Identification of potassium phosphite responsive miRNAs and their targets in potato

English version

Autoři: María Florencia Rey-Burusco ^aff001; Gustavo Raúl Daleo ^aff001; Mariana Laura Feldman ^aff001
Působiště autorů: Instituto de Investigaciones Biológicas-CONICET, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Mar del Plata, Buenos Aires, Argentina ^aff001
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0222346

Souhrn

Micro RNAs (miRNAs) are small single strand non-coding RNAs that regulate gene expression at the post-transcriptional level, either by translational inhibition or mRNA degradation based on the extent of complementarity between the miRNA and its target mRNAs. Potato (Solanum tuberosum L.) is the most important horticultural crop in Argentina. Achieving an integrated control of diseases is crucial for this crop, where frequent agrochemical applications, particularly fungicides, are carried out. A promising strategy is based on promoting induced resistance through the application of environmentally friendly compounds such as phosphites, inorganic salts of phosphorous acid. The use of phosphites in disease control management has proven to be effective. Although the mechanisms underlying their effect remain unclear, we postulated that miRNAs could be involved. Therefore we performed next generation sequencing (NGS) in potato leaves treated and non treated with potassium phosphite (KPhi). We identified 25 miRNAs that were expressed differentially, 14 already annotated in miRBase and 11 mapped to the potato genome as potential new miRNAs. A prediction of miRNA targets showed genes related to pathogen resistance, transcription factors, and oxidative stress. We also analyzed in silico stress and phytohormone responsive cis-acting elements on differentially expressed pre miRNAs. Despite the fact that some of the differentially expressed miRNAs have been already identified, this is to our knowledge the first report identifying miRNAs responsive to a biocompatible stress resistance inducer such as potassium phosphite, in plants. Further characterization of these miRNAs and their target genes might help to elucidate the molecular mechanisms underlying KPhi-induced resistance.

Klíčová slova:

Biology and life sciences – Genetics – Gene expression – Biochemistry – Nucleic acids – Plant science – Organisms – Eukaryota – Plants – Research and analysis methods – Proteins – DNA-binding proteins – Molecular biology – Plant pathology – Gene regulation – Molecular biology techniques – Solanum – RNA – Non-coding RNA – Transcription factors – Regulatory proteins – Hormones – Ecology and environmental sciences – Plant ecology – Plant-environment interactions – Ecology – Plant physiology – Plant defenses – Plant resistance to abiotic stress – Plant anatomy – Leaves – Plant biochemistry – Natural antisense transcripts – MicroRNAs – Sequencing techniques – Plant hormones – Potato – Vegetables – RNA sequencing

Zdroje

1. FAO STAT Food and Agriculture Organization: Crops statistics database. FAO Prod Stat. 2017. www.fao.org/faostat

2. Arora RK, Sharma S, Singh BP. Late blight disease of potato and its management. Potato J. 2014; 4: 16–40.

3. Importance of potato late blight in Argentina, and the effect of fungicide treatments on yield increments over twenty years. Cien Inv Agr. 2009;36: 115–122. doi: 10.4067/S0718-16202009000100011

4. Trejo-Téllez LI, Gómez-Merino FC. Phosphite as an inductor of adaptive responses to stress and stimulator of better plant performance. In: Vats S, editor. Biotic and Abiotic Stress Tolerance in Plants. Springer, Singapore. 2018. doi: 10.1007/978-981-10-9029-5_8

5. Lobato MC, Olivieri FP, Altamiranda EAG, Wolski EA, Daleo GR, Caldiz DO, et al. Phosphite compounds reduce disease severity in potato seed tubers and foliage. Eur J Plant Pathol. 2008;122: 349–358. doi: 10.1007/s10658-008-9299-9

6. Lobato MC, Machinandiarena MF, Tambascio C, Dosio GAA, Caldiz DO, Daleo GR, et al. Effect of foliar applications of phosphite on post-harvest potato tubers. Eur J Plant Pathol. 2011;130: 155–163. doi: 10.1007/s10658-011-9741-2

7. Olivieri FP, Feldman ML, Machinandiarena MF, Lobato MC, Caldiz DO, Daleo GR, et al. Phosphite applications induce molecular modifications in potato tuber periderm and cortex that enhance resistance to pathogens. Crop Prot. 2012;32: 1–6. doi: 10.1016/j.cropro.2011.08.025

8. Burra DD, Berkowitz O, Hedley PE, Morris J, Resjö S, Levander F, et al. Phosphite-induced changes of the transcriptome and secretome in Solanum tuberosum leading to resistance against Phytophthora infestans. BMC Plant Biol. 2014;14: 1–17. doi: 10.1186/1471-2229-14-1

9. Eshraghi L, Anderson J, Aryamanesh N, Shearer B, Mccomb J, Hardy GESJ, et al. Phosphite primed defense responses and enhanced expression of defense genes in Arabidopsis thaliana infected with Phytophthora cinnamomi. Plant Pathol. 2011;60: 1086–1095. doi: 10.1111/j.1365-3059.2011.02471.x

10. Machinandiarena MF, Lobato MC, Feldman ML, Daleo GR, Andreu AB. Potassium phosphite primes defense responses in potato against Phytophthora infestans. J Plant Physiol. 2012;169: 1417–1424. doi: 10.1016/j.jplph.2012.05.005 22727804

11. Oyarburo NS, Machinandiarena MF, Feldman ML, Daleo GR, Andreu AB, Olivieri FP. Potassium phosphite increases tolerance to UV-B in potato. Plant Physiol Biochem. 2015;88: 1–8. doi: 10.1016/j.plaphy.2015.01.003 25596554

12. Dugas D V., Bartel B. MicroRNA regulation of gene expression in plants. Curr Opin Plant Biol. 2004;7: 512–520. doi: 10.1016/j.pbi.2004.07.011 15337093

13. Sunkar R. MicroRNAs with macro-effects on plant stress responses. Semin Cell Dev Biol. 2010;21: 805–811. doi: 10.1016/j.semcdb.2010.04.001 20398781

14. Jones-Rhoades MW, Bartel DP, Bartel B. MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol. 2006;57: 19–53. doi: 10.1146/annurev.arplant.57.032905.105218 16669754

15. Song X, Li Y, Cao X, Qi Y. microRNAs and their regulatory roles in plant-environment interactions. Annu Rev Plant Biol. 2019;70: 1–37. doi: 10.1146/annurev-arplant-050718-100143

16. Jones-Rhoades MW, Bartel DP. Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell. 2004;14: 787–799. doi: 10.1016/j.molcel.2004.05.027 15200956

17. Devi KJ, Chakraborty S, Deb B, Rajwanshi R. Computational identification and functional annotation of microRNAs and their targets from expressed sequence tags (ESTs) and genome survey sequences (GSSs) of coffee (Coffea arabica L.). Plant Gene. 2016;6: 30–42. doi: 10.1016/j.plgene.2016.03.001

18. Zhang R, Marshall D, Bryan GJ, Hornyik C. Identification and characterization of miRNA transcriptome in potato by high-throughput sequencing. PLoS One. 2013;8. doi: 10.1371/journal.pone.0057233 23437348

19. Lakhotia N, Joshi G, Bhardwaj AR, Katiyar-Agarwal S, Agarwal M, Jagannath A, et al. Identification and characterization of miRNAome in root, stem, leaf and tuber developmental stages of potato (Solanum tuberosum L.) by high-throughput sequencing. BMC Plant Biol. 2014;14: 1–16. doi: 10.1186/1471-2229-14-1

20. Zhang W, Luo Y, Gong X, Zeng W, Li S. Computational identification of 48 potato microRNAs and their targets. Comput Biol Chem. 2009;33: 84–93. doi: 10.1016/j.compbiolchem.2008.07.006 18723398

21. Dai X, Zhao PX. PsRNATarget: A plant small RNA target analysis server. Nucleic Acids Res. 2011;39: 155–159. doi: 10.1093/nar/gkq766

22. Varkonyi-Gasic E, Wu R, Wood M, Walton EF, Hellens RP. Protocol: A highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods. 2007;3: 1–12. doi: 10.1186/1746-4811-3-1

23. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real time quantitative PCR and the 2∆∆C(T) Method. Methods. 2001;25(4): 402–408. doi: 10.1006/meth.2001.1262 11846609

24. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 2002;30: e36. doi: 10.1093/nar/30.9.e36 11972351

25. Lescot M. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002;30: 325–327. doi: 10.1093/nar/30.1.325 11752327

26. Alves MS, Dadalto SP, Gonçalves AB, De Souza GB, Barros VA, Fietto LG. Plant bZIP transcription factors responsive to pathogens: A review. Int J Mol Sci. 2013;14: 7815–7828. doi: 10.3390/ijms14047815 23574941

27. Zhou XT, Jia LJ, Wang HY, Zhao P, Wang WY, Liu N, et al. The potato transcription factor StbZIP61 regulates dynamic biosynthesis of salicylic acid in defense against Phytophthora infestans infection. Plant J. 2018;95: 1055–1068. doi: 10.1111/tpj.14010 29952082

28. Nandety RS, Caplan JL, Cavanaugh K, Perroud B, Wroblewski T, Michelmore RW, et al. The role of TIR-NBS and TIR-X proteins in plant basal defense responses. Plant Physiol. 2013; 162: 1459–1472. doi: 10.1104/pp.113.219162 23735504

29. Lee JJ, Park KW, Kwak YS, Ahn JY, Jung YH, Lee BH, et al. Comparative proteomic study between tuberous roots of light orange- and purple-fleshed sweetpotato cultivars. Plant Sci. 2012;193–194: 120–129. doi: 10.1016/j.plantsci.2012.06.003 22794925

30. Slootweg E, Koropacka K, Roosien J, Dees R, Overmars H, Lankhorst RK, et al. Sequence exchange between homologous NB-LRR genes converts virus resistance into nematode resistance, and vice versa. Plant Physiol. 2017;175: 498–510. doi: 10.1104/pp.17.00485 28747428

31. Jiang N, Meng J, Cui J, Sun G, Luan Y. Function identification of miR482b, a negative regulator during tomato resistance to Phytophthora infestans. Hortic Res. Springer US. 2018; 5. doi: 10.1038/s41438-018-0017-2 29507733

32. Tian ZD, Zhang Y, Liu J, Xie CH. Novel potato C2H2-type zinc finger protein gene, StZFP1, which responds to biotic and abiotic stress, plays a role in salt tolerance. Plant Biology. 2010;12: 689–697. doi: 10.1111/j.1438-8677.2009.00276.x 20701691

33. Sun W, Xu XH, Wu X, Wang Y, Lu X, et al. Genome-wide identification of microRNAs and their targets in wild type and phyB mutant provides a key link between microRNAs and the phyB-mediated light signaling pathway in rice. Front Plant Sci. 2015;6: 372. doi: 10.3389/fpls.2015.00372 26074936

34. Zeng LR, Qu S, Bordeos A, Yang C, Baraoidan M, Yan H, et al. Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-Box/Armadillo repeat protein endowed with E3 ubiquitin ligase activity. Plant Cell Online. 2004;16: 2795–2808. doi: 10.1105/tpc.104.025171 15377756

35. Yamanouchi U, Yano M, Lin H, Ashikari M, Yamada K. A rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein. 2002;99: 7530–7535. doi: 10.1073/pnas.112209199

36. Zhang X, Gonzalez-Carranza ZH, Zhang S, Miao Y, Liu C-J, Roberts JA. F-Box proteins in plants. Annu Plant Rev. 2019; 1–21. doi: 10.1002/9781119312994.apr0701

37. Zhang X, Gou M, Guo C, Yang H, Liu C-J. Down-regulation of Kelch domain-containing F-Box protein in Arabidopsis enhances the production of (poly)phenols and tolerance to ultraviolet radiation. Plant Physiol. 2014;167: 337–350. doi: 10.1104/pp.114.249136 25502410

38. Bengtsson T, Weighill D, Proux-Wéra E, Levander F, Resjö S, Burra DD, et al. Proteomics and transcriptomics of the BABA-induced resistance response in potato using a novel functional annotation approach. BMC Genomics. 2014;15: 1–19. doi: 10.1186/1471-2164-15-1

39. Lim S. Analysis of changes in the potato leaf proteome triggered by phosphite reveals functions associated with induced resistance against Phytophthora infestans. Thesis. Dalhousie University. 2012; Available from: http://dalspace.library.dal.ca/handle/10222/15859

40. Lim S, Borza T, Peters RD, Coffin RH, Al-Mughrabi KI, Pinto DM, et al. Proteomics analysis suggests broad functional changes in potato leaves triggered by phosphites and a complex indirect mode of action against Phytophthora infestans. J Proteom. 2013;93: 207–23. doi: 10.1016/j.jprot.2013.03.010

41. Eshraghi L, Anderson JP, Aryamanesh N, McComb JA, Shearer B, Hardy GSJE. Suppression of the auxin response pathway enhances susceptibility to Phytophthora cinnamomi while phosphite-mediated resistance stimulates the auxin signalling pathway. BMC Plant Biol. 2014;14: 1–15. doi: 10.1186/1471-2229-14-1

42. Massoud K, Barchietto T, Le Rudulier T, Pallandre L, Didierlaurent L, Garmier M, et al. Dissecting phosphite-induced priming in Arabidopsis infected with Hyaloperonospora arabidopsidis. Plant Physiol. 2012;159: 286–298. doi: 10.1104/pp.112.194647 22408091

43. Tsuda K, Somssich IE. Transcriptional networks in plant immunity. New Phytol. 2015;206: 932–947. doi: 10.1111/nph.13286 25623163

44. Checker VG, Kushwaha HR, Kumari P, Yadav S. Role of phytohormones in plant defense: Signaling and cross talk. Mol Asp Plant-Pathogen Interact. 2018; 159–184. doi: 10.1007/978-981-10-7371-7_7

Identification of potassium phosphite responsive miRNAs and their targets in potato

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