Abstract
Alternanthera sessilis is a plant popularly known for its medicinal properties. Although there are many studies regarding the pharmacological activity of this species, there is little knowledge at the molecular level of the mechanisms involved in the biosynthesis and regulation of its secondary metabolites, mainly betalains. These pigments have high potential for use in industry and are produced exclusively by plants of the order Caryophyllales, to which this species belongs. The objective of the present study was to evaluate the differential expression of genes by RNA sequencing and the concentration of betalain in plants exposed to methyl jasmonate (MeJa) elicitation for 48 h. A total of 51,390,246 and 43,194,240 clean reads were obtained for the control treatment and MeJA elicited plants, respectively. Alignment of 97,117 transcripts against the AA-NCBI-NR bank using the Diamond program resulted in a total of 25,601 alignments; thus, a gene ontology (GO) annotation was published for 22,520 transcripts. Analysis of differentially expressed genes resulted in a total of 398 downregulated and 692 upregulated genes. The variable databases MapMan and KEGG, which contain metabolites, were more affected by the potential upregulation of MeJa during betalain biosynthesis. In addition, the betalain concentration (amaranthin, betanidin, betaine, and miraxanthin) increased after being elicited. These data demonstrate molecular reprogramming in response to methyl jasmonate elicitation and provides molecular data that serve as a basis for future analyses, mainly regarding the potential of this plant to produce betalamic pigments.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated or analysed during this study are included in this published article.
Change history
30 November 2022
Communicated by update
References
Ahmad N, Rab A, Ahmad N (2016) Light-induced biochemical variations in secondary metabolite production and antioxidant activity in callus cultures of Stevia rebaudiana (Bert). J Photochem Photobiol, B 154:51–56. https://doi.org/10.1016/j.jphotobiol.2015.11.015
Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11(10):1–12. https://doi.org/10.1186/gb-2010-11-10-r106
Attaran E, Major IT, Cruz JA, Rosa BA, Koo AJK, Chen J, Kramer DM, He SY, Howe GA (2014) Temporal dynamics of growth and photosynthesis suppression in response to jasmonate signaling. Plant Physiol 165: 1302– 1314. https://doi.org/10.1104/pp.114.239004
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15): 2114-20. https://doi.org/10.1093/bioinformatics/btu170
Borah A, Yadav RNS, Unni BG (2011) In-vitro antioxidant and free radical scavenging activity of Alternanthera Sessilis. Int J Pharm Sci Res 2:1502–1506
Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12(1):59–60. https://doi.org/10.1038/nmeth.3176
Chen N, Yu Z-H, Xiao X-G (2017) Cytosolic and nuclear Co-localization of betalain biosynthetic enzymes in tobacco suggests that betalains are synthesized in the cytoplasm and/or nucleus of betalanic plant cells. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00831
Cheng R-B, Liu J-H, Xiao Y, Zhang F, Chen J, Ji Q, Zhang L (2015) Deep sequencing reveals the effect of MeJa on scutellarin biosynthesis in Erigeron breviscapus. PLoS ONE 10(12):e0143881. https://doi.org/10.1371/journal.pone.0143881
Cheng M, Huang Z, Hua Q, Shan W, Kuang J, Lu W, Yong-hua QCJ (2017) The WRKY transcription factor HpWRKY44 regulates CytP450-like1 expression in red pitaya fruit (Hylocereus polyrhizus). Hortic Res. https://doi.org/10.1038/hortres.2017.39
Clifford T, Howatson G, West DJ, Stevenson EJ (2015) The potential benefits of red beet root supplementation in health and disease. Nutrients 7:2801–2822. https://doi.org/10.3390/nu7042801
Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676. https://doi.org/10.1093/bioinformatics/bti610
DeGeyter N, Gholami A, Goormachtig S, Goossens A (2012) Transcriptional machineries in jasmonate-elicited plant secondary metabolism. Trends Plant Sci 17:349–359. https://doi.org/10.1016/j.tplants.2012.03.001
Do Amaral MN, Arge LWP, Benitez LC, Danielowski R, da Silveira SF, S, Farias D da R, Oliveira AC, Da Maia, LC, Braga EJB, (2016) Comparative transcriptomics of rice plants under cold, iron, and salt stresses. Funct Integr Genomics 16(5):567–579. https://doi.org/10.1007/s10142-016-0507-y
Fan L, Shi J, Zuo J, Gao L, Lv L, Wang Q (2016) Methyl jasmonate delays postharvest ripening and senescence in the non-climacteric eggplant (Solanum melongena L.) fruit. Postharvest Biol Technol 120:76–83. https://doi.org/10.1016/j.postharvbio.2016.05.010
Farag MA, Mekky H, El-Masry S (2016) Metabolomics driven analysis of Erythrina lysistemon cell suspension culture in response to methyl jasmonate elicitation. J Ad Res 7:681–689. https://doi.org/10.1016/j.jare.2016.07.002
Gandia-Herrero F, Escribano J, Garcia –Carmona F (2005) Betaxanthins as substrates for tyrosinase. an approach to the role of tyrosinase in the biosynthetic pathway of betalains. Plant Physiol 138:421–432
Gandía-Herrero F, García-Carmona F (2013) Biosynthesis of betalains: yellow and violet plant pigments. Trends Plant Sci 18(6):334–341. https://doi.org/10.1016/j.tplants.2013.01.003
Gandía-Herrero F, Escribano J, García-Carmona F (2016) Biological activities of plant pigments betalains. Crit Rev Food Sci Nutr 56:937–945. https://doi.org/10.1016/j.phytochem.2015.06.008
Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Regev A (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8(8):1494–1512. https://doi.org/10.1038/nprot.2013.084
Hoagland DR, Arnon DI (1938) The water-culture method for growing plants without soil. Calif Agric Exp 347:32
Howe GA, Major IT, Koo AJ (2018) Modularity in jasmonate signaling for multistress resilience. Annu Rev Plant Biol 69(1):387–415. https://doi.org/10.1146/annurev-arplant-042817-040047
Kanehisa M, Goto S (2000) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30. https://doi.org/10.1093/nar/28.1.27
Klein FSR, Reis A, Kleinowski AM, Einhardt AM, Deuner S, Amarante L, Peters JA, Braga EJB (2018) Biochemical activity of plants of the genus Alternanthera after UV-C radiation exposure. R Bras Bioci 16(2):37–46
Kopylova E, Noé L, Touzet H (2012) SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 28(24):3211–3217. https://doi.org/10.1093/bioinformatics/bts611
Kota S, Govada VR, Anantha RK, Verma MK (2017) An Investigation into phytochemical constituents, antioxidant, antibacterial and anti-cataract activity of Alternanthera sessilis, a predominant wild leafy vegetable of South India. Biocatal Agric Biotechnol 10:197–203. https://doi.org/10.1016/j.bcab.2017.03.008
Langmead B, Salzberg S (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9(4):357–359. https://doi.org/10.1038/nmeth.1923
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25(16):2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Lindemose S, O’Shea C, Jensen K, Skriver M (2013) Structure, function and networks of transcription factors involved in abiotic stress responses. Int J Mol Sci 14:5842–5878. https://doi.org/10.3390/ijms14035842
Liu J, Osbourn A, Ma P (2015) MYB transcription factors as regulators of phenylpropanoid metabolism in plants. Mol Plant 8:689–708. https://doi.org/10.1016/j.molp.2015.03.012
Livak LJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Lloyd A, Brockman A, Aguirre L, Campbell A, Bean A, Cantero A, Gonzalez A (2017) Advances in the MYB–bHLH–WD Repeat (MBW) Pigment regulatory model: addition of a WRKY factor and co-option of an anthocyanin MYB for betalain regulation. Plant Cell Physiol 58(9):1431–1441. https://doi.org/10.1093/pcp/pcx075
Lopez-Nieves S, Yang Y, Timoneda A, Wang M, Feng T, Smith SA, Brockington SF, Maeda HA (2018) Relaxation of tyrosine pathway regulation underlies the evolution of betalain pigmentation in Caryophyllales. New Phytol 217(2):896–908. https://doi.org/10.1111/nph.14822
Luo H, Zhu Y, Song J, Xu L, Sun C, Zhang X, Chen S (2014) Transcriptional data mining of in response to methyl jasmonate to examine the mechanism of bioactive compound biosynthesis and regulation. Physiol Plant 152(2):241–255. https://doi.org/10.1111/ppl.12193
Lv HJ, Li JJ, Wu YY, Garyali S, Wang Y (2016) Transporter and its engineering for secondary metabolites. Appl Microbiol Biotechnol 100:6119–6130. https://doi.org/10.1007/s00253-016-7605-6
Martinez RM, Longhi-Balbinot DT, Zarpelon AC, Staurengo-Ferrari L, Baracat MM, Georgetti SR (2015) Anti-inflammatory activity of betalain-richdye of Beta vulgaris: effect on edema, leukocyte recruitment, superoxide anion and cytokine production. Arch Pharm Res 38:494–504. https://doi.org/10.1007/s12272-014-0473-7
Matra DD, Kozaki T, Ishii K, Poerwanto R, Inoue E (2016) De novo transcriptome assembly of mangosteen (Garcinia mangostana L.) fruit. Genom 10:35–37. https://doi.org/10.1016/j.gdata.2016.09.003
Mehmood A, Tanveer A, Nadeem MA, Zahir ZA (2014) Comparative allelopathic potencial of metabolites of two Alternanthera species against germination and seedling growht of rice. Planta Daninha 32(1):1–10. https://doi.org/10.1590/S0100-83582014000100001
Miguel MG (2018) Betalains in some species of the Amaranthaceae family: a review. Antioxidants 7(4):53. https://doi.org/10.3390/antiox7040053
Misra RC, Maiti P, Chanotiya CS, Shanker K, Ghosh S (2014) Methyl jasmonate-elicited transcriptional responses and pentacyclic triterpene biosynthesis in Sweet basil. Plant Physiolgy 164:1028–1044. https://doi.org/10.1104/pp.113.232884
Moghe GD, Smith SD (2018) The push and pull of plant specialized metabolism underlies a long-tanding, colorful mystery. New Phytol 217:471–473. https://doi.org/10.1111/nph.14914
Moore BD, Andrew RL, Külheim C, Foley WJ (2014) Explaining intraspecific diversity in plant secondary metabolites in an ecological context. New Phytol 201(3):733–750. https://doi.org/10.1111/nph.12526
Murashige T, Skoog FA (1962) Revised medium for rapid growth and bioessays with tobacco tissue culture. Physiol Plant 15(5):473–497
Murthy HN, Lee E-J, Paek K-Y (2014) Production of secondary metabolites from cell and organ cultures: strategies and approaches for biomass improvement and metabolite accumulation. Plant Cell, Tiss Organ Cult 118(1):1–16. https://doi.org/10.1007/s11240-014-0467-7
Niraimathi KL, Sudha V, Lavanya R, Brindha P (2013) Biosynthesis of silver nanoparticles using Alternanthera sessilis (Linn.) extract and their antimicrobial, antioxidant activities. Colloids Surf, B 102:288–291. https://doi.org/10.1016/j.colsurfb.2012.08.041
O’Brien JA, Vega A, Bouguyon E, Krouk G, Gojon A, Coruzzi G, Gutierrez RA (2016) Nitrate transport, sensing, and responses in plants. Mol Plant 9:837–856. https://doi.org/10.1016/j.molp.2016.05.004
Othman A, Ismail A, Hassan FA, Yusof BKM, Khatib A (2016) Comparative evaluation of nutritional compositions, antioxidant capacities, and phenolic compounds of red and green sessile joyweed (Alternanthera sessilis). J Funct Foods 21:263–271. https://doi.org/10.1016/j.jff.2015.12.014
Pan J, Chen H, Guo B, Liu C (2017) Understanding the molecular mechanisms underlying the effects of light intensity on flavonoid production by RNA-seq analysis in Epimedium pseudowushanense B. L Guo Plos ONE 12(8):e0182348. https://doi.org/10.1371/journal.pone.0182348
Pavarinia DP, Pavarinib SP, Niehuesa M, Lopesa NP (2012) Exogenous influences on plant secondary metabolite levels. Anim Feed Sci Technol 176:5–16. https://doi.org/10.1016/j.anifeedsci.2012.07.002
Polturak G, Aharoni A (2018) ‘“La Vie en Rose”’: biosynthesis, sources, and applications of betalain pigments. Mol Plant 11:7–22. https://doi.org/10.1016/j.molp.2017.10.008
Pratelli R, Pilot G (2014) Regulation of aminoacid metabolic enzymes and transporters in plants. J Exp Bot 65:5535–5556. https://doi.org/10.1093/jxb/eru320
Qingzhu H, Chengjie C, Zhe C, Pengkun C, Yuewen M, Jingyu W, Jian Z, Guibing H, Jietang Z, Yonghua Q (2016) Transcriptomic analysis reveals key genes related to betalain biosynthesis in pulp coloration of Hylocereus polyrhizus. Front Plant Sci 6:1179. https://doi.org/10.3389/fpls.2015.01179
Rahimi P, Abedimanesh S, Namin SAM, Ostadrahimi A (2018) Betalains, the nature-inspired pigments, in health and diseases. Crit Rev Food Sci Nutr 30:1–30. https://doi.org/10.1080/10408398.2018.1479830
Rahnamaie-Tajadod R, Loke K-K, Goh H-H, Noor NM (2017) Differential gene expression analysis in Polygonum minus leaf upon 24 h for methyl Jasmonate elicitation. Front Plant Sci 8:109. https://doi.org/10.3389/fpls.2017.00109
Rodrigues-Brandão I, Kleinowski AM, Einhardt AM, Lima MC, Amarante L, Peters JA, Braga EJB (2014) Salicylic acid on antioxidant activity and betacyan in production from leaves of Alternanthera tenella. Ciência Rural 44(10):1893–1898. https://doi.org/10.1590/0103-8478cr20130873
Rojas CM, Senthil-Kumar M, Tzin V, Mysore K (2014) Regulation of primary plant metabolism during plant-pathogen interactions and its contribution to plant defense. Front Plant Sci 5:17. https://doi.org/10.3389/fpls.2014.00017
Salvesen GS, Hempel A, Coll NS (2015) Protease signaling in animal and plant-regulated cell death. FEBS J 283:2577–2598. https://doi.org/10.1111/febs.13616
Schenck CA, Maeda HA (2018) Tyrosine biosynthesis, metabolism, and catabolism in plants. Phytochemistry 149:82–102. https://doi.org/10.1016/j.phytochem.2018.02.003
Sigurdson GT, Tang P, Giusti MM (2017) Natural colorants: food colorants from natural sources. Annu Rev Food Sci Technol 8(1):261–280. https://doi.org/10.1146/annurev-food-030216-025923
Sullivan ML (2015) Beyond brown: polyphenol oxidases as enzymes of plant specialized metabolism. Front Plant Sci. https://doi.org/10.3389/fpls.2014.00783
Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Stitt M (2004) Mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37(6):914–939. https://doi.org/10.1111/j.1365-313x.2004.02016.x
Verma M, Ghangal R, Sharma R, Sinha AK, Jain M (2014) Transcriptome analysis of Catharanthus roseus for gene discovery and expression profiling. PLoS ONE 9(7):e103583. https://doi.org/10.1371/journal.pone.0103583
Walter TW, Merish S, Tamizhamuthu M (2014) Review of Alternanthera sessilis with reference to traditional siddha medicine. Int J Pharm Phytochem Res 6(2):249–254
Wang Y-N, Tang L, Hou Y, Wang P, Yang H, Wei C-L (2016) Differential transcriptome analysis of leaves of tea plant (Camellia sinensis) provides comprehensive insights into the defense responses to ectropis oblique attack using RNA-Seq. Funct Integr Genomics 16(4):383–398. https://doi.org/10.1007/s10142-016-0491-2
Wang R, Xu S, Wang N, Xia B, Jiang Y, Wang R (2017) Transcriptome analysis of secondary metabolism pathway, transcription factors, and transportes in response to Methyl Jasmonate in Lycoris aurea. Front Plant Sci 7:1971. https://doi.org/10.3389/fpls.2016.01971
Wasternack C, Strnad M (2016) Jasmonate signaling in plant stress responses and development – active and inactive compounds. New Biotechnol 33(5):604–613. https://doi.org/10.1016/j.nbt.2015.11.001
Waszczak C, Carmody M, Kangasjärvi J (2018) Reactive oxygen species in plant signaling. Annu Rev Plant Biol 69(1):209–236. https://doi.org/10.1146/annurev-arplant-042817-040322
Yamamoto K, Kobayashi N, Yoshitama K, Teramoto S, Komamine A (2001) Isolation and purification of tyrosinehydroxylase from callus cultures of Portulaca grandiflora. Plant Cell Physiol 42:969–975. https://doi.org/10.1093/pcp/pce125
Yan Y, Borrego E, Kolomiets VM (2013) Jasmonate biosynthesis, perception and function in plant development and stress responses. Lipid Metabolism 16:1–51. https://doi.org/10.5772/52675
Yanfang Y, Kaikai Z, Liying Y, Xing L, Ying W, Hongwei L, Deyou Q (2018) Identification and characterization of MYC transcription factors in Taxus sp. Gene 675:1–8. https://doi.org/10.1016/j.gene.2018.06.065
Zhang L, Lu X, Shen Q, Chen Y, Wang T, Zhang F, Tang K (2011) Identification of putative artemisia annua ABCG transporter unigenes related to artemisinin yield following expression analysis in different plant tissues and in response to methyl jasmonate and abscisic acid treatments. Plant Mol Biol Report 30(4):838–847. https://doi.org/10.1007/s11105-011-0400-8
Zhou X, Li J, Zhu Y, Ni S, Chen J, Feng X, Zhang Y, Li S, Zhu H, Wen Y (2017) De novo Assembly ofthe Camellia nitidissima transcriptome reveals key genes of flower pigment biosynthesis. Front Plant Sci 8:1545. https://doi.org/10.3389/fpls.2017.01545
Acknowledgements
The authors gratefully acknowledge the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for their financial support and researcher fellowship to EJBB, the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES) and the Research Foundation of Rio Grande do Sul (FAPERGS) for supporting the research.
Funding
This work was carried out under the auspices of the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brazil (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and the Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest in this work.
Additional information
Communicated by A. Królicka.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
11738_2022_3488_MOESM2_ESM.xlsx
Supplementary file2 (XLSX 243 KB) List of differentially expressed genes identified by RNA Seq (FDR < 0.01) in Alternanthera sessilis plants subjected by the action of methyl jasmonate after 48 hours
11738_2022_3488_MOESM3_ESM.xlsx
Supplementary file3 (XLSX 82 KB) List of metabolics pathways altered by the action of methyl jasmonate after 48 hours of elicitation in Alternanthera sessilis according to Kegg
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Milech, C., do Amaral, M.N., Auler, P.A. et al. Betalain accumulation and de novo transcriptome sequencing reveal the potential to increase bioactive compounds in Alternanthera sessilis elicited by methyl jasmonate. Acta Physiol Plant 45, 15 (2023). https://doi.org/10.1007/s11738-022-03488-2
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-022-03488-2