Integrated Analysis of microRNA and RNA-Seq Reveals Phenolic Acid Secretion Metabolism in Continuous Cropping of Polygonatum odoratum
Abstract
:1. Introduction
2. Results
2.1. Rhizosphere Soil Phenolic Acids Contents during the Replanting of P. odoratum
2.2. Analysis of DEGs Related to Phenolic Acid Metabolism
2.3. Differential Expression Profiles of miRNAs and Functional Analysis during the Replanting of P. odoratum
2.4. Identification of the Key miRNA-mRNA Pairs Related to Phenolic Acid Synthesis during the Replanting of P. odoratum
2.5. Regulatory Network of Phenolic Acid Biosynthesis
2.6. Quantitative PCR (qPCR) Validation of the Key mRNA and miRNA Related to Phenolic Acid Synthesis
3. Discussion
4. Materials and Methods
4.1. Plant Materials
4.2. Quantification Analysis of Phenolic Acid from Rhizosphere Soil
4.3. RNA Isolation, Quantification, and Qualification
4.4. RNA-Sequencing Analysis
4.5. Bioinformatics Analysis of Small RNA Sequences
4.6. Quantitative Real-Time PCR Validation
4.7. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Wang, Y.; Fei, Y.; Liu, L.; Xiao, Y.; Pang, Y.; Kang, J.; Wang, Z. Polygonatum odoratum polysaccharides modulate gut microbiota and mitigate experimentally induced obesity in rats. Int. J. Mol. Sci. 2018, 19, 3587. [Google Scholar] [CrossRef] [Green Version]
- Chen, Y.; Yin, L.; Zhang, X.; Wang, Y.; Chen, Q.; Jin, C.; Hu, Y.; Wang, J. Optimization of alkaline extraction and bioactivities of polysaccharides from rhizome of Polygonatum odoratum. Biomed. Res. Int. 2014, 2014, 504896. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ye, X.; Pi, X.; Zheng, W.; Cen, Y.; Ni, J.; Xu, L.; Wu, K.; Liu, W.; Li, L. The methanol extract of Polygonatum odoratum ameliorates colitis by improving intestinal short-chain fatty acids and gas production to regulate microbiota dysbiosis in mice. Front. Nutr. 2022, 9, 899421. [Google Scholar] [CrossRef] [PubMed]
- Wu, H.; Wu, L.; Wang, J.; Zhu, Q.; Lin, S.; Xu, J.; Zheng, C.; Chen, J.; Qin, X.; Fang, C.; et al. Mixed phenolic acids mediated proliferation of pathogens talaromyces helicus and kosakonia sacchari in continuously monocultured radix pseudostellariae rhizosphere soil. Front. Microbiol. 2016, 7, 335. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, Z.; Fu, J.; Zhou, R.; Wang, D. Effects of phenolic acids from ginseng rhizosphere on soil fungi structure, richness and diversity in consecutive monoculturing of ginseng. Saudi. J. Biol. Sci. 2018, 25, 1788–1794. [Google Scholar] [CrossRef]
- Wu, L.; Wang, J.; Huang, W.; Wu, H.; Chen, J.; Yang, Y.; Zhang, Z.; Lin, W. Plant-microbe rhizosphere interactions mediated by Rehmannia glutinosa root exudates under consecutive monoculture. Sci. Rep. 2015, 5, 15871. [Google Scholar] [CrossRef] [Green Version]
- Wu, H.; Xu, J.; Wang, J.; Qin, X.; Wu, L.; Li, Z.; Lin, S.; Lin, W.; Zhu, Q.; Khan, M.U.; et al. Insights into the mechanism of proliferation on the special microbes mediated by phenolic acids in the radix pseudostellariae rhizosphere under continuous monoculture regimes. Front. Plant Sci. 2017, 8, 659. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tan, Y.; Cui, Y.; Li, H.; Kuang, A.; Li, X.; Wei, Y.; Ji, X. Rhizospheric soil and root endogenous fungal diversity and composition in response to continuous Panax notoginseng cropping practices. Microbiol. Res. 2017, 194, 10–19. [Google Scholar] [CrossRef]
- Cui, J.; Zhang, E.; Zhang, X.; Wang, Q.; Liu, Q. Effects of 2,4-di-tert-butylphenol at different concentrations on soil functionality and microbial community structure in the Lanzhou lily rhizosphere. Appl. Soil Ecol. 2022, 172, 104367. [Google Scholar] [CrossRef]
- Wolińska, A.; Kruczyńska, A.; Podlewski, J.; Słomczewski, A.; Grządziel, J.; Gałązka, A.; Kuźniar, A. Does the use of an intercropping mixture really improve the biology of monocultural soils?—A search for bacterial indicators of sensitivity and resistance to long-term maize monoculture. Agronomy 2022, 12, 613. [Google Scholar] [CrossRef]
- Rugova, A.; Puschenreiter, M.; Koellensperger, G.; Hann, S. Elucidating rhizosphere processes by mass spectrometry—A review. Anal Chim Acta 2017, 956, 1–13. [Google Scholar] [CrossRef] [PubMed]
- Vergani, L.; Mapelli, F.; Zanardini, E.; Terzaghi, E.; Di Guardo, A.; Morosini, C.; Raspa, G.; Borin, S. Phyto-rhizoremediation of polychlorinated biphenyl contaminated soils: An outlook on plant-microbe beneficial interactions. Sci. Total Environ. 2017, 575, 1395–1406. [Google Scholar] [CrossRef] [PubMed]
- Ni, X.; Jin, C.; Liu, A.; Chen, Y.; Hu, Y. Physiological and transcriptomic analyses to reveal underlying phenolic acid action in consecutive monoculture problem of Polygonatum odoratum. BMC Plant Biol. 2021, 21, 362. [Google Scholar] [CrossRef]
- Lin, W.; Li, Y.; Lu, Q.; Lu, H.; Li, J. Combined analysis of the metabolome and transcriptome identified candidate genes involved in phenolic acid biosynthesis in the leaves of cyclocarya paliurus. Int. J. Mol. Sci. 2020, 21, 1337. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Weiß, S.; Winkelmann, T. Transcriptome profiling in leaves representing aboveground parts of apple replant disease affected Malus domestica ‘M26’ plants. Sci. Hortic. 2017, 222, 111–125. [Google Scholar] [CrossRef]
- Chen, Y.; Liu, Z.; Tu, N.; Hu, Y.; Jin, C.; Luo, Y.; Liu, A.; Zhang, X. Integrated transcriptome and microRNA profiles analysis reveals molecular mechanisms underlying the consecutive monoculture problem of Polygonatum odoratum. Cell. Mol. Biol. 2020, 66, 47–52. [Google Scholar] [CrossRef]
- Li, Z.F.; Yang, Y.Q.; Xie, D.F.; Zhu, L.F.; Zhang, Z.G.; Lin, W.X. Identification of autotoxic compounds in fibrous roots of Rehmannia (Rehmannia glutinosa Libosch.). PLoS ONE 2012, 7, e28806. [Google Scholar] [CrossRef]
- Li, Z.H.; Wang, Q.; Ruan, X.; Pan, C.D.; Jiang, D.A. Phenolics and plant allelopathy. Molecules 2010, 15, 8933–8952. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lakhotia, N.; Joshi, G.; Bhardwaj, A.R.; Katiyar-Agarwal, S.; Agarwal, M.; Jagannath, A.; Goel, S.; Kumar, A. Identification and characterization of miRNAome in root, stem, leaf and tuber developmental stages of potato (Solanum tuberosum L.) by high-throughput sequencing. BMC Plant Biol. 2014, 14, 6. [Google Scholar] [CrossRef] [Green Version]
- Yang, M.; Lu, H.; Xue, F.; Ma, L. Identifying high confidence microRNAs in the developing seeds of jatropha curcas. Sci. Rep. 2019, 9, 4510. [Google Scholar] [CrossRef] [Green Version]
- Zhang, H.; Jin, W.; Zhu, X.; Liu, L.; He, Z.; Yang, S.; Liang, Z.; Yan, X.; He, Y.; Liu, Y. Identification and characterization of salvia miltiorrhizain miRNAs in response to replanting disease. PLoS ONE. 2016, 11, e0159905. [Google Scholar] [CrossRef] [Green Version]
- Yang, Y.H.; Li, M.J.; Yi, Y.J.; Li, R.F.; Li, C.X.; Yang, H.; Wang, J.; Zhou, J.X.; Shang, S.; Zhang, Z.Y. Integrated miRNA-mRNA analysis reveals the roles of miRNAs in the replanting benefit of Achyranthes bidentata roots. Sci. Rep. 2021, 11, 1628. [Google Scholar] [CrossRef]
- Zhang, X.; Liu, Y.; Fang, Z.; Li, Z.; Yang, L.; Zhuang, M.; Zhang, Y.; Lv, H. Comparative transcriptome analysis between broccoli (Brassica oleracea var. italica) and Wild Cabbage (Brassica macrocarpa Guss.) in response to plasmodiophora brassicae during different infection stages. Front. Plant Sci. 2016, 7, 1929. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tohge, T.; Watanabe, M.; Hoefgen, R.; Fernie, A.R. Shikimate and phenylalanine biosynthesis in the green lineage. Front. Plant Sci. 2013, 4, 62. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, M.; Li, J.; Zhang, R.; Lin, Y.; Xiong, A.; Tan, G.; Luo, Y.; Zhang, Y.; Chen, Q.; Wang, Y.; et al. Combined analysis of the metabolome and transcriptome to explore heat stress responses and adaptation mechanisms in Celery (Apium graveolens L.). Int. J. Mol. Sci. 2022, 23, 3367. [Google Scholar] [CrossRef] [PubMed]
- Liang, X.; Chen, X.; Li, C.; Fan, J.; Guo, Z. Metabolic and transcriptional alternations for defense by interfering OsWRKY62 and OsWRKY76 transcriptions in rice. Sci. Rep. 2017, 7, 2474. [Google Scholar] [CrossRef] [Green Version]
- Huang, L.F.; Song, L.X.; Xia, X.J.; Mao, W.H.; Shi, K.; Zhou, Y.H.; Yu, J.Q. Plant-soil feedbacks and soil sickness: From mechanisms to application in agriculture. J. Chem. Ecol. 2013, 39, 232–242. [Google Scholar] [CrossRef]
- Tian, Y.; Feng, F.; Zhang, B.; Li, M.; Wang, F.; Gu, L.; Chen, A.; Li, Z.; Shan, W.; Wang, X.; et al. Transcriptome analysis reveals metabolic alteration due to consecutive monoculture and abiotic stress stimuli in Rehamannia glutinosa Libosch. Plant Cell Rep. 2017, 36, 859–875. [Google Scholar] [CrossRef]
- Bai, Y.; Wang, G.; Cheng, Y.; Shi, P.; Yang, C.; Yang, H.; Xu, Z. Soil acidification in continuously cropped tobacco alters bacterial community structure and diversity via the accumulation of phenolic acids. Sci. Rep. 2019, 9, 12499. [Google Scholar] [CrossRef] [Green Version]
- Cecchi, A.M.; Koskinen, W.C.; Cheng, H.H.; Haider, K. Sorption?desorption of phenolic acids as affected by soil properties. Biol. Fertil. Soils 2004, 39, 235–242. [Google Scholar] [CrossRef]
- Li, X.; Lewis, E.E.; Liu, Q.; Li, H.; Bai, C.; Wang, Y. Effects of long-term continuous cropping on soil nematode community and soil condition associated with replant problem in strawberry habitat. Sci. Rep. 2016, 6, 30466. [Google Scholar] [CrossRef] [Green Version]
- Kitazawa, H.; Asao, T.; Ban, T.; Pramanik, M.H.R.; Hosoki, T. Autotoxicity of root exudates from strawberry in hydroponic culture. J. Hortic. Sci. Biotechnol. 2005, 80, 677–680. [Google Scholar] [CrossRef]
- Cheynier, V.; Comte, G.; Davies, K.M.; Lattanzio, V.; Martens, S. Plant phenolics: Recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiol. Biochem. 2013, 72, 1–20. [Google Scholar] [CrossRef]
- Xing, B.; Yang, D.; Guo, W.; Liang, Z.; Yan, X.; Zhu, Y.; Liu, Y. Ag+ as a more effective elicitor for production of tanshinones than phenolic acids in Salvia miltiorrhiza hairy roots. Molecules 2014, 20, 309–324. [Google Scholar] [CrossRef] [Green Version]
- Pickl, A.; Schonheit, P. The oxidative pentose phosphate pathway in the haloarchaeon Haloferax volcanii involves a novel type of glucose-6-phosphate dehydrogenase--The archaeal Zwischenferment. FEBS Lett. 2015, 589, 1105–1111. [Google Scholar] [CrossRef] [Green Version]
- Roy, D.; Ward, P. Comparison of fructose-1,6-bisphosphatase gene (fbp) sequences for the identification of Lactobacillus rhamnosus. Curr. Microbiol. 2004, 49, 313–320. [Google Scholar] [CrossRef]
- Leung, P.S.; Preiss, J. Biosynthesis of bacterial glycogen: Primary structure of Salmonella typhimurium ADPglucose synthetase as deduced from the nucleotide sequence of the glgC gene. J. Bacteriol. 1987, 169, 4355–4360. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yoshida, K.; Komae, K. A rice family 9 glycoside hydrolase isozyme with broad substrate specificity for hemicelluloses in type II cell walls. Plant Cell Physiol. 2006, 47, 1541–1554. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ding, D.; Liu, Y.; Xu, Y.; Zheng, P.; Li, H.; Zhang, D.; Sun, J. Improving the production of L-Phenylalanine by identifying Key enzymes through multi-enzyme reaction system in vitro. Sci. Rep. 2016, 6, 32208. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ma, D.; Li, Y.; Zhang, J.; Wang, C.; Qin, H.; Ding, H.; Xie, Y.; Guo, T. Accumulation of phenolic compounds and expression profiles of phenolic acid biosynthesis-related genes in developing grains of white, purple, and red wheat. Front. Plant Sci. 2016, 7, 528. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dong, F.S.; Lv, M.Y.; Wang, J.P.; Shi, X.P.; Liang, X.X.; Liu, Y.W.; Yang, F.; Zhao, H.; Chai, J.F.; Zhou, S. Transcriptome analysis of activated charcoal-induced growth promotion of wheat seedlings in tissue culture. BMC Genet. 2020, 21, 69. [Google Scholar] [CrossRef] [PubMed]
- Muriira, N.G.; Xu, W.; Muchugi, A.; Xu, J.; Liu, A. De novo sequencing and assembly analysis of transcriptome in the Sodom apple (Calotropis gigantea). BMC Genom. 2015, 16, 723. [Google Scholar] [CrossRef] [Green Version]
- Shinoyama, H.; Ichikawa, H.; Nishizawa-Yokoi, A.; Skaptsov, M.; Toki, S. Simultaneous TALEN-mediated knockout of chrysanthemum DMC1 genes confers male and female sterility. Sci. Rep. 2020, 10, 16165. [Google Scholar] [CrossRef]
- Denno, M.E.; Privman, E.; Venton, B.J. Analysis of neurotransmitter tissue content of drosophila melanogaster in different life stages. ACS Chem. Neurosci. 2015, 6, 117–123. [Google Scholar] [CrossRef] [Green Version]
- Chin, L.; Calabro, A.; Rodriguez, E.R.; Tan, C.D.; Walker, E.; Derwin, K.A. Characterization of and host response to tyramine substituted-hyaluronan enriched fascia extracellular matrix. J. Mater. Sci. Mater. Med. 2011, 22, 1465–1477. [Google Scholar] [CrossRef] [Green Version]
- Park, H.L.; Lee, S.W.; Jung, K.H.; Hahn, T.R.; Cho, M.H. Transcriptomic analysis of UV-treated rice leaves reveals UV-induced phytoalexin biosynthetic pathways and their regulatory networks in rice. Phytochemistry 2013, 96, 57–71. [Google Scholar] [CrossRef]
- Wang, J.X.; Gao, J.; Ding, S.L.; Wang, K.; Jiao, J.Q.; Wang, Y.; Sun, T.; Zhou, L.Y.; Long, B.; Zhang, X.J.; et al. Oxidative modification of miR-184 enables It to target Bcl-xL and Bcl-w. Mol. Cell 2015, 59, 50–61. [Google Scholar] [CrossRef] [Green Version]
- Portnoy, V.; Lin, S.H.; Li, K.H.; Burlingame, A.; Hu, Z.H.; Li, H.; Li, L.C. saRNA-guided Ago2 targets the RITA complex to promoters to stimulate transcription. Cell Res. 2016, 26, 320–335. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xiao, M.; Li, J.; Li, W.; Wang, Y.; Wu, F.; Xi, Y.; Zhang, L.; Ding, C.; Luo, H.; Li, Y.; et al. MicroRNAs activate gene transcription epigenetically as an enhancer trigger. RNA Biol. 2017, 14, 1326–1334. [Google Scholar] [CrossRef] [Green Version]
- Prabakaran, M.; Chung, I.M.; Son, N.Y.; Chi, H.Y.; Kim, S.Y.; Yang, Y.J.; Kwon, C.; An, Y.J.; Ahmad, A.; Kim, S.H. Analysis of selected phenolic compounds in organic, pesticide-Free, conventional rice (Oryza sativa L.) using LC-ESI-MS/MS. Molecules 2018, 24, 67. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Haas, B.J.; Papanicolaou, A.; Yassour, M.; Grabherr, M.; Blood, P.D.; Bowden, J.; Couger, M.B.; Eccles, D.; Li, B.; Lieber, M.; et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 2013, 8, 1494–1512. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.; Duan, Y.; Hu, Y.; Li, W.; Sun, D.; Hu, H.; Xie, J. Transcriptome analysis of atemoya pericarp elucidates the role of polysaccharide metabolism in fruit ripening and cracking after harvest. BMC Plant Biol. 2019, 19, 219. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mao, X.; Cai, T.; Olyarchuk, J.G.; Wei, L. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 2005, 21, 3787–3793. [Google Scholar] [CrossRef] [PubMed]
- Zheng, J.; Yang, J.; Yang, X.; Cao, Z.; Cai, S.; Wang, B.; Ye, J.; Fu, M.; Zhang, W.; Rao, S.; et al. Transcriptome and miRNA sequencing analyses reveal the regulatory mechanism of alpha-linolenic acid biosynthesis in Paeonia rockii. Food Res. Int. 2022, 155, 111094. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Hu, X.; Chen, J.; Wang, W.; Xiong, X.; He, C. Integrated mRNA and microRNA transcriptome analysis reveals miRNA regulation in response to PVA in potato. Sci. Rep. 2017, 7, 16925. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wen, M.; Shen, Y.; Shi, S.; Tang, T. miREvo: An integrative microRNA evolutionary analysis platform for next-generation sequencing experiments. BMC Bioinform. 2012, 13, 140. [Google Scholar] [CrossRef] [Green Version]
- Zhou, L.; Chen, J.; Li, Z.; Li, X.; Hu, X.; Huang, Y.; Zhao, X.; Liang, C.; Wang, Y.; Sun, L.; et al. Integrated profiling of microRNAs and mRNAs: microRNAs located on Xq27.3 associate with clear cell renal cell carcinoma. PLoS ONE 2010, 5, e15224. [Google Scholar] [CrossRef] [PubMed]
- Love, M.I.; Huber, W.; Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014, 15, 550. [Google Scholar] [CrossRef] [Green Version]
- Dai, X.; Zhuang, Z.; Zhao, P.X. psRNATarget: A plant small RNA target analysis server (2017 release). Nucleic Acids Res. 2018, 46, W49–W54. [Google Scholar] [CrossRef] [Green Version]
- Young, M.D.; Wakefield, M.J.; Smyth, G.K.; Oshlack, A. Gene ontology analysis for RNA-seq: Accounting for selection bias. Genome Biol. 2010, 11, R14. [Google Scholar] [CrossRef] [Green Version]
- Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25, 402–408. [Google Scholar] [CrossRef] [PubMed]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Wang, Y.; Liu, K.; Zhou, Y.; Chen, Y.; Jin, C.; Hu, Y. Integrated Analysis of microRNA and RNA-Seq Reveals Phenolic Acid Secretion Metabolism in Continuous Cropping of Polygonatum odoratum. Plants 2023, 12, 943. https://doi.org/10.3390/plants12040943
Wang Y, Liu K, Zhou Y, Chen Y, Jin C, Hu Y. Integrated Analysis of microRNA and RNA-Seq Reveals Phenolic Acid Secretion Metabolism in Continuous Cropping of Polygonatum odoratum. Plants. 2023; 12(4):943. https://doi.org/10.3390/plants12040943
Chicago/Turabian StyleWang, Yan, Kaitai Liu, Yunyun Zhou, Yong Chen, Chenzhong Jin, and Yihong Hu. 2023. "Integrated Analysis of microRNA and RNA-Seq Reveals Phenolic Acid Secretion Metabolism in Continuous Cropping of Polygonatum odoratum" Plants 12, no. 4: 943. https://doi.org/10.3390/plants12040943