The Splicing Variant TFIIIA-7ZF of Viroid-Modulated Transcription Factor IIIA Causes Physiological Irregularities in Transgenic Tobacco and Transient Somatic Depression of "Degradome" Characteristic for Developing Pollen
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
18-10515J
Czech Science Foundation
PubMed
35269406
PubMed Central
PMC8909551
DOI
10.3390/cells11050784
PII: cells11050784
Knihovny.cz E-zdroje
- Klíčová slova
- Nicotiana tabacum, nucleolytic enzymes, plant aging, plant morphology changes, plant transformation, transcription factors, viroid,
- MeSH
- malá nekódující RNA * MeSH
- pyl genetika MeSH
- tabák genetika MeSH
- transkripční faktor TFIIIA MeSH
- užívání tabáku MeSH
- viroidy * genetika MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- malá nekódující RNA * MeSH
- transkripční faktor TFIIIA MeSH
Viroids are small, non-coding, pathogenic RNAs with a significant ability of adaptation to several basic cellular processes in plants. TFIIIA-7ZF, a splicing variant of transcription factor IIIA, is involved in replication of nuclear-replicating viroids by DNA-dependent polymerase II. We overexpressed NbTFIIIA-7ZF from Nicotiana benthamiana in tobacco (Nicotiana tabacum) where it caused morphological and physiological deviations like plant stunting, splitting of leaf petioles, pistils or apexes, irregular branching of shoots, formation of double-blade leaves, deformation of main stems, and modification of glandular trichomes. Plant aging and senescence was dramatically delayed in transgenic lines. Factors potentially involved in viroid degradation and elimination in pollen were transiently depressed in transgenic leaves. This depressed "degradome" in young plants involved NtTudor S-like nuclease, dicers, argonoute 5, and pollen extracellular nuclease I showing expression in tobacco anthers and leaves. Analysis of the "degradome" in tobacco leaves transformed with either of two hop viroids confirmed modifications of the "degradome" and TFIIIA expression. Thus, the regulatory network connected to TFIIIA-7ZF could be involved in plant pathogenesis as well as in viroid adaptation to avoid its degradation. These results support the hypothesis on a significant impact of limited TFIIIA-7ZF on viroid elimination in pollen.
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Shastry B. Transcription factor IIIA (TFIIIA) in the second decade. J. Cell Sci. 1996;109:535–539. doi: 10.1242/jcs.109.3.535. PubMed DOI
Engelke D., Ng S., Shastry B., Roeder R. Specific interaction of a purified transcription factor with an internal control region of 5S RNA genes. Cell. 1980;19:717–728. doi: 10.1016/S0092-8674(80)80048-1. PubMed DOI
Pelham H., Brown D. A specific transcription factor that can bind either the 5S RNA gene or 5S RNA. Proc. Natl. Acad. Sci. USA. 1980;77:4170–4174. doi: 10.1073/pnas.77.7.4170. PubMed DOI PMC
Fu Y., Bannach O., Chen H., Teune J.H., Schmitz A., Steger G., Xiong L., Barbazuk W. Alternative splicing of anciently exonized 5S rRNA regulates plant transcription factor TFIIIA. Genome Res. 2009;19:913–921. doi: 10.1101/gr.086876.108. PubMed DOI PMC
Hammond M., Wachter A., Breaker R. A plant 5S ribosomal RNA mimic regulates alternative splicing of transcription factor IIIA pre-mRNAs. Nat. Struct. Mol. Biol. 2009;16:541–549. doi: 10.1038/nsmb.1588. PubMed DOI PMC
Layat E., Cotterell S., Vaillant I., Yukawa Y., Tutois S., Tourmente S. Transcript levels, alternative splicing and proteolytic cleavage of TFIIIA control 5S rRNA accumulation during Arabidopsis thaliana development. Plant J. 2012;71:35–44. doi: 10.1111/j.1365-313X.2012.04948.x. PubMed DOI
Dissanayaka Mudiyanselage S., Qu J., Tian N., Jiang J., Wang Y. Potato spindle tuber viroid RNA-templated transcription: Factors and regulation. Viruses. 2018;10:503. doi: 10.3390/v10090503. PubMed DOI PMC
Navarro B., Flores R., Di Serio F. Advances in viroid-host interactions. Annu. Rev. Virol. 2021;8:305–325. doi: 10.1146/annurev-virology-091919-092331. PubMed DOI
Venkataraman S., Badar U., Shoeb E., Hashim G., AbouHaidar M., Hefferon K. An inside look into biological miniatures: Molecular mechanisms of viroids. Int. J. Mol. Sci. 2021;22:2795. doi: 10.3390/ijms22062795. PubMed DOI PMC
Hadidi A., Randles J., Flores R., Palukaitis P., editors. Viroids and Satellites. Academic Press, Elsevier; Cambridge, MA, USA: 2017.
Matoušek J., Steinbachová L., Drábková L., Kocábek T., Potěšil D., Mishra A., Honys D., Steger G. Elimination of viroids from tobacco pollen involves a decrease in propagation rate and an increase of the degradation processes. Int. J. Mol. Sci. 2020;21:3029. doi: 10.3390/ijms21083029. PubMed DOI PMC
Steinbachová L., Matoušek J., Steger G., Matoušková H., Radišek S., Honys D. Transformation of seed non-transmissible hop viroids in Nicotiana benthamiana causes distortions in male gametophyte development. Plants. 2021;10:2398. doi: 10.3390/plants10112398. PubMed DOI PMC
Wang Y., Qu J., Ji S., Wallace A., Wu J., Li Y., Gopalan V., Ding B. A land plant-specific transcription factor directly enhances transcription of a pathogenic noncoding RNA template by DNA-dependent RNA polymerase II. Plant Cell. 2016;28:1094–1107. doi: 10.1105/tpc.16.00100. PubMed DOI PMC
Jiang J., Smith H., Ren D., Dissanayaka Mudiyanselage S., Dawe A., Wang L., Wang Y. Potato spindle tuber viroid modulates its replication through a direct interaction with a splicing regulator. J. Virol. 2018;92:e01004-18. doi: 10.1128/JVI.01004-18. PubMed DOI PMC
Matoušek J., Kozlová P., Orctová L., Schmitz A., Pešina K., Bannach O., Diermann D., Steger G., Riesner D. Accumulation of viroid-specific small RNAs and increase of nucleolytic activities linked to viroid-caused pathogenesis. Biol. Chem. 2007;388:1–13. doi: 10.1515/BC.2007.001. PubMed DOI
Tupý J., Süss J., Hrabětová E., Říhova L. Developmental changes in gene expression during pollen differentiation and maturation in Nicotiana tabacum L. Biol. Plant. 1983;25:231. doi: 10.1007/BF02902110. DOI
Jim Haseloff J., Siemering K., Prasher D., Hodge S. Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc. Natl. Acad. Sci. USA. 1997;94:2122–2127. doi: 10.1073/pnas.94.6.2122. PubMed DOI PMC
Ruiz M., Voinnet O., Baulcombe D. Initiation and maintenance of virus-induced gene silencing. Plant. Cell. 1998;10:937–946. doi: 10.1105/tpc.10.6.937. PubMed DOI PMC
Horsch R., Fry J., Hoffmann N., Wallroth M., Eichholtz D., Rogers S., Fraley R. A simple and general method for transferring genes into plants. Science. 1985;227:1229–1231. doi: 10.1126/science.227.4691.1229. PubMed DOI
Matoušek J., Siglová K., Jakše J., Radišek S., Brass J., Tsushima T., Guček T., Duraisamy G., Sano T., Steger G. Propagation and some physiological effects of Citrus bark cracking viroid and Apple fruit crinkle viroid in multiple infected hop (Humulus lupulus L.) J. Plant Physiol. 2017;213:166–177. doi: 10.1016/j.jplph.2017.02.014. PubMed DOI
Matoušek J., Schröder A., Trěná L., Reimers M., Baumstark T., Dědič P., Vlasak J., Becker I., Kreuzaler F., Fladung M., et al. Inhibition of viroid infection by antisense RNA expression in transgenic plants. Biol. Chem. Hoppe-Seyler. 1994;375:765–777. doi: 10.1515/bchm3.1994.375.11.765. PubMed DOI
Palukaitis M., Cotts S., Zaitlin M. Detection and identification of viroids and viral nucleic acids by “dot-blot” hybridization. Acta Hortic. 1985;164:109–118. doi: 10.17660/ActaHortic.1985.164.12. DOI
Pfaffl M. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29:e45. doi: 10.1093/nar/29.9.e45. PubMed DOI PMC
Li W., Li X., Chao J., Zhang Z., Wang W., Guo Y. NAC family transcription factors in tobacco and their potential role in regulating leaf senescence. Front. Plant. Sci. 2018;9:1900. doi: 10.3389/fpls.2018.01900. PubMed DOI PMC
Bolger A., Lohse M., Usadel B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120. doi: 10.1093/bioinformatics/btu170. PubMed DOI PMC
Matoušek J., Kocábek T., Patzak J., Füssy Z., Procházková J., Heyerick A. Combinatorial analysis of lupulin gland transcription factors from R2R3Myb, bHLH and WDR families indicates a complex regulation of chs_H1 genes essential for prenylflavonoid biosynthesis in hop (Humulus lupulus L.) BMC Plant Biol. 2012;12:27. doi: 10.1186/1471-2229-12-27. PubMed DOI PMC
Koval’ T., Lipovová P., Podzimek T., Matoušek J., Dušková J., Skálová T., Štěpánková A., Hašek J., Dohnálek J. Crystallization of recombinant bifunctional nuclease TBN1 from tomato. Acta Cryst. D. 2013;69:1192. doi: 10.1107/S1744309110048177. PubMed DOI PMC
Podzimek T., Matoušek J., Lipovová P., Poučková P., Spiwok V., Santrůček J. Biochemical properties of three plant nucleases with anticancer potential. Plant. Sci. 2011;180:343–351. doi: 10.1016/j.plantsci.2010.10.006. PubMed DOI
Ito J., Fukuda H. ZEN1 is a key enzyme in the degradation of nuclear DNA during programmed cell death of tracheary elements. Plant Cell. 2002;14:3201–3211. doi: 10.1105/tpc.006411. PubMed DOI PMC
Pérez-Amador M., Abler M., De Rocher E., Thompson D., van Hoof A., LeBrasseur N., Lers A., Green P. Identification of BFN1, a bifunctional nuclease induced during leaf and stem senescence in Arabidopsis. Plant. Physiol. 2000;122:169–180. doi: 10.1104/pp.122.1.169. PubMed DOI PMC
Farage-Barhom S., Burd S., Sonego L., Mett A., Belausov E., Gidoni D., Lers A. Localization of the Arabidopsis senescence- and cell death-associated BFN1 nuclease: From the ER to fragmented nuclei. Mol. Plant. 2011;4:1062–1073. doi: 10.1093/mp/ssr045. PubMed DOI
Matoušek J., Tupý J. Developmental changes in nuclease and other phosphohydrolase activities in anthers of Nicotiana tabacum L. J. Plant Physiol. 1987;129:351–362. doi: 10.1016/S0176-1617(87)80092-5. DOI
Matoušek J., Orctová L., Škopek J., Pešina K., Steger G. Elimination of hop latent viroid upon developmental activation of pollen nucleases. Biol. Chem. 2008;389:905–918. doi: 10.1515/BC.2008.096. PubMed DOI
Matoušek J., Tupý J. The release of nucleases from tobacco pollen. Plant Sci. Lett. 1983;30:83–89. doi: 10.1016/0304-4211(83)90206-7. DOI
Adkar-Purushothama C., Perreault J. Current overview on viroid-host interactions. Wiley Interdiscip. Rev. RNA. 2020;11:e1570. doi: 10.1002/wrna.1570. PubMed DOI
Flores R., Navarro B., Delgado S., Serra P., Di Serio F. Viroid pathogenesis: A critical appraisal of the role of RNA silencing in triggering the initial molecular lesion. FEMS Microbiol. Rev. 2020;44:386–398. doi: 10.1093/femsre/fuaa011. PubMed DOI
Minoia S., Navarro B., Delgado S., Di Serio F., Flores R. Viroid RNA turnover: Characterization of the subgenomic RNAs of potato spindle tuber viroid accumulating in infected tissues provides insights into decay pathways operating in vivo. Nucleic Acids Res. 2015;43:2313–2325. doi: 10.1093/nar/gkv034. PubMed DOI PMC
Gutierrez-Beltran E., Moschou P., Smertenko A., Bozhkov P. Tudor staphylococcal nuclease links formation of stress granules and processing bodies with mRNA catabolism in Arabidopsis. Plant Cell. 2015;27:926–943. doi: 10.1105/tpc.114.134494. PubMed DOI PMC
Nohales M.Á., Flores R., Darós J. Viroid RNA redirects host DNA ligase 1 to act as an RNA ligase. Proc. Natl. Acad. Sci. USA. 2012;109:13805–13810. doi: 10.1073/pnas.1206187109. PubMed DOI PMC
Matoušek J., Piernikarczyk R., Týcová A., Duraisamy G., Kocábek T., Steger G. Expression of SANT/HTH Myb mRNA, a plant morphogenesis-regulating transcription factor, changes due to viroid infection. J. Plant Physiol. 2015;183:85–94. doi: 10.1016/j.jplph.2015.06.001. PubMed DOI
Eiras M., Nohales M., Kitajima E., Flores R., Daròs J. Ribosomal protein L5 and transcription factor IIIA from Arabidopsis thaliana bind in vitro specifically Potato spindle tuber viroid RNA. Arch. Virol. 2010;156:529–533. doi: 10.1007/s00705-010-0867-x. PubMed DOI
Matoušek J., Kocábek T., Patzak J., Bříza J., Siglová K., Mishra A., Duraisamy G., Týcová A., Ono E., Krofta K. The “putative” role of transcription factors from HlWRKY family in the regulation of the final steps of prenylflavonid and bitter acids biosynthesis in hop (Humulus lupulus L.) Plant Mol. Biol. 2016;92:263–277. doi: 10.1007/s11103-016-0510-7. PubMed DOI
Patzak J., Henychová A., Matoušek J. Developmental regulation of lupulin gland-associated genes in aromatic and bitter hops (Humulus lupulus L.) BMC Plant Biol. 2021;21:534. doi: 10.1186/s12870-021-03292-z. PubMed DOI PMC