007, 2014; Joga et al, 2016; Mao et al., 2007; Zhu and Palli, 2020). Because RNAi technology can realize precision, high efficiency, and pollution-free pest control, it is called “the third revolution in the history of pesticides” (Vogel et al., 2019; Silver et al., 2021; Palli, 2023).

In 2017, the world's first plant-incorporated protectants (PIP) RNA pesticide product, MON87411, was approved for cultivation by the U.S. Environmental Protection Agency (EPA). So far, five PIP RNA pesticide products have been licensed for cultivation. On September 28, 2023, the world's first spray-based Non-PIPs RNAi-based pesticide "Ledprona" has been signed a preliminary license letter by US EPA (Guan et al., 2022; Lu et al., 2023). "Ledprona" is the first commercially available dsRNA insecticide in the world that can be sprayed on plants, targeting potato beetles (Pallis et al., 2023). As an important milestone event, it will open a new era of dsRNA biopesticide research and application.

  Our research team has been working on RNAi-based pesticides for more than a decade. With the accumulation of technology, in August 2020, with the support of investors and this institute, we constructed a company. This company dedicated to the research and development of non-PIP RNAi-based pesticides, including the whole process from target screening, large-scale and low-cost production of dsRNA, and preparations. At present, we have obtained more than 200 effective RNAi insecticidal targets, the production cost of dsRNA has been less than 50 RMB/gram, and we have obtained an efficient delivery system with independent intellectual property rights. Five of our products have obtained the naming letter from the Ministry of Agriculture of China, which has laid the foundation for the registration of drug certificates. More important is the company also received financial support of 4 million yuan from the 14^th Five-Year Plan “National Key Research and Development Program of China”.

Publications

1. Bo Sun^#, Yanjie Shen, Su Chen, Zhenying Shi, Haichao Li*, Xuexia Miao*. A novel transcriptional repressor complex MYB22–TOPLESS–HDAC1 promotes rice resistance to brown planthopper by repressing F3’H expression. New Phytologist, 2023, 239: 720-738.

 

2. Ruobing Guan*, Tong Li*, Guy Smagghe*, Xuexia Miao* and Haichao Li*. Editorial: dsRNA-based pesticides: production, development, and application technology. Frontiers in Bioengineering and Biotechnology, 2023, 11: 1197666 (Invited review).

 

3. Su Chen^#, Bo Sun, Zhenying Shi, Xuexia Miao*, Haichao Li*. Identification of the rice genes and metabolites involved in dual resistance against brown planthopper and rice blast fungus. Plant Cell and Environment, 2022, 45: 1914-929.

 

4. Ruobing Guan^#, Haichao Li, Xuexia Miao*. Commercialization Status and Existing Problems of RNA Biopesticides. Scientia Agricultura Sinica (in Chinese), 2022, 55(15): 2949-2960.

 

5. Xiaofang Yang^#, Xiaoling Zhao, Zhengyan Dai, Feilong Ma, Xuexia Miao*, Zhenying Shi*. OsmiR396/growth regulating factor modulate rice grain size through direct regulation of embryo-specific miR408. Plant Physiology, 2021, 186: 519-533.

5. Xuexia Miao, Guirong Wang, Jiang Zhang and Hongwei Zhao. Chapter 7 (pp: 122-153), In: RNA Interference: from Gene Function to Biopesticides (ed. Wengqing Zhang and Guirong Wang) (in Chinese). Science Press. 2021.

6. Xuexia Miao, Kang He and Ruobing Guan. Chapter 9 (pp: 166-180), In: RNA Interference: from Gene Function to Biopesticides (ed. Wengqing Zhang and Guirong Wang) (in Chinese). Science Press. 2021.

 

7. Ruobing Guan^#, Dongdong Chu, Xinyi Han, Xuexia Miao* and Haichao Li*. Advances in the development of microbial double-stranded RNA production systems for application of RNA interference in agricultural pest control. Frontiers in Bioengineering and Biotechnology, 2021, 9: 953790.

 

8. Huimin Guo^#, Haichao Li, Shirong Zhou, Hongwei Xue*, Xuexia Miao*. Deficiency of mitochondrial outer membrane protein 64 confers rice resistance to both piercing-sucking and chewing insects in rice. Journal of Integrative Plant Biology, 2020, 62(12): 1967-1982.

 

9. Dai Zhengyan^#, Tan Jiang^#, Zhou Cong, Yang Xiaofang, Yang Fang, Zhang Shijuan, Sun Shichen, Miao Xuexia*, Shi Zhenying*. The OsmiR396–OsGRF8–OsF3H-flavonoid pathway mediates resistance to the brown planthopper in rice (Oryza sativa). Plant Biotechnology Journal. 2019. DOI: 10.1111/pbi.13091

 

10. Wang Meiling, Yang Dongyong, Ma Feilong, Zhu Mulan, Shi Zhenying, Miao Xuexia*. OsHLH61-OsbHLH96 influences rice defense to brown planthopper through regulating the pathogen-related genes. Rice. 2019,12(9): 1-12.

 

11. Ma Feilong, Yang Xiaofang, Shi Zhenying*, Miao Xuexia*. Novel crosstalk between ethylene- and jasmonic acid-pathway responses to a piercing–sucking insect in rice. New Phytologist. 2019. doi: 10.1111/nph.16111

 

12. Shaoru Hu^#, Ruobing Guan, Haichao Li, Xuexia Miao*. Application of RNAi in insect pest management: important progress and problems. Acta Entomologica Sinica (in Chinese). 2019, 62(4): 506-515.

 

13. Jiang Tan^#, Meiling Wang^#, Zhenying Shi, Xueixia Miao*. OsEXPA10 mediates the balance between growth and resistance to biotic stress in rice. Plant Cell Reports, 2018, 37(7):993-1002.

 

14. Ruobing Guan^#, Haichao Li^#, Yujie Fan, Shaoru Hu, Olivier Christiaens, Guy Smagghe*, Xuexia Miao*. A nuclease specific to lepidopteran insects suppresses RNAi. Journal of Biological Chemistry. 2018, 293(16): 6011-6021.

 

15. Guan Ruobing^#, Hu Shaoru^#, Li Haichao, Shi Zhenying，Miao Xuexia*. Discerning the sequence specificity of the in vivo dsRNA-processing mode using a high-throughput small RNA sequencing analysis. Frontiers in Physiology. 2018, 9: 1768. Doi: 10.3389/fphys.2018.01768

 

16. Ruobing Guan, Haichao Li, Xuexia Miao*. RNAi pest control and enhanced BT insecticidal efficiency achieved by dsRNA of chymotrypsin-like genes in Ostrinia furnacalis. Journal of Pest Science, 2017, 90: 745-757.

 

17. Haichao Li, Ruobing Guan, Huimin Guo, Xuexia Miao*. New insights into an RNAi approach for plant defence against piercing-sucking and stem-borer insect pests. Plant, Cell & Environment. 2015, 38(11): 2277-2285.

 

18. Zhang Hao, Li Haichao, Guan Ruobing, Miao Xuexia*. Lepidopteran insect species-specific, broad-spectrum, and systemic RNA interference by spraying dsRNA on larvae. Entomologia experimentalis et Applicata. 2015, 155(3): 218-228. DOI: 10.1111/eea.12300

 

19. Huimin Guo, Haichao Li, Shirong Zhou, Hongwei Xue*, Xuexia Miao*. Cis-12-oxo-phytodienoic acid stimulates rice defense response to a piercing-sucking insect. Molecular plant, 2014, 7(11): 1683-1693.