Abstract
Wheat contains the largest number of miR396 family with 17 miR396 in Poaceae. MiR396 regulatory network underlying wheat grain development has not comprehensively been explored. Our results showed that precursor miR396 family in Poaceae exhibited not only conservativeness but also diversification especially in wheat. Five haplotypes were detected in Poaceae species, while 4 haplotypes in wheat with Hap-4 (miR396a) and Hap-5 (miR396n) unique to wheat. GO enrichment analysis of target genes showed that the first 20 enrichment functions of miR396a and miR396n are completely different from each other, and also completely different from miR396(b–g), miR396(h–m), and miR396(o–q). Functional annotation on the 18 target genes shared by miR396(b–g), miR396(h–m), and miR396(o–q) found that 11 of the 18 target genes are growth-regulating factor (GRF) genes. Our results indicated that, during the grain filling stage of wheat, miR396 is involved in the development of grains by regulating the expression of GRF genes (GRF1, GRF6, and GRF9). Although the enrichment function of miR396(b–g), miR396(h–m), and miR396(o–q) is the same, the gene functional networks they formed differ greatly. Our results indicated that polyploidization enriches not only the diversity of miR396 family and its target genes but also gene functional networks in wheat. These results laid foundation for further elucidating function of miR396 gene family underlying wheat grain development.
Similar content being viewed by others
References
Akdogan G, Tufekci ED, Uranbey S, Unver T (2016) miRNA-based drought regulation in wheat. Funct Integrat Genom 16:221–233
Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15(11):2730–2741
Bardou P, Mariette J, Escudie F, Djemiel C, Klopp C (2014) jvenn: an interactive Venn diagram viewer. BMC Bioinform 15:15–29
Barik S, SarkarDas S, Singh A, Gautam V, Kumar P, Majee M, Sarkar AK (2014) Phylogenetic analysis reveals conservation and diversification of micro RNA166 genes among diverse plant species. Genomics 103:114–121
Bazin J, Khan GA, Combier J-P, Bustos-Sanmamed P, Debernardi JM, Rodriguez R, Sorin C, Palatnik J, Hartmann C, Crespi M (2013) miR396 affects mycorrhization and root meristem activity in the legume Medicago truncatula. Plant J 74:920–934
Casadevall R, Rodriguez RE, Debernardi JM, Palatnik JF, Casati P (2013) Repression of growth regulating factors by the microRNA396 inhibits cell proliferation by UV-B radiation in Arabidopsis leaves. Plant Cell 25:3570–3583
Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Ann Rev Plant Biol 58:377–406
Choi D, Kim JH, Kende H (2004) Whole genome analysis of the OsGRF gene family encoding plant-specific putative transcription activators in rice (Oryza sativa L.). Plant Cell Physiol 45:897–904
Debernardi JM, Rodriguez RE, Mecchia MA, Palatnik JF (2012) Functional specialization of the plant miR396 regulatory network through distinct microRNA--target interactions. PLoS Genet 8:e1002419. https://doi.org/10.1371/journal.pgen.1002419
Diao Z, Yu M, Bu S, Duan Y, Zhang L, Wu W (2018) Functional characterization of OsmiR396a in rice (Oryza sativa L.). Plant Growth Regul 85:351–361
Dong B, Wang H, Song A, Liu T, Chen Y, Fang W, Chen S, Chen F, Guan Z, Jiang J (2016) miRNAs are involved in determining the improved vigor of autotetrapoid Chrysanthemum nankingense. Front Plant Sci 7:1412. https://doi.org/10.3389/fpls.2016.01412
Feng G, Xu L, Wang J, Nie G, Bushman BS, Xie W, Yan H, Yang Z, Guan H, Huang L (2018) Integration of small RNAs and transcriptome sequencing uncovers a complex regulatory network during vernalization and heading stages of orchardgrass (Dactylis glomerata L.). BMC Genomics 19:1–14
Ferdous J, Hussain SS, Shi BJ (2015) Role of micro RNA s in plant drought tolerance. Plant Biotech J 13:293–305
Gao F, Wang K, Liu Y, Chen Y, Chen P, Shi Z, Luo J, Jiang D, Fan F, Zhu Y (2015) Blocking miR396 increases rice yield by shaping inflorescence architecture. Nat Plant 2:1–9
Ha M, Lu J, Tian L, Ramachandran V, Kasschau KD, Chapman EJ, Carrington JC, Chen X, Wang X-J, Chen ZJ (2009) Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids. Proc Natl Acad Sci 106:17835–17840
Han R, Jian C, Lv J, Yan Y, Chi Q, Li Z, Wang Q, Zhang J, Liu X, Zhao H (2014) Identification and characterization of microRNAs in the flag leaf and developing seed of wheat (Triticum aestivum L.). BMC Genom 15:289. https://doi.org/10.1186/1471-2164-15-289
Han J, Lee Y, Yeom KH, Kim YK, Jin H, Kim VN (2004) The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev 18:3016–3027
He Z, Zeng J, Ren Y, Chen D, Li W, Gao F, Cao Y, Luo T, Yuan G, Wu X (2017) OsGIF1 positively regulates the sizes of stems, leaves, and grains in rice. Front Plant Sci 8:1730. https://doi.org/10.3389/fpls.2017.01730
Hou G, Du C, Gao H, Liu S, Sun W, Lu H, Kang J, Xie Y, Ma D, Wang C (2020) Identification of microRNAs in developing wheat grain that are potentially involved in regulating grain characteristics and the response to nitrogen levels. BMC Plant Biol 20:87. https://doi.org/10.1186/s12870-020-2296-7.Jin
Jin X, Fu Z, Lv P, Peng Q, Ding D, Li W, Tang J (2015) Identification and characterization of microRNAs during maize grain filling. PloS One 10(5):e0125800. https://doi.org/10.1371/journal.pone.0125800
Jones-Rhoades MW (2012) Conservation and divergence in plant microRNAs. Plant Mol Biol 80:3–16
Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799
Katiyar A, Smita S, Muthusamy SK, Chinnusamy V, Pandey DM, Bansal KC (2015) Identification of novel drought-responsive microRNAs and trans-acting siRNAs from Sorghum bicolor (L.) Moench by high-throughput sequencing analysis. Front Plant Sci 6:506. https://doi.org/10.3389/fpls.2015.00506
Kenan-Eichler M, Leshkowitz D, Tal L, Noor E, Melamed-Bessudo C, Feldman M, Levy AA (2011) Wheat hybridization and polyploidization results in deregulation of small RNAs. Genetics 188:263–272
Khraiwesh B, Arif MA, Seumel GI, Ossowski S, Weigel D, Reski R, Frank W (2010) Transcriptional control of gene expression by microRNAs. Cell 140:111–122
Kim VN (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6:376–385
Kurihara Y, Takashi Y, Watanabe Y (2006) The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri-miRNA in plant microRNA biogenesis. RNA 12:206–212
Kurihara Y, Watanabe Y (2004) Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc Natl Acad Sci 101:12753–12758
Lan Y, Su N, Shen Y, Zhang R, Wu F, Cheng Z, Wang J, Zhang X, Guo X, Lei C (2012) Identification of novel MiRNAs and MiRNA expression profiling during grain development in indica rice. BMC Genomics 13:264. https://doi.org/10.1186/1471-2164-13-264
Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854
Li M, Liang Z, He S, Zeng Y, Jing Y, Fang W, Wu K, Wang G, Ning X, Wang L (2017a) Genome-wide identification of leaf abscission associated microRNAs in sugarcane (Saccharum officinarum L.). BMC Genom 18:754. https://doi.org/10.1186/s12864-017-4053-3
Li A, Liu D, Wu J, Zhao X, Hao M, Geng S, Yan J, Jiang X, Zhang L, Wu J (2014) mRNA and small RNA transcriptomes reveal insights into dynamic homoeolog regulation of allopolyploid heterosis in nascent hexaploid wheat. Plant Cell 26:1878–1900
Li D, Liu Z, Gao L, Wang L, Gao M, Jiao Z, Qiao H, Yang J, Chen M, Yao L (2016) Genome-wide identification and characterization of microRNAs in developing grains of Zea mays L. PLoS One 11:e0153168. https://doi.org/10.1371/journal.pone.0153168
Li T, Ma L, Geng Y, Hao C, Chen X, Zhang X (2015) Small RNA and degradome sequencing reveal complex roles of miRNAs and their targets in developing wheat grains. PLoS One 10:e0139658. https://doi.org/10.1371/journal.pone.0139658
Li X, Xie X, Li J, Cui Y, Hou Y, Zhai L, Wang X, Fu Y, Liu R, Bian S (2017b) Conservation and diversification of the miR166 family in soybean and potential roles of newly identified miR166s. BMC Plant Biol 17:32. https://doi.org/10.1186/s12870-017-0983-9
Liu D, Song Y, Chen Z, Yu D (2009) Ectopic expression of miR396 suppresses GRF target gene expression and alters leaf growth in Arabidopsis. Physiol Plant 136:223–236
Liu D, Yu D (2009) MicroRNA (miR396) negatively regulates expression of ceramidase-like genes in Arabidopsis. Prog Nat Sci 19:781–785
Liu H, Guo S, Xu Y, Li C, Zhang Z, Zhang D, Xu S, Zhang C, Chong K (2014) OsmiR396d-regulated OsGRFs function in floral organogenesis in rice through binding to their targets OsJMJ706 and OsCR4. Plant Physiol 165:160–174
Liu HH, Tian X, Li YJ, Wu CA, Zheng CC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14:836–843
Meng F, Liu H, Wang K, Liu L, Wang S, Zhao Y, Yin J, Li Y (2013) Development-associated microRNAs in grains of wheat (Triticum aestivum L.). BMC Plant Biol 13:140. https://doi.org/10.1186/1471-2229-13-140
Nelissen H, Eeckhout D, Demuynck K, Persiau G, Walton A, van Bel M, Vervoort M, Candaele J, de Block J, Aesaert S (2015) Dynamic changes in ANGUSTIFOLIA3 complex composition reveal a growth regulatory mechanism in the maize leaf. Plant Cell 27:1605–1619
Pan X, Nichols RL, Li C, Zhang B (2019) MicroRNA-target gene responses to root knot nematode (Meloidogyne incognita) infection in cotton (Gossypium hirsutum L.). Genomics 111:383–390
Pasquinelli AE, Ruvkun G (2002) Control of developmental timing by microRNAs and their targets. Ann Rev Cell Develop Biol 18:495–513
Peng T, Sun H, Du Y, Zhang J, Li J, Liu Y, Zhao Y, Zhao Q (2013) Characterization and expression patterns of microRNAs involved in rice grain filling. PloS One 8. https://doi.org/10.1371/journal.pone.0054148
Ragupathy R, Ravichandran S, Mahdi MSR, Huang D, Reimer E, Domaratzki M, Cloutier S (2016) Deep sequencing of wheat sRNA transcriptome reveals distinct temporal expression pattern of miRNAs in response to heat, light and UV. Sci Rep 6:1–15
Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16:1616–1626
Rodriguez RE, Mecchia MA, Debernardi JM, Schommer C, Weigel D, Palatnik JF (2010) Control of cell proliferation in Arabidopsis thaliana by microRNA miR396. Development 137:103–112
Rozas J (2009) DNA sequence polymorphism analysis using DnaSP, in: Bioinformatics for DNA sequence analysis. Springer, pp. 337–350
Seeve CM, Sunkar R, Zheng Y, Liu L, Liu Z, McMullen M, Nelson S, Sharp RE, Oliver MJ (2019) Water-deficit responsive microRNAs in the primary root growth zone of maize. BMC Plant Biol 19:447. https://doi.org/10.1186/s12870-019-2037-y
Shi R, Chiang VL (2005) Facile means for quantifying microRNA expression by real-time PCR. Biotechniques 39:519–525
Singh AK, Furtado A, Brozynska M, Mishra NS, Henry RJ (2018) Phylogeny and molecular evolution of miR820 and miR396 microRNA families in Oryza AA genomes. Trop Plant Biol 11:1–16
Song G, Zhang R, Zhang S, Li Y, Gao J, Han X, Chen M, Wang J, Li W, Li G (2017) Response of microRNAs to cold treatment in the young spikes of common wheat. BMC Genomics 18:212. https://doi.org/10.1186/s12864-017-3556-2
Sun F, Guo G, Du J, Guo W, Peng H, Ni Z, Sun Q, Yao Y (2014) Whole-genome discovery of miRNAs and their targets in wheat (Triticum aestivum L.). BMC Plant Biol 14:142. https://doi.org/10.1186/1471-2229-14-142
Tang Y, Wang F, Zhao J, Xie K, Hong Y, Liu Y (2010) Virus-based microRNA expression for gene functional analysis in plants. Plant Physiol 153:632–641
van der Knaap E, Kim JH, Kende H (2000) A novel gibberellin-induced gene from rice and its potential regulatory role in stem growth. Plant Physiol 122:695–704
Zhang D-F, Li B, Jia G-Q, Zhang T-F, Dai J-R, Li J-S, Wang S-C (2008) Isolation and characterization of genes encoding GRF transcription factors and GIF transcriptional coactivators in maize (Zea mays L.). Plant Sci 175:809–817
Zhang K, Shi X, Zhao X, Ding D, Tang J, Niu J (2015) Investigation of miR396 and growth-regulating factor regulatory network in maize grain filling. Acta Physiol Plant 37:28
Zhu JK (2008) Reconstituting plant miRNA biogenesis. Proc Natl Acad Sci 105:9851–9852
Funding
This study was financially supported by the National Key Research and Development Program of China (2017YFD0301304) and the International Science and Technology Cooperation Projects of Anhui Province (1704e1002232), a Research Foundation for Talented Scholars from Anhui Agricultural University and the introduced leading talent research team for Universities in Anhui Province.
Author information
Authors and Affiliations
Contributions
G.S. and D.W. conceived and designed the research. Y.Y., F.S., and N.C. conducted experiments and analyzed data. D.W. and C.Y.W. contributed new reagents or analytical tools. Y.Y., F.S., N. C., and G.S. wrote the manuscript. All authors read and approved the manuscript.
Corresponding authors
Ethics declarations
Conflict interest
The authors declare that they have no conflict of interest.
Additional information
Handling Editor: Peter Nick
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Yu, Y., Sun, F., Chen, N. et al. MiR396 regulatory network and its expression during grain development in wheat. Protoplasma 258, 103–113 (2021). https://doi.org/10.1007/s00709-020-01556-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-020-01556-3