Small RNAs (sRNAs) are 20-30-nucleotide-long, regulatory, noncoding RNAs that induce silencing of target genes at the transcriptional and posttranscriptional levels. They are key components for cellular functions during plant development, hormone signaling, and stress responses. Generated from the cleavage of double-stranded RNAs (dsRNAs) or RNAs with hairpin structures by Dicer-like proteins (DCLs), they are loaded onto Argonaute (AGO) protein complexes to induce gene silencing of their complementary targets by promoting messenger RNA (mRNA) cleavage or degradation, translation inhibition, DNA methylation, and/or histone modifications. This mechanism of regulating RNA activity, collectively referred to as RNA interference (RNAi), which is an evolutionarily conserved process in eukaryotes. Plant RNAi pathways play a fundamental role in plant immunity against viruses and have been exploited via genetic engineering to control disease. Plant viruses of RNA origin that contain double-stranded RNA are targeted by the RNA-silencing machinery to produce virus-derived small RNAs (vsRNAs). Some vsRNAs serve as an effector to repress host immunity by capturing host RNAi pathways. High-throughput sequencing (HTS) strategies have been used to identify endogenous sRNA profiles, the "sRNAome", and analyze expression in various perennial plants. Therefore, the review examines the current knowledge of sRNAs in perennial plants and fruits, describes the development and implementation of RNA interference (RNAi) in providing resistance against economically important viruses, and explores sRNA targets that are important in regulating a variety of biological processes.

Division of Crop Protection and Plant Health Crop Research Institute Prague 161 06 Czech Republic

United States Department of Agriculture Agricultural Research Service Appalachian Fruit Research Station Kearneysville WV 25430 USA

Zobrazit více v PubMed

Meng Y., Shao C., Wang H., Chen M. The regulatory activities of plant microRNAs: A more dynamic perspective. Plant Physiol. 2011;157:1583–1595. doi: 10.1104/pp.111.187088. PubMed DOI PMC

Ameres S.L., Zamore P.D. Diversifying microRNA sequence and function. Nat. Rev. Mol. Cell Biol. 2013;14:475–488. doi: 10.1038/nrm3611. PubMed DOI

Zhang C. Novel functions for small RNA molecules. Curr. Opin. Mol. Ther. 2009;11:641–651. PubMed PMC

Mahy B.W.J., van Regenmortel M.H.V. Desk Encyclopedia of Plant and Fungal Virology. Academic Press; Cambridge, MA, USA: 2009.

Nicaise V. Crop immunity against viruses: Outcomes and future challenges. Front. Plant Sci. 2014;5:660. doi: 10.3389/fpls.2014.00660. PubMed DOI PMC

Loebenstein G., Katis N. Control of plant virus diseases seed-propagated crops. In: Gad L., Nikolaos K., editors. Advance Virus Research. Academic Press; Cambridge, MA, USA: 2014. PubMed

Sahu P.P., Prasad M. Application of molecular antiviral compounds: Novel approach for durable resistance against geminiviruses. Mol. Biol. Rep. 2015;42:1157–1162. doi: 10.1007/s11033-015-3852-3. PubMed DOI

Singh A., Taneja J., Dasgupta I., Mukherjee S.K. Development of plants resistant to tomato geminiviruses using artificial trans-acting small interfering RNA. Mol. Plant Pathol. 2015;16:724–734. doi: 10.1111/mpp.12229. PubMed DOI PMC

Singh K., Wegulo S.N., Skoracka A., Kundu J.K. Wheat streak mosaic virus: A century old virus with rising importance worldwide. Mol. Plant Pathol. 2018;19:2193–2206. doi: 10.1111/mpp.12683. PubMed DOI PMC

Zorzatto C., Machado J.P.B., Lopes K.V.G., Nascimento K.J.T., Pereira W.A., Brustolini O.J.B., Reis P.A.B., Calil I.P., Deguchi M., Sachetto-Martins G., et al. NIK1-mediated translation suppression functions as a plant antiviral immunity mechanism. Nature. 2015;520:679–682. doi: 10.1038/nature14171. PubMed DOI PMC

Wang M., Lu Y., Botella J., Mao Y., Hua K., Zhu J.K. Gene targeting by homology-directed repair in rice using a Geminivirus-based CRISPR/Cas9 System. Mol. Plant. 2017;10:1007–1010. doi: 10.1016/j.molp.2017.03.002. PubMed DOI

Fahim M., Millar A.A., Wood C.C., Larkin P.J. Resistance to wheat streak mosaic virus generated by expression of an artificial polycistronic microRNA in wheat. Plant Biotechnol. J. 2012;10:150–163. doi: 10.1111/j.1467-7652.2011.00647.x. PubMed DOI

Reyes C.A., De Francesco A., Pena E.J., Costa N., Plata M.I., Sendin L., Castagnaro A.P., García M.L. Resistance to citrus psorosis virus in transgenic sweet orange plants is triggered by coat protein-RNA silencing. J. Biotechnol. 2011;151:151–158. doi: 10.1016/j.jbiotec.2010.11.007. PubMed DOI

Zrachya A., Glick E., Levy Y., Arazi T., Citovsky V., Gafni Y. Suppressor of RNA silencing encoded by tomato yellow curl virus-Israel. Virology. 2007;358:159–165. doi: 10.1016/j.virol.2006.08.016. PubMed DOI

Ilardi V., Tavazza M. Biotechnological strategies and tools for Plum pox virus resistance: Trans-, intra-, cis-genesis, and beyond. Front. Plant Sci. 2015;6:379. doi: 10.3389/fpls.2015.00379. PubMed DOI PMC

Kamthan A., Chaudhuri A., Kamthan M., Datta A. Small RNAs in plants: Recent development and application for crop improvement. Front. Plant Sci. 2015;6:208. doi: 10.3389/fpls.2015.00208. PubMed DOI PMC

Baulcombe D.C. RNA silencing in plants. Nature. 2004;431:356–363. doi: 10.1038/nature02874. PubMed DOI

Ding S.W. RNA-based antiviral immunity. Nat. Rev. Immunol. 2010;10:632–644. doi: 10.1038/nri2824. PubMed DOI

Margis R., Fusaro A.F., Smith N.A., Curtin S.J., Watson J.M., Finnegan E.J., Waterhouse P.M. The evolution and diversification of Dicers in plants. FEBS Lett. 2006;580:2442–2450. doi: 10.1016/j.febslet.2006.03.072. PubMed DOI

Huntzinger E., Izaurralde E. Gene silencing by microRNAs: Contributions of translational repression and mRNA decay. Nat. Rev. Genet. 2011;12:99–110. doi: 10.1038/nrg2936. PubMed DOI

Bartel D.P. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell. 2004;116:281–297. doi: 10.1016/S0092-8674(04)00045-5. PubMed DOI

Khraiwesh B., Arif M.A., Seumel G.I., Ossowski S., Weigel D., Reski R., Frank W. Transcriptional control of gene expression by microRNAs. Cell. 2010;140:111–122. doi: 10.1016/j.cell.2009.12.023. PubMed DOI

Law J.A., Jacobsen S.E. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 2010;11:204–220. doi: 10.1038/nrg2719. PubMed DOI PMC

Pooggin M.M. RNAi-mediated resistance to viruses: A critical assessment of methodologies. Curr. Opin. Virol. 2017;26:28–35. doi: 10.1016/j.coviro.2017.07.010. PubMed DOI

Borges F., Martienssen R.A. The expanding world of small RNAs in plants. Nat. Rev. Mol. Cell Biol. 2015;16:727–741. doi: 10.1038/nrm4085. PubMed DOI PMC

Jia R., Zhao H., Huang J., Kong H., Zhang Y., Guo J., Huang Q., Guo Y., Wei Q., Zuo J., et al. Use of RNAi technology to develop a PRSV-resistant transgenic papaya. Sci. Reports. 2015;7:12636. doi: 10.1038/s41598-017-13049-0. PubMed DOI PMC

Khalid A., Zhang Q., Yasir M., Li F. Small RNA Based genetic engineering for plant viral resistance: Application in crop protection. Front. Microbiol. 2017;8:43. doi: 10.3389/fmicb.2017.00043. PubMed DOI PMC

Scorza R., Callahan A., Dardick C., Ravelonandro M., Polak J., Malinowski T., Zagrai I., Cambra M., Kamenova I. Genetic engineering of Plum pox virus resistance: ‘HoneySweet’ plum—from concept to product. Plant Cell Tiss. Organ. Cult. 2013;115:1–12. doi: 10.1007/s11240-013-0339-6. DOI

Aragão F.J., Nogueira E.O., Tinoco M.L., Faria J.C. Molecular characterization of the first commercial transgenic common bean immune to the Bean golden mosaic virus. J. Biotechnol. 2013;166:42–50. doi: 10.1016/j.jbiotec.2013.04.009. PubMed DOI

Parent J.S., Jauvion V., Bouché N., Béclin C., Hachet M., Zytnicki M., Vaucheret H. Posttranscriptional gene silencing triggered by sense transgenes involves uncapped antisense RNA and differs from silencing intentionally triggered by antisense transgenes. Nucleic Acids Res. 2015;43:8464–8475. doi: 10.1093/nar/gkv753. PubMed DOI PMC

Baumberger N., Baulcombe D.C. Arabidopsis ARGONAUTE1 is an RNA slicer that selectively recruits microRNAs and short interfering RNAs. Proc. Natl. Acad. Sci. USA. 2005;102:11928–11933. doi: 10.1073/pnas.0505461102. PubMed DOI PMC

Gonsalves D. Transgenic Papaya: A Case Study on the Theoretical and Practical Application of Virus Resistance. In: Vasil I.K., editor. Plant Biotechnology 2002 and Beyond, Proceedings of the 10th IAPTC&B Congress, Orlando, FL, USA, 23–28 June 2002. Springer; Berlin, Germany: 2003. pp. 115–118.

Kung Y.J., You B.J., Raja J.A.J., Chen K.C., Huang C.H., Bau H.J., Yang C.F., Huang C.H., Chang C.P., Yeh S.D. Nucleotide sequence-homology-independent breakdown of transgenic resistance by more virulent virus strains and a potential solution. Sci. Rep. 2015;5:9804. doi: 10.1038/srep09804. PubMed DOI PMC

Tennant P., Fermin G., Fitch M.M., Manshardt R.M., Slightom J.L., Gonsalves D. Papaya ringspot virus resistance of transgenic Rainbow and SunUp is affected by gene dosage, plant development, and coat protein homology. Eur. J. Plant Pathol. 2001;107:645–653. doi: 10.1023/A:1017936226557. DOI

Scorza R., Ravelonandro M., Callahan A.M., Cordts J.M., Fuchs M., Dunez J., Gonsalves D. Transgenic plum (Prunus domestica L.) express the plum pox virus coat protein gene. Plant Cell Rep. 1994;14:18–22. doi: 10.1007/BF00233291. PubMed DOI

Scorza R., Callahan A., Levy L., Damsteegt V., Webb K., Ravelonandro M. Posttranscriptional gene silencing in plum pox virus resistant transgenic European plum containing the Plum pox potyvirus coat protein gene. Trans. Res. 2001;1054:1–9. PubMed

Hily J.M., Scorza R., Webb K., Ravelonandro M. Accumulation of the long class of siRNA is associated with resistance to plum pox virus throughout the life cycle of a transgenic woody perennial plum tree. Mol. Plant Microbe Interact. 2005;18:794–799. doi: 10.1094/MPMI-18-0794. PubMed DOI

Kundu J.K., Briard P., Hily J.M., Ravelonandro M., Scorza R. Role of the 25–26 nt siRNA in the resistance of transgenic Prunus domestica graft inoculated with plum pox virus. Virus Genes. 2008;36:215–220. doi: 10.1007/s11262-007-0176-y. PubMed DOI

Han Y., Grierson D. Relationship between small antisense RNAs and aberrant RNAs associated with sense transgene mediated gene silencing in tomato. Plant J. 2002;29:509–519. doi: 10.1046/j.1365-313x.2002.01236.x. PubMed DOI

Scorza R., Georgi L., Callahan A., Petri C., Hily J.M., Dardick C., Damsteegt V., Ravelonandro M. Hairpin Plum pox virus coat protein (hpPPV-CP) structure in ‘HoneySweet’ C5 plum provides PPV resistance when genetically engineered into plum (Prunus domestica) seedlings. Julius Kühn Archiv. 2010;427:141–146.

Ravelonandro M., Briard P., Hily J.M., Scorza R., Lomberk D. Evaluation of plum pox virus (PPV) CP and P1 constructs on sharka resistance in plum (Prunus domestica) Acta Hort. 2015;1063:63–70. doi: 10.17660/ActaHortic.2015.1063.7. DOI

Hily J.M., Ravelonandro M., Damsteegt V., Bassett C., Petri C., Liu Z., Scorza R. Plum pox virus coat protein gene intron hairpin RNA construct provides resistance to Plum pox virus in Nicotiana benthamiana and Prunus domestica. J. Am. Soc. Hort. Sci. 2007;132:850–858. doi: 10.21273/JASHS.132.6.850. DOI

Dolgov S., Mikhaylov R., Serova T., Shulga O., Firsov A. Pathogen-derived methods for improving resistance of transgenic plums (Prunus domestica L.) for Plum pox virus infection. Julius Kühn Archiv. 2010;427:133–140.

Monticelli S., Di Nicola-Negri E., Gentile A., Damiano C., Ilardi V. Production and in vitro assessment of transgenic plums for resistance to Plum pox virus: A feasible, environmental riskfree, cost-effective approach. Ann. Appl. Biol. 2012;161:293–301. doi: 10.1111/j.1744-7348.2012.00573.x. DOI

García-Almodóvar R.C., Clemente-Moreno M.J., Díaz-Vivancos P., Petri C., Rubio M., Padilla I.M.G., Ilardi P.V., Burgos L. Greenhouse evaluation confirms in vitro sharka resistance of genetically engineered h-UTR/P1 plum plants. Plant Cell Tiss. Org. 2015;120:791–796. doi: 10.1007/s11240-014-0629-7. DOI

Wang A., Tian L., Huang T.S., Brown D.C.W., Svircev A.M., Stobbs L.W., Miki B., Sanfaçon H. The development of genetic resistance to Plum pox virus in transgenic Nicotiana benthamiana and Prunus domestica. Acta Hort. 2009;839:665–672. doi: 10.17660/ActaHortic.2009.839.91. DOI

Wang A., Tian L., Brown D.C.W., Svircev A.M., Stobbs L.W., Sanfaçon H. Generation of efficient resistance to Plum pox virus (PPV) in Nicotiana benthamiana and Prunus domestica expressing triple-intron-spanned double-hairpin RNAs simultaneously targeting 5′ and 3′ conserved genomic regions of PPV. Acta Hort. 2013;1063:77–84. doi: 10.17660/ActaHortic.2015.1063.9. DOI

Laimer da Camara Machado M., da Camara A., Hanzer V., Weiss H., Regner F., Steinkellner H., Mattanovich D., Plail R., Knapp E., Kalthoff B., et al. Regeneration of transgenic plants of Prunus armeniaca containing the coat protein gene of Plum pox virus. Plant Cell Rep. 1992;11:25–29. doi: 10.1007/BF00231834. PubMed DOI

Vu T., Choudhury N.R., Mukherjee S.K. Transgenic tomato plants expressing artificial microRNAs for silencing the pre-coat and coat proteins of a begomovirus, Tomato leaf curl New Delhi virus, show tolerance to virus infection. Virus Res. 2013;172:35–45. doi: 10.1016/j.virusres.2012.12.008. PubMed DOI

Ammara U.E., Mansoor S., Saeed M., Amin I., Briddon R.W., Al-Sadi A.M. RNA interference-based resistance in transgenic tomato plants against tomato yellow leaf curl virus- Oman (TYLCV-OM) and its associated betasatellite. Virol. J. 2015;12:38. doi: 10.1186/s12985-015-0263-y. PubMed DOI PMC

Pandolfini T., Molesini B., Avesani L., Spena A., Polverari A. Expression of self-complementary hairpin RNA under the control of the rolC promoter confers systemic disease resistance to Plum pox virus without preventing local infection. BMC Biotech. 2003;3:7. doi: 10.1186/1472-6750-3-7. PubMed DOI PMC

Zhang S.C., Tian L.M., Svircev A., Brown D.C.W., Sibbald S., Schneider K.E., Barszcz E.B. Engineering resistance to Plum pox virus (PPV) through the expression of PPV specific hairpin RNAs in transgenic plants. Can. J. Plant Pathol. 2006;28:263–270. doi: 10.1080/07060660609507295. DOI

Wang X., Kohalmi S.E., Svircev A., Wang A., Sanfaçon H., Tian L. Silencing of the host factor eIF(iso)4E gene confers plum pox virus resistance in plum. PLoS ONE. 2013;8:e50627. doi: 10.1371/journal.pone.0050627. PubMed DOI PMC

Song G.Q., Sink K.C., Walworth A.E., Cook M.A., Allison R.F., Lang G.A. Engineering cherry rootstocks with resistance to prunus necrotic ring spot virus through RNAi-mediated silencing. Plant Biotech. J. 2013;11:702–708. doi: 10.1111/pbi.12060. PubMed DOI

Shekhawat U.K.S., Ganapathi T.R., Hadapad A.B. Transgenic banana plants expressing small interfering RNAs targeted against viral replication initiation gene display high-level resistance to banana bunchy top virus infection. J. Gen. Virol. 2012;93:1804–1813. doi: 10.1099/vir.0.041871-0. PubMed DOI

Duan C.G., Fang Y.Y., Zhou B.J., Zhao J.H., Hou W.N., Zhu H., Ding S.W., Guo H.S. Suppression of Arabidopsis ARGONAUTE1-mediated slicing, transgene-induced RNA silencing, and DNA methylation by distinct domains of the cucumber mosaic virus 2b protein. Plant Cell. 2012;24:259–274. doi: 10.1105/tpc.111.092718. PubMed DOI PMC

Ai T., Zhang L., Gao Z., Zhu C.X., Guo X. Highly efficient virus resistance mediated by artificial microRNAs that target the suppressor of PVX and PVY in plants. Plant Biol. 2011;13:304–316. doi: 10.1111/j.1438-8677.2010.00374.x. PubMed DOI

Zhao D., Song G.Q. Rootstock-to-scion transfer of transgene-derived small interfering RNAs and their effect on virus resistance in nontransgenic sweet cherry. Plant Biotechnol. J. 2014;12:1319–1328. doi: 10.1111/pbi.12243. PubMed DOI

Härtl K., Denton A., Franz-Oberdorf K., Hoffmann T., Spornraft M., Usadel B., Schwab W. Early metabolic and transcriptional variations in fruit of natural white-fruited Fragaria vesca genotypes. Sci. Reports. 2017;7:45113. doi: 10.1038/srep45113. PubMed DOI PMC

Flachowsky H., Tränkner C., Szankowski I., Waidmann S., Hanke M.V., Treutter D., Fischer T.C. RNA-mediated gene silencing signals are not graft transmissible from the rootstock to the scion in greenhouse-grown apple plants Malus sp. Int. J Mol. Sci. 2012;13:9992–10009. doi: 10.3390/ijms13089992. PubMed DOI PMC

Kasai A., Bai S., Li T., Harada T. Graft- transmitted siRNA signal from the root induces visual manifestation of endogenous post- transcriptional gene silencing in the scion. PLoS ONE. 2011;6:e16895. doi: 10.1371/journal.pone.0016895. PubMed DOI PMC

Ali E.M., Kobayashi K., Yamaoka N., Ishikawa M., Nishiguchi M. Graft transmission of RNA silencing to non- transgenic scions for conferring virus resistance in tobacco. PLoS ONE. 2013;8:e63257. PubMed PMC

Kanehira A., Yamada K., Iwaya T., Tsuwamoto R., Kasai A., Nakazono M., Harada T. Apple phloem cells contain some mRNAs transported over long distances. Tree Genet. Genom. 2010;5:635–642. doi: 10.1007/s11295-010-0279-9. DOI

Hanley-Bowdoin L., Bejarano E.R., Robertson D., Mansoor S. Geminiviruses: Masters at redirecting and reprogramming plant processes. Nat. Rev. Microbiol. 2013;11:777–788. doi: 10.1038/nrmicro3117. PubMed DOI

Ehrenfeld N., Romano E., Serrano C., Arce-Johnson P. Replicase mediated resistance against potato leafroll virus in potato desiree plants. Biol. Res. 2005;37:71–82. doi: 10.4067/S0716-97602004000100008. PubMed DOI

Barakat A., Wall P.K., Diloreto S., Depamphilis C.W., Carlson J.E. Conservation and divergence of microRNAs in Populus. BMC Genom. 2007;8:481. doi: 10.1186/1471-2164-8-481. PubMed DOI PMC

Huang J.-H., Lin X.-J., Zhang L.-Y., Wang X.-D., Fan G.-C., Chen L.-S. MicroRNA sequencing revealed citrus adaptation to long-term boron toxicity through modulation of root development by miR319 and miR171. Int. J. Mol. Sci. 2019;20:1422. doi: 10.3390/ijms20061422. PubMed DOI PMC

Zhang Y., Yu M., Yu H., Han J., Song C., Ma R., Fang J. Computational identification of microRNAs in peach expressed sequence tags and validation of their precise sequences by miRRACE. Mol. Biol. Rep. 2012;39:1975–1987. doi: 10.1007/s11033-011-0944-6. PubMed DOI

Zhu H., Xia R., Zhao B., An Y.Q., Dardick C.D., Callahan A.M., Liu Z. Unique expression, processing regulation, and regulatory network of peach (Prunus persica) miRNAs. BMC Plant Biol. 2012;12:149. doi: 10.1186/1471-2229-12-149. PubMed DOI PMC

Cuperus J.T., Fahlgren N., Carrington J.C. Evolution and functional diversification of MIRNA genes. Plant. Cell. 2011;23:431–442. doi: 10.1105/tpc.110.082784. PubMed DOI PMC

Quinn C., Iriyama R., Fernando D. Expression patterns of conserved microRNAs in the male gametophyte of loblolly pine (Pinus taeda) Plant. Reprod. 2014;27:69–78. doi: 10.1007/s00497-014-0241-3. PubMed DOI

Nystedt B., Street N.R., Wetterbom A., Zuccolo A., Lin Y.C., Scofield D.G., Vezzi F., Delhomme N., Giacomello S., Alexeyenko A., et al. The Norway spruce genome sequence and conifer genome evolution. Nature. 2013;497:579–584. doi: 10.1038/nature12211. PubMed DOI

Lu S., Sun Y.H., Amerson H., Chiang V.L. MicroRNAs in loblolly pine (Pinus taeda L.) and their association with fusiform rust gall development. Plant. J. 2007;51:1077–1098. doi: 10.1111/j.1365-313X.2007.03208.x. PubMed DOI

Morin R.D., Aksay G., Dolgosheina E., Ebhardt H.A., Magrini V., Mardis E.R., Sahinalp S.C., Unrau P.J. Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa. Genome Res. 2008;18:571–584. doi: 10.1101/gr.6897308. PubMed DOI PMC

Zhang S., Zhou J., Han S., Yang W., Li W., Wei H., Li X., Qi L. Four abiotic stress-induced mirna families differentially regulated in the embryogenic and non-embryogenic callus tissues of Larix leptolepis. Biochem. Biophys. Res. Commun. 2010;398:355–360. doi: 10.1016/j.bbrc.2010.06.056. PubMed DOI

Liu Y., Han S., Ding X., Li X., Zhang L., Li W., Xu H., Li Z., Qi L. Transcriptome analysis of mRNA and miRNA in somatic embryos of Larix leptolepis subjected to hydrogen treatment. Int. J. Mol. Sci. 2016;17:1951. doi: 10.3390/ijms17111951. PubMed DOI PMC

Zhang J., Wu T., Li L., Han S., Li X., Zhang S., Qi L. Dynamic expression of small RNA populations in larch (Larix leptolepis) Planta. 2013;237:89–101. doi: 10.1007/s00425-012-1753-4. PubMed DOI

Yakovlev I., Fossdal C.G., Johnsen Ø. MicroRNAs, the epigenetic memory and climatic adaptation in Norway spruce. New Phytol. 2010;187:1154–1169. doi: 10.1111/j.1469-8137.2010.03341.x. PubMed DOI

Dolgosheina E.V., Morin R.D., Aksay G., Sahinalp S.C., Magrini V., Mardis E.R., Mattsson J., Unrau P.J. Conifers have a unique small RNA silencing signature. RNA. 2008;14:1508–1515. doi: 10.1261/rna.1052008. PubMed DOI PMC

Carthew R.W., Sontheimer E.J. Origins and Mechanisms of miRNAs and siRNAs. Cell. 2009;136:642–655. doi: 10.1016/j.cell.2009.01.035. PubMed DOI PMC

Puzey J.R., Karger A., Axtell M., Kramer E.M. Deep annotation of Populus trichocarpa microRNAs from diverse tissue sets. PLoS ONE. 2012;7:e33034. doi: 10.1371/journal.pone.0033034. PubMed DOI PMC

Lu S., Sun Y.H., Shi R., Clark C., Li L., Chiang V.L. Novel and mechanical stress- responsive microRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant. Cell. 2005;17:2186–2203. doi: 10.1105/tpc.105.033456. PubMed DOI PMC

Klevebring D., Street N.R., Fahlgren N., Kasschau K.D., Carrington J.C., Joakim L., Jansson S. Genome-wide profiling of Populus small RNAs. BMC Genomics. 2009;10 doi: 10.1186/1471-2164-10-620. PubMed DOI PMC

Rajagopalan R., Vaucheret H., Trejo J., Bartel D.P. A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev. 2006;20:3407–3425. doi: 10.1101/gad.1476406. PubMed DOI PMC

Sunkar R., Zhu J.K. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant. Cell. 2004;16:2001–2019. doi: 10.1105/tpc.104.022830. PubMed DOI PMC

Lu S., Sun Y.H., Chiang V.L. Stress-responsive microRNAs in Populus. Plant. J. 2008;55:131–151. doi: 10.1111/j.1365-313X.2008.03497.x. PubMed DOI

Li B., Qin Y., Duan H., Yin W., Xia X. Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica. J. Exp. Bot. 2011;62:3765–3779. doi: 10.1093/jxb/err051. PubMed DOI PMC

Xia R., Zhu H., An Y.Q., Beers E.P., Liu Z. Apple miRNAs and tasiRNAs with novel regulatory networks. Genome Biol. 2012;13:R47. doi: 10.1186/gb-2012-13-6-r47. PubMed DOI PMC

Vazquez F., Vaucheret H., Rajagopalan R., Lepers C., Gasciolli V., Mallory A.C., Hilbert J.L., Bartel D.P., Crété P. Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol. Cell. 2004;16:69–79. doi: 10.1016/j.molcel.2004.09.028. PubMed DOI

Varkonyi-Gasic E., Gould N., Sandanayaka M., Sutherland P., MacDiarmid R.M. Characterisation of microRNAs from apple (Malus domestica ‘Royal Gala’) vascular tissue and phloem sap. BMC Plant Biol. 2010;10:159. doi: 10.1186/1471-2229-10-159. PubMed DOI PMC

Dubos C., Stracke R., Grotewold E., Weisshaar B., Martin C., Lepiniec L. MYB transcription factors in Arabidopsis. Trends Plant. Sci. 2010;15:573–581. doi: 10.1016/j.tplants.2010.06.005. PubMed DOI

Kuhn D.E., Martin M.M., Feldman D.S., Terry A.V., Jr., Nuovo G.J., Elton T.S. Experimental validation of miRNA targets. Methods. 2008;44:47–54. doi: 10.1016/j.ymeth.2007.09.005. PubMed DOI PMC

Reyes J.L., Chua N.H. ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J. 2007;49:592–606. doi: 10.1111/j.1365-313X.2006.02980.x. PubMed DOI

Williams L., Grigg S.P., Xie M., Christensen S., Fletcher J.C. Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. Development. 2007;132:3657–3668. doi: 10.1242/dev.01942. PubMed DOI

Constabel C.P., Yip L., Patton J.J., Christopher M.E. Polyphenol oxidase from hybrid poplar; Cloning and expression in response to wounding and herbivory. Plant Physiol. 2000;124:285–295. doi: 10.1104/pp.124.1.285. PubMed DOI PMC

Achard P., Herr A., Baulcombe D.C., Harberd N.P. Modulation of floral development by a gibberellin-regulated microRNA. Development. 2004;131:3357–3365. doi: 10.1242/dev.01206. PubMed DOI

Gong X., Bewley D.J. A GAMYB-like gene in tomato and its expression during seed germination. Planta. 2008;228:563–572. doi: 10.1007/s00425-008-0759-4. PubMed DOI

Gandikota M., Birkenbihl R.P., Höhmann S., Cardon G.H., Saedler H., Huijser P. The miRNA156/157 recognition element in the 3′ UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J. 2007;49:683–693. doi: 10.1111/j.1365-313X.2006.02983.x. PubMed DOI

Schneider D.A., French S.L., Osheim Y.N., Bailey A.O., Vu L., Dodd J., Yates J.R., Beyer A.L., Nomura M. RNA polymerase II elongation factors Spt4p and Spt5p play roles in transcription elongation by RNA polymerase I and rRNA processing. Proc. Natl. Acad. Sci. USA. 2006;103:12707–12712. doi: 10.1073/pnas.0605686103. PubMed DOI PMC

Yamaguchi M., Mitsuda N., Ohtani M., Ohme-Takagi M., Kato K., Demura T. Vascular-Related NAC-DOMAIN7 directly regulates the expression of a broad range of genes for xylem vessel formation. Plant J. 2011;66:579–590. doi: 10.1111/j.1365-313X.2011.04514.x. PubMed DOI

Wan L.-C., Wang F., Guo X., Lu S., Qiu Z., Zhao Y., Zhang H., Lin J. Identification and characterization of small non-coding RNAs from Chinese fir by high throughput sequencing. BMC Plant Biol. 2012;12:146. doi: 10.1186/1471-2229-12-146. PubMed DOI PMC