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Morphogenesis, ultrastructure, and chemical profiling of trichomes in Artemisia argyi H. Lév. & Vaniot (Asteraceae)

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Abstract

Main conclusion

Glandular trichomes of Artemisia argyi H. Lév. & Vaniot are the key tissues for the production of flavonoid and terpenoid metabolites.

Abstract

Artemisia argyi H. Lév. & Vaniot is an herbaceous perennial plant that has been widely used in traditional medicine for thousands of years. Glandular trichomes (GTs) and nonglandular trichomes (NGTs) have been reported on the leaf surface of A. argyi. The aim of this study was to elucidate the morphogenetic process and to analyze the metabolites of trichomes in A. argyi. The morphogenesis of GTs and NGTs was characterized using light, scanning, and transmission electron microscopy. The constituents of GTs were analyzed using laser microdissection combined with gas and liquid chromatography–mass spectrometry. Five developmental stages of two types of GTs and four developmental stages of one type of NGTs were observed. Two types of mature GT and one type of NGT were composed of 10, 5, and 4–6 cells, respectively. A large storage cavity was detected between the cuticle and cell walls in the first type of mature GT. Large nuclei, nucleoli, and mitochondria were observed in the basal and intermediate cells of the second type of GT. In addition, large vacuoles were observed in the basal and apical cells, and large nuclei were observed in the middle cells of NGTs. One monoterpene and seven flavonoids were identified in GTs of A. argyi. We suggest that GTs are the key tissues for the production of bioactive metabolites in A. argyi. This study provides an important theoretical basis and technical approach for clarifying the regulatory mechanisms for trichome development and bioactive metabolite biosynthesis in A. argyi.

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References

  • Abad MJ, Bedoya LM, Apaza L, Bermejo P (2012) The Artemisia L. Genus: a review of bioactive essential oils. Molecules 17:2542–2566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cappelletti EM, Caniato R, Appendino G (1986) Localization of the cytotoxic hydroperoxyeudesmanolides in Artemisia umbelliformis. Biochem Syst Ecol 14:183–190

    Article  CAS  Google Scholar 

  • Chang, J. Yu T, Yang QH, Li CX, Xiong C, Gao SH, Xie QM, Zheng FY, Li HX, Tian ZD, Yang CX, Ye ZB (2018) Hair, encoding a single C2H2 zinc-finger protein, regulates multicellular trichome formation in tomato. Plant J 96: 90–102

  • Chinese Pharmacopoeia Commission (2020) Pharmacopoeia of the People’s Republic of China. Chinese Medical Science and Technology Press, Beijing, China

    Google Scholar 

  • Cui ZH, Huang XZ, Li C, Li Z, Li MJ, Gu L, Gao L, Liu DH, Zhang ZY (2020) Morphology, distribution, density and chemical composition of glandular trichomes in Artemisia argyi (Asteraceae). Int J Agric Biol 24:359–365

    CAS  Google Scholar 

  • Cui LL, Wang XZ, Lu J, Tian J, Wang L, Qu JJ, Liu ZH, Wei JF (2021) Rapid identification of chemical constituents in Artemisia argyi Le´vi. et Vant by UPLC-Q–Exactive–MS/MS. J Food Quality 2021: 5597327

  • Duke SO, Paul RN (1993) Development and fine structure of the glandular trichomes of Artemisia annua L. Inter J Plant Sci 154:107–118

    Article  Google Scholar 

  • Duke MV, Paul RN, Elsohly HN, Sturtz G, Duke SO (1994) Localization of artemisinin and artemisitene in foliar tissues of glanded and glandless biotypes of Artemisia annua L. Inter J Plant Sci 155:365–372

    Article  Google Scholar 

  • Feng ZX, Bartholomew ES, Liu ZY, Cui YY, Dong YM, Li S, Wu HY, Ren HZ, Liu XW (2021) Glandular trichomes: new focus on horticultural crops. Hortic Res 8:158

    Article  PubMed  PubMed Central  Google Scholar 

  • Gao SH, Gao YN, Xiong C, Yu G, Chang J, Yang QH, Yang CX, Ye ZB (2017) The tomato B-type cyclin gene, SlCycB2, plays key roles in reproductive organ development, trichome initiation, terpenoids biosynthesis and Prodenia litura defense. Plant Sci 262:103–114

    Article  CAS  PubMed  Google Scholar 

  • Han BS, Xin ZQ, Ma SS, Liu WB, Zhang BY, Ran L, Yi LZ, Ren DB (2017) Comprehensive characterization and identification of antioxidants in Folium Artemisiae argyi using high-resolution tandem mass spectrometry. J Chromatogr B 1063:84–92

    Article  CAS  Google Scholar 

  • Hu ZH (2012) Anatomy of plant secretory structure. Shanghai Science and Technology Press, Shanghai, China

    Google Scholar 

  • Huang XZ, Zhang Y, Wang X, Gao L, Guo LP, Kang LP (2018) Comparison of moxa yield rate of Artemisiae argyi Folium from different origins based on laboratory production techniques. Chin J Exp Tradit Med Form 24:40–45

    Google Scholar 

  • Konarska A, Łotocka B (2020) Glandular trichomes of Robinia viscosa Vent. var. hartwigii (Koehne) Ashe (Faboideae, Fabaceae)—morphology, histochemistry and ultrastructure. Planta 252:102

  • Lan XY, Zhu LB, Huang XZ, Liu DH, Hao QX, Zhou L, Yang J, Guo LP, Zhang Y, Kang LP (2021) Study on identification and quantitation of main compounds in Artemisiae Argyi Folium. Chin Tradit Herbal Drugs 52:7630–7637

    Google Scholar 

  • Lim MY, Zhang XY, Huang J, Liu L, Liu YT, Zhao BX, Hu H, He FR, Xie JJ, Qiu DS (2021) Study of thermal behavior of moxa floss using thermogravimetric and pyrolysis-GC/MS analyses. Evid Based Complement Alternat Med 2021:6298565

    PubMed  PubMed Central  Google Scholar 

  • Liu DG, Chen YJ, Wan XL, Shi NN, Huang LQ, Wan DR (2017) Artemisiae argyi folium and its geo-authentic crude drug qi ai. J Tradit Chin Med Sci 4:20–23

    Google Scholar 

  • Liu YH, Liu DD, Khan AR, Liu BH, Wu MJ, Huang LL, Wu JY, Song G, Ni HW, Ying HM, Yu H, Gan YB (2018) NbGIS regulates glandular trichome initiation through GA signaling in tobacco. Plant Mol Biol 98:153–167

    Article  CAS  PubMed  Google Scholar 

  • Liu LC, Liu CC, Wu QN (2021) Research progress of plant glandular trichomes. Chin Tradit Herbal Drugs 52:883–893

    Google Scholar 

  • Luo DD, Peng HS, Zhang Y, Huang XZ, Zhan ZL, Liu DH, Kang LP, Huang LQ (2020) Comparison of chemical components between Artemisia stolonifera and Artemisia argyi using UPLC–Q-TOF–MS. China J Chin Materia Med 45:4057–4064

    Google Scholar 

  • Luo DD, Pen HS, Kang LP, Miao YH, Liu DH, Huang LQ (2021) Morphological comparison of glandular and non-glandular trichomes between Artemisia stolonifera and A. argyi. China J Chin Materia Med 46:4319–4329

    Google Scholar 

  • Lusa MG, Cardoso EC, Machado SR (2015) Trichomes related to an unusual method of water retention and protection of the stem apex in an arid zone perennial species. AoB Plants 7:1–10

    Article  CAS  Google Scholar 

  • Maurya S, Chandra M, Yadav RK, Narnoliya LK, Sangwan RS, Bansal S, Sangwan NS (2019) Interspecies comparative features of trichomes in Ocimum reveal insights for biosynthesis of specialized essential oil metabolites. Protoplasma 256:893–907

    Article  CAS  PubMed  Google Scholar 

  • Muravnik LE, Kostina OV, Shavarda AL (2016) Glandular trichomes of Tussilago farfara (Senecioneae, Asteraceae). Planta 244:737–752

    Article  CAS  PubMed  Google Scholar 

  • Muravnik LE, Kostina OV, Mosina AA (2019) Glandular trichomes of the leaves in three Doronicum species (Senecioneae, Asteraceae): morphology, histochemistry, and ultrastructure. Protoplasma 256:789–803

    Article  CAS  PubMed  Google Scholar 

  • Naydenova GK, Georgiev GI (2013) Physiological function of non-glandular trichomes in red clover (Trifolium pratense L.). J Agric Sci Belgrade 58:217–222

    Article  Google Scholar 

  • Pesch M, Schultheiß I, Klopffleisch K, Uhrig JF, Koegl M, Clemen CS, Simon R, Weidtkamp-Peters S, Hülskamp M (2015) TRANSPARENT TESTA GLABRA1 and GLABRA1 compete for binding to GLABRA3 in Arabidopsis. Plant Physiol 168:584–597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramsay NA, Glover BJ (2005) MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trends Plant Sci 10:63–70

    Article  CAS  PubMed  Google Scholar 

  • Riddick EW, Simmons AM (2014) Do plant trichomes cause more harm than good to predatory insects. Pest Manag Sci 70:1655–1665

    Article  CAS  PubMed  Google Scholar 

  • Schuurink R, Tissier A (2020) Glandular trichomes: micro-organs with model status? New Phytol 225:2251–2266

    Article  PubMed  Google Scholar 

  • Seol GH, Kim KY (2016) Eucalyptol and its role in chronic diseases. Adv Exp Med Biol 929:389–398

    Article  CAS  PubMed  Google Scholar 

  • Shi P, Fu XQ, Shen Q, Liu M, Pan QF, Tang YL, Jiang WM, Lv ZY, Yan TX, Ma YN, Chen MH, Hao XL, Liu P, Li L, Sun XF, Tang KX (2018) The roles of AaMIXTA1 in regulating the initiation of glandular trichomes and cuticle biosynthesis in Artemisia annua. New Phytol 217:261–276

    Article  CAS  PubMed  Google Scholar 

  • Silva SCDM, Tozin LRDS, Rodrigues TM (2016) Morphological and histochemical characterization of the secretory sites of bioactive compounds in leaves of Lantana camara L. (Verbenaceae). Botany 94:321–336

    Article  Google Scholar 

  • Slone JH, Kelsey RG (1985) Isolation and purification of glandular secretory cells from Artemisia tridentata (ssp. vaseyana) by Percoll density gradient centrifugation. Am J Bot 72:1445–1451

    Article  Google Scholar 

  • Song XW, Wen X, He JW, Zhao H, Li SM, Wang MY (2019) Phytochemical components and biological activities of Artemisia argyi. J Funct Foods 52:648–662

    Article  CAS  Google Scholar 

  • Tan HX, Xiao L, Gao SH, Li Q, Chen JF, Xiao Y, Ji Q, Chen RB, Chen WS, Zhang L (2015) Trichome and artemisinin regulator 1 is required for trichome development and artemisinin biosynthesis in Artemisia annua. Mol Plant 8:1396–1411

    Article  CAS  PubMed  Google Scholar 

  • Tang QY, Fu W, Zhou YF, Zhou DZ (2014) Observation glandular trichomes and analysis volatile substance for three kinds of Artemisia using SPME–GC–MS. J Hubei University Nationalities 32:371–374

    Google Scholar 

  • The Plant List. (2017). Missouri Botanical Garden and Royal Botanic Gardens, Kew. (2017). http://www.mobot.org/theplantlist/ Accessed 2017

  • Tissier A (2012) Glandular trichomes: what comes after expressed sequence tags? Plant J 70:51–68

    Article  CAS  PubMed  Google Scholar 

  • Vargas W, Fortuna-Perez AP, Lewis GP, Piva TC, Vatanparast M, Machado SR (2019) Ultrastructure and secretion of glandular trichomes in species of subtribe Cajaninae Benth (Leguminosae, Phaseoleae). Protoplasma 256:431–445

    Article  PubMed  Google Scholar 

  • Verma SKM (2017) Trichome: role of promoter and cis-regulatory elements, and effect of gamma radiation, UV radiation, methylation, phosphorylation. Inter J Pure Applied Bio 5:284–292

    Article  Google Scholar 

  • Xiao JQ, Liu WY, Sun HP, Li W, Koike K, Kikuchi T, Yamada T, Li D, Feng F, Zhang J (2019) Bioactivity-based analysis and chemical characterization of hypoglycemic and antioxidant components from Artemisia argyi. Bioorg Chem 92:103268

  • Xu HY, Zhang FX, Liu BX, Huhman DV, Sumner LW, Dixon RA, Wang GD (2013) Characterization of the formation of branched short-chain fatty acid: CoAs for bitter acid biosynthesis in hop glandular trichomes. Mol Plant 6:1301–1317

    Article  CAS  PubMed  Google Scholar 

  • Xu J, van Herwijnen ZO, Dräger DB, Sui C, Haring MA, Schuurink RC (2018) SlMYC1 regulates type VI glandular trichome formation and terpene biosynthesis in tomato glandular cells. Plant Cell 30:2988–3005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan TX, Chen MH, Shen Q, Li L, Fu XQ, Pan QF, Tang YL, Shi P, Lv ZY, Jiang WM, Ma YN, Hao XL, Sun XF, Tang KX (2016) HOMEODOMAIN PROTEIN 1 is required for jasmonate-mediated glandular trichome initiation in Artemisia annua. New Phytol 213:1145–1155

    Article  PubMed  CAS  Google Scholar 

  • Yan TX, Li L, Xie LH, Chen MH, Shen Q, Pan QF, Fu XQ, Shi P, Tang YL, Huang HY, Huang YW, Huang YR, Tang KX (2018) A novel HD-ZIP IV/MIXTA complex promotes glandular trichome initiation and cuticle development in Artemisia annua. New Phytol 218:567–578

    Article  CAS  PubMed  Google Scholar 

  • Yang CX, Li HX, Zhang JH, Luo ZD, Gong PJ, Zhang CJ, Li JH, Wang TT, Zhang YY, Lu YE, Ye ZB (2011) A regulatory gene induces trichome formation and embryo lethality in tomato. Proc Natl Acad Sci 108:11836–11841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang K, Huang XZ, Wang LL, Chen SQ (2020a) Surface observation of Artemisia argyi folium from different areas using scanning electron microscopy. J Chin Electron Microsc Society 39:173–180

    Google Scholar 

  • Yang CQ, Marillonnet S, Tissier A (2021) The Scarecrow-like transcription factor SlSCL3 regulates volatile terpene biosynthesis and glandular trichome size in Tomato (Solanum lycopersicum). Plant J 107:1102–1118

    Article  CAS  PubMed  Google Scholar 

  • Yang MT, Kuo TF, Chung KF, Liang YC, Yang CW, Lin CY, Feng CS, Chen ZW, Lee TH, Hsiao CL, Yang WC (2020b) Authentication, phytochemical characterization and antibacterial activity of two Artemisia species. Food Chem 333:127458

  • Zhang Y, Kang LP, Li HM, Huang XZ, Liu XY, Guo LP, Huang LQ (2019) Characterization of moxa floss combustion by TG/DSC, TG-FTIR and IR. Bioresource Technol 288:121516

  • Zhou PN, Yin MJ, Dai SL, Bao K, Song CL, Liu CC, Wu QN (2021) Multi-omics analysis of the bioactive constituents biosynthesis of glandular trichome in Perilla frutescens. BMC Plant Biol 21:277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu B (2018) On the considerations about heating materials and temperature of moxibustion in clinical practice. Acupunct Res 43:63–67

    Google Scholar 

Download references

Acknowledgements

This work was supported by the National Key Research and Development Program of China (2017YFC1700704), the National Natural Science Foundation of China (81803661), Special Project for the Construction of Modern Agricultural Industrial Technology System (CARS-21), and Traditional Chinese Medicine Industry Technology System of Henan Province.

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Authors and Affiliations

  1. College of Agriculture, Fujian Agriculture and Forestry University, Fuzhou, 350002, China

    Zhanhu Cui & Zhongyi Zhang

  2. Henan Province Key Laboratory of Zhang Zhongjing Formulae and Herbs for Immunoregulation, Nanyang Institute of Technology, Nanyang, 473004, China

    Mengzhi Li, Chao Li & Xianzhang Huang

  3. Anhui University of Chinese Medicine, Hefei, 230012, China

    Xiaojing Han & Huasheng Peng

  4. Experimental Center, Shandong University of Traditional Chinese Medicine, Jinan, 250355, China

    Hongyan Liu

  5. Hubei University of Chinese Medicine, Wuhan, 430065, China

    Dahui Liu

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  1. Zhanhu Cui
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Cui, Z., Li, M., Han, X. et al. Morphogenesis, ultrastructure, and chemical profiling of trichomes in Artemisia argyi H. Lév. & Vaniot (Asteraceae). Planta 255, 102 (2022). https://doi.org/10.1007/s00425-022-03889-0

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