Abstract
Plant microRNAs (miRNAs) are short, non-coding RNA molecules. They mediate RNA silencing and regulate a series of target mRNAs involved in plant development, metabolism, and responses to different ecological environments. As one of important medicinal plants, Atractylodes lancea has a high medicinal significance and commercial value. Mao and Dabie are two ecotypes of A. lancea which mainly distributes in Mao Mountain and Dabie Mountain, respectively. To better understand the genomic information and germplasm resource characteristics, miRNA profiling analysis by high-throughput sequencing was performed to identify rhizome miRNAs of two A. lancea ecotypes. A transcriptomic database was established to identify miRNAs precursors and their target transcripts. By comparing small RNAs and the transcriptomic database, 270 known miRNAs of 46 miRNA families and 91 novel miRNAs were identified, plus hundreds of putative targets. Using Mireap software, 5 and 12 of 22 significant differentially expressed miRNAs were involved in ecotype formation and terpenoid metabolism, respectively, which was verified by qRT-PCR tests. These results are an important resource to better understand the biological mechanism of terpene formation and A. lancea adaptation to different ecological environment.
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References
Baek D, Kim MC, Chun HJ, Kang S, Park HC, Shin G, Park J, Shen M, Hong H, Kim WY (2013) Regulation of miR399f transcription by AtMYB2 affects phosphate starvation responses in Arabidopsis. Plant Physiol 161:362–373
Baek D, Chun HJ, Kang SH, Shin G, Park SJ, Hong H, Kim C, Kim DH, Lee SY, Kim MC, Yun DJ (2016) A role for Arabidopsis miR399f in salt, drought, and ABA signaling. Mol Cells 39:111–118
Bao D, Ganbaatar O, Cui XQ, Yu RN, Bao WH, Falk B, Wuriyanghan H (2017) Down-regulation of genes coding for core RNAi components and disease resistance proteins via corresponding microRNAs might be correlated with successful Soybean mosaic virus infection in soybean. Mol Plant Pathol 19:948–960
Cao X, Fan G, Cao L, Deng M, Zhao Z, Niu S, Wang Z, Wang Y (2017) Drought stress-induced changes of microRNAs in diploid and autotetraploid Paulownia tomentosa. Genes Genom 39:77–86
Dai Z, Wang J, Zhu M, Miao X, Shi Z (2016) OsMADS1 represses microRNA172 in elongation of palea/lemma development in rice. Front Plant Sci 7:1891–1900
Ganie SA, Dey N, Mondal TK (2016) Promoter methylation regulates the abundance of osa-miR393a in contrasting rice genotypes under salinity stress. Funct Integr Genomic 16:1–11
Geng Z, Liu J, Li D, Zhao G, Liu X, Dou H, Lv L, Zhang H, Wang Y (2021) A conserved miR394-targeted F-box gene positively regulates drought resistance in foxtail millet. J Plant Biol 64:243–252
Guo C, Jiang Y, Shi M, Wu X, Wu G (2021) ABI5 acts downstream of miR159 to delay vegetative phase change in Arabidopsis. New Phytol 231:339–350
Gupta OP, Karkute SG, Banerjee S, Meena NL, Dahuja A (2017) Contemporary understanding of miRNA-based regulation of secondary metabolites biosynthesis in plants. Front Plant Sci 8:374
Gupta K, Mishra SK, Gupta S, Pandey S, Panigrahi J, Wani SH (2021) Functional role of miRNAs: key players in soybean improvement. Phyton-Int J Exp Bot OT 90:1339–1362
Huang QQ, Huang X, Deng J, Liu HG, Liu YW, Yu K, Huang BS (2016) Differential gene expression between leaf and rhizome in Atractylodes lancea: a comparative transcriptome analysis. Front Plant Sci 7:348–436
Jiang D, Wang H, Li T, Kang C, Guo X, Zhang Y, Wang S, Guo L (2019) Research progress of the effects of environmental stress on medical plant Atractylodes Lancea. World Chin Med 14:2829–2834
Khan A, Shrestha A, Shaju M, Panigrahi KC, Dey N (2020a) Identification of miRNA Targets by AtFT overexpression in tobacco. Plant Mol Biol Rep 38:48–61
Khan S, Ali A, Saifi M, Saxena P, Abdin MZ (2020b) Identification and the potential involvement of miRNAs in the regulation of artemisinin biosynthesis in A. annua. Sci Rep 10:13614
Kim HY, Hong SH, Kim YW, Lee IH, Jun JH, Phee BK, Rupak T, Jeong H, Lee Y, Hong BS, Nam HG, Woo HR, Lim PO (2014) Gene regulatory cascade of senescence-associated NAC transcription factors activated by ETHYLENE-INSENSITIVE2-mediated leaf senescence signalling in Arabidopsis. J Exp Bot 65:4023–4036
Li Y, Wan L, Bi S, Wan X, Li Z, Cao J, Tong Z, Xu H, He F, Li X (2017) Identification of drought-responsive microRNAs from roots and leaves of alfalfa by high-throughput sequencing. Gene 8:119–134
Lin Y, Zhang L, Zhao Y, Wang Z, Liu H, Zhang L, Zhang Y, Fu Y, Wu J, Ge Y, Zhang W, Zhou S (2020) Comparative analysis and functional identification of temperature-sensitive miRNA in Arabidopsis anthers. Biochem Bioph Res Co 532:1–10
Liu M, Yu H, Zhao G, Huang Q, Lu Y, Ouyang B (2018) Identification of drought-responsive microRNAs in tomato using high-throughput sequencing. Funct Integr Genomic 18:67–78
Lu J, Chen W, Zhou B, Chen Y, Wang X, An R, Yang M (2020) Distinguishing the rhizomes of Atractylodes japonica, Atractylodes chinensis, and Atractylodes lancea by comprehensive two-dimensional gas chromatography coupled with mass spectrometry combined with multivariate data analysis. Pharmacogn Mag 16:654–661
Megha S, Basu U, Kav NNV (2018) Regulation of low temperature stress in plants by microRNAs. Plant Cell Environ 41:1–15
National Commission of Chinese Pharmacopoeia (2020) Pharmacopoeia of Peoples Republic of China part I. The Medicine Science and Technology Press of China, Beijing, p 168
Pagano L, Rossi R, Paesano L, Marmiroli N, Marmiroli M (2021) miRNA regulation and stress adaptation in plants. Environ Exp Bot 184:104369
Pani A, Mahapatra RK, Behera N, Naik PK (2011) Computational Identification of Sweet Wormwood (Artemisia annua) microRNA and Their mRNA Targets. Genom Proteom Bioinf 9:200–210
Pegler JL, Nguyen DQ, Oultram JMJ, Cpl G, Eamens AL (2021) Molecular manipulation of the MiR396/GRF expression module alters the salt stress response of Arabidopsis thaliana. Agron 11:1751–1772
Prakash P, Ghosliya D, Gupta V (2015) Identification of conserved and novel microRNAs in Catharanthus roseus by deep sequencing and computational prediction of their potential targets. Gene 554:181–195
Qiu DY, Pan XP, Wilson IW, Li FL, Liu M, Teng WJ, Zhang BH (2009) High throughput sequencing technology reveals that the taxoid elicitor methyl jasmonate regulates microRNA expression in Chinese yew (Taxus chinensis). Gene 436:37–44
Singroha G, Sharma P, Sunkur R (2021) Current status of microRNA-mediated regulation of drought stress responses in cereals. Physiol Plantarum 172:1808–1821
Song X, Li Y, Cao X, Qi Y (2019) MicroRNAs and their regulatory roles in plant-environment interactions. Annu Rev Plant Biol 70:489–525
Tsusaka T, Makino B, Ohsawa R, Ezura H (2019) Genetic and environmental factors influencing the contents of essential oil compounds in Atractylodes lancea. PLoS ONE 14:e0217522
Wang H, Li Y, Chern M, Zhu Y, Zhang LL, Lu JH, Li XP, Dang WQ, Ma XC, Yang ZR, Yao SZ, Zhao ZX, Fan J, Huang YY, Zhang JW, Pu M, Wang J, He M, Li WT, Chen XW, Wu XJ, Li SG, Li P, Li Y, Ronald PC, Wang WM (2021) Suppression of rice miR168 improves yield, flowering time and immunity. Nat Plants 7:129–136
Xie Y, Zhou Q, Zhao Y, Li Q, Liu Y, Ma M, Wang B, Shen R, Zheng Z, Wang H (2020) FHY3 and FAR1 integrate light signals with the miR156-SPL module-mediated aging pathway to regulate Arabidopsis flowering. Mol Plant 13:483–498
Xie D, Chen M, Niu J, Wang L, Li Y, Fang X, Li P, Qi Y (2021) Phase separation of SERRATE drives dicing body assembly and promotes miRNA processing in Arabidopsis. Nat Cell Biol 23:32–39
Yuan W, Suo J, Shi B, Zhou C, Bai B, Bian H, Zhu M, Han N (2019) The barley miR393 has multiple roles in regulation of seedling growth, stomatal density, and drought stress tolerance. Plant Physiol Bioch 142:303–311
Zhang W, Ouyang Z, Zhao M, Wei Y, Peng H, Wang Q, Guo L (2015) The influences of inorganic elements in soil on the development of famous—region Atractylodes lancea (Thunb.) DC. Pharmacogn Mag 11:337–344
Zhang F, Luo X, Zhou Y, Xie J (2016) Genome-wide identification of conserved microRNA and their response to drought stress in Dongxiang wild rice (Oryza rufipogon Griff.). Biotechnol Lett 38:711–721
Zhang WJ, Zhao ZY, Chang LK, Cao Y, Wang S, Kang CZ, Wang HY, Zhou L, Huang LQ, Guo LP (2021) Atractylodis Rhizoma: a review of its traditional uses, phytochemistry, pharmacology, toxicology and quality control. J Ethnopharmacol 266:113415
Zhao H, Shi X, Shen C, Chen C, Qu C, Patel G, Zhou W, Kai G (2022) Comparative analysis of miRNA expression profiles provides insight into regulation of biosynthesis of flavonoids and terpenoids between two varieties of Toona sinensis sprouts. J Plant Biol 65:291–310
Zhou J, Fang L, Wang X, Zhang J, Guo LP, Huang LQ (2012) Comparison of the volatile compounds of crude and processed Atractylodis rhizome analyzed by GC-MS. Afr J Pharm Pharmacol 6:2155–2160
Acknowledgements
The authors express their sincere thanks to the National Natural Science Foundation of China (Grant nos. 32000254 and 31670341) for their support.
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National Natural Science Foundation of China, 32000254 and 31670341.
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KY and BH: designed the research. JD: and LC: performed the experiments, acquired and analyzed data, and drafted the manuscript. AZ: calculated the data and revised the manuscript. LG: and KY: have been involved in revising the manuscript critically for important intellectual content. MW and WW: contributed plants materials. All authors read and approved the final manuscript.
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Deng, J., Chen, L., Zhang, A. et al. Comparative Analysis and Functional Identification of Rhizome miRNAs of Two Atractylodes lancea Ecotypes. J. Plant Biol. 66, 135–145 (2023). https://doi.org/10.1007/s12374-023-09381-w
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DOI: https://doi.org/10.1007/s12374-023-09381-w