Udział niskocząsteczkowych regulatorowych RNA (siRNA i miRNA) w regulacji szlaku transdukcji sygnału auksyn

• Authors: Paulina Glazińska , Milena Kulasek , Michał Grzeca , Waldemar Wojciechowski , Katarzyna Marciniak , Emilia Wilmowicz , Jan Kopcewicz

Title variants

EN

Involvement of low molecular weight regulatory RNAs (siRNAs and miRNAs) in regulation of auxin signal transduction pathway

• Languages of publication: PL EN

Abstracts

PL

Auksyna wpływa na większość procesów wzrostu i rozwoju roślin. Szlak transdukcji sygnału auksyn tworzony jest przez komponenty białkowe, z których kluczowe są: receptory z rodziny TAAR (TIR1 oraz AFB1-3), represory odpowiedzi na auksynę AUX/IAA i czynniki transkrypcyjne AUXIN RESPONSE FACTOR (ARF). Aktywność genów kodujących niektóre elementy tego szlaku jest regulowana przez niskocząsteczkowe regulatorowe RNA, miRNA (micro RNA), i siRNA (short-interfering RNA), endogenne, niekodujące małe RNA (small RNA, sRNA) o długości 20-25 nukleotydów, różniące się sposobem powstawania (prekursorowymi molekułami i szlakami syntezy) oraz funkcją. Sekwencje TIR1 i AFB1-3 zawierają miejsce docelowe dla miR393 i drugorzędowe dla siTAAR. Transkrypt genu IAA28 jest celem dla miR847. Ekspresja genów: ARF10, ARF16 i ARF17 podlega bezpośredniej kontroli przez miR160, ARF6 i ARF8 przez miR167, natomiast ekspresja ARF2-4 podlega regulacji przez miR390 za pośrednictwem ta-siRNA pochodzącego z locus TAS3. sRNA wpływają przede wszystkim na lokalizację tkankową i czasową opisanych elementów szlaku auksynowego.

EN

Auxin affects almost all of the growth and development processes in plants. The auxin signal transduction pathway involves a number of proteins, among which the key elements are: TAAR auxin receptors (TIR1 and AFB1-3), AUX/IAA auxin response repressors and Auxin Response Factor (ARF) transcription factors. The activity of genes encoding some components of this pathway is affected by regulatory low-molecular-weight RNAs - miRNA (micro RNA) and siRNA (short-interfering RNA) - endogenous non-coding 20-25 nucleotides long small RNA (sRNA), differing in the way of formation (precursor molecules and biosynthesis pathways) and function. TIR1 and AFB1-3 contain miR393 target sequence and siTAAR secondary target site. IAA28 transcripts are targeted by miR847. Expression of ARF10, ARF16 i ARF17 is directly controlled by miR160, ARF6 and ARF8 by miR167, and ARF2-4 indirectly by miR390 through TAS3-derived ta-siRNAs. sRNAs influence primarily the tissue and temporal localization of described components of the auxin signal transduction pathway.

Keywords

PL

auksyna; miRNA; szlak transdukcji sygnału auksynowego; regulacja ekspresji genów; sRNA; siRNA; ta-siRNA

• Journal: Kosmos
• Year: 2016
• Volume: 65
• Issue: 3
• Pages: 399-410

Dates

published

2016

Contributors

author

Paulina Glazińska

• Katedra Fizjologii Roślin i Biotechnologii, Wydział Biologii i Ochrony Środowiska, Uniwersytet Mikołaja Kopernika, Lwowska 1, 87-100 Toruń, Polska
• Chair of Plant Physiology and Biotechnology, Faculty of Biology and Environmental Protection, Nicolaus Copernicus University, Lwowska 1 Street, 87 100 Torun, Poland

author

Milena Kulasek

• Katedra Fizjologii Roślin i Biotechnologii, Wydział Biologii i Ochrony Środowiska, Uniwersytet Mikołaja Kopernika, Lwowska 1, 87-100 Toruń, Polska
• Chair of Plant Physiology and Biotechnology, Faculty of Biology and Environmental Protection, Nicolaus Copernicus University, Lwowska 1 Street, 87 100 Torun, Poland

author

Michał Grzeca

• Katedra Fizjologii Roślin i Biotechnologii, Wydział Biologii i Ochrony Środowiska, Uniwersytet Mikołaja Kopernika, Lwowska 1, 87-100 Toruń, Polska
• Chair of Plant Physiology and Biotechnology, Faculty of Biology and Environmental Protection, Nicolaus Copernicus University, Lwowska 1 Street, 87 100 Torun, Poland

author

Waldemar Wojciechowski

• Katedra Fizjologii Roślin i Biotechnologii, Wydział Biologii i Ochrony Środowiska, Uniwersytet Mikołaja Kopernika, Lwowska 1, 87-100 Toruń, Polska
• Chair of Plant Physiology and Biotechnology, Faculty of Biology and Environmental Protection, Nicolaus Copernicus University, Lwowska 1 Street, 87 100 Torun, Poland

author

Katarzyna Marciniak

• Katedra Fizjologii Roślin i Biotechnologii, Wydział Biologii i Ochrony Środowiska, Uniwersytet Mikołaja Kopernika, Lwowska 1, 87-100 Toruń, Polska
• Chair of Plant Physiology and Biotechnology, Faculty of Biology and Environmental Protection, Nicolaus Copernicus University, Lwowska 1 Street, 87 100 Torun, Poland

author

Emilia Wilmowicz

• Katedra Fizjologii Roślin i Biotechnologii, Wydział Biologii i Ochrony Środowiska, Uniwersytet Mikołaja Kopernika, Lwowska 1, 87-100 Toruń, Polska
• Chair of Plant Physiology and Biotechnology, Faculty of Biology and Environmental Protection, Nicolaus Copernicus University, Lwowska 1 Street, 87 100 Torun, Poland

author

Jan Kopcewicz

• Katedra Fizjologii Roślin i Biotechnologii, Wydział Biologii i Ochrony Środowiska, Uniwersytet Mikołaja Kopernika, Lwowska 1, 87-100 Toruń, Polska
• Chair of Plant Physiology and Biotechnology, Faculty of Biology and Environmental Protection, Nicolaus Copernicus University, Lwowska 1 Street, 87 100 Torun, Poland

References

• Adenot X., Elmayan T., Lauressergues D., Boutet S., Bouché N., Gasciolli V., Vaucheret H., 2006. DRB4-Dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr. Biol. 16, 927-932.
• Axtell M.J., Snyder J.A., Bartel D. P., 2007. Common functions for diverse small RNAs of land plants. Plant Cell 19, 1750-1769.
• Blevins T., Rajeswaran R., Shivaprasad P. V., Beknazariants D., Si-Ammour A., Park H.-S., Vazquez F., Robertson D., Meins F. Jr., Hohn T., Pooggin M. M., 2006. Four plant Dicers mediate viral small RNA biogenesis and DNA virus induced silencing. Nucl. Acids Res. 34, 6233-6246.
• Bonnet E., Van de Peer Y., Rouzé P., 2006. The small RNA world of plants. New Phytologist 171, 451-468.
• Brioudes F., Joly C., Szécsi J., Varaud E., Leroux J., Bellvert F., Bertrand C., Bendahmane M., 2009. Jasmonate controls late development stages of petal growth in Arabidopsis thaliana. Plant J Cell Mol Biol 60, 1070-1080.
• Brodersen P., Voinnet O., 2006. The diversity of RNA silencing pathways in plants. Trends Genet. TIG 22, 268-280.
• Brodersen P., Sakvarelidze-Achard L., Bruun-Rasmussen M., Dunoyer P., Yamamoto Y. Y., Sieburth L., Voinnet O., 2008. Widespread translational inhibition by plant miRNAs and siRNAs. Science 320, 1185-1190.
• Chen X., 2005. MicroRNA biogenesis and function in plants. FEBS Lett. 579, 5923-5931.
• Chen X., 2009. Small RNAs and their roles in plant development. Ann. Rev. Cell Develop. Biol. 25, 21-44.
• Chitwood D. H., Guo M., Nogueira F. T. S., Timmermans M. C. P., 2007. Establishing leaf polarity: the role of small RNAs and positional signals in the shoot apex. Development 134, 813-823.
• Chitwood D. H., Nogueira F. T. S., Howell M. D., Montgomery T. A., Carrington J. C., Timmermans M. C. P., 2009. Pattern formation via small RNA mobility. Genes Develop. 23, 549-554.
• Csorba T., Pantaleo V., Burgyán J., 2009. RNA silencing: an antiviral mechanism. Adv. Virus Res. 75, 35-71.
• Curaba J., Singh M. B., Bhalla P. L., 2014. miRNAs in the crosstalk between phytohormone signalling pathways. J. Exp. Bot. 65, 1425-1438.
• Depuydt S., Hardtke C. S., 2011. Hormone signalling crosstalk in plant growth regulation. Curr. Biol. 21, R365-R373.
• Dharmasiri N., Dharmasiri S., Estelle M., 2005. The F-box protein TIR1 is an auxin receptor. Nature 435, 441-445.
• Dharmasiri N., Dharmasiri S., Weijers D., Lechner E., Yamada M., Hobbie L., Ehrismann J. S., Jürgens G., Estelle M., 2005. Plant development is regulated by a family of auxin receptor F box proteins. Develop. Cell 9, 109-119.
• Duan C.-G., Wang C.-H., Guo H.-S., 2012. Application of RNA silencing to plant disease resistance. Silence 3, 5.
• Ebert M. S., Sharp P. A., 2012. Roles for microRNAs in conferring robustness to biological processes. Cell 149, 515-524.
• Ellis C. M., Nagpal P., Young J. C., Hagen G., Guilfoyle T. J., Reed J. W., 2005. AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 132, 4563-4574.
• Glazińska P., Bracha J., Wilmowicz E., Kopcewicz J., 2011. Udział mikro RNA w rozwoju generatywnym roślin. Kosmos 60, 141-152.
• Gómez G., Martínez G., Pallás V., 2008. Viroid-induced symptoms in Nicotiana benthamiana plants are dependent on RDR6 activity. Plant Physiol. 148, 414-423.
• Griffiths-Jones S., 2004. The microRNA Registry. Nucleic Acids Res. 32, 109-111.
• Griffiths-Jones S., Grocock R. J., van Dongen S., Bateman A., Enright A. J., 2006. miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 34, D140-144.
• Griffiths-Jones S., Saini H.K., van Dongen S., Enright A. J., 2008. miRBase: tools for microRNA genomics. Nucleic Acids Res. 36, 154-158.
• Guilfoyle T. J., Hagen G., 2007. Auxin response factors. Curr. Opin. Plant Biol. 10, 453-460.
• Gutierrez L., Bussell J. D., Pacurar D. I., Schwambach J., Pacurar M., Bellini C., 2009. Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. Plant Cell 21, 3119-3132.
• Hejka T., Kowalczyk S., 2006. Zależna od ubikwityny proteoliza białek w regulacji procesów wzrostu i rozwoju roślin. Post. Biol. Kom. 33, 159-174.
• Henderson I. R., Zhang X., Lu C., Johnson L., Meyers B. C., Green P. J., Jacobsen S. E., 2006. Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning. Nature Genet. 38, 721-725.
• Hohn T., Vazquez F., 2011. RNA silencing pathways of plants: silencing and its suppression by plant DNA viruses. Biochi. Biophys. Acta 1809, 588-600.
• Hunter C., Willmann M. R., Wu G., Yoshikawa M., de la Luz Gutiérrez-Nava M., Poethig S. R., 2006. Trans-acting siRNA-mediated repression of ETTIN and ARF4 regulates heteroblasty in Arabidopsis. Development 133, 2973-2981.
• Katiyar-Agarwal S., Jin H., 2010. Role of small RNAs in host-microbe interactions. Ann. Rev. Phytopathol. 48, 225-246.
• Kepinski S., Leyser O., 2005. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435, 446-451.
• Kozomara A., Griffiths-Jones S., 2011. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 39, 152-157.
• Kruszka K., Pieczynski M., Windels D., Bielewicz D., Jarmolowski A., Szweykowska-Kulinska Z., Vazquez F., 2012. Role of microRNAs and other sRNAs of plants in their changing environments. J. Plant Physiol. 169, 1664-1672.
• Lanet E., Delannoy E., Sormani R., Floris M., Brodersen P., Crété P., Voinnet O., Robaglia C., 2009. Biochemical evidence for translational repression by Arabidopsis microRNAs. Plant Cell 21, 1762-1768.
• Lau S., Jürgens G., De Smet I., 2008. The evolving complexity of the auxin pathway. Plant Cell 20, 1738-1746.
• Li H., Dong Y., Yin H., Wang N., Yang J., Liu X., Wang Y., Wu J., Li X., 2011. Characterization of the stress associated microRNAs in Glycine max by deep sequencing. BMC Plant Biol. 11, 170.
• Liscum E., Reed J. W., 2002. Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol. Biol. 49, 387-400.
• Liu P.-P., Montgomery T.A., Fahlgren N., Kasschau K.D., Nonogaki H., Carrington J.C., 2007. Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J. 52, 133-146.
• Llave C., 2010. Virus-derived small interfering RNAs at the core of plant-virus interactions. Trends Plant Sci. 15, 701-707.
• Mallory A., Vaucheret H., 2010. Form, function, and regulation of ARGONAUTE proteins. Plant Cell 22, 3879-3889.
• Mallory A. C., Bartel D. P., Bartel B., 2005. MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17, 1360-1375.
• Marciniak K., Turowski T., Wilmowicz E., Frankowski K., Kęsy J., Kopcewicz J., 2010. Ligazy ubikwitynowo-białkowe w szlakach sygnałowych auksyn, jasmonianów i giberelin. Post. Biol. Kom. 37, 409-432.
• Marin E., Jouannet V., Herz A., Lokerse A. S., Weijers D., Vaucheret H., Nussaume L., Crespi M. D., Maizel A., 2010. miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22, 1104-1117.
• Martin R. C., Liu P.-P., Goloviznina N. A., Nonogaki H., 2010. MicroRNA, seeds, and Darwin?: diverse function of miRNA in seed biology and plant responses to stress. J. Exp. Bot. 61, 2229-2234.
• miRBase. (b.d.). Pobrano 22 wrzesień 2015, z http://www.mirbase.org/
• Mlotshwa S., Pruss G.J., Peragine A., Endres M.W., Li J., Chen X., Poethig R.S., Bowman L.H., Vance V., 2008. DICER-LIKE2 plays a primary role in transitive silencing of transgenes in Arabidopsis. PloS One 3, e1755.
• Mockaitis K., Estelle M., 2008. Auxin receptors and plant development: a new signaling paradigm. Ann. Rev. Cell Develop. Biol. 24, 55-80.
• Montgomery T. A., Howell M. D., Cuperus J. T., Li D., Hansen J. E., Alexander A. L., Chapman E. J., Fahlgren N., Allen E., Carrington J. C., 2008. Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133, 128-141.
• Mosher R .A., Melnyk C. W., 2010. siRNAs and DNA methylation: seedy epigenetics. Trends Plant Sci. 15, 204-210.
• Nagpal P., Ellis C. M., Weber H., Ploense S. E., Barkawi L. S., Guilfoyle T. J., Hagen G., Alonso J. M., Cohen J. D., Farmer E. E., Ecker J. R., Reed J.W., 2005. Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132, 4107-4118.
• Nakazawa Y., Hiraguri A., Moriyama H., Fukuhara T., 2007. The dsRNA-binding protein DRB4 interacts with the Dicer-like protein DCL4 in vivo and functions in the trans-acting siRNA pathway. Plant Mol. Biol. 63, 777-785.
• Navarro B., Gisel A., Rodio M.-E., Delgado S., Flores R., Di Serio F., 2012. Viroids: how to infect a host and cause disease without encoding proteins. Biochimie 94, 1474-1480.
• Navarro L., Dunoyer P., Jay F., Arnold B., Dharmasiri N., Estelle M., Voinnet O., Jones J. D. G., 2006. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312, 436-439.
• Nemhauser J. L., Feldman L. J., Zambryski P. C., 2000. Auxin and ETTIN in Arabidopsis gynoecium morphogenesis. Development 127, 3877-3888.
• Nowakowska P., Kopcewicz J., 2006. Symplastowy transport bialek i RNA u roslin. Post. Biol. Kom. 3, 473-491.
• Okushima Y., Overvoorde P. J., Arima K., Alonso J. M., Chan A., Chang C., Ecker J. R., Hughes B., Lui A., Nguyen D., Onodera C., Quach H., Smith A., Yu G., Theologis A., 2005. Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17, 444-463.
• Ostrowski M., Jakubowska A., 2008. Receptory auksyn. Post. Biol. Kom. 35, 79-95.
• Parry G., Estelle M., 2006. Auxin receptors: a new role for F-box proteins. Curr. Opin. Cell Biol. 18, 152-156.
• Peragine A., Yoshikawa M., Wu G., Albrecht H. L., Poethig R. S., 2004. SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Develop. 18, 2368-2379.
• Piya S., Shrestha S. K., Binder B., Stewart C. N., Hewezi T., 2014. Protein-protein interaction and gene co-expression maps of ARFs and Aux/IAAs in Arabidopsis. Plant Syst. Synthet. Biol. 5, 744.
• Quint M., Gray W. M., 2006. Auxin signaling. Curr. Opin. Plant Biol. 9, 448-453.
• Rogers K., Chen X., 2013. Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25, 2383-2399.
• Ru P., Xu L., Ma H., Huang H., 2006. Plant fertility defects induced by the enhanced expression of microRNA167. Cell Res. 16, 457-465.
• Rubio-Somoza I., Weigel D., 2011. MicroRNA networks and developmental plasticity in plants. Trends Plant Sci. 16, 258-264.
• Si-Ammour A., Windels D., Arn-Bouldoires E., Kutter C., Ailhas J., Meins F., Vazquez F., 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.
• Vaucheret H., 2006. Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Develop. 20, 759-771.
• Vazquez F., 2006. Arabidopsis endogenous small RNAs: highways and byways. Trends Plant Sci. 11, 460-468.
• Vazquez F., Hohn T., 2013. Biogenesis and Biological Activity of Secondary siRNAs in Plants. Scientifica 2013, 783253.
• Vazquez F., Vaucheret H., Rajagopalan R., Lepers C., Gasciolli V., Mallory A. C., Hilbert J. L., Bartel D. P., Crété P., 2004. Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol. Cell 16, 69-79.
• Vernoux T., Brunoud G., Farcot E., Morin V., Van den Daele H., Legrand J., Oliva M., Das P., Larrieu A., Wells D., Guedon Y., Armitage L., Picard F., Guyomarch S., Cellier C., Parry G., Koumprogiou R., Doonan J. H., Estelle M., Godin C., Kepinski S., Bennett M., De Veylder L., Traas J., 2011. The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Mol. Syst. Biol. 7, 508.
• Vidal E. A., Araus V., Lu C., Parry G., Green P. J., Coruzzi G. M., Gutiérrez R. A., 2010. Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 107, 4477-4482.
• Voinnet O., 2009. Origin, biogenesis, and activity of plant microRNAs. Cell 136, 669-687.
• Wang J.-J., Guo H.-S., 2015. Cleavage of INDOLE-3-ACETIC ACID INDUCIBLE28 mRNA by microRNA847 upregulates auxin signaling to modulate cell proliferation and lateral organ growth in Arabidopsis. Plant Cell 27, 574-590.
• Wang J.-W., Wang L.-J., Mao Y.-B., Cai W.-J., Xue H.-W., Chen X.-Y., 2005. Control of root cap formation by MicroRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17, 2204-2216.
• Wang L., Hua D., He J., Duan Y., Chen Z., Hong X., Gong Z., 2011. Auxin Response Factor2 (ARF2) and its regulated homeodomain gene HB33 mediate abscisic acid response in Arabidopsis. PLoS Genet. 7, e1002172.
• Windels D., Vazquez F., 2011. miR393: integrator of environmental cues in auxin signaling? Plant Signal. Behav. 6, 1672-1675.
• Woodward A. W., Bartel B., 2005. A receptor for auxin. Plant Cell 17, 2425-2429.
• Wu M.-F., Tian Q., Reed J. W., 2006. Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133, 4211-4218.
• Yang J. H., Han S. J., Yoon E. K., Lee W. S., 2006. Evidence of an auxin signal pathway, microRNA167-ARF8-GH3, and its response to exogenous auxin in cultured rice cells. Nucleic Acids Res. 34, 1892-1899.
• Yoon E. K., Yang J. H., Lim J., Kim S. H., Kim S.-K., Lee W. S., 2010. Auxin regulation of the microRNA390-dependent transacting small interfering RNA pathway in Arabidopsis lateral root development. Nucleic Acids Res. 38, 1382-1391.
• Yoshikawa M., Peragine A., Park M. Y., Poethig R. S., 2005. A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Develop. 19, 2164-2175.
• Zhang X., Zhang X., Singh J., Li D., Qu F., 2012. Temperature-dependent survival of Turnip crinkle virus-infected arabidopsis plants relies on an RNA silencing-based defense that requires dcl2, AGO2, and HEN1. J. Virol. 86, 6847-6854.
• Zhao C.-Z., Xia H., Frazier T. P., Yao Y.-Y., Bi Y.-P., Li A.-Q., Li M.J., Li C. S., Zhang B. H., Wang X.-J., 2010. Deep sequencing identifies novel and conserved microRNAs in peanuts (Arachis hypogaea L.). BMC Plant Biol. 10, 3.