Comparative de novo transcriptomics and untargeted metabolomic analyses elucidate complicated mechanisms regulating celery (Apium graveolens L.) responses to selenium stimuli


Autoři: Chenghao Zhang aff001;  Baoyu Xu aff001;  Cheng-Ri Zhao aff002;  Junwei Sun aff003;  Qixian Lai aff004;  Chenliang Yu aff001
Působiště autorů: Institute of Agricultural Equipment, Zhejiang Academy of Agricultural Sciences, Hangzhou, China aff001;  Department of Horticulture & Landscape Architecture, Agricultural college of Yanbian University, Yanji, China aff002;  College of Modern Science and Technology, China Jiliang University, Hangzhou, China aff003;  Key Labortatory of Creative Agricultrue, Ministry of Agriculture, Zhejiang Academy of Agricultural Sciences, Hangzhou, China aff004
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226752

Souhrn

Presently, concern regarding the effects of selenium (Se) on the environment and organisms worldwide is increasing. Too much Se in the soil is harmful to plants. In this study, Illumina RNA sequencing and the untargeted metabolome of control and Se-treated celery seedlings were analyzed. In total, 297,911,046 clean reads were obtained and assembled into 150,218 transcripts (50,876 unigenes). A total of 36,287 unigenes were annotated using different databases. Additionally, 8,907 differentially expressed genes, including 5,319 up- and 3,588 downregulated genes, were identified between mock and Se-treated plants. “Phenylpropanoid biosynthesis” was the most enriched KEGG pathway. A total of 24 sulfur and selenocompound metabolic unigenes were differentially expressed. Furthermore, 1,774 metabolites and 237 significant differentially accumulated metabolites were identified using the untargeted metabolomic approach. We conducted correlation analyses of enriched KEGG pathways of differentially expressed genes and accumulated metabolites. Our findings suggested that candidate genes and metabolites involved in important biological pathways may regulate Se tolerance in celery. The results increase our understanding of the molecular mechanism responsible for celery’s adaptation to Se stress.

Klíčová slova:

Gene expression – Metabolic pathways – Metabolites – Metabolomics – Phosphates – Sequence databases – Transcriptome analysis – Xenobiotic metabolism


Zdroje

1. Terry N, de Souza MP, Am TAZ. Selenium in higher plants [Review]. Annu Rev Plant Phys.2000;51: 401–432.

2. Rayman MP, Thompson AJ, Bekaert B, Catterick J, Galassini R, Hall E, et al. Randomized controlled trial of the effect of selenium supplementation on thyroid function in the elderly in the United Kingdom. AmJ Clin Nutr.2008;87: 370–378.

3. Fordyce F.Selenium geochemistry and health. Ambio.2007;36: 94–97. doi: 10.1579/0044-7447(2007)36[94:sgah]2.0.co;2 17408199

4. Karasinski J, Wrobel K, Escobosa ARC, Konopka A, Bulska E, Wrobel K. Allium cepa L. response to Sodium Selenite (Se(IV)) studied in plant roots by a LC-MS-based proteomic approach. Journal of Agricultural and Food Chem.2017;65: 3995–4004.

5. Van Hoewyk D. A tale of two toxicities: malformed selenoproteins and oxidative stress both contribute to selenium stress in plants. Ann Bot 2013;112: 965–972. doi: 10.1093/aob/mct163 23904445

6. Duran P, Acuna JJ, Jorquera MA, Azcon R, Borie F, Cornejo P et al. Enhanced selenium content in wheat grain by co-inoculation of selenobacteria and arbuscular mycorrhizal fungi: A preliminary study as a potential Se biofortification strategy. J Cereal Sci.2013;57: 275–280.

7. Chen QX, Shi WM, Wang XC. Selenium speciation and distribution characteristics in the Rhizosphere soil of rice (Oryza sativa L.) seedlings. Commun Soil SciPlan 2010;41: 1411–1425.

8. Ramos SJ, Faquin V, Guilherme LRG, Castro EM, Avila FW, Carvalho GS, et al. Selenium biofortification and antioxidant activity in lettuce plants fed with selenate and selenite. Plant Soil Environ.2010;56: 584–588.

9. Shardendu, Salhani N, Boulyga SF, Stengel E. Phytoremediation of selenium by two helophyte species in subsurface flow constructed wetland. Chemosphere.2006;50: 967–973.

10. Fellowes JW, Pattrick RAD, Boothman C, Al Lawati WMM, van Dongen BE, Charnock JM, et al. Microbial selenium transformations in seleniferous soils. Eur J Soil Sci.2013;64: 629–638.

11. Pyrzynska K. Determination of selenium species in environmental samples. Microchim Acta. 2002;140: 55–62.

12. Banuelos GS, Lin ZQ. Phytoremediation management of selenium-laden drainage sediments in the San Luis Drain: a greenhouse feasibility study. Ecotox Environ Safe.2005;62: 309–316.

13. Zhao CY, Ren JG, Xue CZ, Lin ED. Study on the relationship between soil selenium and plant selenium uptake. Plant Soil.2005;277: 197–206.

14. White PJ. Selenium accumulation by plants. Ann Bot.2016;117: 217–235. doi: 10.1093/aob/mcv180 26718221

15. Sors TG, Ellis DR, Na GN, Lahner B, Lee S, Leustek T, et al. Analysis of sulfur and selenium assimilation in Astragalus plants with varying capacities to accumulate selenium. Plant J.2005;42: 785–797. doi: 10.1111/j.1365-313X.2005.02413.x 15941393

16. Shibagaki N, Rose A, McDermott JP, Fujiwara T, Hayashi H, Yoneyama T, et al. Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulfate transporter required for efficient transport of sulfate into roots. Plant J.2002;29: 475–486. doi: 10.1046/j.0960-7412.2001.01232.x 11846880

17. Hopkins L, Parmar S, Bouranis DL, Howarth JR, Hawkesford MJ. Coordinated expression of sulfate uptake and components of the sulfate assimilatory pathway in maize. Plant Biology.2004;6: 408–414. doi: 10.1055/s-2004-820872 15248123

18. Cabannes E, Buchner P, Broadley MR, Hawkesford MJ. A Comparison of sulfate and selenium accumulation in relation to the expression of sulfate transporter genes in Astragalus Species. Plant Physiol.2011;157: 2227–2239. doi: 10.1104/pp.111.183897 21972267

19. Zhao XQ, Mitani N, Yamaji N, Shen RF, Ma JF. Involvement of silicon influx transporter OsNIP2;1 in selenite uptake in rice. Plant Physiol.2010;153: 1871–1877. doi: 10.1104/pp.110.157867 20498338

20. Zhang LH, Hu B, Li W, Che RH, Deng K, Li H, et al. OsPT2, a phosphate transporter, is involved in the active uptake of selenite in rice. New Phytol.2014;201: 1183–1191. doi: 10.1111/nph.12596 24491113

21. Song ZP, Shao HF, Huang HG, Shen Y, Wang LZ, Wu FY, et al. Overexpression of the phosphate transporter gene OsPT8 improves the Pi and selenium contents in Nicotiana tabacum. Environ ExpBot.2017;137: 158–165.

22. Hartikainen H, Xue TL, Piironen V. Selenium as an anti-oxidant and pro-oxidant in ryegrass. Plant and Soil.2000; 225: 193–200.

23. Fernandes J, Hu X, Smith MR, Go YM, Jones DP. Selenium at the redox interface of the genome, metabolome and exposome. Free Radical BioMed.2018;127: 215–227.

24. Strickler SR, Bombarely A, Mueller LA. Designing a transcriptome next-generation sequencing project for a nonmodel plant species. Am J Bot.2012;99: 257–266. doi: 10.3732/ajb.1100292 22268224

25. Dianat M, Veisi A, Ahangarpour A, Fathi MH. The effect of hydro-alcoholic celery (Apiumgraveolens) leaf extract on cardiovascular parameters and lipid profile in animal model of hypertension induced by fructose. Avicenna Journal of Phytomedicine. 2015;5: 203. 26101753

26. Li MY, Hou XL, Wang F, Tan GF, Xu ZS, Xiong AS. Advances in the research of celery, an important Apiaceae vegetable crop. Crit Rev Biotechnol. 2018;38: 172–183. doi: 10.1080/07388551.2017.1312275 28423952

27. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnology.2011;29: 644–U130.

28. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol.2014;15.

29. Young MD, Wakefield MJ, Smyth GK, Oshlack A. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Bio.2010;11.

30. Mao XZ, Cai T, Olyarchuk JG, Wei LP. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics.2005;21: 3787–3793. doi: 10.1093/bioinformatics/bti430 15817693

31. Gauri M, Ali SJ, Khan MS. A Review of Apium graveolens (Karafs) with special reference to Unani Medicine. International Archives of Integreated Medicine.2015;2:131–136.

32. Feng K, Hou XL, Li MY, Jiang Q, Xu ZS,Liu JX et al. CeleryDB: a genomic database for celery. Database (Oxford) 2018.

33. Huang W, Ma HY, Huang Y, Li Y, Wang GL, Jiang Q, et al. Comparative proteomic analysis provides novel insights into chlorophyll biosynthesis in celery under temperature stress. Physiol Plant.2017;161: 468–485. doi: 10.1111/ppl.12609 28767140

34. Jia XL, Wang GL, Xiong F, Yu XR, Xu ZS, Wang F, et al. De novo assembly, transcriptome characterization, lignin accumulation, and anatomic characteristics: novel insights into lignin biosynthesis during celery leaf development. Sci Rep.2015;5: 8259. doi: 10.1038/srep08259 25651889

35. Li MY, Wang F, Jiang Q, Ma J, Xiong AS. Identification of SSRs and differentially expressed genes in two cultivars of celery (Apium graveolens L.) by deep transcriptome sequencing. Hortic Res. 2014;1: 10. doi: 10.1038/hortres.2014.10 26504532

36. Cao D, Liu YL, Ma LL, Jin XF, Guo GY, Tan RR, et al. Transcriptome analysis of differentially expressed genes involved in selenium accumulation in tea plant (Camellia sinensis). PloS One.2018; 13: e0197506 doi: 10.1371/journal.pone.0197506 29856771

37. Tian M, Xu X, Liu F, Fan X, Pan S. Untargeted metabolomics reveals predominant alterations in primary metabolites of broccoli sprouts in response to pre-harvest selenium treatment. Food Res Int.2018; 111: 205–211. doi: 10.1016/j.foodres.2018.04.020 30007678

38. Fiehn O Metabolomics—the link between genotypes and phenotypes. Plant Mol Biol.2002;48: 155–171. 11860207

39. Lee YS, Park HS, Lee DK, Jayakodi M, Kim NH, Lee SC, et al. Comparative analysis of the transcriptomes and primary metabolite profiles of adventitious roots of five Panax ginseng cultivars. J Ginseng Res.2017;41: 60–68. doi: 10.1016/j.jgr.2015.12.012 28123323

40. Cakir O, Candar-Cakir B, Zhang BH. Small RNA and degradome sequencing reveals important microRNA function in Astragalus chrysochlorus response to selenium stimuli. Plant Biotechnol J.2016;14: 543–556. doi: 10.1111/pbi.12397 25998129

41. Cakir O, Turgut-Kara N, Ari S, Zhang B. De novo transcriptome assembly and comparative analysis elucidate complicated mechanism regulating Astragalus chrysochlorus response to selenium stimuli. PloS One. 2015;10.

42. Pilon-Smits EAH Selenium in plants. In: Lüttge U, Beyschlag W, editors. Progress in Botany: 2015; Vol 76. Cham: Springer International Publishing. pp. 93–107.

43. Hatzfeld Y, Lee S, Lee M, Leustek T, Saito K. Functional characterization of a gene encoding a fourth ATP sulfurylase isoform from Arabidopsis thaliana. Gene.2000;248: 51–58. doi: 10.1016/s0378-1119(00)00132-3 10806350

44. Koprivova A, Kopriva S. Hormonal control of sulfate uptake and assimilation. Plant Mol Biol.2016;91: 617–627. doi: 10.1007/s11103-016-0438-y 26810064

45. Shen C, Yang Y, Liu K, Zhang L, Guo H, Sun T. et al. Involvement of endogenous salicylic acid in iron-deficiency responses in Arabidopsis. J Exp Bot.2016;67: 4179–4193. doi: 10.1093/jxb/erw196 27208542

46. Zhan YH, Zhang CH, Zheng QX, Huang ZA, Yu CL. Cadmium stress inhibits the growth of primary roots by interfering auxin homeostasis in Sorghum bicolor seedlings. J Plant Biol.2017;60: 593–603.

47. Shen C, Yue R, Yang Y, Zhang L, Sun T, Tie S, et al. OsARF16 is involved in cytokinin-mediated inhibition of phosphate transport and phosphate signaling in rice (Oryza sativa L.). PLoS One.2014;9: e112906. doi: 10.1371/journal.pone.0112906 25386911

48. Xu Y, Zhang S, Guo H, Wang S, Xu L, Li C, et al. OsABCB14 functions in auxin transport and iron homeostasis in rice (Oryza sativa L.). Plant J.2014;79: 106–117. doi: 10.1111/tpj.12544 24798203

49. Van Hoewyk D, Takahashi H, Inoue E, Hess A, Tamaoki M, Pilon-Smits EAH. Transcriptome analyses give insights into selenium-stress responses and selenium tolerance mechanisms in Arabidopsis. Physiologia Plantarum.2008;132: 236–253. doi: 10.1111/j.1399-3054.2007.01002.x 18251864

50. Dong X. SA, JA, ethylene, and disease resistance in plants. Curr Opin Plant Biol.1998;1: 316–323. doi: 10.1016/1369-5266(88)80053-0 10066607

51. Bianga J, Govasmark E, Szpunar J. Characterization of selenium incorporation into wheat proteins by two-dimensional gel electrophoresis-laser ablation ICP MS followed by capillary HPLC-ICP MS and electrospray linear trap quadrupole orbitrap MS. Anal Chem.2013;85: 2037–2043. doi: 10.1021/ac3033799 23330978

52. Arnaudguilhem C, Bierla K, Ouerdane L, Preud’Homme H, Yiannikouris A, Lobinski R. Selenium metabolomics in yeast using complementary reversed-phase/hydrophilic ion interaction (HILIC) liquid chromatography–electrospray hybrid quadrupole trap/Orbitrap mass spectrometry. Analytica Chimica Acta.2012;757: 26–38. doi: 10.1016/j.aca.2012.10.029 23206393

53. Bierla K, Szpunar J, Yiannikouris A, Lobinski R. Comprehensive speciation of selenium in selenium-rich yeast. Trac-Trends Anal Chem.2012;41: 122–132.

54. Bierla K, Bianga J, Ouerdane L, Szpunar J, Yiannikouris A, Lobinski R. (2013) A comparative study of the Se/S substitution in methionine and cysteine in Se-enriched yeast using an inductively coupled plasma mass spectrometry (ICP MS)-assisted proteomics approach. J. Proteomics.2013;87: 26–39. doi: 10.1016/j.jprot.2013.05.010 23702330

55. Korkina LG. Phenylpropanoids as naturally occurring antioxidants: From plant defense to human health. Cell Mol Biol.2007;53: 15–25.

56. Castelluccio C, Paganga G, Melikian N, Bolwell GP, Pridham J, Sampson J. Antioxidant Potential Of Intermediates In Phenylpropanoid Metabolism In Higher-Plants. FEBS Letters.1995;368: 188–192. doi: 10.1016/0014-5793(95)00639-q 7615079

57. Agati G, Azzarello E, Pollastri S, Tattini M. Flavonoids as antioxidants in plants: Location and functional significance. Plant Sci.2012;196: 67–76. doi: 10.1016/j.plantsci.2012.07.014 23017900


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