Fast and furious: The rapid turnover of microRNAs in plants

Zhonglong Guo , Yixiang Yang , Xiaozeng Yang

Journal of Systematics and Evolution ›› 2025, Vol. 63 ›› Issue (3) : 510 -522.

PDF
Journal of Systematics and Evolution ›› 2025, Vol. 63 ›› Issue (3) : 510 -522. DOI: 10.1111/jse.13158
Review

Fast and furious: The rapid turnover of microRNAs in plants

Author information +
History +
PDF

Abstract

Plant miRNAs exhibit a dynamic and complex evolutionary landscape. Despite their rapid turnover, miRNAs play crucial roles in regulating key biological processes, underscoring their functional significance even when evolutionarily transient. This review explores the phenomenon of miRNA turnover through a comprehensive survey of miRNA conservation across land plants. We discuss how de novo miRNAs overcome challenges such as transcriptional activation, structural requirements for biogenesis, and functional integration into gene regulatory networks. Furthermore, we review the mechanisms of miRNA origination, including inverted duplication of target genes, derivation from retrotransposons or DNA transposons, spontaneous evolution, and a newly proposed mechanism through template switching mutations. Duplication of existing miRNAs plays a significant role in miRNA family expansion, driving the functional diversification and strengthening regulatory networks. While the phenomenon of miRNA loss has been preliminarily explored, its mechanisms remain insufficiently understood. To address this, we proposed three detailed steps to advance research into miRNA loss. This review provides an integrated perspective on the gain, expansion, and loss of plant miRNAs, offering insights into their evolutionary and biological significance.

Keywords

expansion / gain / loss / microRNAs / plants

Cite this article

Download citation ▾
Zhonglong Guo, Yixiang Yang, Xiaozeng Yang. Fast and furious: The rapid turnover of microRNAs in plants. Journal of Systematics and Evolution, 2025, 63(3): 510-522 DOI:10.1111/jse.13158

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Abrouk M, Zhang R, Murat F, Li A, Pont C, Mao L, Salse J. 2012. Grass microRNA gene paleohistory unveils new insights into gene dosage balance in subgenome partitioning after whole-genome duplication. Plant Cell 24: 1776-1792.

[2]

Allen E, Xie Z, Gustafson AM, Sung GH, Spatafora JW, Carrington JC. 2004. Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nature Genetics 36: 1282-1290.

[3]

Arribas-Hernández L. 2024. Macroloops for microRNAs: Shall we revise the maximum allowed size? Plant Cell 36: 1572-1573.

[4]

Avesson L, Reimegård J, Wagner EG, Söderbom F. 2012. MicroRNAs in amoebozoa: Deep sequencing of the small RNA population in the social amoeba Dictyostelium discoideum reveals developmentally regulated microRNAs. RNA 18: 1771-1782.

[5]

Axtell MJ. 2008. Evolution of microRNAs and their targets: Are all microRNAs biologically relevant? Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms 1779: 725-734.

[6]

Axtell MJ, Bartel DP. 2005. Antiquity of microRNAs and their targets in land plants. Plant Cell 17: 1658-1673.

[7]

Axtell MJ, Westholm JO, Lai EC. 2011. Vive la différence: Biogenesis and evolution of microRNAs in plants and animals. Genome Biology 12: 221.

[8]

Baldrich P, Beric A, Meyers BC. 2018. Despacito: The slow evolutionary changes in plant microRNAs. Current Opinion in Plant Biology 42: 16-22.

[9]

Bartel DP. 2018. Metazoan microRNAs. Cell 173: 20-51.

[10]

Begun DJ, Lindfors HA, Kern AD, Jones CD. 2007. Evidence for de novo evolution of testis-expressed genes in the Drosophila yakuba/Drosophila erecta clade. Genetics 176: 1131-1137.

[11]

Castel SE, Martienssen RA. 2013. RNA interference in the nucleus: Roles for small RNAs in transcription, epigenetics and beyond. Nature Reviews Genetics 14: 100-112.

[12]

Chen K, Rajewsky N. 2007. The evolution of gene regulation by transcription factors and microRNAs. Nature Reviews Genetics 8: 93-103.

[13]

Chen X. 2009. Small RNAs and their roles in plant development. Annual Review of Cell and Developmental Biology 25: 21-44.

[14]

Chen X, Rechavi O. 2022. Plant and animal small RNA communications between cells and organisms. Nature Reviews Molecular Cell Biology 23: 185-203.

[15]

Cock JM, Liu F, Duan D, Bourdareau S, Lipinska AP, Coelho SM, Tarver JE. 2017. Rapid evolution of microRNA loci in the brown algae. Genome Biology and Evolution 9: 740-749.

[16]

Creasey KM, Zhai J, Borges F, Van Ex F, Regulski M, Meyers BC, Martienssen RA. 2014. MiRNAs trigger widespread epigenetically activated siRNAs from transposons in Arabidopsis. Nature 508: 411-415.

[17]

Cui J, You C, Chen X. 2017. The evolution of microRNAs in plants. Current Opinion in Plant Biology 35: 61-67.

[18]

Cuperus JT, Fahlgren N, Carrington JC. 2011. Evolution and functional diversification of miRNA genes. Plant Cell 23: 431-442.

[19]

Deline B, Greenwood JM, Clark JW, Puttick MN, Peterson KJ, Donoghue PCJ. 2018. Evolution of metazoan morphological disparity. Proceedings of the National Academy of Sciences USA 115: E8909-e8918.

[20]

Dexheimer PJ, Cochella L. 2020. MicroRNAs: From mechanism to organism. Frontiers in Cell and Developmental Biology 8: 409.

[21]

Dunoyer P, Himber C, Ruiz-Ferrer V, Alioua A, Voinnet O. 2007. Intra- and intercellular RNA interference in Arabidopsis thaliana requires components of the microRNA and heterochromatic silencing pathways. Nature Genetics 39: 848-856.

[22]

Dutra BE, Lovett ST. 2006. Cis and trans-acting effects on a mutational hotspot involving a replication template switch. Journal of Molecular Biology 356: 300-311.

[23]

Fahlgren N, Jogdeo S, Kasschau KD, Sullivan CM, Chapman EJ, Laubinger S, Smith LM, Dasenko M, Givan SA, Weigel D, Carrington JC. 2010. MicroRNA gene evolution in Arabidopsis lyrata and Arabidopsis thaliana. Plant Cell 22: 1074-1089.

[24]

Felippes FF, Schneeberger K, Dezulian T, Huson DH, Weigel D. 2008. Evolution of Arabidopsis thaliana microRNAs from random sequences. RNA 14: 2455-2459.

[25]

Fridrich A, Modepalli V, Lewandowska M, Aharoni R, Moran Y. 2020. Unravelling the developmental and functional significance of an ancient argonaute duplication. Nature Communications 11: 6187.

[26]

Gao Z, Li J, Li L, Yang Y, Li J, Fu C, Zhu D, He H, Cai H, Li L. 2021. Structural and functional analyses of hub microRNAs in an integrated gene regulatory network of Arabidopsis. Genomics. Proteomics and Bioinformatics 20: 747-764.

[27]

Gramzow L, Lobbes D, Innard N, Theißen G. 2020. Independent origin of miRNA genes controlling homologous target genes by partial inverted duplication of antisense-transcribed sequences. Plant Journal 101: 401-419.

[28]

Guddeti S, Zhang DC, Li AL, Leseberg CH, Kang H, Li XG, Zhai WX, Johns MA, Mao L. 2005. Molecular evolution of the rice miR395 gene family. Cell Research 15: 631-638.

[29]

Guo X, Zhang Z, Gerstein MB, Zheng D. 2009. Small RNAs originated from pseudogenes: Cis- or trans-acting? PLOS Computational Biology 5: e1000449.

[30]

Guo Y, Wang S, Yu K, Wang HL, Xu H, Song C, Zhao Y, Wen J, Fu C, Li Y, Wang S, Zhang X, Zhang Y, Cao Y, Shao F, Wang X, Deng X, Chen T, Zhao Q, Li L, Wang G, Grünhofer P, Schreiber L, Li Y, Song G, Dixon RA, Lin J. 2023. Manipulating microRNA miR408 enhances both biomass yield and saccharification efficiency in poplar. Nature Communications 14: 4285.

[31]

Guo Z, Xu Z, Li L, Xu K-W. 2024. Species-specific miRNAs contribute to the divergence between deciduous and evergreen species in Ilex. Plants (Basel) 13: 1429.

[32]

Guo Z, Kuang Z, Deng Y, Li L, Yang X. 2022a. Identification of species-specific microRNAs provides insights into dynamic evolution of microRNAs in plants. International Journal of Molecular Sciences 23: 14273.

[33]

Guo Z, Kuang Z, Tao Y, Wang H, Wan M, Hao C, Shen F, Yang X, Li L. 2022b. Miniature inverted-repeat transposable elements drive rapid microRNA diversification in angiosperms. Molecular Biology and Evolution 39: 11.

[34]

Guo Z, Kuang Z, Wang Y, Zhao Y, Tao Y, Cheng C, Yang J, Lu X, Hao C, Wang T, Cao X, Wei J, Li L, Yang X. 2020. Pmiren: A comprehensive encyclopedia of plant miRNAs. Nucleic Acids Research 48: D1114-D1121.

[35]

Guo Z, Kuang Z, Zhao Y, Deng Y, He H, Wan M, Tao Y, Wang D, Wei J, Li L, Yang X. 2022c. Pmiren2.0: From data annotation to functional exploration of plant microRNAs. Nucleic Acids Research 50: D1475-D1482.

[36]

Hajieghrari Behzad FN. 2020. Investigation on the conserved microRNA genes in higher plants. Plant Molecular Biology Reporter 39: 10-23.

[37]

Han J, Lee Y, Yeom K-H, Nam J-W, Heo I, Rhee J-K, Sohn SY, Cho Y, Zhang B-T, Kim VN. 2006. Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 125: 887-901.

[38]

Hao C, Yang Y, Du J, Deng XW, Li L. 2022. The PCY-SAG14 phytocyanin module regulated by PIFs and miR408 promotes dark-induced leaf senescence in Arabidopsis. Proceedings of the National Academy of Sciences USA 119: e2116623119.

[39]

Henderson IR, Zhang X, Lu C, Johnson L, Meyers BC, Green PJ, Jacobsen SE. 2006. Dissecting Arabidopsis thaliana dicer function in small RNA processing, gene silencing and DNA methylation patterning. Nature Genetics 38: 721-725.

[40]

Huang D, Feurtado JA, Smith MA, Flatman LK, Koh C, Cutler AJ. 2017. Long noncoding miRNA gene represses wheat β-diketone waxes. Proceedings of the National Academy of Sciences USA 114: e3149-e3158.

[41]

Huang T, Li Y, Wang W, Xu L, Li J, Qi Y. 2022. Evolution of lmiRNAs and their targets from MITEs for rice adaptation. Journal of Integrative Plant Biology 64: 2411-2424.

[42]

Jaiswal S, Iquebal MA, Arora V, Sheoran S, Sharma P, Angadi UB, Dahiya V, Singh R, Tiwari R, Singh GP, Rai A, Kumar D. 2019. Development of species specific putative miRNA and its target prediction tool in wheat (Triticum aestivum L.). Scientific Reports 9: 3790.

[43]

Jiang A, Guo Z, Pan J, Yang Y, Zhuang Y, Zuo D, Hao C, Gao Z, Xin P, Chu J, Zhong S, Li L. 2021. The PIF1-miR408-PLANTACYANIN repression cascade regulates light-dependent seed germination. Plant Cell 33: 1506-1529.

[44]

Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X, Qian Q, Li J. 2010. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nature Genetics 42: 541-544.

[45]

Jo A, Lee HE, Kim HS. 2019. Identification and expression analysis of a novel miRNA derived from ERV-E1 LTR in Equus caballus. Gene 687: 238-245.

[46]

Jones-Rhoades MW. 2012. Conservation and divergence in plant microRNAs. Plant Molecular Biology 80: 3-16.

[47]

Jones-Rhoades MW, Bartel DP. 2004. Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Molecular Cell 14: 787-799.

[48]

Jones-Rhoades MW, Bartel DP, Bartel B. 2006. MicroRNAs and their regulatory roles in plants. Annual Review Plant Biology 57: 19-53.

[49]

Kasschau KD, Fahlgren N, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Carrington JC. 2007. Genome-wide profiling and analysis of Arabidopsis siRNAs. PLoS Biology 5: e57.

[50]

Kim K, Baek SC, Lee YY, Bastiaanssen C, Kim J, Kim H, Kim VN. 2021. A quantitative map of human primary microRNA processing sites. Molecular Cell 81: 3422-3439.

[51]

Kim Y-K, Kim VN. 2007. Processing of intronic microRNAs. The EMBO Journal 26: 775-783.

[52]

Knop K, Stepien A, Barciszewska-Pacak M, Taube M, Bielewicz D, Michalak M, Borst JW, Jarmolowski A, Szweykowska-Kulinska Z. 2016. Active 5′ splice sites regulate the biogenesis efficiency of Arabidopsis microRNAs derived from intron-containing genes. Nucleic Acids Research 45: 2757-2775.

[53]

Ko J-H, Prassinos C, Han K-H. 2006. Developmental and seasonal expression of PtaHB1, a Populus gene encoding a class iii HD-Zip protein, is closely associated with secondary growth and inversely correlated with the level of microRNA (miR166). New Phytologist 169: 469-478.

[54]

Kuang Z, Wang Y, Li L, Yang X. 2019. Mirdeep-p2: Accurate and fast analysis of the microRNA transcriptome in plants. Bioinformatics 35: 2521-2522.

[55]

Kumar S, Suleski M, Craig JM, Kasprowicz AE, Sanderford M, Li M, Stecher G, Hedges SB. 2022. Timetree 5: An expanded resource for species divergence times. Molecular Biology and Evolution 39: msac174.

[56]

Langschied F, Leisegang MS, Brandes RP, Ebersberger I. 2023. Ncortho: Efficient and reliable identification of miRNA orthologs. Nucleic Acids Research 51: e71.

[57]

Lee HE, Jo A, Im J, Cha HJ, Kim WJ, Kim HH, Kim DS, Kim W, Yang TJ, Kim HS. 2019. Characterization of the long terminal repeat of the endogenous retrovirus-derived microRNAs in the olive flounder. Scientific Reports 9: 14007.

[58]

Li A, Mao L. 2007. Evolution of plant microRNA gene families. Cell Research 17: 212-218.

[59]

Li G, Chen C, Chen P, Meyers BC, Xia R. 2024. sRNAminer: A multifunctional toolkit for next-generation sequencing small RNA data mining in plants. Science Bulletin 69: 784-791.

[60]

Li T, Chen J, Qiu S, Zhang Y, Wang P, Yang L, Lu Y, Shi J. 2012. Deep sequencing and microarray hybridization identify conserved and species-specific microRNAs during somatic embryogenesis in hybrid yellow poplar. PLoS One 7: e43451.

[61]

Lian H, Wang L, Ma N, Zhou CM, Han L, Zhang TQ, Wang JW. 2021. Redundant and specific roles of individual miR172 genes in plant development. PLoS Biology 19: e3001044.

[62]

Liang G, Yang F, Yu D. 2010. MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. Plant Journal 62: 1046-1057.

[63]

Lim LP, Lau NC, Weinstein EG, Abdelhakim A, Yekta S, Rhoades MW, Burge CB, Bartel DP. 2003. The microRNAs of Caenorhabditis elegans. Genes & Development 17: 991-1008.

[64]

Liu H, Yu H, Tang G, Huang T. 2018. Small but powerful: Function of microRNAs in plant development. Plant Cell Reports 37: 515-528.

[65]

Liu T, Fang C, Ma Y, Shen Y, Li C, Li Q, Wang M, Liu S, Zhang J, Zhou Z, Yang R, Wang Z, Tian Z. 2016. Global investigation of the co-evolution of miRNA genes and microRNA targets during soybean domestication. Plant Journal 85: 396-409.

[66]

Llave C, Kasschau KD, Rector MA, Carrington JC. 2002. Endogenous and silencing-associated small RNAs in plants. Plant Cell 14: 1605-1619.

[67]

Löytynoja A. 2022. Thousands of human mutation clusters are explained by short-range template switching. Genome Research 32: 1437-1447.

[68]

Löytynoja A, Goldman N. 2017. Short template switch events explain mutation clusters in the human genome. Genome Research 27: 1039-1049.

[69]

Lu J, Shen Y, Wu Q, Kumar S, He B, Shi S, Carthew RW, Wang SM, Wu CI. 2008. The birth and death of microRNA genes in Drosophila. Nature Genetics 40: 351-355.

[70]

Lyu Y, Shen Y, Li H, Chen Y, Guo L, Zhao Y, Hungate E, Shi S, Wu CI, Tang T. 2014. New microRNAs in Drosophila - birth, death and cycles of adaptive evolution. PLoS Genetics 10: e1004096.

[71]

Ma Z, Coruh C, Axtell MJ. 2010. Arabidopsis lyrata small RNAs: Transient miRNA and small interfering RNA loci within the Arabidopsis genus. Plant Cell 22: 1090-1103.

[72]

Maher C, Stein L, Ware D. 2006. Evolution of Arabidopsis microRNA families through duplication events. Genome Research 16: 510-519.

[73]

Mallory AC, Bartel DP, Bartel B. 2005. MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17: 1360-1375.

[74]

Matzke M, Matzke AJM, Kooter JM. 2001a. RNA: Guiding gene silencing. Science 293: 1080-1083.

[75]

Matzke MA, Matzke AJM, Pruss GJ, Vance VB. 2001b. RNA-based silencing strategies in plants. Current Opinion in Genetics & Development 11: 221-227.

[76]

McKeown M, Schubert M, Preston JC, Fjellheim S. 2017. Evolution of the miR5200- FLOWERING LOCUS T flowering time regulon in the temperate grass subfamily Pooideae. Molecular Phylogenetics and Evolution 114: 111-121.

[77]

Mette MF, van der Winden J, Matzke M, Matzke AJM. 2002. Short RNAs can identify new candidate transposable element families in Arabidopsis. Plant Physiology 130: 6-9.

[78]

Meunier J, Lemoine F, Soumillon M, Liechti A, Weier M, Guschanski K, Hu H, Khaitovich P, Kaessmann H. 2013. Birth and expression evolution of mammalian microRNA genes. Genome Research 23: 34-45.

[79]

Michael JA, Westholm JO, Lai EC. 2011. Vive la diérence: Biogenesis and evolution of microRNAs in plants and animals. Genome Biology 12: 221.

[80]

Millar AA. 2020. The function of miRNAs in plants. Plants (Basel) 9: 198.

[81]

Mönttinen HAM, Löytynoja A. 2022. Template switching in DNA replication can create and maintain RNA hairpins. Proceedings of the National Academy of Sciences USA 119: e2107005119.

[82]

Mönttinen HAM, Frilander MJ, Löytynoja A. 2023. Generation of de novo miRNAs from template switching during DNA replication. Proceedings of the National Academy of Sciences USA 120: e2310752120.

[83]

Moran Y, Agron M, Praher D, Technau U. 2017. The evolutionary origin of plant and animal microRNAs. Nature Ecology and Evolution 1: 27.

[84]

Morea EGO, da Silva EM, e Silva GFF, Valente GT, Barrera Rojas CH, Vincentz M, Nogueira FTS. 2016. Functional and evolutionary analyses of the miR156 and miR529 families in land plants. BMC Plant Biology 16: 40.

[85]

Nithin C, Patwa N, Thomas A, Bahadur RP, Basak J. 2015. Computational prediction of miRNAs and their targets in Phaseolus vulgaris using simple sequence repeat signatures. BMC Plant Biology 15: 140.

[86]

Nozawa M, Miura S, Nei M. 2012. Origins and evolution of microRNA genes in plant species. Genome Biology and Evolution 4: 230-239.

[87]

Ohno DS. 1970. Evolution by gene duplication. Berlin, Heidelberg: Springer.

[88]

Ó'Maoiléidigh DS, van Driel AD, Singh A, Sang Q, Le Bec N, Vincent C, de Olalla EBG, Vayssières A, Romera Branchat M, Severing E, Martinez Gallegos R, Coupland G. 2021. Systematic analyses of the MIR172 family members of Arabidopsis define their distinct roles in regulation of APETALA2 during floral transition. PLoS Biology 19: e3001043.

[89]

Pagano L, Rossi R, Paesano L, Marmiroli N, Marmiroli M. 2021. MiRNA regulation and stress adaptation in plants. Environmental and Experimental Botany 184: 104369.

[90]

Palatnik JF, Wollmann H, Schommer C, Schwab R, Boisbouvier J, Rodriguez R, Warthmann N, Allen E, Dezulian T, Huson D, Carrington JC, Weigel D. 2007. Sequence and expression differences underlie functional specialization of Arabidopsis microRNAs miR159 and miR319. Developmental Cell 13: 115-125.

[91]

Pan J, Huang D, Guo Z, Kuang Z, Zhang H, Xie X, Ma Z, Gao S, Lerdau MT, Chu C, Li L. 2018. Overexpression of microRNA408 enhances photosynthesis, growth, and seed yield in diverse plants. Journal of Integrative Plant Biology 60: 323-340.

[92]

Patel VD, Capra JA. 2017. Ancient human miRNAs are more likely to have broad functions and disease associations than young miRNAs. BMC Genomics 18: 672.

[93]

Piriyapongsa J, Jordan IK. 2007. A family of human microRNA genes from miniature inverted-repeat transposable elements. PLoS One 2: e203.

[94]

Piriyapongsa J, Jordan IK. 2008. Dual coding of siRNAs and miRNAs by plant transposable elements. RNA 14: 814-821.

[95]

Piriyapongsa J, Marino-Ramirez L, Jordan IK. 2007. Origin and evolution of human microRNAs from transposable elements. Genetics 176: 1323-1337.

[96]

Rajagopalan R, Vaucheret H, Trejo J, Bartel DP. 2006. A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes & Development 20: 3407-3425.

[97]

Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP. 2002. MicroRNAs in plants. Genes & Development 16: 1616-1626.

[98]

Ripley LS. 1982. Model for the participation of quasi-palindromic DNA sequences in frameshift mutation. Proceedings of the National Academy of Sciences USA 79: 4128-4132.

[99]

Rosatti S, Rojas AML, Moro B, Suarez Irina P, Bologna Nicolas G, Chorostecki U, Palatnik Javier F. 2024. Principles of miRNA/miRNA* function in plant MIRNA processing. Nucleic Acids Research 52: 8356-8369.

[100]

Sakaguchi J, Watanabe Y. 2012. miR165/166 and the development of land plants. Development, Growth & Differentiation 54: 93-99.

[101]

Sempere LF, Cole CN, McPeek MA, Peterson KJ. 2006. The phylogenetic distribution of metazoan microRNAs: Insights into evolutionary complexity and constraint. Journal of Experimental Zoology Part B 306: 575-588.

[102]

Shang R, Lee S, Senavirathne G, Lai EC. 2023. MicroRNAs in action: Biogenesis, function and regulation. Nature Reviews Genetics 24: 816-833.

[103]

Shi X, Yang H, Chen C, Hou J, Ji T, Cheng J, Birchler JA. 2022. Dosage-sensitive miRNAs trigger modulation of gene expression during genomic imbalance in maize. Nature Communications 13: 3014.

[104]

Singh AK, Singh N, Kumar S, Kumari J, Singh R, Gaba S, Yadav MC, Grover M, Chaurasia S, Kumar R. 2020. Identification and evolutionary analysis of polycistronic miRNA clusters in domesticated and wild wheat. Genomics 112: 2334-2348.

[105]

Smalheiser NR, Torvik VI. 2005. Mammalian microRNAs derived from genomic repeats. Trends in Genetics 21: 322-326.

[106]

Smith LM, Burbano HA, Wang X, Fitz J, Wang G, Ural-Blimke Y, Weigel D. 2015. Rapid divergence and high diversity of miRNAs and miRNA targets in the Camelineae. Plant Journal 81: 597-610.

[107]

Song X, Li Y, Cao X, Qi Y. 2019. MicroRNAs and their regulatory roles in plant-environment interactions. Annual Review of Plant Biology 70: 489-525.

[108]

Sun C, Wu J, Liang J, Schnable JC, Yang W, Cheng F, Wang X. 2015. Impacts of whole-genome triplication on miRNA evolution in Brassica rapa. Genome Biology and Evolution 7: 3085-3096.

[109]

Sun J, Zhou M, Mao Z, Li C. 2012. Characterization and evolution of microRNA genes derived from repetitive elements and duplication events in plants. PLoS One 7: e34092.

[110]

Sunkar R, Li YF, Jagadeeswaran G. 2012. Functions of microRNAs in plant stress responses. Trends in Plant Science 17: 196-203.

[111]

Svoboda P, Di Cara A. 2006. Hairpin RNA: A secondary structure of primary importance. Cellular and Molecular Life Sciences 63: 901-908.

[112]

Tarver JE, Cormier A, Pinzón N, Taylor RS, Carré W, Strittmatter M, Seitz H, Coelho SM, Cock JM. 2015. MicroRNAs and the evolution of complex multicellularity: Identification of a large, diverse complement of microRNAs in the brown alga Ectocarpus. Nucleic Acids Research 43: 6384-6398.

[113]

Tarver JE, Taylor RS, Puttick MN, Lloyd GT, Pett W, Fromm B, Schirrmeister BE, Pisani D, Peterson KJ, Donoghue PCJ. 2018. Well-annotated microRNAomes do not evidence pervasive miRNA loss. Genome Biology and Evolution 10: 1457-1470.

[114]

Vaucheret H, Voinnet O. 2023. The plant siRNA landscape. Plant Cell 36: 246-275.

[115]

Voinnet O. 2004. Shaping small RNAs in plants by gene duplication. Nature Genetics 36: 1245-1246.

[116]

Voinnet O. 2009. Origin, biogenesis, and activity of plant microRNAs. Cell 136: 669-687.

[117]

Walker CR, Scally A, De Maio N, Goldman N. 2021. Short-range template switching in great ape genomes explored using pair hidden Markov models. PLoS Genetics 17: e1009221.

[118]

Wang JW, Czech B, Weigel D. 2009. Mir156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138: 738-749.

[119]

Wang JW, Wang LJ, Mao YB, Cai WJ, Xue HW, Chen XY. 2005. Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17: 2204-2216.

[120]

Wang WQ, Liu XF, Zhu YJ, Zhu JZ, Liu C, Wang ZY, Shen XX, Allan AC, Yin XR. 2024. Identification of miRNA858 long-loop precursors in seed plants. Plant Cell 36: 1637-1654.

[121]

Wang Y, Tang X, Lu J. 2023. Convergent and divergent evolution of microRNA-mediated regulation in metazoans. Biological Reviews of the Cambridge Philosophical Society 99: 525-545.

[122]

Wang Y, Luo J, Zhang H, Lu J. 2016. MicroRNAs in the same clusters evolve to coordinately regulate functionally related genes. Molecular Biology and Evolution 33: 2232-2247.

[123]

Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C, Qi Y. 2010. DNA methylation mediated by a microRNA pathway. Molecular Cell 38: 465-475.

[124]

Xia R, Xu J, Arikit S, Meyers BC. 2015. Extensive families of miRNAs and PHAS loci in norway spruce demonstrate the origins of complex phasiRNA networks in seed plants. Molecular Biology and Evolution 32: 2905-2918.

[125]

Xie L, Gong X, Yang K, Huang Y, Zhang S, Shen L, Sun Y, Wu D, Ye C, Zhu Q-H, Fan L. 2024. Technology-enabled great leap in deciphering plant genomes. Nature Plants 10: 551-566.

[126]

Yang X, Li L. 2011. miRdeep-P: A computational tool for analyzing the microRNA transcriptome in plants. Bioinformatics 27: 2614-2615.

[127]

Yang Y, Xu L, Hao C, Wan M, Tao Y, Zhuang Y, Su Y, Li L. 2024. The microRNA408-plantacyanin module balances plant growth and drought resistance by regulating reactive oxygen species homeostasis in guard cells. Plant Cell 36: 4338-4355.

[128]

Zhang F, Yang J, Zhang N, Wu J, Si H. 2022a. Roles of micrornas in abiotic stress response and characteristics regulation of plant. Frontiers in Plant Science 13: 919243.

[129]

Zhang H, Guo Z, Zhuang Y, Suo Y, Du J, Gao Z, Pan J, Li L, Wang T, Xiao L, Qin G, Jiao Y, Cai H, Li L. 2021. MicroRNA775 regulates intrinsic leaf size and reduces cell wall pectin levels by targeting a galactosyltransferase gene in Arabidopsis. Plant Cell 33: 581-602.

[130]

Zhang J. 2003. Evolution by gene duplication: An update. Trends in Ecology & Evolution 18: 292-298.

[131]

Zhang R, Wang YQ, Su B. 2008. Molecular evolution of a primate-specific microRNA family. Molecular Biology and Evolution 25: 1493-1502.

[132]

Zhang T, Zhai J, Zhang X, Ling L, Li M, Xie S, Song M, Ma C. 2022b. Interactive web-based annotation of plant microRNAs with iwa-miRNA. Genomics, Proteomics & Bioinformatics 20: 557-567.

[133]

Zhang W, Gao S, Zhou X, Xia J, Chellappan P, Zhou X, Zhang X, Jin H. 2010. Multiple distinct small RNAs originate from the same microRNA precursors. Genome Biology 11: R81.

[134]

Zhang Y, Jiang W-K, Gao L-Z. 2011. Evolution of microRNA genes in Oryza sativa and Arabidopsis thaliana: An update of the inverted duplication model. PLoS One 6: e28073.

[135]

Zhang Y, Xia R, Kuang H, Meyers BC. 2016. The diversification of plant NBS-LRR defense genes directs the evolution of microRNAs that target them. Molecular Biology and Evolution 33: 2692-2705.

[136]

Zhao M, Meyers BC, Cai C, Xu W, Ma J. 2015. Evolutionary patterns and coevolutionary consequences of miRNA genes and microrna targets triggered by multiple mechanisms of genomic duplications in soybean. Plant Cell 27: 546-562.

[137]

Zhu H, Chen C, Zeng J, Yun Z, Liu Y, Qu H, Jiang Y, Duan X, Xia R. 2020. MicroRNA528, a hub regulator modulating ROS homeostasis via targeting of a diverse set of genes encoding copper-containing proteins in monocots. New Phytologist 225: 385-399.

[138]

Zolotarov G, Fromm B, Legnini I, Ayoub S, Polese G, Maselli V, Chabot PJ, Vinther J, Styfhals R, Seuntjens E, Di Cosmo A, Peterson KJ, Rajewsky N. 2022. MicroRNAs are deeply linked to the emergence of the complex octopus brain. Science Advances 8: eadd9938.

RIGHTS & PERMISSIONS

2025 Institute of Botany, Chinese Academy of Sciences.

AI Summary AI Mindmap
PDF

41

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/