Abstract
Polyploidization is an important feature of speciation that results from genome doubling. Tetraploid plants often have better physical characteristics than their diploid counterparts, and Paulownia is no exception. In our previous studies, several genes related to timber quality and abiotic stress resistance were identified in Paulownia tomentosa and Paulownia fortunei. However, the genes related to disease resistance and high biomass were not confirmed. In this study, small RNA and transcriptome sequencing were performed to analyze changes in microRNA (miRNA) and mRNA expression levels in tetraploid Paulownia tomentosa × Paulownia fortunei and Paulownia australis and their diploid counterparts. A total of 930 common differentially expressed genes and 66 (19 known and 47 novel) common differentially expressed miRNAs were detected in the two tetraploid vs. diploid comparisons. Twenty-two miRNA target genes were predicted, and the regulatory functions of the miRNA–target gene pairs were analyzed, of which the novel miR327- SGT1 HOMOLOG PROTEIN At5g65490 (PAU019930.1) and pau-miR2111a-MYB-RELATED TRANSCRIPTION FACTOR (PAU011118.1) interacting pairs were predicted to co-regulate disease resistance in tetraploid Paulownia. The pau-miR157i-SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE 15 (PAU009402.1) and novel miR10-PUTATIVE PENTATRICOPEPTIDE REPEAT-CONTAINING PROTEIN At5g65820 (PAU012281.1) interacting pairs were predicted to co-regulate high biomass in tetraploid Paulownia. The expression trends of the miRNA and candidate target genes were validated by qRT-PCR. The results will help to accelerate genetic gain in Paulownia breeding programs to develop superior varieties.
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References
Audic S, Claverie J (1997) The significance of digital gene expression profiles. Genom Res 7:986
Austin M, Muskett P, Kahn K, Feys B, Jones J, Parker J (2002) Regulatory role of SGT1 in early R gene-mediated plant defenses. Science 295:2077–2080
Axtell MJ, Meyers BC (2018) Revisiting criteria for plant miRNA annotation in the era of big data. Plant Cell 30(2):272–284
Azevedo C, Betsuyaku S, Peart J, Takahashi A, Noël L, Sadanandom A, Casais C, Parker J, Shirasu K (2014) Role of SGT1 in resistance protein accumulation in plant immunity. Embo J 25:2007–2016
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300
Broberg P (2005) A comparative review of estimates of the proportion unchanged genes and the false discovery rate. BMC Bioinformatics 6:199
Cao XB, Xu EK, Zhai XQ, Dong YP, Fan GQ (2017) Combined Analysis of mRNAs and miRNAs to identify genes related to biological characteristics of autotetraploid Paulownia. Forests 8:501
Choi JJ, Klosterman SJ, Hadwiger LA (2004) A promoter from pea gene DRR206 is suitable to regulate an elicitor-coding gene and develop disease resistance. Phytopathology 94:651–660
Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155-159
Deng MJ, Zhang XS, Fan GQ, Zhao ZL, Dong YP, Wei Z (2013a) Physiological responses to salt stress of tetraploid Paulownia australis and Paulownia fortunei plants. J Henan Agric Univ 47:698–702
Deng MJ, Zhang XS, Fan GQ, Zhao ZL, Dong YP, Wei Z (2013b) Comparative studies on physiological responses to salt stress in tetraploid Paulownia plants. J Cent South Univ For Technol 33:42–46
Denman RB (1993) Using RNAFOLD to predict the activity of small catalytic RNAs. Biotechniques 15:1090–1095
Dudits D, Torok K, Cseri A, Paul K, Nagy AV, Nagy B, Sass L, Ferenc G, Vankova R, Dobrev P (2016) Response of organ structure and physiology to autotetraploidization in early development of energy willow Salix viminalis. Plant Physiol 170:1504–1523
Fan GQ, Yang Z, Cao YC, Liu F, Jia F (2006) Autotetraploid induction of Paulownia elongata with colchine. J Nuclear Agric Sci 20:473–472
Fan GQ, Wei Z, Yang Z (2009) Induction of autotetraploid of Paulownia australis and its in vitro plantlet regeneration. J Northwest A & F Univ 37:83–90
Fan GQ, Wang LM, Dong YP, Zhao ZL, Deng MJ, Niu SY, Zhang XS, Cao XB (2017) Genome of Paulownia (Paulownia fortunei) illuminates the related transcripts, miRNA and proteins for salt resistance. Sci Rep 7:1285
Haunsberger SJ, Connolly NMC, Prehn JHM (2017) miRNA meConverter: an R/Bioconductor package for translating mature miRNA names to different miRBase versions. Bioinformatics 33:592–593
He J, Xu M, Willmann MR, Mccormick K, Hu T, Yang L, Starker CG, Voytas DF, Meyers BC, Poethig RS (2018) Threshold-dependent repression of SPL gene expression by miR156/miR157 controls vegetative phase change in Arabidopsis thaliana. PLoS Genet 14:e1007337.
Hwang IS, Hwang BK (2010) Role of the pepper cytochrome P450 gene CaCYP450A in defense responses against microbial pathogens. Planta 232:1409–1421
Jiang J, Yue W, Bao Z, Fang T, Fang Y, Wang Y (2015) Digital gene expression analysis of gene expression differences within Brassica diploids and allopolyploids. BMC Plant Biol 15:22
Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J (2005) Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462–467
Kong W, Yu X, Chen H, Liu L, Xiao Y, Wang Y, Wang C, Lin Y, Yu Y, Wang C (2016) The catalytic subunit of magnesium-protoporphyrin IX monomethyl ester cyclase forms a chloroplast complex to regulate chlorophyll biosynthesis in rice. Plant Mol Biol 92:177–191
Krikorian AD (1988) Paulownia in China: cultivation and utilization. Econ Bot 42:283–283
Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323
Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25:1966–1967
Li YS, Fan GQ, Dong YP, Zhao ZL, Deng MJ, Cao XB, Xu EK, Niu S (2014) Identification of genes related to the phenotypic variations of a synthesized Paulownia (Paulownia tomentosa× Paulownia fortunei) autotetraploid. Gene 553:75–83
Liu Y, Shi C, Mu X, Chao L, Ke S, Zhu W, Yang Q (2015) Cloning and expression of a wild eggplant cytochrome P450 gene, StoCYP77A2, involved in plant resistance to Verticillium dahliae. Plant Biotechnol Rep 9:167–177
Liu N, Tu L, Wang L, Hu H, Xu J, Zhang X (2017) MicroRNA 157-targeted SPL genes regulate floral organ size and ovule production in cotton. Bmc Plant Biol 17:7
Manning K, Tör M, Poole M, Hong Y, Thompson AJ, King GJ, Giovannoni JJ, Seymour GB (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet 38:948–952
Masterson J (1994) Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264:421–424
Mei W, Liu S, Schnable JC, Yeh CT, Springer NM, Schnable PS, Barbazuk WB (2017) A comprehensive analysis of alternative splicing in paleopolyploid Maize. Front Plant Sci 8:694
Mortazavi A, Williams BA, Mccue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621
Murashige T, Skoog F (2010) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497
Nakamura H, Muramatsu M, Hakata M, Ueno O, Nagamura Y, Hirochika H, Takano M, Ichikawa H (2009) Ectopic overexpression of the transcription factor OsGLK1 induces chloroplast development in non-green rice cells. Plant Cell Physiol 50:1933–1949
Nawrocki EP, Burge SW, Bateman A, Daub J, Eberhardt RY, Eddy SR, Floden EW, Gardner PP, Jones TA, Tate J (2015) Rfam 12.0: updates to the RNA families database. Nucleic Acids Res 43:D130-137
Niu S, Fan G, Xu E, Deng M, Zhao Z, Dong Y (2014) Transcriptome/degradome-wide discovery of microRNAs and transcript targets in two Paulownia australis genotypes. PLoS ONE 9:e106736
Pruitt KD, Tatusova T, Maglott DR (2005) NCBI Reference Sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 33:D501–D504
Ranaeisiadat E, Fabret C, Seijo B, Dardel F, Grosjean H, Noninlecomte S (2013) RNA- methyltransferase TrmA is a dual-specific enzyme responsible for C5-methylation of uridine in both tmRNA and tRNA. RNA Biol 10:572–578
Saminathan T, Nimmakayala P, Manohar S, Malkaram S, Almeida A, Cantrell R, Tomason Y, Abburi L, Rahman MA, Vajja VG (2015) Differential gene expression and alternative splicing between diploid and tetraploid watermelon. J Exp Bot 66:1369–1385
Schwartz SH, Léon-Kloosterziel KM, Koornneef M, Zeevaart JA (1997) Biochemical characterization of the aba2 and aba3 mutants in Arabidopsis thaliana. Plant Physiol 114:161–166
Seneviratne HK, Dalisay DS, Kim KW, Moinuddin SG, Yang H, Hartshorn CM, Davin LB, Lewis NG (2015) Non-host disease resistance response in pea (Pisum sativum) pods: biochemical function of DRR206 and phytoalexin pathway localization. Phytochemistry 113:140–148
Seo PJ, Park CM (2010) MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis. New Phytol 186:471–483
Shan T, Wei R, Xu H, Du L, Liu X, Zhang Z (2016) The wheat R2R3-MYB transcription factor TaRIM1 participates in resistance response against the pathogen Rhizoctonia cerealis infection through regulating defense genes. Sci Rep 6:28777
Shikata M, Yamaguchi H, Sasaki K, Ohtsubo N (2012) Overexpression of Arabidopsis miR157b induces bushy architecture and delayed phase transition in Torenia fournieri. Planta 236:1027–1035
Su N, Hu M, Wu D, Wu F, Fei G, Lan Y, Chen X, Shu X, Zhang X, Guo X (2012) Disruption of a rice pentatricopeptide repeat protein causes a seedling-specific albino phenotype and its utilization to enhance seed purity in hybrid rice production. Plant Physiol 159:227–238
Tamayo-Ordóñez MC, Espinosa-Barrera LA, Tamayo-Ordóñez YJ, Ayil-Gutiérrez B, Sánchez- Teyer LF (2016) Advances and perspectives in the generation of polyploid plant species. Euphytica 209:1–22
Tatusov RL, Galperin MY, Natale DA, Koonin EV (2000) The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28:33–36
Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105–1111
Wang Y, Nowak G, Culley D, Hadwiger LA, Fristensky B (1999) Constitutive expression of pea defense gene DRR206 confers resistance to blackleg (Leptosphaeria maculans) disease in transgenic canola (Brassica napus). Mol Plant Microbe Interact 12:410–418
Wang JW, Park MY, Wang LJ, Koo Y, Chen XY, Weigel D, Poethig RS (2011) MiRNA control of vegetative phase change in trees. PLoS Genet 7:e1002012
Wang Y, Zhang XS, Deng MJ, Zhao ZL, Fan GQ (2013) Study on photosynthetic characteristics of diploid and tetraploid Paulownia australis. J Jiangxi Agric 25:39–42
Wang XD, Zhao ZL, Fan GQ, Zhang XS, Wang AT, Li YS, Wang AT (2014) The growth characteristics of five different varieties of tetraploid Paulownia. J West China For Sci 4:72–77
Wang M, Wang P, Liang F, Ye Z, Li J, Shen C, Pei L, Wang F, Hu J, Tu L, Lindsey K, He D, Zhang X (2017a) A global survey of alternative splicing in allopolyploid cotton: landscape, complexity and regulation. New Phytol 217:163–178
Wang Y, Ding G, Gu T, Ding J, Li Y (2017b) Bioinformatic and expression analyses on carotenoid dioxygenase genes in fruit development and abiotic stress responses in Fragaria vesca. Mol Genet Genom 292:895–907
Wang Z, Fan GQ, Dong YP, Zhai XQ, Deng MJ, Zhao ZL, Liu WS, Cao Y (2017c) Implications of polyploidy events on the phenotype, microstructure, and proteome of Paulownia australis. PLoS ONE 12:e0172633
Wu HJ, Ma YK, Chen T, Wang M, Wang XJ (2012) PsRobot: a web-based plant small RNA meta-analysis toolbox. Nucleic Acids Res 40:22–28
Wu S, Ren X, Li Y, Guo W, Lei X, Yao J, Yang X (2017) Effect of dietary astragalus polysaccharide supplements on testicular miRNA expression profiles and enzymatic changes of breeder cocks. Sci Rep 7:38864
Xu EK, Fan GQ, Niu SY, Zhao ZL, Deng MJ, Dong YP (2015) Transcriptome sequencing and comparative analysis of diploid and autotetraploid Paulownia australis. Tree Genet Genom 11:1–13
Yang L, Lou Y, Peng Z, Zhao H, Sun H, Gao Z (2015) Molecular characterization and primary functional analysis of PeMPEC, a magnesium-protoporphyrin IX monomethyl ester cyclase gene of bamboo (Phyllostachys edulis). Plant Cell Rep 34:2001–2011
Ye J, McGinnis S, Madden TL (2006) BLAST: improvements for better sequence analysis. Nucleic acids Res 34:W6–W9
Zhai XQ, Niu SY, Ren YY, Fan GQ (2016) Discovery and profiling of microRNAs and their targets in Paulownia ‘Yuza 1’ plants via high-throughput sequencing and degradome analysis. Gene Genom 38:757–766
Zhang XS, Zhai XQ, Fan GQ, Deng MJ, Zhao ZL (2012) Observation on microstructure of leaves and stress tolerance analysis of different tetraploid Paulownia. J Henan Agric Univ 46:646–650
Zhang XS, Fan GQ, Zhao ZL, Cao XB, Zhao GL, Deng MJ, Dong YP (2013a) Analysis of diploid and its autotetraploid Paulownia tomentosa ×Paulownia fortunei with AFLP and MSAP. Sci Silv Sin 49:167–172
Zhang XS, Liu RN, Fan GQ, Zhao ZL, Deng MJ (2013b) Study on the physiological response of tetraploid Paulownia to drought. J Henan Agric Univ 47:543–547
Zhang XS, Zhai XQ, Deng MJ, Dong YP, Zhao ZL, Fan GQ (2013c) Comparative Studies on physiological responses of diploid paulownia and its tetraploid to drought stress. J Henan Agric Univ 42:118–123
Zhang XS, Zhai XQ, Zhao ZL, Deng MJ, Fan GQ (2013d) Study on the photosynthetic characteristics of different species of tetraploid Paulownia plants. J Henan Agric Univ 47:400–404
Zhang J, Xiao J, Li YQ, Su BD, Xu HM, Shan XY, Song CW, Xie JB, Li RL (2017) PDM3, a pentatricopeptide repeat-containing protein, affects chloroplast development. J Exp Bot 68:5615–5627
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We would like to thank Margaret Biswas, PhD, from Liwen Bianji, Edanz Group China (www.liwenbianji.cn/ac), for editing the English text of this manuscript.
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Supplementary file1 Online Resource 1: Table S1 Primers of DEGs and DEMs for qRT-PCR analysis. Online Resource 1: Table S2 Statistics of clean reads mapped to reference gene and genome. Online Resource 1: Table S3 The common expression DEGs in the two diploid and tetraploid paulownia species. Online Resource 1: Table S4 The DEGs matched to the alternative splicing event corresponding genes. Online Resource 1: Table S5 Classification of Paulownia’ RNAs of diploid and tetraploid libraries *: unannotated. Online Resource 1: Table S6 Known miRNA in the two tetraploid and diploid paulownias. Online Resource 1: Table S7 New miRNA in the two tetraploid and diploid paulownias. Online Resource 1: Table S8 Common expression known DEMs in the two tetraploid and diploid paulownias. Online Resource 1: Table S9 Common expression new DEMs in the two tetraploid and diploid paulownias (7Z 294 KB)
11738_2020_3160_MOESM2_ESM.7z
Supplementary file2 Online Resource 2:Figure S1 Correlation coefficients of the gene expression of duplicate samples. Online Resource 2: Figure S2 The DEGs in the two tetraploid and diploid paulownias. Online Resource 2: Figure S3 The number of alternative splicing events and their corresponding genes. Online Resource 2: Figure S4 The pictures of the RNA separation and spectrophotometer measurements results A: The picture of RNA separations of PA2 and PA4 with three biological replicates, B: The picture of RNA separations of PTF2 and PTF4 with three biological replicates, C: The results of RNA concentrations and qualities measurements of the two diploid and tetraploid paulownias. Online Resource 2:Figure S1 Correlation coefficients of the gene expression of duplicate samples. Online Resource 2: Figure S2 The DEGs in the two tetraploid and diploid paulownias. Online Resource 2: Figure S3 The number of alternative splicing events and their corresponding genes. Online Resource 2: Figure S4 The pictures of the RNA separation and spectrophotometer measurements results A: The picture of RNA separations of PA2 and PA4 with three biological replicates, B: The picture of RNA separations of PTF2 and PTF4 with three biological replicates, C: The results of RNA concentrations and qualities measurements of the two diploid and tetraploid paulownias. (7Z 195 KB)
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Cao, X., Zhai, X., Xu, E. et al. Genome-wide identification of candidate genes related to disease resistance and high biomass in tetraploid Paulownia. Acta Physiol Plant 42, 171 (2020). https://doi.org/10.1007/s11738-020-03160-7
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DOI: https://doi.org/10.1007/s11738-020-03160-7