Dynamic Changes of Phytohormone Concentrations during Prunella vulgaris L. Development and Impact of Rosmarinic Acid Accumulation through Exogenous ABA Application

Authors

  • Qian Su College of Pharmacy, Hunan University of Chinese Medicine, 410208 Changsha, China; Key Laboratory for Quality Evaluation of Bulk Herbs of Hunan Province, Hunan University of Chinese Medicine, 410208 Changsha, China Author
  • Yan Lin College of Pharmacy, Hunan University of Chinese Medicine, 410208 Changsha, China; Key Laboratory for Quality Evaluation of Bulk Herbs of Hunan Province, Hunan University of Chinese Medicine, 410208 Changsha, China Author
  • Bohou Xia College of Pharmacy, Hunan University of Chinese Medicine, 410208 Changsha, China; Key Laboratory for Quality Evaluation of Bulk Herbs of Hunan Province, Hunan University of Chinese Medicine, 410208 Changsha, China Author
  • Yamei Li College of Pharmacy, Hunan University of Chinese Medicine, 410208 Changsha, China; Key Laboratory for Quality Evaluation of Bulk Herbs of Hunan Province, Hunan University of Chinese Medicine, 410208 Changsha, China Author
  • Jingchen Xie College of Pharmacy, Hunan University of Chinese Medicine, 410208 Changsha, China; Key Laboratory for Quality Evaluation of Bulk Herbs of Hunan Province, Hunan University of Chinese Medicine, 410208 Changsha, China Author
  • Ping Wu College of Pharmacy, Hunan University of Chinese Medicine, 410208 Changsha, China; Key Laboratory for Quality Evaluation of Bulk Herbs of Hunan Province, Hunan University of Chinese Medicine, 410208 Changsha, China Author
  • Zhimin Zhang College of Pharmacy, Hunan University of Chinese Medicine, 410208 Changsha, China; Key Laboratory for Quality Evaluation of Bulk Herbs of Hunan Province, Hunan University of Chinese Medicine, 410208 Changsha, China Author
  • Limei Lin College of Pharmacy, Hunan University of Chinese Medicine, 410208 Changsha, China; Key Laboratory for Quality Evaluation of Bulk Herbs of Hunan Province, Hunan University of Chinese Medicine, 410208 Changsha, China Author

DOI:

https://doi.org/10.62767/jecacm503.8204

Keywords:

Prunella vulgaris L., phytohormone, secondary metabolites, abscisic acid, rosmarinic acid

Abstract

Background: Plant hormones not only participate in regulating the growth and development process of plants, but also play an important regulatory role in the synthesis of secondary metabolites. Prunella vulgaris L. (P. vulgaris) is a perennial herb that has a long history for use as a kind of medicinal and edible plant. In order to understand the relationship between plant hormones and Prunella vulgaris L. (P. vulgaris) development. Methods: The quantification of indoleacetic acid (IAA), salicylic acid (SA), jasmonates (JAs), abscisic acid (ABA), 1-aminocyclopropane-1-carboxylic acid (ACC) and cytokinins (CKs) of P. vulgaris during development was performed by a liquid chromatography-mass spectrometry (LC-MS). Furthermore, the effect of exogenous ABA on rosmarinic acid (RA) accumulation was verified. Results: Nuts formation was related to the concentrations of IAA, ABA and ACC in the green-fruit stage, and IAA and ABA levels increased rapidly in this stage. High IAA concentrations can promote an increase in ACC. SA, JAs, ethylene (ET) and ABA were related to the defence response of plants to pathogens. SA concentrations increased sharply after the turning stage, while the concentration of JAs, which are antagonistic to SA, was low. The decrease in ABA concentration after this period may be related to the antagonistic effect of IAA or SA. The CKs trans-zeatin (tZ) and trans-zeatin riboside (tZR) promoted the growth and development of early P. vulgaris, and their concentrations decreased in the late period, leading to withering and senescence of P. vulgaris. The CKs cis-zeatin (cZ) and N6-(2-isopentenyl) adenine (iP) were presumed to be present in nuts. After elicitation with 10 μg/mL ABA, an increase of RA content was observed (p < 0.05). Conclusion: This study can provide an improved basis for elucidating the growth and development mechanism of P. vulgaris in the future, as well as a better understand of the effects of ABA application on RA accumulations.

References

Zhang Z, Xia B, Li Y, et al. Comparative proteomic analysis of Prunella vulgaris L. spica ripening. Journal of Proteomics 2021; 232: 104028.

Bai Y, Xia B, Xie W, et al. Phytochemistry and pharmacological activities of the genus Prunella. Food Chemistry 2016; 204: 483-496.

Li BY, Hu Y, Li J, et al. Ursolic acid from Prunella vulgaris L. efficiently inhibits IHNV infection in vitro and in vivo. Virus Research 2019; 273: 197741.

Zheng XQ, Song LX, Han ZZ, et al. Pentacyclic triterpenoids from spikes of Prunella vulgaris L. with thyroid tumour cell cytostatic bioactivities. Natural Product Research 2022; 18: 1-9.

Zhang Z, Zhou Y, Lin Y, et al. GC-MS-based metabolomics research on the anti-hyperlipidaemic activity of Prunella vulgaris L. polysaccharides. International Journal of Biological Macromolecules 2020; 159: 461-473.

Pan L, Zeng W, Niu L, et al. PpYUC11, a strong candidate gene for the stony hard phenotype in peach (Prunus persica L. Batsch), participates in IAA biosynthesis during fruit ripening. Journal of Experimental Botany 2015; 66(22): 7031-7044.

Jia HF, Chai YM, Li CL, et al. Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiology 2011; 157(1): 188-199.

Fujita M, Fujita Y, Noutoshi Y, et al. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Current Opinion in Plant Biology 2006; 9(4): 436-442.

Kim HJ, Ryu H, Hong SH, et al. Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 2006; 103(3): 814-819.

National Pharmacopoeia Committee. Chinese Pharmacopoeia; Chemical Industry Press: Beijing, China, 2020.

Trócsányi E, György Z, Zámboriné-Németh É. New insights into rosmarinic acid biosynthesis based on molecular studies. Current Plant Biology 2020; 23: 100162.

Kim J, Lee JG, Hong Y, et al. Analysis of eight phytohormone concentrations, expression levels of ABA biosynthesis genes, and ripening-related transcription factors during fruit development in strawberry. Journal of Plant Physiology 2019; 239: 52-60.

Tong Q, Liu L, Zhao Y, et al. Transcriptome Remodeling in Response to Leaf Removal and Exogenous Abscisic Acid in Berries of Grapevine (Vitis vinifera L.) Fruit Cuttings. Horticulturae 2022; 8(10): 905.

Burkart S, Manderscheid R, Wittich KP, et al. Elevated CO2 effects on canopy and soil water flux parameters measured using a large chamber in crops grown with free-air CO2 enrichment. Plant Biology 2011; 13(2): 258-269.

Mousavi SM, Shabani L. Rosmarinic acid accumulation in Melissa officinalis shoot cultures is mediated by ABA. Biologia Plantarum 2019; 63: 418-424.

Zhang J, Jia W, Yang J, et al. Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Research 2006; 97(1): 111-119.

Gagné S, Cluzet S, Mérillon JM, et al. ABA initiates anthocyanin production in grape cell cultures. Journal of Plant Growth Regulation 2011; 30(1): 1-10.

Hao G, Ji H, Li Y, et al. Exogenous ABA and polyamines enhanced salvianolic acids contents in hairy root cultures of Salvia miltiorrhiza Bge. f. alba. Plant Omics 2012; 5(5): 446-452.

Ibrahim MH, Jaafar HZ. Abscisic acid induced changes in production of primary and secondary metabolites, photosynthetic capacity, antioxidant capability, antioxidant enzymes and lipoxygenase inhibitory activity of Orthosiphon stamineus Benth. Molecules 2013; 18(7): 7957-7976.

Liang Z, Ma Y, Xu T, et al. Effects of abscisic acid, gibberellin, ethylene and their interactions on production of phenolic acids in salvia miltiorrhiza bunge hairy roots. PLoS One 2013; 8(9): e72806.

Villalobos-González L, Peña-Neira A, Ibáñez F, et al. Long-term effects of abscisic acid (ABA) on the grape berry phenylpropanoid pathway: Gene expression and metabolite content. Plant Physiology and Biochemistry 2016; 105: 213-223.

Murcia G, Fontana A, Pontin M, et al. ABA and GA3 regulate the synthesis of primary and secondary metabolites related to alleviation from biotic and abiotic stresses in grapevine. Phytochemistry 2017; 135: 34-52.

Flores G, Blanch GP, del Castillo MLR. Abscisic acid treated olive seeds as a natural source of bioactive compounds. LWT 2018; 90: 556-561.

Cai WJ, Ye TT, Wang Q, et al. A rapid approach to investigate spatiotemporal distribution of phytohormones in rice. Plant Methods 2016; 12: 47.

Xue LJ, Zhang JJ, Xue HW. Genome-wide analysis of the complex transcriptional networks of rice developing seeds. PLoS One 2012; 7(2): e31081.

Benková E, Ivanchenko MG, Friml J, et al. A morphogenetic trigger: is there an emerging concept in plant developmental biology? Trends in Plant Science 2009; 14(4): 189-193.

Enders TA, Strader LC. Auxin activity: Past, present, and future. American Journal of Botany 2015; 102(2): 180-196.

Li N, Han X, Feng D, et al. Signaling Crosstalk between Salicylic Acid and Ethylene/Jasmonate in Plant Defense: Do We Understand What They Are Whispering? International Journal of Molecular Sciences 2019; 20(3): 671.

Bürger M, Chory J. Stressed Out About Hormones: How Plants Orchestrate Immunity. Cell Host & Microbe 2019; 26(2): 163-172.

Vlot AC, Dempsey DA, Klessig DF. Salicylic Acid, a multifaceted hormone to combat disease. Annual Review of Phytopathology 2009; 47: 177-206.

Métraux JP, Signer H, Ryals J, et al. Increase in salicylic Acid at the onset of systemic acquired resistance in cucumber. Science 1990; 250(4983): 1004-1006.

Mauch-Mani B, Mauch F. The role of abscisic acid in plant-pathogen interactions. Current Opinion in Plant Biology 2005; 8(4): 409-414.

LeNoble ME, Spollen WG, Sharp RE. Maintenance of shoot growth by endogenous ABA: genetic assessment of the involvement of ethylene suppression. Journal of Experimental Botany 2004; 55(395): 237-245.

Audenaert K, De Meyer GB, Höfte MM. Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiology 2002; 128(2): 491-501.

Thaler JS, Bostock RM. Interactions between abscisic‐acid‐mediated responses and plant resistance to pathogens and insects. Ecology 2004; 85(1): 48-58.

Jia H, Jiu S, Zhang C, et al. Abscisic acid and sucrose regulate tomato and strawberry fruit ripening through the abscisic acid-stress-ripening transcription factor. Plant Biotechnology Journal 2016; 14(10): 2045-2065.

Reeves I, Emery RJ. Seasonal patterns of cytokinins and microclimate and the mediation of gas exchange among canopy layers of mature Acer saccharum trees. Tree Physiology 2007; 27(11): 1635-1645.

Hönig M, Plíhalová L, Husičková A, et al. Role of Cytokinins in Senescence, Antioxidant Defence and Photosynthesis. International Journal of Molecular Sciences 2018; 19(12): 4045.

Hallmark HT, Rashotte AM. Cytokinin isopentenyladenine and its glucoside isopentenyladenine-9G delay leaf senescence through activation of cytokinin-associated genes. Plant Direct 2020; 4(12): e00292.

Koyama T. A hidden link between leaf development and senescence. Plant Science 2018; 276: 105-110.

Toscano S, Trivellini A, Ferrante A, et al. Physiological mechanisms for delaying the leaf yellowing of potted geranium plants. Scientia Horticulturae 2018; 242: 146-154.

Mok DWS, Mok MC. Cytokinin metabolism and action. Annual Review of Plant Physiology and Plant Molecular Biology 2001; 52: 89-118.

Nordström A, Tarkowski P, Tarkowska D, et al. Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin-cytokinin-regulated development. Proceedings of the National Academy of Sciences of the United States of America 2004; 101(21): 8039-8044.

Werner T, Köllmer I, Bartrina I, et al. New insights into the biology of cytokinin degradation. Plant Biology 2006: 8(3): 371-381.

Bielach A, Hrtyan M, Tognetti VB. Plants under Stress: Involvement of Auxin and Cytokinin. International Journal of Molecular Sciences 2017; 18(7): 1427.

Jones B, Gunnerås SA, Petersson SV, et al. Cytokinin regulation of auxin synthesis in Arabidopsis involves a homeostatic feedback loop regulated via auxin and cytokinin signal transduction. Plant Cell 2010; 22(9): 2956-2969.

Kučerová D, Kollárová K, Vatehová Z, et al. Interaction of galactoglucomannan oligosaccharides with auxin involves changes in flavonoid accumulation. Plant Physiology and Biochemistry 2016; 98: 155-161.

Lee Y, Lee DE, Lee HS, et al. Influence of auxins, cytokinins, and nitrogen on production of rutin from callus and adventitious roots of the white mulberry tree (Morus alba L.). Plant Cell Tissue and Organ Culture (PCTOC) 2011; 105(1): 9-19.

Deikman J, Hammer PE. Induction of Anthocyanin Accumulation by Cytokinins in Arabidopsis thaliana. Plant Physiology 1995,108(1):47-57.

Misra N, Misra R, Mariam A, et al. Salicylic acid alters antioxidant and phenolics metabolism in Catharanthus roseus grown under salinity stress. African Journal of Traditional, Complementary and Alternative Medicines (AJTCAM) 2014; 11(5): 118-125.

Silva-Navas J, Moreno-Risueno MA, Manzano C, et al. Flavonols Mediate Root Phototropism and Growth through Regulation of Proliferation-to-Differentiation Transition. Plant Cell 2016; 28(6): 1372-1387.

Zhao J, Chen L, Ma A, et al. R3-MYB transcription factor LcMYBx from Litchi chinensis negatively regulates anthocyanin biosynthesis by ectopic expression in tobacco. Gene 2022; 812: 146105.

Cusido RM, Onrubia M, Sabater-Jara AB, et al. A rational approach to improving the biotechnological production of taxanes in plant cell cultures of Taxus spp. Biotechnology Advances 2014; 32(6): 1157-1167.

Xia J, Ma YJ, Wang Y, et al. Deciphering transcriptome profiles of tetraploid Artemisia annua plants with high artemisinin content. Plant Physiology and Biochemistry 2018; 130: 112-126.

Lenka SK, Nims NE, Vongpaseuth K, et al. Jasmonate-responsive expression of paclitaxel biosynthesis genes in Taxus cuspidata cultured cells is negatively regulated by the bHLH transcription factors TcJAMYC1, TcJAMYC2, and TcJAMYC4. Frontiers in Plant Science 2015; 6: 115.

Zhang F, Fu X, Lv Z, et al. A basic leucine zipper transcription factor, AabZIP1, connects abscisic acid signaling with artemisinin biosynthesis in Artemisia annua. Molecular Plant 2015; 8(1): 163-175.

Pasquali G, Goddijn OJ, de Waal A, et al. Coordinated regulation of two indole alkaloid biosynthetic genes from Catharanthus roseus by auxin and elicitors. Plant Molecular Biology 1992; 18(6): 1121-1131.

Zhou M, Memelink J. Jasmonate-responsive transcription factors regulating plant secondary metabolism. Biotechnology Advances 2016; 34(4): 441-449.

Zayed R, Wink M. Induction of pyridine alkaloid formation in transformed root cultures of Nicotiana tabacum. Zeitschrift fur Naturforschung - Section C Journal of Biosciences 2009; 64(11-12): 869-874.

Malka SK, Cheng Y. Possible Interactions between the Biosynthetic Pathways of Indole Glucosinolate and Auxin. Frontiers in Plant Science 2017; 8: 2131.

Kageyama A, Ishizaki K, Kohchi T, et al. Abscisic acid induces biosynthesis of bisbibenzyls and tolerance to UV-C in the liverwort Marchantia polymorpha. Phytochemistry 2015; 117: 547-553.

Khaleghnezhad V, Yousefi AR, Tavakoli A, et al. Interactive effects of abscisic acid and temperature on rosmarinic acid, total phenolic compounds, anthocyanin, carotenoid and flavonoid content of dragonhead (Dracocephalum moldavica L.). Scientia Horticulturae 2019; 250: 302-309.

Xiao Y, Zhang L, Gao S, et al. The c4h, tat, hppr and hppd genes prompted engineering of rosmarinic acid biosynthetic pathway in Salvia miltiorrhiza hairy root cultures. PLoS One 2011; 6(12): e29713.

Shen L, Ren J, Jin W, et al. Role of NO signal in ABA-induced phenolic acids accumulation in Salvia miltiorrhiza hairy roots. Sheng Wu Gong Cheng Xue Bao 2016; 32(2): 222-230.

Cui B, Liang Z, Liu Y, et al. Effects of ABA and its biosynthetic inhibitor fluridone on accumulation of penolic acids and activity of PAL and TAT in hairy root of Salvia miltiorrhiza. Zhongguo Zhong Yao Za Zhi 2012; 37(6): 754-759.

Weiss D, Ori N. Mechanisms of cross talk between gibberellin and other hormones. Plant Physiology 2007; 144(3): 1240-1246.

Jiang Y, Joyce DC. ABA effects on ethylene production, PAL activity, anthocyanin and phenolic contents of strawberry fruit. Plant Growth Regulation 2003; 39(2): 171-174.

Published

2024-07-10

Data Availability Statement

Data will be made available on request.

Issue

Section

Original Research

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