Abstract
Plant microRNAs (miRNA) act as important regulators of gene expression and carry potential uses in plant genetic engineering. Lignin is an abundant biopolymer in plants, conferring strength to the cell wall. Most of the recalcitrance of the lignocellulosic biomass to produce biofuels is due to the chemical nature of lignin and its interaction with the other components of the cell wall. Thus, understanding lignin biosynthesis and deposition is crucial for the biofuel industry, and interfering in RNA (iRNA) may be a valuable tool to produce transgenic plants with reduced lignin concentration and/or modified composition. Here we report on the miRNA profile of Eucalyptus grandis and E. globulus in which 28 conserved and 19 novel miRNAs were found. We identified 316 putative targets of known and 110 putative targets of novel miRNAs. No significant differences in miRNA expression were found between tension and opposite wood samples. Gene Ontology enrichment analysis returned several attractive targets for identified miRNAs, among which are laccases and transcription factors that may regulate the expression of lignin biosynthesis.
Similar content being viewed by others
Data availability
The data set of microRNA sequencing are available under request.
References
Abdel-Ghany SE, Pilon M (2008) MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. J Biol Chem 283:15932–15945. https://doi.org/10.1074/jbc.M801406200
Aguayo MG, Quintupill L, Castillo R et al (2010) Determination of differences in anatomical and chemical characteristics of tension and opposite wood of 8-year old Eucalyptus globulus. Maderas Cienc y Tecnol 12:241–251
Al-Haddad JM, Kang K-Y, Mansfield SD, Telewski FW (2013) Chemical responses to modified lignin composition in tension wood of hybrid poplar (Populus tremula × Populus alba). Tree Physiol 33:365–373. https://doi.org/10.1093/treephys/tpt017
Alexa A, Rahnenführer J (2009) Gene set enrichment analysis with topGO. Bioconductor Improv 27:1–26
Ambawat S, Sharma P, Yadav NR, Yadav RC (2013) MYB transcription factor genes as regulators for plant responses: an overview. Physiol Mol Biol plants an Int J Funct plant Biol 19:307–321. https://doi.org/10.1007/s12298-013-0179-1
Anders S, Huber W (2012) Differential expression of RNA-Seq data at the gene level–the DESeq package. https://rdrr.io/bioc/DESeq/f/inst/doc/DESeq.pdf
Andrews S (2017) FASTQC. A quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/
Aoyama W, Matsumura A, Tsutsumi Y, Nishida T (2001) Lignification and peroxidase in tension wood of Eucalyptus viminalis seedlings. J Wood Sci 47:419–424. https://doi.org/10.1007/BF00767892
Aparicio-Puerta E, Lebrón R, Rueda A et al (2019) sRNAbench and sRNAtoolbox 2019: intuitive fast small RNA profiling and differential expression. Nucleic Acids Res 47:W530–W535. https://doi.org/10.1093/nar/gkz415
Axtell MJ, Westholm JO, Lai EC (2011) Vive la différence: biogenesis and evolution of microRNAs in plants and animals. Genome Biol 12:221. https://doi.org/10.1186/gb-2011-12-4-221
Bahin M, Noël BF, Murigneux V et al (2019) ALFA: annotation landscape for aligned reads. BMC Genomics 20:250. https://doi.org/10.1186/s12864-019-5624-2
Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297. https://doi.org/10.1016/S0092-8674(04)00045-5
Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546. https://doi.org/10.1146/annurev.arplant.54.031902.134938
Bonawitz ND, Chapple C (2010) The genetics of lignin biosynthesis: Connecting genotype to phenotype. Annu Rev Genet 44:337–363. https://doi.org/10.1146/annurev-genet-102209-163508
Borges F, Martienssen RA (2015) The expanding world of small RNAs in plants. Nat Rev Mol Cell Biol 16:727–741. https://doi.org/10.1038/nrm4085
Brereton NJB, Ahmed F, Sykes D et al (2015) X-ray micro-computed tomography in willow reveals tissue patterning of reaction wood and delay in programmed cell death. BMC Plant Biol 15:83. https://doi.org/10.1186/s12870-015-0438-0
Camacho C, Coulouris G, Avagyan V et al (2009) BLAST+: architecture and applications. BMC Bioinformatics 10:421. https://doi.org/10.1186/1471-2105-10-421
Cesarino I, Araújo P, Domingues AP Jr, Mazzafera P (2012) An overview of lignin metabolism and its effect on biomass recalcitrance. Rev Bras Bot 35:303–311
Chen Z-H, Bao M-L, Sun Y-Z et al (2011) Regulation of auxin response by miR393-targeted transport inhibitor response protein1 is involved in normal development in Arabidopsis. Plant Mol Biol 77:619–629. https://doi.org/10.1007/s11103-011-9838-1
Cui J, You C, Chen X (2017) The evolution of microRNAs in plants. Curr Opin Plant Biol 35:61–67. https://doi.org/10.1016/j.pbi.2016.11.006
Curaba J, Talbot M, Li Z, Helliwell C (2013) Over-expression of microRNA171 affects phase transitions and floral meristem determinancy in barley. BMC Plant Biol 13:6. https://doi.org/10.1186/1471-2229-13-6
Dai X, Zhuang Z, Zhao PX (2018) psRNATarget: a plant small RNA target analysis server (2017 release). Nucleic Acids Res 46:W49–W54. https://doi.org/10.1093/nar/gky316
Ding C, Shen T, Ran N et al (2022) Integrated degradome and Srna sequencing revealed miRNA-mRNA regulatory networks between the phloem and developing xylem of poplar. Int J Mol Sci 23:4537. https://doi.org/10.3390/ijms23094537
Dong H, Lei J, Ding L et al (2013) MicroRNA: function, detection, and bioanalysis. Chem Rev 113:6207–6233. https://doi.org/10.1021/cr300362f
Du J, Groover A (2010) Transcriptional regulation of secondary growth and wood formation. J Integr Plant Biol 52:17–27. https://doi.org/10.1111/j.1744-7909.2010.00901.x
Du S, Yamamoto F (2007) An overview of the biology of reaction wood formation. J Integr Plant Biol 49:131–143. https://doi.org/10.1111/j.1744-7909.2007.00427.x
Ewels P, Magnusson M, Lundin S, Käller M (2016) MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics 32:3047–3048. https://doi.org/10.1093/bioinformatics/btw354
Ferreira V, Boyero L, Calvo C et al (2019) A global assessment of the effects of eucalyptus plantations on stream ecosystem functioning. Ecosystems 22:629–642. https://doi.org/10.1007/s10021-018-0292-7
Gaddam SR, Bhatia C, Gautam H et al (2022) Ethylene regulates miRNA-mediated lignin biosynthesis and leaf serration in Arabidopsis thaliana. Biochem Biophys Res Commun 605:51–55. https://doi.org/10.1016/J.BBRC.2022.03.037
Grattapaglia D, Kirst M (2008) Eucalyptus applied genomics: from gene sequences to breeding tools. New Phytol 179:911–929. https://doi.org/10.1111/j.1469-8137.2008.02503.x
Guan X, Pang M, Nah G et al (2014) miR828 and miR858 regulate homoeologous MYB2 gene functions in Arabidopsis trichome and cotton fibre development. Nat Commun 5:3050. https://doi.org/10.1038/ncomms4050
Guo C, Xu Y, Shi M et al (2017) Repression of miR156 by miR159 regulates the timing of the juvenile-to-adult transition in Arabidopsis. Plant Cell 29:1293–1304. https://doi.org/10.1105/tpc.16.00975
Ha M, Kim VN (2014) Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol 15:509–524. https://doi.org/10.1038/nrm3838
Harakava R (2005) Genes encoding enzymes of the lignin biosynthesis pathway in Eucalyptus. enetics Mol Biol 28:601–607
He L, Hannon GJ (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5:522–531. https://doi.org/10.1038/nrg1379
Hirsch S, Oldroyd GED (2009) GRAS-domain transcription factors that regulate plant development. Plant Signal Behav 4:698–700. https://doi.org/10.4161/psb.4.8.9176
Hossain MS, Hoang NT, Yan Z et al (2019) Characterization of the spatial and temporal expression of two soybean miRNAs identifies SCL6 as a novel regulator of soybean nodulation. Front Plant Sci 10:475
Iwakawa H, Tomari Y (2015) The functions of microRNAs: mRNA decay and translational repression. Trends Cell Biol 25:651–665. https://doi.org/10.1016/j.tcb.2015.07.011
Jiang N, Meng J, Cui J et al (2018) Function identification of miR482b, a negative regulator during tomato resistance to Phytophthora infestans. Hortic Res 5:9. https://doi.org/10.1038/s41438-018-0017-2
Johansen DA (1940) Plant Microtechnique. (McGraw-Hill Publications in the Botanical Sciences). McGraw-Hill Book Co., Inc., New York and London
Kalvari I, Argasinska J, Quinones-Olvera N et al (2018) Rfam 13.0: shifting to a genome-centric resource for non-coding RNA families. Nucleic Acids Res 46:D335–D342. https://doi.org/10.1093/nar/gkx1038
Karlova R, van Haarst JC, Maliepaard C et al (2013) Identification of microRNA targets in tomato fruit development using high-throughput sequencing and degradome analysis. J Exp Bot 64:1863–1878. https://doi.org/10.1093/jxb/ert049
Kopylova E, Noé L, Touzet H (2012) SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 28:3211–3217. https://doi.org/10.1093/bioinformatics/bts611
Koyama T, Sato F, Ohme-Takagi M (2017) Roles of miR319 and TCP transcription factors in leaf development. Plant Physiol 175:874–885. https://doi.org/10.1104/pp.17.00732
Kozomara A, Birgaoanu M, Griffiths-Jones S (2019) miRBase: from microRNA sequences to function. Nucleic Acids Res 47:D155–D162. https://doi.org/10.1093/nar/gky1141
Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25. https://doi.org/10.1186/gb-2009-10-3-r25
Levy A, Szwerdszarf D, Abu-Abied M et al (2014) Profiling microRNAs in Eucalyptus grandis reveals no mutual relationship between alterations in miR156 and miR172 expression and adventitious root induction during development. BMC Genomics 15:524. https://doi.org/10.1186/1471-2164-15-524
Li H, Handsaker B, Wysoker A et al (2010) 1000 genome project data processing subgroup. The sequence alignment/map (SAM) format and SAMtools. Bioinformatics 25:2078–2079
Lin Z, Li Q, Yin Q et al (2018) Identification of novel miRNAs and their target genes in Eucalyptus grandis. Tree Genet Genomes 14:60. https://doi.org/10.1007/s11295-018-1273-x
Lu S, Li Q, Wei H et al (2013) Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa. Proc Natl Acad Sci 110: 10848–10853. https://doi.org/10.1073/pnas.1308936110
Lu S, Sun Y-H, Shi R et al (2005) Novel and mechanical stress–responsive microRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell 17:2186–2203. https://doi.org/10.1105/tpc.105.033456
Ma Z, Hu X, Cai W et al (2014) Arabidopsis miR171-targeted scarecrow-like proteins bind to GTcis-elements and mediate gibberellin-regulated chlorophyll biosynthesis under light conditions. PLos Genet 10:e1004519
Martin M (2011) CUTADAPT removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10
Mattinen M-L, Suortti T, Gosselink RJA et al (2008) Polymerization of different lignins by laccase. BioResources 3:549–565
McNair GR (2009) Whole-tree and tension wood-associated expression profiles of microRNAs in Eucalyptus trees. University of Pretoria, Pretoria, South Africa
Moura JCMSJCMS, Bonine CAVCAV, Oliveira JFV et al (2010) Abiotic and Biotic Stresses and Changes in the Lignin Content and Composition in Plants. J Integr Plant Biol 52:360–376. https://doi.org/10.1111/j.1744-7909.2010.00892.x
Myburg AA, Grattapaglia D, Tuskan GA et al (2014) The genome of Eucalyptus grandis. Nature 510:356–362. https://doi.org/10.1038/nature13308
Nakhooda M, Jain SM (2016) A review of eucalyptus propagation and conservation. Propag Ornam Plants 16:101–119
Ong SS, Wickneswari R (2011) Expression profile of small RNAs in Acacia mangium secondary xylem tissue with contrasting lignin content - potential regulatory sequences in monolignol biosynthetic pathway. BMC Genomics 12:S13. https://doi.org/10.1186/1471-2164-12-S3-S13
Pappas M, de Pappas CR, Grattapaglia GJ et al (2015) Genome-wide discovery and validation of Eucalyptus small RNAs reveals variable patterns of conservation and diversity across species of Myrtaceae. BMC Genomics 16:1113. https://doi.org/10.1186/s12864-015-2322-6
Pilate G, Chabbert B, Cathala B et al (2004) Lignification and tension wood. C R Biol 327:889–901. https://doi.org/10.1016/j.crvi.2004.07.006
Quang TH, Hallingbäck H, Gyllenstrand N et al (2012) Expression of genes of cellulose and lignin synthesis in Eucalyptus urophylla and its relation to some economic traits. Trees 26:893–901. https://doi.org/10.1007/s00468-011-0664-5
Ranocha P, Chabannes M, Chamayou S et al (2002) Laccase Down-Regulation Causes Alterations in Phenolic Metabolism and Cell Wall Structure in Poplar. Plant Physiol 129 145 LP – 155. https://doi.org/10.1104/pp.010988
Rogers LA, Dubos C, Cullis IF et al (2005) Light, the circadian clock, and sugar perception in the control of lignin biosynthesis. J Exp Bot 56:1651–1663. https://doi.org/10.1093/jxb/eri162
Saadaoui E, Ben Yahia K, Dhahri S et al (2017) An overview of adaptative responses to drought stress in spp. For Stud 67:86–96. https://doi.org/10.1515/fsmu-2017-0014
Sanei M, Chen X (2015) Mechanisms of microRNA turnover. Curr Opin Plant Biol 27:199–206. https://doi.org/10.1016/j.pbi.2015.07.008
Schommer C, Palatnik JF, Aggarwal P et al (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol 6:e230. https://doi.org/10.1371/journal.pbio.0060230
Sharma D, Tiwari M, Pandey A et al (2016) MicroRNA858 is a potential regulator of phenylpropanoid pathway and plant development. Plant Physiol 171:944–959. https://doi.org/10.1104/pp.15.01831
Si-Ammour A, Windels D, Arn-Bouldoires E et al (2011) miR393 and secondary siRNAs regulate expression of the TIR1/AFB2 auxin receptor clade and auxin-related development of Arabidopsis leaves. Plant Physiol 157:683–691. https://doi.org/10.1104/pp.111.180083
Strohm A, Baldwin K, Masson P (2012) Multiple roles for membrane-associated protein trafficking and signaling in gravitropism. Front. Plant Sci 3:274
Tocquard K, Lopez D, Decourteix M et al (2014) The molecular mechanisms of reaction wood induction. In: Gardiner B, Barnett J, Saranpää P, Gril J (eds) The biology of reaction wood. Springer, pp 107–138
Unnikrishnan BV, Shankaranarayana GD (2020) Insights into microRNAs and their targets associated with lignin composition in Eucalyptus camaldulensis. Plant Gene 24:100248. https://doi.org/10.1016/j.plgene.2020.100248
Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687. https://doi.org/10.1016/j.cell.2009.01.046
Wang C-Y, Zhang S, Yu Y et al (2014) MiR397b regulates both lignin content and seed number in Arabidopsis via modulating a laccase involved in lignin biosynthesis. Plant Biotechnol J 12:1132–1142. https://doi.org/10.1111/pbi.12222
Wang J-W, Park MY, Wang L-J et al (2011) MiRNA control of vegetative phase change in trees. PLOS Genet 7:e1002012
Weng J-K, Chapple C (2010) The origin and evolution of lignin biosynthesis. New Phytol 187:273–285. https://doi.org/10.1111/j.1469-8137.2010.03327.x
Xie M, Zhang S, Yu B (2015) microRNA biogenesis, degradation and activity in plants. Cell Mol Life Sci 72:87–99. https://doi.org/10.1007/s00018-014-1728-7
Xing L, Zhang D, Li Y et al (2014) Genome-wide identification of vegetative phase transition-associated microRNAs and target predictions using degradome sequencing in Malus hupehensis. BMC Genomics 15:1125. https://doi.org/10.1186/1471-2164-15-1125
Yanhui C, Xiaoyuan Y, Kun H et al (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol Biol 60:107–124. https://doi.org/10.1007/s11103-005-2910-y
Zhan N, Wang Z, Xie Y et al (2021) Expression patterns and regulation of non-coding RNAs during synthesis of cellulose in Eucalyptus grandis Hill. Forests 12:1565. https://doi.org/10.3390/f12111565
Zhang L, Ge X, Du J et al (2021) Genome-wide identification of long non-coding RNAs and their potential functions in poplar growth and phenylalanine biosynthesis. Front Genet 12. https://doi.org/10.3389/fgene.2021.762678
Zhao Q, Nakashima J, Chen F et al (2013) LACCASE is necessary and nonredundant with PEROXIDASE for lignin polymerization during vascular development in Arabidopsis. Plant Cell 25:3976–3987. https://doi.org/10.1105/tpc.113.117770
Zhao W, Meng X, Xu J et al (2022) Integrated mRNA and small RNA sequencing reveals microRNAs associated with xylem development in Dalbergia odorifera. Front Genet 13. https://doi.org/10.3389/fgene.2022.883422
Acknowledgements
This work was partially granted by São Paulo Foundation (FAPESP grants − 2011/51949-5 and 2014/23230-4). PM thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq-Brazil) for a research fellowship.
Author information
Authors and Affiliations
Contributions
FTT, AAV and URS carried out the experiments and analysis, GAGP and MFC helped in the bioinformatic analysis, PM designed the research, FTT, AAV and PM wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
There is no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
40626_2022_259_MOESM1_ESM.png
Supplementary material 1 Fig. S1 Stem was bent to 45° using a metal rod to induce lignification using the reaction wood model. Stems were stained with phloroglucinol-HCl for lignin visualization (E. grandis A and B; E. globulus C and D) and lignin concentration was determined in control, tension wood (TW) and opposite wood (OW). (PNG 422.0 kb)
40626_2022_259_MOESM2_ESM.png
Supplementary material 2 Fig. S2 Putative target enzyme differential expression E. globulus (a) and E. grandis (b). The heatmap shows upregulation in darker blue and downregulation in darker red. (Blank cells for PRXs refer to enzymes that have not been named in the Peroxibase database) (PNG 87.0 kb)
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Tolentino, F.T., Vasconcelos, A.A., Souza, U.R. et al. Identification of microRNAs and their expression profiles on tension and opposite wood of Eucalyptus. Theor. Exp. Plant Physiol. 34, 485–500 (2022). https://doi.org/10.1007/s40626-022-00259-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40626-022-00259-9