miRNA expression differentiation induced by polyploidization in newly formed triploids of black poplar

Wenting XU; Xue WANG; Huichun LIU; Jiaqiang ZHANG; Jianghua ZHOU; Rongxin GOU; Kaiyuan ZHU

doi:10.15835/nbha50312964

Authors

Wenting XU Zhejiang Institute of Landscape Plants and Flowers, Zhejiang Academy of Agricultural Sciences, Hangzhou 311251; Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants of Ministry of Education, Key Laboratory of Forest Trees and Ornamental Plants biological engineering of State Forestry Administration, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, 100083 (CN)
Xue WANG Institute of Grassland, Flowers and Ecology, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097 (CN)
Huichun LIU Zhejiang Institute of Landscape Plants and Flowers, Zhejiang Academy of Agricultural Sciences, Hangzhou 311251 (CN)
Jiaqiang ZHANG Zhejiang Institute of Landscape Plants and Flowers, Zhejiang Academy of Agricultural Sciences, Hangzhou 311251 (CN)
Jianghua ZHOU Zhejiang Institute of Landscape Plants and Flowers, Zhejiang Academy of Agricultural Sciences, Hangzhou 311251 (CN)
Rongxin GOU Institute of Grassland, Flowers and Ecology, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097 (CN)
Kaiyuan ZHU Zhejiang Institute of Landscape Plants and Flowers, Zhejiang Academy of Agricultural Sciences, Hangzhou 311251 (CN)

DOI:

https://doi.org/10.15835/nbha50312964

Keywords:

miRNA, newly formed triploid, poplar polyploidization

Abstract

During whole genomic duplication (WGD) events, micro RNAs (miRNAs) are involved in stabilization of chromatin and genome and epigenetic regulation of gene expression. In this study, a newly induced triploid group of hybrids between sect. Tacamahaca and sect. Aigeiros in Populus, was characterized for genome-wide miRNA expression after WGD. Seven miRNA libraries (male parent, female parent, group of triploid offspring’s, group of diploid offspring, and three triploid individuals) were constructed and variation of miRNA expression from diploid parents to triploid offspring’s as well as distinction between triploid and diploid offspring were analyzed. The results showed that a total of 240 miRNAs were predicted including 187 known miRNAs and 53 novel miRNAs. 81.25% of miRNAs in triploid offspring were non-additively expressed in which 52.31% were down-regulated. A novel miRNA with 24nt in length choosing adenine as its first base was found in triploid offspring group suggesting its potential role in regulation of DNA methylation after WGD. A total of 18 novel miRNAs were specifically expressed in the library of triploid group. Targeted genes of different expressed miRNAs in three comparison sets (triploid offspring group vs female parent, male parent, and diploid offspring group) were all enriched in ADP binding (GO: 0043531; FDR < 0.05). KEGG enrichment pathway of all three comparison sets was plant-pathogen interaction. This study revealed an essential role of miRNAs involving in epigenetic regulation after WGD in poplar and provided a good model for further studies of polyploidization advantages in woody plant.

References

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. The Plant Cell 24:1776-1792. https://doi.org/10.1105/tpc.112.095752

Axtell MJ (2013). Classification and comparison of small RNAs from plants. Annual Review of Plant Biology 64:137-159. https://doi.org/10.1146/annurev-arplant-050312-120043

Barakat A, Wall PK, DiLoreto S, dePamphilis CW, Carlson JE (2007). Conservation and divergence of microRNAs in Populus. BMC Genomics 8:481. https://doi.org/10.1186/1471-2164-8-481

Birchler J, Yang H (2022). The multiple fates of gene duplications: Deletion, hypofunctionalization, subfunctionalization, neofunctionalization, dosage balance constraints, and neutral variation. The Plant Cell 34:2466-2474. https://doi.org/10.1093/plcell/koac076

Carrington JC, Ambros V (2003). Role of microRNAs in plant and animal development. Science 301:336-338. https://doi.org/10.1126/science.1085242

Chalhoub B, Denoeud F, Liu S, Parkin IAP, Tang H, Wang X, ... Wincker P (2014). Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345:950-953. https://doi.org/10.1126/science.1253435

Chávez Montes R, Rosas-Cárdenas D, De Paoli E, Accerbi M, Rymarquis LA, Mahalingam G, ... De Folter S (2014). Sample sequencing of vascular plants demonstrates widespread conservation and divergence of microRNAs. Nature Communications 5:3722. https://doi.org/10.1038/ncomms4722

Chellappan P, Xia J, Zhou X, Gao S, Zhang X, Coutino G, ... Jin H (2010). siRNAs from miRNA sites mediate DNA methylation of target genes. Nucleic Acids Research 38:6883-6894. https://doi.org/10.1093/nar/gkq590

Chen ZJ (2007). Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annual Review of Plant Biology 58:377-406. https://doi.org/10.1146/annurev.arplant.58.032806.103835

Chen ZJ (2013). Genomic and epigenetic insights into the molecular bases of heterosis. Nature Reviews Genetics 14:471-482. https://doi.org/10.1038/nrg3503

Ding M, Chen ZJ (2018). Epigenetic perspectives on the evolution and domestication of polyploid plant and crops. Current Opinion in Plant Biology 42:37-48. https://doi.org/10.1016/j.pbi.2018.02.003

Edwards D, Murray JAH, Smith AG (1998). Multiple genes encoding the conserved CCAAT-Box transcription factor complex are expressed in Arabidopsis. Plant Physiology 117:1015-1022. https://doi.org/10.2307/4278359

Friedlander MR, Mackowiak SD, Li N, Chen W, Rajewsky N (2011). miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Research 40:37-52. https://doi.org/10.1093/nar/gkr688

Gyorfy MF, Miller ER, Conover JL, Grover CE, Wendel JF, Sloan DB, Sharbrough J (2021). Nuclear-cytoplasmic balance: whole genome duplications induce elevated organellar genome copy number. The Plant Journal 108:219-230. https://doi.org/10.1111/tpj.15436

Ha M, Lu J, Tian L, Ramachandran V, Kasschau KD, Chapman EJ, ... Chen ZJ (2009). Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids. Proceedings of the National Academy of Sciences 106:17835-17840. https://doi.org/10.1073/pnas.0907003106

Hughes TE, Langdale JA, Kelly S (2014). The impact of widespread regulatory neofunctionalization on homeolog gene evolution following whole-genome duplication in maize. Genome Research 24:1348-1355. https://doi.org/10.1101/gr.172684.114

Initiative AG (2000). Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796-815. https://doi.org/10.1038/35048692

Jackson S, Chen ZJ (2010). Genomic and expression plasticity of polyploidy. Current Opinion in Plant Biology 13:153-159. https://doi.org/10.1016/j.pbi.2009.11.004

Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, ... Yamanishi Y (2008). KEGG for linking genomes to life and the environment. Nucleic Acids Research 36:D480-484. https://doi.org/10.1093/nar/gkm882

Kim JH, Woo HR, Kim J, Lim PO, Lee IC, Choi SH, ... Nam HG (2009). Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science 323:1053-1057. https://doi.org/10.1126/science.1166386

Li A, Liu D, Wu J, Zhao X, Hao M, Geng S, ... Mao L (2014). mRNA and small RNA transcriptomes reveal insights into dynamic homoeolog regulation of allopolyploid heterosis in nascent hexaploid Wheat. The Plant Cell 26:1878-1900. https://doi.org/10.1105/tpc.114.124388

Liu Z, Xin M, Qin J, Peng H, Ni Z, Yao Y, Sun Q (2015). Temporal transcriptome profiling reveals expression partitioning of homeologous genes contributing to heat and drought acclimation in wheat (Triticum aestivum L.). BMC Plant Biology 15:1-20. https://doi.org/10.1186/s12870-015-0511-8

Lynch M, Conery JS (2000). The Evolutionary fate and consequences of duplicate genes. Science 290:1151-1155. https://doi.org/10.1126/science.290.5494.1151

Mallory AC, Vaucheret H (2006). Functions of microRNAs and related small RNAs in plants. Nature Genetics 38:S37-S37. https://doi.org/10.1038/ng1791

Mao X, Cai T, Olyarchuk JG, Wei L (2005). Automated genome annotation and pathway identification using the KEGG orthology (KO) as a controlled vocabulary. Bioinformatics 21:3787-3793. https://doi.org/10.1093/bioinformatics/bti430

Mi S, Cai T, Hu Y, Chen Y, Hodges E, Ni F, ... Qi Y (2008). Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5’ terminal nucleotide. Cell 133:116-127. https://doi.org/10.1016/j.cell.2008.02.034

Montgomery TA, Howell MD, Cuperus JT, Li D, Hansen JE, Alexander AL, ... Carrington JC (2008). Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133:128-141. https://doi.org/10.1016/j.cell.2008.02.033

Ng DW, Lu J, Chen ZJ (2012). Big roles for small RNAs in polyploidy, hybrid vigor, and hybrid incompatibility. Current Opinion in Plant Biology 15:154-161. https://doi.org/10.1016/j.pbi.2012.01.007

Ozkan H, Levy AA, Feldman M (2001). Allopolyploidy-induced rapid genome evolution in the Wheat (Aegilops-Triticum) group. The Plant Cell 13:1735. https: //doi.org/10.2307/3871315

Peer YV, Mizrachi E, Marchal K (2017). The evolutionary significance of polyploidy. Nature Reviews Genetics 18:411-424. https://doi.org/10.1038/nrg.2017.26

Qiao X, Li Q, Yin H, Qi K, Li L, Wang R, ... Paterson AH (2019). Gene duplication and evolution in recurring polyploidization–diploidization cycles in plants. Genome Biology 20:38. https://doi.org/10.1186/s13059-019-1650-2

Ren YY, Chen L, Zhang YY, Kang XY, Zhang ZY, Wang YW (2012). Identification of novel and conserved Populus tomentosa microRNA as components of a response to water stress. Functional and Integrative Genomics 12:327-339. https://doi.org/10.1007/s10142-012-0271-6

Renny-Byfield S, Wendel JF (2014). Doubling down on genomes: polyploidy and crop plants. American Journal of Botany 101:1711-1725. https://doi.org/10.3732/ajb.1400119

Shi T, Rahmani RS, Gugger PF, Wang M, Li H, Zhang Y, … Chen J (2020). Distinct expression and methylation patterns for genes with different fates following a single whole-genome duplication in flowering plants. Molecular Biology and Evolution 37:2394-2413. https://doi.org/10.1093/molbev/msaa105

Soltis PS, Marchant DB, Van de Peer Y, Soltis DE (2015). Polyploidy and genome evolution in plants. Current Opinion in Genetics & Development 35:119-125. https://doi.org/10.1016/j.gde.2015.11.003

Stull GW, Qu XJ, Parins-Fukuchi C, Yang YY, Yang JB, Yang ZY, ... Yi TS (2021). Gene duplications and phylogenomic conflict underlie major pulses of phenotypic evolution in gymnosperms. Nature Plants 7:1015-1025. https://doi.org/10.1038/s41477-021-00964-4

Suo Y, Min Y, Dong C, Wang Y, Cheng S, Kang X (2017). MicroRNA expression changes following synthesis of three full-sib Populus triploid populations with diﬀerent heterozygosities. Plant Molecular Biology 95:215-225. https://doi.org/10.1007/s11103-017-0627-3

Vanneste K, Van de Peer Y, Maere S (2013). Inference of genome duplications from age distributions revisited. Molecular Biology and Evolution 30:177-190. https://doi.org/10.1093/molbev/mss214

Vazquez F, Legrand S, Windels D (2010). The biosynthetic pathways and biological scopes of plant small RNAs. Trends in Plant Science 15:337-345. https://doi.org/10.1371/journal.pone.0015224

Wang J, Tian L, Lee HS, Wei NE, Jiang H, Watson B, … Chen ZJ (2006). Genome wide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172:507-517. https://doi.org/10.1534/genetics.105.047894

Wang JL, Tian L, Madlung A, Lee HS, Chen M, Lee JJ, ... Chen ZJ (2004). Stochastic and epigenetic changes of gene expression in Arabidopsis polyploids. Genetics Society of America 167:1961-1973. https://doi.org/10.1534/genetics.104.027896

Wen M, Shen Y, Shi S, Tang T (2012). miREvo: An Integrative microRNA Evolutionary Analysis Platform for Next-generation Sequencing Experiments. BMC Bioinformatics 13:140. https://doi.org/10.1186/1471-2105-13-140

Wendel JF, Jackson SA, Meyers BC, Rod AW (2016). Evolution of plant genome architecture. Genome Biology 17:37. https://doi.org/10.1186/s13059-016-0908-1

Wendel JF, Jackson SA, Meyers BC, Wing RA (2016). Evolution of plant genome architecture. Genome Biology 17:37. https://doi.org/10.1186/s13059-016-0908-1

Wenkel S, Turck F, Singer K, Gissot L, Gourrierec JL, Samach A, Coupland G (2006). CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis. The Plant Cell 18:2971-2984. https://doi.org/10.1105/tpc.106.043299

Wu HJ, Ma YK, Chen T, Wang M, Wang XJ (2012). PsRobot: a web-based plant small RNA meta-analysis toolbox. Nucleic Acids Research 40:W22-W28. https://doi.org/10.1093/nar/gks554

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. https://doi.org/10.1016/j.molcel.2010.03.008

Xu MY, Zhang L, Li WW, Hu XL, Wang MB, Fan YL, ... Wang L (2013). Stress-induced early flowering is mediated by miR169 in Arabidopsis thaliana. Journal of Experimental Botany 65:89-101. https://doi.org/10.1093/jxb/ert353

Xu W, Guo L, Zhang Y, Zhao J, Wei Z, Zhang J (2019). An improved method for high-temperature induced embryo sac chromosome doubling in Populus simonii Carr. × P. nigra var. italica (Moench.) Kochne, an interspecifc hybrid of Tacamahaca and Aigeiros poplars. Scientific Reports 9:551. https://doi.org/10.1038/s41598-018-37297-w

Yoo MJ, Liu X, Pires C, Soltis PS, Soltis DE (2014). Nonadditive gene expression in polyploids. Annual Review of Genetics 48:485-517. https://doi.org/10.1146/annurev-genet-120213-092159

Zhang L, Zhao J, Bi H, Yang X, Zhang Z, Su Y, ... Ma T (2021) Bioinformatic analysis of chromatin organization and biased expression of duplicated genes between two poplars with a common whole-genome duplication. Horticulture Research 8:62. https://doi.org/10.1038/s41438-021-00494-2

Zhao B, Ge L, Liang R, Li W, Ruan K, Lin H, Jin Y (2009). Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Molecular Biology 10:29. https://doi.org/10.1186/1471-2199-10-29

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. https://doi.org/10.1105/tpc.15.00048

Zhou L, Chen J, Li Z, Li X, Hu X, Huang Y, ... Zhang X (2010). Integrated profiling of microRNAs and mRNAs: microRNAs located on Xq27.3 associate with clear cell renal cell carcinoma. PLoS One 5:e15224. https://doi.org/10.1371/journal.pone.0015224