Plant Diversity ›› 2023, Vol. 45 ›› Issue (01): 104-116.DOI: 10.1016/j.pld.2022.02.003
2,3-Butanediol from the leachates of pine needles induces the resistance of Panax notoginseng to the leaf pathogen Alternaria panax
Tian-Yao Lia,b,c, Chen Yeb,c, Yi-Jie Zhangb,c, Jun-Xing Zhangb,c, Min Yangb,c, Xia-Hong Heb,c,d, Xin-Yue Meib,c, Yi-Xiang Liub,c, You-Yong Zhua,b,c, Hui-Chuan Huangb,c, Shu-Sheng Zhub,c
- a. School of Agriculture, Yunnan University, Kunming, 650500, China;
b. State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University, Kunming, 650201, China;
c. Key Laboratory of Agro-Biodiversity and Pest Management of Education Ministry of China, Yunnan Agricultural University, Kunming, 650201, China;
d. Southwest Forestry University, Kunming, 650224, China
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收稿日期:2021-12-30修回日期:2022-02-19发布日期:2023-02-23 -
通讯作者:Hui-Chuan Huang,E-mail:absklhhc@gmail.com;Shu-Sheng Zhu,E-mail:sszhu@ynau.edu.cn -
基金资助:This work was supported by the National Key Research and Development Program of China (2017YFC1702502), the Major Science and Technology Project in Yunnan Province (202102AE090042; 202102AA310048-2), Science and Technology Project of Kunming (2021JH002), Innovative Research Team of Science and Technology in Yunnan Province (202105AE160016).
2,3-Butanediol from the leachates of pine needles induces the resistance of Panax notoginseng to the leaf pathogen Alternaria panax
Tian-Yao Lia,b,c, Chen Yeb,c, Yi-Jie Zhangb,c, Jun-Xing Zhangb,c, Min Yangb,c, Xia-Hong Heb,c,d, Xin-Yue Meib,c, Yi-Xiang Liub,c, You-Yong Zhua,b,c, Hui-Chuan Huangb,c, Shu-Sheng Zhub,c
- a. School of Agriculture, Yunnan University, Kunming, 650500, China;
b. State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University, Kunming, 650201, China;
c. Key Laboratory of Agro-Biodiversity and Pest Management of Education Ministry of China, Yunnan Agricultural University, Kunming, 650201, China;
d. Southwest Forestry University, Kunming, 650224, China
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Received:2021-12-30Revised:2022-02-19Published:2023-02-23 -
Contact:Hui-Chuan Huang,E-mail:absklhhc@gmail.com;Shu-Sheng Zhu,E-mail:sszhu@ynau.edu.cn -
Supported by:This work was supported by the National Key Research and Development Program of China (2017YFC1702502), the Major Science and Technology Project in Yunnan Province (202102AE090042; 202102AA310048-2), Science and Technology Project of Kunming (2021JH002), Innovative Research Team of Science and Technology in Yunnan Province (202105AE160016).
摘要： Compared with the use of monocultures in the field, cultivation of medicinal herbs in forests is an effective strategy to alleviate disease. Chemical interactions between herbs and trees play an important role in disease suppression in forests. We evaluated the ability of leachates from needles of Pinus armandii to induce resistance in Panax notoginseng leaves, identified the components via gas chromatography-mass spectrometry (GC-MS), and then deciphered the mechanism of 2,3-Butanediol as the main component in the leachates responsible for resistance induction via RNA sequencing (RNA-seq). Prespraying leachates and 2,3-Butanediol onto leaves could induce the resistance of P. notoginseng to Alternaria panax. The RNA-seq results showed that prespraying 2,3-Butanediol onto leaves with or without A. panax infection upregulated the expression of large number of genes, many of which are involved in transcription factor activity and the mitogen-activated protein kinase (MAPK) signaling pathway. Specifically, 2,3-Butanediol spraying resulted in jasmonic acid (JA) -mediated induced systemic resistance (ISR) by activating MYC2 and ERF1. Moreover, 2,3-Butanediol induced systemic acquired resistance (SAR) by upregulating pattern-triggered immunity (PTI)- and effector-triggered immunity (ETI)-related genes and activated camalexin biosynthesis through activation of WRKY33. Overall, 2,3-Butanediol from the leachates of pine needles could activate the resistance of P. notoginseng to leaf disease infection through ISR, SAR and camalexin biosynthesis. Thus, 2,3-Butanediol is worth developing as a chemical inducer for agricultural production.
引用本文
Tian-Yao Li, Chen Ye, Yi-Jie Zhang, Jun-Xing Zhang, Min Yang, Xia-Hong He, Xin-Yue Mei, Yi-Xiang Liu, You-Yong Zhu, Hui-Chuan Huang, Shu-Sheng Zhu. 2,3-Butanediol from the leachates of pine needles induces the resistance of Panax notoginseng to the leaf pathogen Alternaria panax[J]. Plant Diversity, 2023, 45(01): 104-116.
Tian-Yao Li, Chen Ye, Yi-Jie Zhang, Jun-Xing Zhang, Min Yang, Xia-Hong He, Xin-Yue Mei, Yi-Xiang Liu, You-Yong Zhu, Hui-Chuan Huang, Shu-Sheng Zhu. 2,3-Butanediol from the leachates of pine needles induces the resistance of Panax notoginseng to the leaf pathogen Alternaria panax[J]. Plant Diversity, 2023, 45(01): 104-116.
| [1] Ahuja, I., Kissen, R., Bones, A.M., 2012. Phytoalexins in defense against pathogens. Trends Plant Sci. 17, 73-90 [2] Albuquerque, M.B., Santos, R.C., Lima, L.M., et al., 2010. Allelopathy, an alternative tool to improve cropping systems. A review. Agron. Sustain. Dev. 31, 379-395 [3] Asai, T., Tena, G., Plotnikova, J., et al., 2002. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977-983 [4] Bachheti, A., Sharma, A., Bachheti, R.K., et al., 2019. Plant allelochemicals and their various applications. In:Co-Evolution of Secondary Metabolites, Reference Series in Phytochemistry. pp. 1-25 [5] Breeze, E., 2019. Master MYCs:MYC2, the jasmonate signaling "master switch." Plant Cell 31, 9-10 [6] Chen, Y., Dong, J., Bennetzen, J.L., et al., 2017. Integrating transcriptome and microRNA analysis identifies genes and microRNAs for AHO-induced systemic acquired resistance in N. tabacum. Sci. Rep. 7, 12504 [7] Chen, S., Guo, B., 2004. Sustainable utilization of Chinese material medicine resources. World Science and Technology-Modernization of Traditional Chinese Medicine and Materia Medica [8] Chinchilla, D., Shan, L., He, P., et al., 2009. One for all:the receptor-associated kinase BAK1. Trends Plant Sci. 14, 535-541 [9] Chomel, M., Baldy, V., Guittonny, M., et al., 2020. Litter leachates have stronger impact than leaf litter on Folsomia candida fitness. Soil Biol. Biochem. 147 [10] Colson-Hanks, E.S., Deverall, B.J., 2001. Effect of 2,6-dichloroisonicotinic acid, its formulation materials and benzothiadiazole on systemic resistance to alternaria leaf spot in cotton. Plant Pathol. 49, 171-178 [11] Conrath, U., 2006. Systemic acquired resistance. Plant Signal. Behav. 1, 179-184 [12] Cortes-Barco, A.M., Goodwin, P.H., Hsiang, T., 2010a. Comparison of induced resistance activated by benzothiadiazole, (2R,3R)-butanediol and an isoparaffin mixture against anthracnose of Nicotiana benthamiana. Plant Pathol. 59, 643-653 [13] Cortes-Barco, A.M., Hsiang, T., Goodwin, P.H., 2010b. Induced systemic resistance against three foliar diseases of Agrostis stolonifera by (2R,3R)-butanediol or an isoparaffin mixture. Ann. Appl. Biol. 157, 179-189 [14] De Araujo, A.A., Roussos, S., 2002. A technique for mycelial development of ectomycorrhizal fungi on agar media. Appl. Biochem. Biotechnol. 98-100, 311-318 [15] Ding, X., Yang, M., Huang, H., et al., 2015. Priming maize resistance by its neighbors:activating 1,4-benzoxazine-3-ones synthesis and defense gene expression to alleviate leaf disease. Front. Plant Sci. 6, 830 [16] Donald, P.F., 2004. Society for conservation biology biodiversity impacts of some agricultural commodity production systems. Conserv. Biol. 18, 17-37 [17] Dusa, A., 2019. Draw Venn Diagrams[R Package Venn version 1.8] [18] Encinas-Villarejo, S., Maldonado, A.M., Amil-Ruiz, F., et al., 2009. Evidence for a positive regulatory role of strawberry (Fragaria x ananassa) Fa WRKY1 and Arabidopsis at WRKY75 proteins in resistance. J. Exp. Bot. 60, 3043-3065 [19] Gaba, S., Lescourret, F., Boudsocq, S., et al., 2014. Multiple cropping systems as drivers for providing multiple ecosystem services:from concepts to design. Agron. Sustain. Dev. 35, 607-623 [20] Glazebrook, J., 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205-227 [21] Guerra, T., Schilling, S., Hake, K., et al., 2020. Calcium-dependent protein kinase 5 links calcium signaling with N-hydroxy-l-pipecolic acid- and SARD1-dependent immune memory in systemic acquired resistance. New Phytol. 225, 310-325 [22] Guo, C., Guo, R., Xu, X., et al., 2014. Evolution and expression analysis of the grape (Vitis vinifera L.) WRKY gene family. J. Exp. Bot. 65, 1513-1528 [23] Harel, Y.M., Mehari, Z.H., Rav-David, D., et al., 2014. Systemic resistance to gray mold induced in tomato by benzothiadiazole and Trichoderma harzianum T39. Phytopathology 104, 150-157 [24] Hickman, R., Van Verk, M.C., Van Dijken, A.J.H., et al., 2017. Architecture and dynamics of the jasmonic acid gene regulatory network. Plant Cell 29, 2086-2105 [25] Mapk Group, 2002. Mitogen-activated protein kinase cascades in plants:a new nomenclature. Trends Plant Sci. 7, 301-308 [26] Ivette Perfecto, John Vandermeer, 2008. Biodiversity conservation in tropical agroecosystems:a new conservation paradigm. Annals of the New York Academy of ences p.173-200 [27] Jing, S.Q., Jiang, H.P., Liu, F.Y., et al., 2009. Canparison of seven ginsenoside contents in shengshaishen hongshen and linxiashen. Chinese Archives of Traditional Chinese Medicine [28] Kadota, Y., Liebrand, T.W.H., Goto, Y., et al., 2019. Quantitative phosphoproteomic analysis reveals common regulatory mechanisms between effector- and PAMP-triggered immunity in plants. New Phytol. 221, 2160-2175 [29] Kato-Noguchi, H., Fushimi, Y., Tanaka, Y., et al., 2011. Allelopathy of red pine:isolation and identification of an allelopathic substance in red pine needles. Plant Growth Regul. 65, 299-304 [30] Keesing, F., Ostfeld, R., 2015. Ecology. Is biodiversity good for your health? Science (New York, N.Y.) 349, 235-236 [31] Kim, D., Langmead, B., Salzberg, S.L., 2015a. HISAT:a fast spliced aligner with low memory requirements. Nat. Methods 12, 357-360 [32] Kim, Y.J., Zhang, D., Yang, D.C., 2015b. Biosynthesis and biotechnological production of ginsenosides. Biotechnol. Adv. 33, 717-735 [33] Li, B., Dewey, C., 2011. Li B, Dewey CN. RSEM:accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinf. 12:323. BMC bioinformatics 12, 323 [34] Li, C., He, X., Zhu, S., et al., 2006. Crop diversity for yield increase. PLoS One 4, e8049 [35] Li, J., Kolbasov, V., Pang, Z., et al., 2021. Evaluation of the control effect of SAR inducers against citrus Huanglongbing applied by foliar spray, soil drench or trunk injection. Phytopathology Research 3 [36] Liu, Y., Zhang, S., 2004. Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16, 3386-3399 [37] Livak, K., Schmittgen, T., 2000. Analysis of relative gene expression data using real-time quantitative PCR and the 2-△△Ct method. Method. Methods. 25 [38] Lorenzo, O., Piqueras, R., Sanchez-Serrano, J.J., et al., 2003. ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15, 165-178 [39] Luo, L., Guo, C., Wang, L., et al., 2019. Negative plant-soil feedback driven by Re-assemblage of the rhizosphere microbiome with the growth of panax notoginseng. Front. Microbiol. 10, 1597 [40] Luo, L.-F., Yang, L., Yan, Z.-X., et al., 2020. Ginsenosides in root exudates of Panax notoginseng drive the change of soil microbiota through carbon source different utilization. Plant Soil 455, 139-153 [41] Ma, X., Claus, L.A.N., Leslie, M.E., et al., 2020. Ligand-induced monoubiquitination of BIK1 regulates plant immunity. Nature 581, 199-203 [42] Maeda, T., Ishiwari, H., 2012. Tiadinil, a plant activator of systemic acquired resistance, boosts the production of herbivore-induced plant volatiles that attract the predatory mite Neoseiulus womersleyi in the tea plant Camellia sinensis. Exp. Appl. Acarol. 58, 247-258 [43] Mancuso, C., Santangelo, R., 2017. Panax ginseng and Panax quinquefolius:from pharmacology to toxicology. Food Chem. Toxicol. 107, 362-372 [44] Mao, G., Meng, X., Liu, Y., et al., 2011. Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23, 1639-1653 [45] Maobe, M.A.G., Gatebe, E., Gitu, L., et al., 2012. Profile of heavy metals in selected medicinal plants used for the treatment of diabetes, malaria and pneumonia in Kisii region, Southwest Kenya. Global J. Pharmacol. 6, 245-251 [46] Meng, X., Xu, J., He, Y., et al., 2013. Phosphorylation of an ERF transcription factor by Arabidopsis MPK3/MPK6 regulates plant defense gene induction and fungal resistance. Plant Cell 25, 1126-1142 [47] Mhlongo, M.I., Piater, L.A., Madala, N.E., et al., 2018. The chemistry of plant-microbe interactions in the rhizosphere and the potential for metabolomics to reveal signaling related to defense priming and induced systemic resistance. Front. Plant Sci. 9, 112 [48] Mundt, C., 2002. Use of multiline cultivars and cultivar mixtures for disease management. Annu. Rev. Phytopathol. 40, 381-410 [49] Newton, A., Begg, G., Swanston, J., 2008. Deployment of diversity for enhanced crop function. Ann. Appl. Biol. 154, 309-322 [50] Nishizawa, A., Yabuta, Y., Yoshida, E., et al., 2006. Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J. 48, 535-547 [51] Onate-Sanchez, L., Anderson, J.P., Young, J., et al., 2007. AtERF14, a member of the ERF family of transcription factors, plays a nonredundant role in plant defense. Plant Physiol 143, 400-409 [52] Pelissier, R., Violle, C., Morel, J.B., 2021. Plant immunity:good fences make good neighbors? Curr. Opin. Plant Biol. 62, 102045 [53] Pertea, M., Pertea, G.M., Antonescu, C.M., et al., 2015. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat. Biotechnol. 33, 290-295 [54] Piasecka, A., Jedrzejczak-Rey, N., Bednarek, P., 2015. Secondary metabolites in plant innate immunity:conserved function of divergent chemicals. New Phytol. 206, 948-964 [55] Pieterse, C.M., Van der Does, D., Zamioudis, C., et al., 2012. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28, 489-521 [56] Pieterse, C.M., Zamioudis, C., Berendsen, R., et al., 2014. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52, 347-375 [57] Poelman, E., van Loon, J., Dicke, M., 2008. Consequences of plant defense for biodiversity at higher trophic levels. Trends Plant Sci. 13, 534-541 [58] Thomas, P., 2003. EIN3-dependent regulation of plant ethylene hormone signaling by two arabidopsis F box proteins:EBF1 and EBF2. J. Cell. 6 [59] Raivo Kolde, 2019. Pheatmap:Pretty Heatmaps. R Package Version 1.0.12 [60] Rentel, M.C., Lecourieux, D., Ouaked, F., et al., 2004. OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427, 858-861 [61] Ritchie, M.E., Phipson, B., Wu, D., et al., 2015. Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47 [62] Sellam, A., Iacomi-Vasilescu, B., Hudhomme, P., et al., 2007. In vitro antifungal activity of brassinin, camalexin and two isothiocyanates against the crucifer pathogens Alternaria brassicicola and Alternaria brassicae. Plant Pathol. 56, 296-301 [63] Shettima, A.Y., Karumi, Y., Sodipo, O.A., et al., 2013. Gas chromatography-mass spectrometry (GC-MS) analysis of bioactive components of ethyl acetate root extract of Guiera senegalensis J.F. Gmel. Journal of Applied Pharmaceutical Science 3, 146-150 [64] Shi, Y., Liu, X., Fang, Y., et al., 2018. 2, 3-Butanediol activated disease-resistance of creeping bentgrass by inducing phytohormone and antioxidant responses. Plant Physiol. Biochem. 129, 244-250 [65] Solano, R., Stepanova, A., Chao, Q., et al., 1998. Nuclear events in ethylene signaling:a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. J Genes Development 12 [66] Song, S., Huang, H., Gao, H., et al., 2014. Interaction between MYC2 and ETHYLENE INSENSITIVE3 modulates antagonism between jasmonate and ethylene signaling in Arabidopsis. Plant Cell 26, 263-279 [67] Spoel, S.H., Dong, X., 2012. How do plants achieve immunity? Defence without specialized immune cells. Nat. Rev. Immunol. 12, 89-100 [68] Su, J., Yang, L., Zhu, Q., et al., 2018. Active photosynthetic inhibition mediated by MPK3/MPK6 is critical to effector-triggered immunity. PLoS Biol. 16, e2004122 [69] Suzuki, N., Miller, G., Morales, J., et al., 2011. Respiratory burst oxidases:the engines of ROS signaling. Curr. Opin. Plant Biol. 14, 691-699 [70] Syu, M.J., 2001. Biological production of 2,3-butanediol. Appl. Microbiol. Biotechnol. 55, 10-18 [71] Taha, S.M., Gadalla, S.A., 2017. Development of an efficient method for multi residue analysis of 160 pesticides in herbal plant by ethyl acetate hexane mixture with direct injection to GC-MS/MS. Talanta 174, 767-779 [72] Team, D., 2013. R:A Language and Environment for Statistical Computing Team RDCVienna, Austria2006 [73] Thomma, B., Nelissen, I., Eggermont, K., et al., 1999. Deficiency in phytoalexin production causes enhanced susceptibilty of Arabidopsis thaliana to the fungus Alternaria brassicola. Plant J.:for cell and molecular biology 19, 163-171 [74] Thomma, B.P., Nurnberger, T., Joosten, M.H., 2011. Of PAMPs and effectors:the blurred PTI-ETI dichotomy. Plant Cell 23, 4-15 [75] Tscharntke, T., Clough, Y., Bhagwat, S., et al., 2011. Multifunctional shade-tree management in tropical agroforestry landscapes-a review. J. Appl. Ecol. 48, 619-629 [76] Tsuda, K., Katagiri, F., 2010. Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr. Opin. Plant Biol. 13, 459-465 [77] Tsuda, K., Mine, A., Bethke, G., et al., 2013. Dual regulation of gene expression mediated by extended MAPK activation and salicylic acid contributes to robust innate immunity in Arabidopsis thaliana. PLoS Genet. 9, e1004015 [78] Van den Berg, N., Swart, V., Backer, R., et al., 2021. Advances in understanding defense mechanisms in persea americana against phytophthora cinnamomi. Front. Plant Sci. 12, 636339 [79] Venegas-Molina, J., Molina-Hidalgo, F.J., Clicque, E., et al., 2021. Why and how to dig into plant metabolite-protein interactions. Trends Plant Sci. 26, 472-483 [80] Verma, S.S., Yajima, W.R., Rahman, M.H., et al., 2012. A cysteine-rich antimicrobial peptide from Pinus monticola (PmAMP1) confers resistance to multiple fungal pathogens in canola (Brassica napus). Plant Mol. Biol. 79, 61-74 [81] Vlot, A.C., Sales, J.H., Lenk, M., et al., 2020. Systemic Propagation of Immunity in Plants. New Phytologist [82] Wang, R., He, F., Ning, Y., et al., 2020. Fine-tuning of RBOH-mediated ROS signaling in plant immunity. Trends Plant Sci. 25, 1060-1062 [83] Wei, W., Yang, M., Liu, Y., et al., 2018. Fertilizer N application rate impacts plant-soil feedback in a sanqi production system. Sci. Total Environ. 633, 796-807 [84] Wu, Hongmiao, Xia, J., Qin, X., et al., 2020. Underlying mechanism of wild radix pseudostellariae in tolerance to disease under the natural forest cover. Front. Microbiol. 11 [85] Yan, Z.Y., 2012. Major tasks and challenges for resources science of Chinese medicinal materials. Pharmacy & Clinics of Chinese Materia Medica [86] Yang, H., 2016. Main Practice and Effects of Chinese Herbal Medicine Planting under Forest Development in Xiji County. Modern Agricultural Science & Technology [87] Yang, T., Chen, Y.J., Duan, C.L., et al., 2006. The methodology for artificial identification of panax notoginseng resistance to black spot disease. J. Yunnan Agric. Univ. 21, 549-548 [88] Yang, M., Zhang, Y., Qi, L., et al., 2014. Plant-plant-microbe mechanisms involved in soil-borne disease suppression on a maize and pepper intercropping system. PLoS One 9, e115052 [89] Yang, M., Zhang, X., Xu, Y., et al., 2015. Autotoxic ginsenosides in the rhizosphere contribute to the replant failure of Panax notoginseng. PLoS One 10, e0118555 [90] Yang, Z., Liu, G., Zhang, G., et al., 2021. The chromosome-scale high quality genome assembly of Panax notoginseng provides insight into dencichine biosynthesis. Plant biotechnology journal 19 [91] Ye, C., Y. Fang, H, J. Liu, H., et al., 2019. Current status of soil sickness research on Panax notoginseng in Yunnan, China. Allelopathy J. 47, 1-14 [92] Ye, C., Liu, Y., Zhang, J., et al., 2021. α-Terpineol fumigation alleviates negative plant-soil feedbacks of Panax notoginseng via suppressing Ascomycota and enriching antagonistic bacteria. Phytopathology Research 3 [93] Yu, G., Wang, L.G., Han, Y., et al., 2012. clusterProfiler:an R package for comparing biological themes among gene clusters. Omics 16, 284-287 [94] Yu, X., Feng, B., He, P., et al., 2017. From chaos to harmony:responses and signaling upon microbial pattern recognition. Annu. Rev. Phytopathol. 55, 109-137 [95] Zeng, W., Jia, L., 2009. Antimicrobial activities of pine needle extracts. Food Sci. (N. Y.) 30, 87-90 [96] Zhang, S., Klessig, D.F., 2001. MAPK cascades in plant defense signaling. Trends Plant Sci. 6, 520-527 [97] Zhang, X., Yang, T., Lin, Q., et al., 2011a. Isolation and identification of an acetoin high production bacterium that can reverse transform 2,3-butanediol to acetoin at the decline phase of fermentation. World J. Microbiol. Biotechnol. 27, 2785-2790 [98] Zhang, Y., Sun, H., Song, X., et al., 2011b. Studied on soil microbial community structure about wild ginseng under forest. Res. Soil Water Conserv. 18, 169-173 [99] Zhang, X., Zhu, Z., An, F., et al., 2014. Jasmonate-activated MYC2 represses ETHYLENE INSENSITIVE3 activity to antagonize ethylene-promoted apical hook formation in Arabidopsis. Plant Cell 26, 1105-1117 [100] Zhang, S., Chen, C., Lu, W., et al., 2018. Phytochemistry, pharmacology, and clinical use of Panax notoginseng flowers buds:active Components and Uses of Panax notoginseng Flowers. Phytother Res. 32 [101] Zhong, L.L., Yang, W., Lam, W.C., et al., 2020. Potential targets for treatment of coronavirus disease 2019 (COVID-19):a review of qing-fei-pai-du-tang and its major herbs. Am. J. Chin. Med. 48 [102] Zhou, P., Xie, W., He, S., et al., 2019. Ginsenoside Rb1 as an anti-diabetic agent and its underlying mechanism analysis. Cells 8, 204 [103] Zhu, S., Morel, J.B., 2019. Molecular mechanisms underlying microbial disease control in intercropping. Mol. Plant Microbe Interact. 32, 20-24 |
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