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Abstract:

MicroRNAs (miRNAs) are short, single stranded RNA molecules that regulate the stability and translation of messenger RNAs in diverse eukaryotic groups. Several miRNA genes are of ancient origin and have been maintained in the genomes of animal and plant taxa for hundreds of millions of years, playing key roles in development and physiology. In the last decade, genome and small RNA (sRNA) sequencing of several plant species have helped unveil the evolutionary history of land plants. Among these, the fern group (monilophytes) occupies a key phylogenetic position, as it represents the closest extant cousin taxon of seed plants, i.e. gymno-and angiosperms. However, in spite of their evolutionary, economic and ecological importance, no fern genome has been sequenced yet and few genomic resources are available for this group. Here, we sequenced the small RNA fraction of an epiphytic South American fern, Pleopeltis minima (Polypodiaceae), and compared it to plant miRNA databases, allowing for the identification of miRNA families that are shared by all land plants, shared by all vascular plants (tracheophytes) or shared by euphyllophytes (ferns and seed plants) only. Using the recently described transcriptome of another fern, Lygodium japonicum, we also estimated the degree of conservation of fern miRNA targets in relation to other plant groups. Our results pinpoint the origin of several miRNA families in the land plant evolutionary tree with more precision and are a resource for future genomic and functional studies of fern miRNAs. © 2017 Berruezo et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Registro:

Documento: Artículo
Título:Sequencing of small RNAs of the fern Pleopeltis minima (Polypodiaceae) offers insight into the evolution of the microrna repertoire in land plants
Autor:Berruezo, F.; De Souza, F.S.J.; Picca, P.I.; Nemirovsky, S.I.; Tosar, L.M.; Rivero, M.; Mentaberry, A.N.; Zelada, A.M.
Filiación:Laboratorio de Agrobiotecnología, Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Instituto de Investigaciones en Ingenieria Gene Tica y Biologia Molecular Dr Hector N. Torres, Buenos Aires, Argentina
Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Instituto de Química Biológica, Facultad de Ciencias Exactas y Naturales (IQUIBICEN, CONICET-UBA), Universidad de Buenos Aires, Buenos Aires, Argentina
Instituto de Biodiversidad y Biología Experimental y Aplicada, Consejo Nacional de Investigaciones Científicas y Técnicas-Universidad de Buenos Aires, Buenos Aires, Argentina
Instituto de Agrobiotecnología de Rosario (INDEAR), Rosario, Santa Fe, Argentina
Palabras clave:microRNA; plant RNA; transcriptome; messenger RNA; microRNA; plant RNA; Article; Embryophyta; euphyllophyte; fern; functional genomics; genetic conservation; Lygodium japonicum; nonhuman; phylogenetic tree; Pleopeltis minima; Polypodiaceae; protein family; RNA analysis; RNA sequence; seed plant; South American; vascular plant; conserved sequence; genetics; metabolism; molecular evolution; nucleotide sequence; phylogeny; procedures; sequence analysis; Base Sequence; Conserved Sequence; Evolution, Molecular; Ferns; MicroRNAs; Phylogeny; RNA, Messenger; RNA, Plant; Sequence Analysis, RNA
Año:2017
Volumen:12
Número:5
DOI: http://dx.doi.org/10.1371/journal.pone.0177573
Título revista:PLoS ONE
Título revista abreviado:PLoS ONE
ISSN:19326203
CODEN:POLNC
CAS:MicroRNAs; RNA, Messenger; RNA, Plant
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_19326203_v12_n5_p_Berruezo

Referencias:

  • Kenrick, P., Crane, P.R., The origin and early evolution of plants on land (1997) Nature, 389, pp. 33-39
  • Becker, B., Marin, B., Streptophyte algae and the origin of embryophytes (2009) Ann Bot., 103, pp. 999-1004. , https://doi.org/10.1093/aob/mcp044, PMID: 19273476
  • Pires, N.D., Dolan, L., Morphological evolution in land plants: New designs with old genes (2012) Philos Trans R Soc Lond B Biol Sci., 367, pp. 508-518. , https://doi.org/10.1098/rstb.2011.0252, PMID: 22232763
  • Rensing, S.A., Lang, D., Zimmer, A.D., Terry, A., Salamov, A., Shapiro, H., The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants (2008) Science., 319, pp. 64-69. , https://doi.org/10.1126/science.1150646, PMID: 18079367
  • Banks, J.A., Nishiyama, T., Hasebe, M., Bowman, J.L., Gribskov, M., DePamphilis, C., The Selaginella genome identifies genetic changes associated with the evolution of vascular plants (2011) Science., 332, pp. 960-963. , https://doi.org/10.1126/science.1203810, PMID: 21551031
  • Nystedt, B., Street, N.R., Wetterbom, A., Zuccolo, A., Lin, Y.C., Scofield, D.G., The Norway spruce genome sequence and conifer genome evolution (2013) Nature., 497, pp. 579-584. , https://doi.org/10.1038/nature12211, PMID: 23698360
  • Birol, I., Raymond, A., Jackman, S.D., Assembling the 20 Gb white spruce (Picea glauca) genome from whole-genome shotgun sequencing data (2013) Bioinformatics., 29, pp. 1492-1497. , https://doi.org/10.1093/bioinformatics/btt178, PMID: 23698863
  • Zimin, A., Stevens, K.A., Crepeau, M.W., Sequencing and assembly of the 22-Gb loblolly pine genome (2014) Genetics., 196, pp. 875-890. , https://doi.org/10.1534/genetics.113.159715, PMID: 24653210
  • Neale, D.B., Wegrzyn, J.L., Stevens, K.A., Decoding the massive genome of loblolly pine using haploid DNA and novel assembly strategies (2014) Genome Biol., 15, p. R59. , https://doi.org/10.1186/gb-2014-15-3-r59, PMID: 24647006
  • Plavskin, Y., Timmermans, M.C., Small RNA-regulated networks and the evolution of novel structures in plants (2012) Cold Spring Harb Symp Quant Biol., 77, pp. 221-233. , https://doi.org/10.1101/sqb.2013.77.014878, PMID: 23302808
  • Taylor, R.S., Tarver, J.E., Hiscock, S.J., Donoghue, P.C., Evolutionary history of plant microRNAs (2014) Trends Plant Sci., 19, pp. 175-182. , https://doi.org/10.1016/j.tplants.2013.11.008, PMID: 24405820
  • Axtell, M.J., Classification and comparison of small RNAs from plants (2013) Annu Rev Plant Biol., 64, pp. 137-159. , https://doi.org/10.1146/annurev-arplant-050312-120043, PMID: 23330790
  • Axtell, M.J., Snyder, J.A., Bartel, D.P., Common functions for diverse small RNAs of land plants (2007) Plant Cell., 19, pp. 1750-1769. , https://doi.org/10.1105/tpc.107.051706, PMID: 17601824
  • Jones-Rhoades, M.W., Conservation and divergence in plant microRNAs (2012) Plant Mol Biol., 80, pp. 3-16. , https://doi.org/10.1007/s11103-011-9829-2, PMID: 21996939
  • Sun, G., MicroRNAs and their diverse functions in plants (2012) Plant Mol Biol., 80, pp. 17-36. , https://doi.org/10.1007/s11103-011-9817-6, PMID: 21874378
  • Wu, G., Plant microRNAs and development (2013) J Genet Genomics., 40, pp. 217-230. , https://doi.org/10.1016/j.jgg.2013.04.002, PMID: 23706297
  • Pryer, K.M., Schuettpelz, E., Wolf, P.G., Schneider, H., Smith, A.R., Cranfill, R., Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences (2004) Am J Bot., 91, pp. 1582-1598. , https://doi.org/10.3732/ajb.91.10.1582, PMID: 21652310
  • Sessa, E.B., Banks, J.A., Barker, M.S., Der Duffy, J.P.A.M., Graham, S.W., Between two fern genomes (2014) Gigascience., 3, p. 15. , https://doi.org/10.1186/2047-217X-3-15, PMID: 25324969
  • Wolf, P.G., Sessa, E.B., Marchant, D.B., Li, F.W., Rothfels, C.J., Sigel, E.M., An exploration into fern genome space (2015) Genome Biol Evol., 7, pp. 2533-2544. , https://doi.org/10.1093/gbe/evv163, PMID: 26311176
  • Aya, K., Kobayashi, M., Tanaka, J., Ohyanagi, H., Suzuki, T., Yano, K., De novo transcriptome assembly of a fern, Lygodium japonicum, and a web resource database, Ljtrans DB (2015) Plant Cell Physiol., 56, p. e5. , https://doi.org/10.1093/pcp/pcu184, PMID: 25480117
  • Vanneste, K., Sterck, L., Myburg, A.A., Van De Peer, Y., Mizrachi, E., Horsetails are ancient polyploids: Evidence from (2015) Equisetum Giganteum. Plant Cell., 27 (6), pp. 1567-1578. , https://doi.org/10.1105/tpc.15.00157, Jun, PMID: 26002871
  • Axtell, M.J., Bartel, D.P., Antiquity of microRNAs and their targets in land plants (2005) Plant Cell., 17, pp. 1658-1673. , https://doi.org/10.1105/tpc.105.032185, PMID: 15849273
  • Chávez Montes, R.A., De Fátima Rosas-Cárdenas, F., De Paoli, E., Accerbi, M., Rymarquis, L.A., Mahalingam, G., Sample sequencing of vascular plants demonstrates widespread conservation and divergence of microRNAs (2014) Nat Commun., 5, p. 3722. , https://doi.org/10.1038/ncomms4722, PMID: 24759728
  • Schneider, H., Schuettpelz, E., Pryer, K.M., Cranfill, R., Magallón, S., Lupia, R., Ferns diversified in the shadow of angiosperms (2004) Nature., 428, pp. 553-557. , https://doi.org/10.1038/nature02361, PMID: 15058303
  • Wickett, N.J., Mirarab, S., Nguyen, N., Warnow, T., Carpenter, E., Matasci, N., Phylotranscriptomic analysis of the origin and early diversification of land plants (2014) Proc Natl Acad Sci USA., 111, pp. E4859-E4868. , https://doi.org/10.1073/pnas.1323926111, PMID: 25355905
  • Ruhfel, B.R., Gitzendanner, M.A., Soltis, P.S., Soltis, D.E., Burleigh, J.G., From algae to angiosperms-inferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes (2014) BMC Evol Biol., 14, p. 23. , https://doi.org/10.1186/1471-2148-14-23, PMID: 24533922
  • Prado, J., Hirai, R.Y., A new combination in Pleopeltis and some nomenclatural notes related to illustrations validating fern names (2010) Am Fern J., 100, pp. 189-194
  • Mai Morente, P., (2014) Flora Epífita Vascular de Uruguay Con Énfasis en Helechos (Polypodiofitas), , https://www.colibri.udelar.edu.uy/handle/123456789/4055, Tesis de maestría Universidad de la República (Uruguay). Facultad de Ciencias-PEDECIBA
  • Proctor, M.C.F., Tuba, Z., Poikilohydry and homoihydry: Antithesis or spectrum of possibilities? (2002) New Phytol., 156, pp. 327-349
  • Coruh, C., Cho, S.H., Shahid, S., Liu, Q., Wierzbicki, A., Axtell, M.J., Comprehensive annotation of physcomitrella patens small RNA loci reveals that the heterochromatic short interfering RNA pathway is largely conserved in land plants (2015) Plant Cell., 27, pp. 2148-2162. , https://doi.org/10.1105/tpc.15.00228, PMID: 26209555
  • Kozomara, A., Griffiths-Jones, S., MiRBase: Annotating high confidence microRNAs using deep sequencing data (2014) Nucleic Acids Res., 42, pp. D68-D73. , https://doi.org/10.1093/nar/gkt1181, PMID: 24275495
  • Zhang, S.D., Ling, L.Z., Zhang, Q.F., Xu, J.D., Cheng, L., Evolutionary comparison of two combinatorial regulators of SBP-Box genes, MiR156 and MiR529, in plants (2015) PLoS One., 10, p. e0124621. , https://doi.org/10.1371/journal.pone.0124621, PMID: 25909360
  • Morea, E.G., Da Silva, E.M., Silva, G.F., Valente, G.T., Barrera Rojas, C.H., Vincentz, M., Nogueira, F.T., Functional and evolutionary analyses of the miR156 and miR529 families in land plants (2016) BMC Plant Biol., 16, p. 40. , https://doi.org/10.1186/s12870-016-0716-5, PMID: 26841873
  • Palatnik, J.F., Wollmann, H., Schommer, C., Schwab, R., Boisbouvier, J., Rodriguez, R., Sequence and expression differences underlie functional specialization of Arabidopsis microRNAs miR159 and miR319 (2007) Dev Cell., 13, pp. 115-125. , https://doi.org/10.1016/j.devcel.2007.04.012, PMID: 17609114
  • Li, Y., Li, C., Ding, G., Jin, Y., Evolution of MIR159/319 microRNA genes and their post-transcriptional regulatory link to siRNA pathways (2011) BMC Evol Biol., 11, p. 122. , https://doi.org/10.1186/1471-2148-11-122, PMID: 21569383
  • Tsuzuki, M., Nishihama, R., Ishizaki, K., Kurihara, Y., Matsui, M., Bowman, J.L., Profiling and characterization of small RNAs in the liverwort, Marchantia polymorpha, belonging to the first diverged land plants (2016) Plant Cell Physiol., 57, pp. 359-372. , https://doi.org/10.1093/pcp/pcv182, PMID: 26589267
  • Mi, S., Cai, T., Hu, Y., Chen, Y., Hodges, E., Ni, F., Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5' terminal nucleotide (2008) Cell., 133, pp. 116-127. , https://doi.org/10.1016/j.cell.2008.02.034, PMID: 18342361
  • Wan, L.C., Wang, F., Guo, X., Lu, S., Qiu, Z., Zhao, Y., Identification and characterization of small noncoding RNAs from Chinese fir by high throughput sequencing (2012) BMC Plant Biol., 12, p. 146. , https://doi.org/10.1186/1471-2229-12-146, PMID: 22894611
  • Hao, D.C., Yang, L., Xiao, P.G., Liu, M., Identification of Taxus microRNAs and their targets with high-throughput sequencing and degradome analysis (2012) Physiol Plant., 146, pp. 388-403. , https://doi.org/10.1111/j.1399-3054.2012.01668.x, PMID: 22708792
  • Zhang, Q., Li, J., Sang, Y., Xing, S., Wu, Q., Liu, X., Identification and Characterization of MicroRNAs in Ginkgo biloba var. Epiphylla Mak (2015) PLoS One., 10, p. e0127184. , https://doi.org/10.1371/journal.pone.0127184, PMID: 25978425
  • Xia, R., Xu, J., Arikit, S., Meyers, B.C., Extensive families of miRNAs and PHAS Loci in Norway spruce demonstrate the origins of complex phasiRNA networks in seed plants (2015) Mol Biol Evol., 32, pp. 2905-2918. , https://doi.org/10.1093/molbev/msv164, PMID: 26318183
  • Alaba, S., Piszczalka, P., Pietrykowska, H., Pacak, A.M., Sierocka, I., Nuc, P.W., The liverwort Pellia endiviifolia shares microtranscriptomic traits that are common to green algae and land plants (2015) New Phytol., 206, pp. 352-367. , https://doi.org/10.1111/nph.13220, PMID: 25530158
  • Lin, P.C., Lu, C.W., Shen, B.N., Lee, G.Z., Bowman, J.L., Arteaga-Vazquez, M.A., Identification of miRNAs and their targets in the liverwort, Marchantia polymorpha by Integrating RNA-seq and degradome analyses (2016) Plant Cell Physiol., 57, pp. 339-358. , https://doi.org/10.1093/pcp/pcw020, PMID: 26861787
  • Jagtap, S., Shivaprasad, P.V., Diversity, expression and mRNA targeting abilities of Argonaute-targeting miRNAs among selected vascular plants (2014) BMC Genomics., 15, p. 1049. , https://doi.org/10.1186/1471-2164-15-1049, PMID: 25443390
  • Addo-Quaye, C., Snyder, J.A., Park, Y.B., Li, Y.F., Sunkar, R., Axtell, M.J., Sliced microRNA targets and precise loop-first processing of MIR319 hairpins revealed by analysis of the Physcomitrella patens degradome (2009) RNA., 15, pp. 2112-2121. , https://doi.org/10.1261/rna.1774909, PMID: 19850910
  • Dai, X., Zhao, P.X., PsRNATarget: A plant small RNA target analysis server (2011) Nucleic Acids Res., 39, pp. W155-W159. , https://doi.org/10.1093/nar/gkr319, PMID: 21622958
  • Vasco, A., Smalls, T.L., Graham, S.W., Cooper, E.D., Wong, G.K., Stevenson, D.W., Challenging the paradigms of leaf evolution: Class III HD-Zips in ferns and lycophytes (2016) New Phytol., 212, pp. 745-758. , https://doi.org/10.1111/nph.14075, PMID: 27385116
  • Axtell, M.J., Jan, C., Rajagopalan, R., Bartel, D.P., A two-hit trigger for siRNA biogenesis in plants (2006) Cell., 127, pp. 565-577. , https://doi.org/10.1016/j.cell.2006.09.032, PMID: 17081978
  • Krasnikova, M.S., Goryunov, D.V., Troitsky, A.V., Solovyev, A.G., Ozerova, L.V., Morozov, S.Y., Peculiar evolutionary history of miR390-guided TAS3-like genes in land plants (2013) ScientificWorldJournal., 2013, p. 924153. , https://doi.org/10.1155/2013/924153, PMID: 24302881
  • Addo-Quaye, C., Eshoo, T.W., Bartel, D.P., Axtell, M.J., Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome (2008) Curr Biol., 18, pp. 758-762. , https://doi.org/10.1016/j.cub.2008.04.042, PMID: 18472421
  • Vazquez, F., Gasciolli, V., Crété, P., Vaucheret, H., The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing (2004) Curr Biol., 14, pp. 346-351. , https://doi.org/10.1016/j.cub.2004.01.035, PMID: 14972688
  • Rodriguez, R.E., Debernardi, J.M., Palatnik, J.F., Morphogenesis of simple leaves: Regulation of leaf size and shape (2014) Wiley Interdiscip Rev Dev Biol., 3, pp. 41-57. , https://doi.org/10.1002/wdev.115, PMID: 24902833
  • Juarez, M.T., Kui, J.S., Thomas, J., Heller, B.A., Timmermans MC. MicroRNA-mediated repression of rolled leaf1 specifies maize leaf polarity (2004) Nature., 428, pp. 84-88. , https://doi.org/10.1038/nature02363, PMID: 14999285
  • Kidner, C.A., Martienssen, R.A., Spatially restricted microRNA directs leaf polarity through ARGONAUTE1 (2004) Nature., 428, pp. 81-84. , https://doi.org/10.1038/nature02366, PMID: 14999284
  • Vasco, A., Moran, R.C., Ambrose, B.A., The evolution, morphology, and development of fern leaves (2013) Front Plant Sci., 4, p. 345. , https://doi.org/10.3389/fpls.2013.00345, PMID: 24027574
  • Arazi, T., MicroRNAs in the moss Physcomitrella patens (2012) Plant Mol Biol., 80, pp. 55-65. , https://doi.org/10.1007/s11103-011-9761-5, PMID: 21373961
  • Llorente, B., De Souza, F.S., Soto, G., Meyer, C., Alonso, G.D., Flawiá, M.M., Selective pressure against horizontally acquired prokaryotic genes as a driving force of plastid evolution (2016) Sci Rep., 6, p. 19036. , https://doi.org/10.1038/srep19036, PMID: 26750147
  • Koi, S., Hisanaga, T., Sato, K., Shimamura, M., Yamato, K.T., Ishizaki, K., An evolutionarily conserved plant RKD factor controls germ cell differentiation (2016) Curr Biol., 26, pp. 1775-1781. , https://doi.org/10.1016/j.cub.2016.05.013, PMID: 27345165
  • Rövekamp, M., Bowman, J.L., Grossniklaus, U., Marchantia MpRKD regulates the gametophyte-sporophyte transition by keeping egg cells quiescent in the absence of fertilization (2016) Curr Biol., 26, pp. 1782-1789. , https://doi.org/10.1016/j.cub.2016.05.028, PMID: 27345166
  • Koszegi, D., Johnston, A.J., Rutten, T., Czihal, A., Altschmied, L., Kumlehn, J., Members of the RKD transcription factor family induce an egg cell-like gene expression program (2011) Plant J., 67, pp. 280-291. , https://doi.org/10.1111/j.1365-313X.2011.04592.x, PMID: 21457369

Citas:

---------- APA ----------
Berruezo, F., De Souza, F.S.J., Picca, P.I., Nemirovsky, S.I., Tosar, L.M., Rivero, M., Mentaberry, A.N.,..., Zelada, A.M. (2017) . Sequencing of small RNAs of the fern Pleopeltis minima (Polypodiaceae) offers insight into the evolution of the microrna repertoire in land plants. PLoS ONE, 12(5).
http://dx.doi.org/10.1371/journal.pone.0177573
---------- CHICAGO ----------
Berruezo, F., De Souza, F.S.J., Picca, P.I., Nemirovsky, S.I., Tosar, L.M., Rivero, M., et al. "Sequencing of small RNAs of the fern Pleopeltis minima (Polypodiaceae) offers insight into the evolution of the microrna repertoire in land plants" . PLoS ONE 12, no. 5 (2017).
http://dx.doi.org/10.1371/journal.pone.0177573
---------- MLA ----------
Berruezo, F., De Souza, F.S.J., Picca, P.I., Nemirovsky, S.I., Tosar, L.M., Rivero, M., et al. "Sequencing of small RNAs of the fern Pleopeltis minima (Polypodiaceae) offers insight into the evolution of the microrna repertoire in land plants" . PLoS ONE, vol. 12, no. 5, 2017.
http://dx.doi.org/10.1371/journal.pone.0177573
---------- VANCOUVER ----------
Berruezo, F., De Souza, F.S.J., Picca, P.I., Nemirovsky, S.I., Tosar, L.M., Rivero, M., et al. Sequencing of small RNAs of the fern Pleopeltis minima (Polypodiaceae) offers insight into the evolution of the microrna repertoire in land plants. PLoS ONE. 2017;12(5).
http://dx.doi.org/10.1371/journal.pone.0177573