Untargeted metabolomic analysis of the metabolites in roots of Pugionium cornutum seedlings under drought stress
Zhaoxin Wu![https://orcid.org/0000-0002-9207-0924](/media/client/orcid_16x16.png)
![https://orcid.org/0000-0002-9534-2403](/media/client/orcid_16x16.png)
A
Abstract
Pugionium cornutum is an annual or biennial xerophyte distributed in arid regions, with drought resistance properties. While previous studies have predominantly focused on the physiological changes of P. cornutum, the understanding of its metabolite variations remains limited. In this study, untargeted metabolomic technology was performed to analyse the change of metabolites in the roots of P. cornutum seedlings under drought stress. Our findings revealed that compared to the R1, the root water potential and the number of lateral roots increased, while the length of the tap root and fresh weight increased first and then decreased. In the R1–R2, a total of 45 differential metabolites (DMs) were identified, whereas in the R1–R3 82 DMs were observed. Subsequently, KEGG analysis revealed a significant enrichment of microbial metabolism in diverse environments and aminobenzoate degradation in the R1–R2, and phenylpropanoid biosynthesis, ubiquinone, and other terpenoid-quinone biosynthesis and isoquinoline alkaloid biosynthesis were significantly enriched in the R1–R3. The upregulation DMs, including L-arginosuccinate, L-tyrosine, p-coumarate, caffeate, ferulate, vanillin, coniferin, 5-aminopentanoate, 2-methylmaleate and 2-furoate in P. cornutum seedlings may play a crucial role in enhancing root growth and improving drought resistance. These findings provide a basis for future investigations into the underlying mechanisms of drought resistance in P. cornutum.
Keywords: Brassicaceae, drought stress, metabolites, physiology, Pugionium cornutum, root, untargeted metabolomics, xerophyte.
References
Alizadeh Yeloojeh K, Saeidi G, Sabzalian MR (2020) Drought stress improves the composition of secondary metabolites in safflower flower at the expense of reduction in seed yield and oil content. Industrial Crops and Products 154, 112496.
| Crossref | Google Scholar |
Bartwal A, Mall R, Lohani P, Guru SK, Arora S (2013) Role of secondary metabolites and brassinosteroids in plant defense against environmental stresses. Journal of Plant Growth Regulation 32, 216-232.
| Crossref | Google Scholar |
Bashir W, Anwar S, Zhao Q, Hussain I, Xie F (2019) Interactive effect of drought and cadmium stress on soybean root morphology and gene expression. Ecotoxicology and Environmental Safety 175, 90-101.
| Crossref | Google Scholar | PubMed |
Bettaieb I, Zakhama N, Wannes WA, et al. (2009) Water deficit effects on Salvia officinalis fatty acids and essential oils composition. Scientia Horticulturae 120(2), 271-275.
| Crossref | Google Scholar |
Coners H, Leuschner C (2005) In situ measurement of fine root water absorption in three temperate tree species – temporal variability and control by soil and atmospheric factors. Basic and Applied Ecology 6, 395-405.
| Crossref | Google Scholar |
Good AG, Zaplachinski ST (1994) The effects of drought stress on free amino acid accumulation and protein synthesis in Brassica napus. Physiologia Plantarum 90(1), 9-14.
| Crossref | Google Scholar |
Goufo P, Moutinho-Pereira JM, Jorge TF, et al. (2017) Cowpea (Vigna unguiculata L. walp.) metabolomics: osmoprotection as a physiological strategy for drought stress resistance and improved yield. Frontiers in Plant Science 8, 586.
| Crossref | Google Scholar | PubMed |
Havaux M, Kloppstech K (2001) The protective functions of carotenoid and flavonoid pigments against excess visible radiation at chilling temperature investigated in Arabidopsis npq and tt mutants. Planta 213, 953-966.
| Crossref | Google Scholar |
Hura T, Hura K, Dziurka K, Ostrowska A, Bączek-Kwinta R, Grzesiak M (2012) An increase in the content of cell wall-bound phenolics correlates with the productivity of triticale under soil drought. Journal of Plant Physiology 169, 1728-1736.
| Crossref | Google Scholar | PubMed |
Jia B, Gao LF, Zhang WH, Guo F, Li TJ, Liu Y, Jin DD, Wu Y, Liu HX (2023) Metabolomics analysis of watermelon seedlings under drought stress. Molecular Plant Breeding 21, 7161-7170.
| Google Scholar |
Jiang ZR (2000) Probe into drought-resisting mechanism of Ammopitanthus mongolicus (Maxim) Cheng F. Journal of Desert Research 20(1), 71-74.
| Google Scholar |
Khan AL, Hussain J, Hamayun M, Gilani SA, Ahmad S, Rehman G, Kim Y-H, Kang S-M, Lee I-J (2010) Secondary metabolites from Inula britannica L. and their biological activities. Molecules 15, 1562-1577.
| Crossref | Google Scholar | PubMed |
Khan N, Bano A, Rahman MA, et al. (2019) UPLC-HRMS-based untargeted metabolic profiling reveals changes in chickpea (Cicer arietinum) metabolome following long-term drought stress. Plant, Cell & Environment 42(1), 115-132.
| Crossref | Google Scholar |
Kleinwächter M, Selmar D (2015) New insights explain that drought stress enhances the quality of spice and medicinal plants: potential applications. Agronomy for Sustainable Development 35, 121-131.
| Crossref | Google Scholar |
Koevoets IT, Venema JH, Elzenga JTM, Testerink C (2016) Roots withstanding their environment: exploiting root system architecture responses to abiotic stress to improve crop tolerance. Frontiers in Plant Science 7, 1335.
| Crossref | Google Scholar | PubMed |
Kumar R, Bohra A, Pandey AK, Pandey MK, Kumar A (2017) Metabolomics for plant improvement: status and prospects. Frontiers in Plant Science 8, 1302.
| Crossref | Google Scholar | PubMed |
Li H, Li C, Zhang C, Chen B, Hui L, Shen Y (2015) Compositional and gastrointestinal prokinetic studies of Pugionium (L.). Food Chemistry 186, 285-291.
| Crossref | Google Scholar | PubMed |
Lim E-K, Li Y, Parr A, et al. (2001) Identification of glucosyltransferase genes involved in sinapate metabolism and lignin synthesis in Arabidopsis. Journal of Biological Chemistry 276(6), 4344-4349.
| Crossref | Google Scholar | PubMed |
Liu C, Liu Y, Guo K, et al. (2011) Effect of drought on pigments, osmotic adjustment and antioxidant enzymes in six woody plant species in karst habitats of southwestern China. Environmental and Experimental Botany 71(2), 174-183.
| Crossref | Google Scholar |
Liu Y, Li P, Xu GC, Xiao L, Ren ZP, Li ZB (2017) Growth, morphological, and physiological responses to drought stress in Bothriochloa ischaemum. Frontiers in Plant Science 8, 230.
| Crossref | Google Scholar |
Luo D-D, Wang C-K, Ying J (2019) Stomatal regulation of plants in response to drought stress. Chinese Journal of Applied Ecology 30(12), 4333-4343.
| Crossref | Google Scholar | PubMed |
Ma F-J, Li D-D, Cai J, et al. (2012) Responses of wheat seedlings root growth and leaf photosynthesis to drought stress. Chinese Journal of Applied Ecology 23(3), 724-730.
| Google Scholar | PubMed |
Ma C, Xu J, Han L, Tian G, Huang F (2016) Advance in sinapic acid and its biological activities. China Oils and Fats 41(5), 75-79.
| Google Scholar |
Maeda H, Dudareva N (2012) The shikimate pathway and aromatic amino acid biosynthesis in plants. Annual Review of Plant Biology 63, 73-105.
| Crossref | Google Scholar | PubMed |
Moellering ER, Muthan B, Benning C (2010) Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330, 226-228.
| Crossref | Google Scholar | PubMed |
Morcol TB, Wysocki K, Sankaran RP, Matthews PD, Kennelly EJ (2020) UPLC-QTof-MSE metabolomics reveals changes in leaf primary and secondary metabolism of hop (Humulus lupulus L.) plants under drought stress. Journal of Agricultural and Food Chemistry 68(49), 14698-14708.
| Crossref | Google Scholar |
Men Y, Wang D, Li B, Su Y, Chen G (2018) Effects of drought stress on the antioxidant system, osmolytes and secondary metabolites of Saposhnikovia divaricata seedlings. Acta Physiologiae Plantarum 40(11), 191.
| Crossref | Google Scholar |
Okazaki Y, Saito K (2014) Roles of lipids as signaling molecules and mitigators during stress response in plants. The Plant Journal 79, 584-596.
| Crossref | Google Scholar | PubMed |
Patel MK, Kumar M, Li W, Luo Y, Burritt DJ, Alkan N, Tran L-SP (2020) Enhancing salt tolerance of plants: from metabolic reprogramming to exogenous chemical treatments and molecular approaches. Cells 9, 2492.
| Crossref | Google Scholar | PubMed |
Shi Y, Wu X, Tang Y, Mi J, Wan X (2020) Metabonomic analysis of Chenopodium quinoa under water stress at flowering stage. Journal of Henan Agricultural University 54(6), 921-930.
| Google Scholar |
Terazawa M, Okuyama H, Miyake M (1984) Isolation of coniferin and syringin from the cambial tissue and inner-bark of some angiospermous woods. Journal of the Japan Wood Research Society 30, 409-412.
| Google Scholar |
Thiel A, Muffler K, Tippkötter N, et al. (2015) A novel integrated downstream processing approach to recover sinapic acid, phytic acid and proteins from rapeseed meal. Journal of Chemical Technology and Biotechnology 90(11), 1999-2006.
| Crossref | Google Scholar |
Treml J, Šmejkal K (2016) Flavonoids as potent scavengers of hydroxyl radicals. Comprehensive Reviews in Food Science and Food Safety 15, 720-738.
| Crossref | Google Scholar | PubMed |
Tsuji Y, Fukushima K (2004) Behavior of monolignol glucosides in angiosperms. Journal of Agricultural and Food Chemistry 52(25), 7651-7659.
| Crossref | Google Scholar | PubMed |
Tzin V, Galili G (2010) The biosynthetic pathways for shikimate and aromatic amino acids in Arabidopsis thaliana. The Arabidopsis Book 8, e0132.
| Crossref | Google Scholar |
Wang H, Zhang HQ, Wu HY, Zhou K (2009) Study of anti-oxidation effects of Balanophora involucrate and trans-coniferin. Journal of China Three Gorges University (Natural Sciences) 31(3), 99-101.
| Google Scholar |
Wang Q, Abbott RJ, Yu Q-S, et al. (2013) Pleistocene climate change and the origin of two desert plant species, Pugionium cornutum and Pugionium dolabratum (Brassicaceae), in northwest China. New Phytologist 199(1), 277-287.
| Crossref | Google Scholar |
Wang Y, Hu S, Wang Y, Zhang J, Yang ZG, Liu Y, Zhu CX, Tian XY (2017a) Research advance in the Mongolian plateau endemic plant Pugionium cornutum (L.) Gaertn. Journal of Northern Agriculture 45(1), 111-117.
| Google Scholar |
Wang P, Zhang XL, Shi L (2017b) Changes of photosynthetic pharacteristics and chlorophyll fluorescence parameters of Pugionium cornutum (L.) Gaertn seedlings leaf under drought stress. Agricultural Research in the Arid Areas 35(3), 159-163.
| Google Scholar |
Wang X, Guo R, Li M, Liu Y, Zhao M, Fu H, Liu X, Wang S, Shi L (2019) Metabolomics reveals the drought-tolerance mechanism in wild soybean (Glycine soja). Acta Physiologiae Plantarum 41, 161.
| Crossref | Google Scholar |
Xu HY, Li XL (2020) A metabolomics analysis of the effect of water deficit on the freezing tolerance of alfalfa (Medicago sativa). Acta Prataculturae Sinica 2(91), 106-116.
| Google Scholar |
Yadav AK, Carroll AJ, Estavillo GM, et al. (2019) Wheat drought tolerance in the field is predicted by amino acid responses to glasshouse-imposed drought. Journal of Experimental Botany 70(18), 4931-4948.
| Crossref | Google Scholar | PubMed |
Yang L, Fountain JC, Ji P, Ni X, Chen S, Lee RD, Kemerait RC, Guo B (2018) Deciphering drought-induced metabolic responses and regulation in developing maize kernels. Plant Biotechnology Journal 16, 1616-1628.
| Crossref | Google Scholar | PubMed |
Yuan J-J, Sun X-C, Li J-P, Du T, Wang H-Z (2021) Metabolomics analysis of Codonopsis pilosula under drought stress based on LC-MS. Chinese Journal of Experimental Traditional Medical Formulae 27(24), 145-152.
| Google Scholar |
Zhang F, Chen W (2021) Research progress of metabolomics in plant stress biology. Biotechnology Bulletin 37(8), 1-11.
| Crossref | Google Scholar |
Zhang XL, Wang P, Shi L, Yang J (2016) Root morphology and antioxidant enzyme activity of Pugionium cornutum (L.) Gaertn under drought stress. Agricultural Research in the Arid Areas 34(3), 160-164.
| Crossref | Google Scholar |
Zhang FL, Jia LX, Yang ZR, Hao LZ, Huang XM, Zhang XY (2021) Optimization of extraction technology and GC-MS analysis of essential oil from Pugionium cornutum (L.) Gaertn. fruit. Food Research and Development 42(15), 40-46.
| Google Scholar |
Zhao C-X, Deng X-P, Shan L (2005) Changes in root hydraulic conductivity during wheat evolution. Journal of Integrative Plant Biology 47, 302-310.
| Crossref | Google Scholar |
Zheng QL, Yang ZR, Zhang FL, Zhang XY, Hao LZ (2018) Response of reactive oxygen species scavenging system to drought stress in Pugionium Gaertn. Acta Botanica Boreali-Occidentalia Sinica 38(9), 1674-1682.
| Google Scholar |
Zhou JR, Kong GZ (2011) Effects of drought and iron salt stress on fatty acid content in Pinus tabulaeformis Carr. seeds. Bulletin of Biology 46(12), 51-52.
| Google Scholar |