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Effect of of boron toxicity on miR393 expression at moderate and severe levels in Arabidopsis thaliana

Year 2020, Volume: 5 Issue: 4, 183 - 191, 29.12.2020
https://doi.org/10.30728/boron.783209

Abstract

miR393, one of the microRNA (miRNA) families preserved in plants, plays a role in many critical developmental processes. In this study, expression levels of miR393 were determined in Arabidopsis thaliana exposed to 1 mM (1B) and 3 mM (3B) boric acid by Stem-Loop (SL) quantitative reverse transcription polymerase chain reaction method. In addition, genes targeted by miR393 in Arabidopsis thaliana and Gene Ontology Enrichment analysis of these genes were performed. After application of toxic levels of B in Arabidopsis thaliana plant, a decrease in the growth of Arabidopsis seedlings and chlorosis on the leaf tips of the seedlings were observed. While 1B application caused a 2.9 fold increase in miR393 expression, 3B application caused a 2.7 fold increase in this expression. According to the mature sequences (5p and 3p) at the 5 'and 3' ends of miR393, the main target genes are; Auxin signaling F-box, S-adenosyl-L-methionine-dependent methyltransferases superfamily protein, kinesin-like calmodulin-binding protein, Leucine-rich receptor-like protein kinase family protein, 1-deoxy-D-xylulose 5-phosphate synthase 3, ARM repeat superfamily protein, myb-like HTH transcriptional regulator family protein and bHLH, and WRKY33 transcription factors. On the other hand, according to the Gene Ontology (GO) Enrichment analysis, the main Biological Processes of the genes targeted by miR393 are as follows: The auxin-activated signaling pathway, the cellular response to auxin, various developmental processes, and different cellular responses. Molecular functions can be categorized as auxin binding, inositol hexakisphosphate binding and hormone and alcohol binding. As a result, growth retardation detected under B toxicity may be related to miR393 targeted auxin regulation and associated transcription factors such as bHLH.

References

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  • [6] Bennett W. F., Nutrient Deficiencies and Toxicities in Crop Plants. APS Press, St Paul, MN, USA, 1993.
  • [7] Fitzpatrick K. L., Reid R. J., The involvement of aquaglyceroporins in transport of boron in barley roots. Plant Cell Environ., 32: 1357-1365, 2009.
  • [8] Blokhina O., Virolainen E., Fagerstedt K. V., Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann. Bot. Lond.) 91, 179-194, 2003.
  • [9] Cervilla L. M., Blasco B., Rios J. J., Rosales M. A., Sanchez-Rodriguez E., et al.,. Parameters symptomatic for boron toxicity in leaves of tomato plants. J. Bot., 1-17, 2012.
  • [10] Pardossi A., Romani M., Carmassi G., Guidi L., Landi M., Incrocci L., Maggini R., Puccinelli M., Vacca W., Ziliani M.,. Boron accumulation and tolerance in sweet basil (Ocimum basilicum L.) with green or purple leaves. Plant Soil., 395, 375-389, 2015.
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  • [29] Wu J., Zhang Y., Zhang H., Huang H., Folta K. M., et al., Whole genome wide expression profiles of Vitis amurensis grape responding to downy mildew by using Solexa sequencing technology. BMC Plant Biology, 10: 234, 2010.
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  • [50] Si-Ammour A., Windels D., Arn-Bouldoires E., Kutter C., Ailhas J., Meins F., Vazquez F., 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, 2011.
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  • [52] Windels D., Bielewicz D., Ebneter M., Jarmolowski A., Szweykowska-Kulinska Z., Vazquez F., miR393 is required for production of proper auxin signalling outputs, PLoS One, 9, e95972, 2014.
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  • [60] Dharmasiri S., Estelle M., The role of regulated protein degradation in auxin response, Plant Mol. Biol., 49, 401-409, 2002.
  • [61] Long R., Li M., Li X., Gao Y., Zhang T., Sun Y., Kang J., et al., A novel miRNA sponge form efficiently inhibits the activity of miR393 and enhances the salt tolerance and ABA insensitivity in Arabidopsis thaliana, Plant Mol. Biol. Rep., 35, 409-415, 2017.

Orta ve şiddetli seviyelerde bor toksisitesinin Arabidopsis thaliana’da miR393 ekspresyonu üzerine etkisi

Year 2020, Volume: 5 Issue: 4, 183 - 191, 29.12.2020
https://doi.org/10.30728/boron.783209

Abstract

Bitkilerde korunmuş olan mikroRNA (miRNA) ailelerinden biri olan miR393, birçok kritik gelişimsel süreçlerde rol oynamaktadır. Bu çalışmada, Stem-Loop (SL) kantitatif ters transkripsiyon polimeraz zincir reaksiyonu yöntemi ile 1 mM (1B) ve 3 mM (3B) borik aside maruz kalan Arabidopsis thaliana'da miR393’ün ekspresyon seviyeleri belirlenmiştir. Ayrıca, miR393’ün Arabidopsis thaliana’da hedeflediği genler ve bu genlerin Gen Ontoloji Zenginleştirme analizi yapılmıştır. Arabidopsis thaliana bitkisinde toksik seviyelerde B uygulaması sonrası, Arabidopsis fideciklerinin büyümesinde düşüş ve fideciklerin yaprak uçlarında klorosis gözlemlenmiştir. Arabidopsis thaliana’da 1B uygulaması miR393 ekspresyonu 2,9 kat artırırken, 3B uygulaması 2.7’lik bir artışa sebep olmuştur. miR393’ün 5’ve 3’ ucundaki olgun dizilere göre (5p ve 3p) başlıca hedef genleri; auxin sinyal F-box, S-adenosil-L-metiyonin- bağımlı metiltransferaz süper familya proteini, Kinezin benzeri kalmodulin-bağlanma proteini, Lösin-zengin reseptör benzeri protein kinaz familya proteini, 1- deoksi-D-ksilüloz 5-fosfat sentaz, ARM tekrar süper familya proteini, myb-benzeri HTH transkripsiyonel regülatör familya proteini ve bHLH, ve WRKY33 transkripsiyon faktörleridir. Öte yandan, miR393’ün hedeflediği genlerin Gen Ontoloji (GO) Zenginleştirme analizine göre başlıca Biyolojik Süreçleri şu şekildedir: Oksin ile aktifleşmiş sinyal yolağı, oksin uyarısına hücresel cevap, çeşitli gelişim süreçleri ve farklı hücresel cevaplardır. Moleküler Fonksiyonlar ise, oksin bağlayıcı, inositol heksakisfosfat bağlayıcı ve hormon ve alkol bağlayıcı şeklinde kategorize edilebilir. Sonuç olarak, B toksisitesi altında tespit edilen büyüme geriliği miR393 hedefli oksin regülasyonu ve bHLH gibi ilişkili transkripsiyon faktörleri ile ilgili olabilir.

References

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  • [2] Landi,M., Degl’Innocenti E., Pardossi A., Guidi L., Antioxidant and photosynthetic responses in plants under boron toxicity: a review. Am. J. Agric. Biol. Sci., 7, 255-270, 2012.
  • [3] Nable R. O., Ba~nuelos G. S., Paull J. G.,. Boron toxicity. Plant Soil, 193, 181-198, 1997.
  • [4] Mengel K., Kirkby E. A., Principles of Plant Nutrition, fifth ed. International Potash Institute, Bern, Switzerland, 2001.
  • [5] Reid R., Hajes J. E., Post A., Stangoulis J.C.R., Graham, R.D., 2004. A critical analysis of the causes of boron toxicity in plants. Plant Cell Environ., 25, 1405-1414.
  • [6] Bennett W. F., Nutrient Deficiencies and Toxicities in Crop Plants. APS Press, St Paul, MN, USA, 1993.
  • [7] Fitzpatrick K. L., Reid R. J., The involvement of aquaglyceroporins in transport of boron in barley roots. Plant Cell Environ., 32: 1357-1365, 2009.
  • [8] Blokhina O., Virolainen E., Fagerstedt K. V., Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann. Bot. Lond.) 91, 179-194, 2003.
  • [9] Cervilla L. M., Blasco B., Rios J. J., Rosales M. A., Sanchez-Rodriguez E., et al.,. Parameters symptomatic for boron toxicity in leaves of tomato plants. J. Bot., 1-17, 2012.
  • [10] Pardossi A., Romani M., Carmassi G., Guidi L., Landi M., Incrocci L., Maggini R., Puccinelli M., Vacca W., Ziliani M.,. Boron accumulation and tolerance in sweet basil (Ocimum basilicum L.) with green or purple leaves. Plant Soil., 395, 375-389, 2015.
  • [11] Ardıc M., Sekmen A. H., Tokur S., Ozdemir F., Turkan I., Antioxidant response of chickpea plants subjected to boron toxicity. Plant Biol., 11, 328-338, 2009.
  • [12] Öz M. T., Yilmaz R., Eyidoǧan F., de Graaff L., Yücel M., Öktem H. A., Microarray Analysis of Late Response to boron toxicity in barley (Hordeum vulgare L.) leaves. Turkish Journal of Agriculture and Forestry, 33, 191-202, 2009.
  • [13] Kayıhan C., Öz M. T., Eyidoğan F., Yücel M., Öktem H. A., Physiological, biochemical, and transcriptomic responses to boron toxicity in leaf and root tissues of contrasting wheat cultivars. Plant Molecular Biology Reporter, 35: 97-109, 2017.
  • [14] Zhang B., (2015). MicroRNA: a new target for improving plant tolerance to abiotic stress. Journal of Experimental Botany, 66 (7): 1749-1761.
  • [15] Kramer M. F., Stem-loop RT-qPCR for miRNAs. Current Protocols in Molecular Biology 15 (1): 15.10.1-15.10.15, 2011.
  • [16] Gautam V., Singh A., Singh S., Sarkar A. K., An efficient LCM based method for tissue specific expression analysis of genes and miRNAs. Scientific Reports, 6: 21577, 2016.
  • [17] Balcells I., Cirera S., Busk P. K., Specific and sensitive quantitative RT-PCR of miRNAs with DNA primers. BMC Biotechnol., 11: 70, 2011.
  • [18] Murashige, T., Skoog, F., A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant., 15, 473-497, 1962.
  • [19] Varkonyi-Gasic E., Wu R., Wood M., Walton E. F., Hellens R. P., Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods, 3: 12, 2007.
  • [20] Kayıhan D. S., Kayıhan C., Çiftçi Y. Ö. Excess boron responsive regulations of antioxidative mechanism at physio-biochemical and molecular levels in Arabidopsis thaliana. Plant Physiology and Biochemistry, 109: 337-345, 2016.
  • [21] Kozomara A., Birgaoanu M., Griffiths-Jones S., miRBase: from microRNA sequences to function. Nucleic acids research,, 47(D1), D155-D162, 2019.
  • [22] Dai X., Zhuang Z., Zhao P. X., psRNATarget: a plant small RNA target analysis server (2017 release). Nucleic acids research,, 46(W1), W49-W54, 2018.
  • [23] Mi H., Muruganujan A., Ebert D., Huang X., Thomas P.D., PANTHER version 14: more genomes, a new PANTHER GO-slim and improvements in enrichment analysis tools. Nucleic acids research, 47(D1), D419-D426, 2019.
  • [24] Llave C., Xie Z., Kasschau K. D., Carrington J. C., Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science, 297 (5589): 2053-2056, 2002
  • [25] Bartel D., MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116: 281-297, 2004.
  • [26] Jones-Rhoades M. W., Bartel D. P., Computational identification of plant microRNAs and their targets, including a stressinduced miRNA. Molecular Cell, 14: 787-799, 2004
  • [27] Zhang B. H., Pan X. P., Wang Q. L., Cobb G. P., Anderson T. A., Identification and characterization of new plant microRNAs using EST analysis. Cell Research, 15: 336-360. 2005.
  • [28] Hsieh L. C., Lin S. I., Shih A. C. C., Chen J. W, Lin W. Y., et al., Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiology, 151: 2120-2132, 2009.
  • [29] Wu J., Zhang Y., Zhang H., Huang H., Folta K. M., et al., Whole genome wide expression profiles of Vitis amurensis grape responding to downy mildew by using Solexa sequencing technology. BMC Plant Biology, 10: 234, 2010.
  • [30] Ozhuner E., Eldem V., Ipek A., Okay S., Sakcali S., et al., Boron stress responsive microRNAs and their targets in barley. PLoS ONE, 8 (3): e59543, 2013.
  • [31] Huang J. H., Qi Y. P., Wen S. X., Guo P., Chen X. M., et al., Illumina microRNA profiles reveal the involvement of miR397a in citrus adaptation to long-term boron toxicity via modulating secondary cell-wall biosynthesis. Scientific Reports, 6: 22900, 2016.
  • [32] Kayihan D. S., Kayihan C., Çiftçi Y. O., Moderate level of toxic boron causes diferential regulation of microRNAs related to jasmonate and ethylene metabolisms in Arabidopsis thaliana. Turk Journal of Botany, 43: 167-172, 2019.
  • [33] Kepinski S., Leyser O., The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature, 435(7041):446–451, 2005.
  • [34] Dharmasiri N., Dharmasiri S., Estelle M., The F-box protein TIR1 is an auxin receptor. Nature, 435(7041):441–445, 2005.
  • [35] Dharmasiri N., Dharmasiri S., Weijers D., Lechner E., Yamada M., Hobbie L., Ehrismann J. S., Jurgens G., Estelle M., Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell., 9(1):109–119, 2005.
  • [36] Vidal E. A., Araus V, Lu C., Parry G., Green P. J., Coruzzi G. M., Gutierrez R. A., Nitrate-responsive miR393/AFB3 regulatory modüle controls root system architecture in Arabidopsis thaliana. Proc Natl Acad Sci USA., 107(9):4477–4482, 2010.
  • [37] Si-Ammour A., Windels D., Arn-Bouldoires E., Kutter C., Ailhas J., Meins F., et al., 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, 2011.
  • [38] Chen Z. H., Bao M. L., Sun Y. Z., Yang Y. J., Xu X. H., Wang J. H. et al., Regulation of auxin response by miR393-targeted transport inhibitör response protein 1 is involved in normal development in Arabidopsis. Plant Mol. Biol., 77: 619–629, 2011.
  • [39] Windels D., Bielewicz D., Ebneter M., Jarmolowski A., Szweykowska Kulinska Z., Vazquez F., miR393 is required for production of proper auxin signalling outputs. PLoS One, 9: e95972, 2014. [40] Sunkar R., Zhu J. K., Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell, 16: 2001-2019, 2004.
  • [41] Navarro L., Dunoyer P., Jay F., Arnold B., Dharmasiri N., Estelle M., et al., A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science, 312: 436–439, 2006.
  • [42] Gao P., Bai X., Yang L., Lv D., Pan X., Li Y., et al., osa-MIR393: a salinity- and alkaline stress-related microRNA gene. Mol. Biol. Rep., 38: 237–242, 2011.
  • [43] Bian H., Xie Y., Guo F., Han N., Ma S., Zeng Z., et al., Distinctive expression patterns and roles of the miRNA393/TIR1 homolog modüle in regulating flag leaf inclination and primary and crown root growth in rice (Oryza sativa). New Phytol., 196: 149–161, 2012.
  • [44] Xia K., Wang R., Ou X., Fang Z., Tian C., Duan J., et al., OsTIR1 and OsAFB2 downregulation via OsmiR393 overexpression leads to more tillers, early flowering and less tolerance to salt and drought in rice. PLoS One, 7: e30039, 2012. [45] Zhao .B, Liang R., Ge L., Li W., Xiao H., Lin H., Ruan K., Jin Y., Identification of drought-induced microRNAs in rice. Biochemical and Biophysical Research Communications, 354, 585–590, 2007.
  • [46] Ferreira T. H., Gentile A., Vilela R. D., Costa G. G., Dias L. I., Endres L., Menossi M.,. microRNAs associated with drought response in the bioenergy crop sugarcane (Saccharum spp.). PLoS One, 7, e46703, 2012.
  • [47] Dharmasiri S., Estelle M., The role of regulated protein degradation in auxin response. Plant Molecular Biology., 49, 401–409, 2002.
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There are 59 citations in total.

Details

Primary Language Turkish
Journal Section Research Article
Authors

Ceyhun Kayıhan

Publication Date December 29, 2020
Acceptance Date November 11, 2020
Published in Issue Year 2020 Volume: 5 Issue: 4

Cite

APA Kayıhan, C. (2020). Orta ve şiddetli seviyelerde bor toksisitesinin Arabidopsis thaliana’da miR393 ekspresyonu üzerine etkisi. Journal of Boron, 5(4), 183-191. https://doi.org/10.30728/boron.783209

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