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, 251:7 | Cite as

Up-regulation of microRNA targets correlates with symptom severity in Citrus sinensis plants infected with two different isolates of citrus psorosis virus

  • Facundo E. Marmisolle
  • Ailín Arizmendi
  • Andrés Ribone
  • Máximo Rivarola
  • María L. García
  • Carina A. ReyesEmail author
Original Article
First Online:

Abstract

Main conclusion

miRNA targets from Citrus sinensis are predicted and validated using degradome data. They show an up-regulation upon infection with CPsV, with a positive correlation between target expression and symptom severity.

Abstract

Sweet orange (Citrus sinensis) may suffer from disease symptoms induced by virus infections, thus resulting in drastic economic losses. Infection of sweet orange plants with two isolates of citrus psorosis virus (CPsV), expressing different symptomatologies, alters the accumulation of a set of endogenous microRNAs (miRNAs). Here, we predicted ten putative targets from four down-regulated miRNAs: three belonging to the CCAAT-binding transcription factor family (CBFAs); an Ethylene-responsive transcription factor (RAP2-7); an Integrase-type DNA-binding superfamily protein (AP2B); Transport inhibitor response 1 (TIR1); GRR1-like protein 1-related (GRR1); Argonaute 2-related (AGO2), Argonaute 7 (AGO7), and a long non-coding RNA (ncRNA). We validated six of them through analysis of leaf degradome data. Expressions of the validated targets increase in infected samples compared to healthy tissue, showing a more striking up-regulation those samples with higher symptom severity. This study contributes to the understanding of the miRNA-mediated regulation of important transcripts in Citrus sinensis through target validation and shed light in the manner a virus can alter host regulatory mechanisms leading to symptom expression.

Keywords

CPsV Degradome analysis MicroRNAs Sweet orange Targets 

Abbreviations

AGO2

Argonaute 2-related

AGO7

Argonaute 7

AP2B

Integrase-type DNA-binding superfamily protein

CBF

CCAAT-binding transcription factor

CPsV

Citrus psorosis virus

GRR1

GRR1-like protein 1-related

ncRNA

Non-coding RNA

RAP2-7

Ethylene-responsive transcription factor

Targets

Targeting specific transcript RNAs

TIR1

Transport inhibitor response 1

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Notes

Acknowledgements

We thank Dr. Carmen Hernández Fort and Dr. Eduardo J. Peña for critical reading of the manuscript. We also thank Romina N. Ramos for help with statistical analysis and A.E. Claudio A. Gómez (Laboratorio de Protección Vegetal y Biotecnología, EEA-Concordia, INTA) for providing Citrus sinensis plants.

Supplementary material

425_2019_3294_MOESM1_ESM.pdf (477 kb)
Fig. S1 Target plot (t-plot) of validated miRNAs targets in Citrus sinensis. The abundance of each signature is plotted as a function of its position in the transcript. Slicing site (red dot) coincides with a high stack of reads (PDF 476 kb)
425_2019_3294_MOESM2_ESM.tif (163.2 mb)
Table S1 Oligonucleotides used for primers. All sequences ID were taken from http://citrus.hzau.edu.cn. The respective annealing temperatures used in qPCR analysis are indicated. Primer efficiency (E) was calculated as: 10(-1/slope). Slope shows the correlation between the number of copies and the Ct mean for each pair of primers. The  % Efficiency = (E – 1) × 100% (TIFF 167115 kb)

References

  1. Addo-Quaye C, Miller W, Axtell MJ (2009) CleaveLand: a pipeline for using degradome data to find cleaved small RNA targets. Bioinformatics 25(1):130–131.  https://doi.org/10.1093/bioinformatics/btn604 CrossRefPubMedGoogle Scholar
  2. Alam MM, Tanaka T, Nakamura H, Ichikawa H et al (2015) Overexpression of a rice heme activator protein gene (OsHAP2E) confers resistance to pathogens, salinity and drought, and increases photosynthesis and tiller number. Plant Biotechnol J 13:85–96.  https://doi.org/10.1111/pbi.12239 CrossRefPubMedGoogle Scholar
  3. Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221.  https://doi.org/10.1016/j.cell.2005.04.004 CrossRefPubMedGoogle Scholar
  4. Alvarado VY, Scholthof HB (2011) AGO2: a new argonaute compromising plant virus accumulation. Front Plant Sci 2:112.  https://doi.org/10.3389/fpls.2011.00112 CrossRefPubMedGoogle Scholar
  5. Bahieldin A, Atef A, Edris S, Gadalla NO et al (2016) Ethylene responsive transcription factor ERF109 retards PCD and improves salt tolerance in plant. BMC Plant Biol 16:216.  https://doi.org/10.1186/s12870-016-0908-z CrossRefPubMedPubMedCentralGoogle Scholar
  6. Ballif J, Endo S, Kotani M, MacAdam J, Wu Y (2011) Over-expression of HAP3b enhances primary root elongation in Arabidopsis. Plant Physiol Biochem 49:579–583.  https://doi.org/10.1016/j.plaphy.2011.01.013 CrossRefPubMedGoogle Scholar
  7. Bartel DP (2004) microRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297.  https://doi.org/10.1016/S0092-8674(04)00045-5 CrossRefPubMedGoogle Scholar
  8. Bazzini AA, Hopp HE, Beachy RN, Asurmendi S (2007) Infection and coaccumulation of tobacco mosaic virus proteins alter microRNA levels, correlating with symptom and plant development. Proc Natl Acad Sci USA 104:12157–12162.  https://doi.org/10.1073/pnas.0705114104 CrossRefPubMedGoogle Scholar
  9. Boava LP, Cristofani-Yaly M, Mafra VS, Kubo K et al (2011) Global gene expression of Poncirus trifoliata, Citrus sunki and their hybrids under infection of Phytophthora parasitica. BMC Genomics 12:1–13.  https://doi.org/10.1186/1471-2164-12-39 CrossRefGoogle Scholar
  10. Borniego MB, Karlin D, Pena EJ, Robles Luna G, Garcia ML (2016) Bioinformatic and mutational analysis of ophiovirus movement proteins, belonging to the 30 K superfamily. Virology 498:172–180.  https://doi.org/10.1016/j.virol.2016.08.027 CrossRefPubMedGoogle Scholar
  11. Brousse C, Liu Q, Beauclair L, Deremetz A, Axtell MJ, Bouche N (2014) A non-canonical plant microRNA target site. Nucleic Acids Res 42:5270–5279.  https://doi.org/10.1093/nar/gku157 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cardon GH, Höhmann S, Nettesheim K, Saedler H, Huijser P (1997) Functional analysis of the Arabidopsis thaliana SBP-box gene SPL3: a novel gene involved in the floral transition. Plant J 12:367–377.  https://doi.org/10.1046/j.1365-313X.1997.12020367.x CrossRefPubMedGoogle Scholar
  13. Cardon G, Höhmann S, Klein J, Nettesheim K, Saedler H, Huijser P (1999) Molecular characterisation of the Arabidopsis SBP-box genes. Gene 237(1):91–104.  https://doi.org/10.1016/S0378-1119(99)00308-X CrossRefPubMedGoogle Scholar
  14. Chen J, Feng J, Liao Q, Chen S, Zhang J, Lang Q et al (2012) Analysis of tomato microRNAs expression profile induced by Cucumovirus and Tobamovirus infections. J Nanosci Nanotechnol 12(1):143–150.  https://doi.org/10.1166/jnn.2012.5112 CrossRefPubMedGoogle Scholar
  15. Chorostecki U, Palatnik JF (2014) comTAR: a web tool for the prediction and characterization of conserved microRNA targets in plants. Bioinformatics 30(14):2066–2067.  https://doi.org/10.1093/bioinformatics/btu147 CrossRefPubMedGoogle Scholar
  16. Cui LG, Shan JX, Shi M, Gao JP, Lin HX (2014) The miR156-SPL9-DFR pathway coordinates the relationship between development and abiotic stress tolerance in plants. Plant J 80(6):1108–1117.  https://doi.org/10.1111/tpj.12712 CrossRefPubMedGoogle Scholar
  17. Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155–W159.  https://doi.org/10.1093/nar/gkr319 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Dangl JL, Horvath DM, Staskawicz BJ (2013) Pivoting the plant immune system from dissection to deployment. Science 341:746–751.  https://doi.org/10.1126/science.1236011 CrossRefPubMedGoogle Scholar
  19. Danós E (1990) La psorosis de los cítricos: la epidemia en curso en Argentina y el desafío de su control. En Revista de Investigaciones Agropecuarias, International Foundation for Science (IFS) e Instituto Nacional de Tecnología Agropecuaria (INTA) edn: pp 265–277Google Scholar
  20. Dharmasiri N, Dharmasiri S, Weijers D, Lechner E et al (2005) Plant development is regulated by a family of auxin receptor F-box proteins. Dev Cell 9:109–119.  https://doi.org/10.1016/j.devcel.2005.05.014 CrossRefPubMedGoogle Scholar
  21. Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11:539–548.  https://doi.org/10.1038/nrg2812 CrossRefPubMedGoogle Scholar
  22. Du Z, Xiao D, Wu J, Jia D, Yuan Z et al (2011) p2 of rice stripe virus (RSV) interacts with OsSGS3 and is a silencing suppressor. Mol Plant Pathol 12(8):808–814.  https://doi.org/10.1111/j.1364-3703.2011.00716.x CrossRefPubMedPubMedCentralGoogle Scholar
  23. García ML, Derrick KS, Grau O (1993) Citrus psorosis associated virus and citrus ringspot virus belong to a new virus group. In: Moreno P, da Graça JV, Timmer LW (eds) Proc 12th conference intern organization of citrus virologists. IOCV, University of California, Riverside, pp 430–431Google Scholar
  24. García ML, Bo ED, da Graca JV, Gago-Zachert S et al (2017) ICTV virus taxonomy profile: ophioviridae. J Gen Virol 98:1161–1162.  https://doi.org/10.1099/jgv.0.000836 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Garnsey SM, Timmer LW (1980) Mechanical transmissibility of citrus ringspot virus isolates from Florida, Texas, and California. In: Calavan EC, Garnsey SM, Timmer LW (eds) Proc 8th conference intern organization of citrus virologists. IOCV, Riverside, pp 174–179Google Scholar
  26. Garnsey SM, Youtsey CO, Bridges GD, Burnett HC (1976) A necrotic ringspot-like virus found in a ‘Star Ruby’ grapefruit tree imported without authorization from Texas. Proc Fla State Hortic Soc 89:63–67Google Scholar
  27. Gómez CA (2019) Metodologías de diagnóstico de CPsV (psorosis) en cítricos. (3200). https://inta.gob.ar/sites/default/files/inta_concordia_metodologia_de_diagnostico_de_psorosis_en_citricos.pdf. Accessed 20 Nov 2019
  28. Harvey JJW, Lewsey MG, Patel K, Westwood J et al (2011) An antiviral defense role of AGO2 in plants. PLoS One 6(1):e14639.  https://doi.org/10.1371/journal.pone.0014639 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hou C, Lee W, Chou H, Chen A, Chou S, Chen H (2016) Global analysis of truncated RNA ends reveals new insights into ribosome stalling in plants. The Plant Cell 28:2398–2416.  https://doi.org/10.1105/tpc.16.00295 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Jagtap S, Shivaprasad PV (2014) Diversity, expression and mRNA targeting abilities of Argonaute-targeting miRNAs among selected vascular plants. BMC Genomics 15(1):1049.  https://doi.org/10.1186/1471-2164-15-1049 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Jin D, Wang Y, Zhao Y, Chen M (2013) microRNAs and their cross-talks in plant development. J Gen Genomics 40:161–170.  https://doi.org/10.1016/j.jgg.2013.02.003 CrossRefGoogle Scholar
  32. Jones P, Binns D, Chang HY, Fraser M et al (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30:1236–1240.  https://doi.org/10.1093/bioinformatics/btu031 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799CrossRefGoogle Scholar
  34. Jones-Rhoades MW, Bartel DP, Bartel B (2006) microRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53.  https://doi.org/10.1146/annurev.arplant.57.032905.105218 CrossRefPubMedGoogle Scholar
  35. Khraiwesh B, Zhu JK, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. BiochimBiophys Acta 1819:137–148.  https://doi.org/10.1016/j.bbagrm.2011.05.001 CrossRefGoogle Scholar
  36. Klein J, Saedler H, Huijser P (1996) A new family of DNA binding proteins includes putative transcriptional regulators of the Antirrhinum majus floral meristem identity gene Squamosa. Mol Gen Genet 250(1):7–16.  https://doi.org/10.1007/bf02191820 CrossRefPubMedGoogle Scholar
  37. Langmead B (2010) Aligning short sequencing reads with Bowtie. Curr Protoc Bioinform 11:11–17.  https://doi.org/10.1002/0471250953.bi1107s32 CrossRefGoogle Scholar
  38. Lee H, Fischer RL, Goldberg RB, Harada JJ (2003) Arabidopsis LEAFY COTYLEDON1 represents a functionally specialized subunit of the CCAAT binding transcription factor. Proc Natl Acad Sci USA 100:2152–2156.  https://doi.org/10.1073/pnas.0437909100 CrossRefPubMedGoogle Scholar
  39. Li WX, Oono Y, Zhu J, He XJ et al (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and post-transcriptionally to promote drought resistance. Plant Cell 20:2238–2251.  https://doi.org/10.1105/tpc.108.059444 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Li S, Le B, Ma X, Li S, You C et al (2016) Biogenesis of phased siRNAs on membrane-bound polysomes in Arabidopsis. ELife 5:e22750.  https://doi.org/10.7554/elife.22750 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Liang C, Liu H, Hao J, Li J, Luo L (2019) Expression profiling and regulatory network of cucumber microRNAs and their putative target genes in response to cucumber green mottle mosaic virus infection. Arch Virol 164:1121–1134.  https://doi.org/10.1007/s00705-019-04152-w CrossRefPubMedPubMedCentralGoogle Scholar
  42. Liu JX, Howell SH (2010) Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell 22:2930–2942.  https://doi.org/10.1105/tpc.110.078154 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Liu Y, Wang L, Chen D, Wu X et al (2014) Genome-wide comparison of microRNAs and their targeted transcripts among leaf, flower and fruit of sweet orange. BMC Genomics 15(1):695.  https://doi.org/10.1186/1471-2164-15-695 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Martin S, Garcia ML, Troisi A, Rubio L et al (2006) Genetic variation of populations of citrus psorosis virus. J Gen Virol 87:3097–3102.  https://doi.org/10.1099/vir.0.81742-0 CrossRefPubMedGoogle Scholar
  45. Mu J, Tan H, Hong S, Liang Y, Zuo J (2013) Arabidopsis transcription factor genes NF-YA1, 5, 6, and 9 play redundant roles in male gametogenesis, embryogenesis, and seed development. Mol Plant 6:188–201.  https://doi.org/10.1093/mp/sss061 CrossRefPubMedGoogle Scholar
  46. Naum-Onganı́a G, Gago-Zachert S, Peña EJ et al (2003) Citrus psorosis virus RNA 1 is of negative polarity and potentially encodes in its complementary strand a 24 K protein of unknown function and 280 K putative RNA dependent RNA polymerase. Virus Res 96:49–61.  https://doi.org/10.1016/S0168-1702(03)00172-2 CrossRefPubMedGoogle Scholar
  47. Padmanabhan MS, Ma S, Burch-Smith TM, Czymmek K et al (2013) Novel positive regulatory role for the SPL6 transcription factor in the N TIR-NB-LRR receptor-mediated plant innate immunity. PLoS Pathog 9:e1003235.  https://doi.org/10.1371/journal.ppat.1003235 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Pagnussat GC, Yu HJ, Ngo QA, Rajani S et al (2005) Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development 132:603–614.  https://doi.org/10.1242/dev.01595 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Peña EJ, Robles Luna G, Zanek MC, Borniego MB et al (2012) Citrus psorosis and mirafiori lettuce big-vein ophiovirus coat proteins localize to the cytoplasm and self interact in vivo. Virus Res 170:34–43.  https://doi.org/10.1016/j.virusres.2012.08.005 CrossRefPubMedGoogle Scholar
  50. Qu F, Ye X, Morris TJ (2008) Arabidopsis DRB4, AGO1, AGO7 and RDR6 participate in a DCL4-initiated antiviral RNA silencing pathway negatively regulated by DCL1. Proc Natl Acad Sci USA 105:14732–14737.  https://doi.org/10.1073/pnas.0805760105 CrossRefPubMedGoogle Scholar
  51. Reyes CA, Ocolotobiche EE, Marmisolle FE, Robles Luna G et al (2016) Citrus psorosis virus 24 K protein interacts with citrus miRNA precursors, affects their processing and subsequent miRNA accumulation and target expression. Mol Plant Pathol 17(3):317–329.  https://doi.org/10.1111/mpp.12282 CrossRefPubMedGoogle Scholar
  52. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110(4):513–520.  https://doi.org/10.1016/S0092867402008632 CrossRefPubMedGoogle Scholar
  53. Robles Luna G, Peña EJ, Borniego MB, Heinlein M, Garcia ML (2013) Ophioviruses CPsV and MiLBVV movement protein is encoded in RNA 2 and interacts with the coat protein. Virology 441(2):152–161.  https://doi.org/10.1016/j.virol.2013.03.019 CrossRefPubMedGoogle Scholar
  54. Robles Luna G, Reyes CA, Peña EJ, Ocolotobiche E et al (2017) Identification and characterization of two RNA silencing suppressors encoded by ophioviruses. Virus Res 235:96–105.  https://doi.org/10.1016/j.virusres.2017.04.013 CrossRefPubMedGoogle Scholar
  55. Robles Luna G, Peña EJ, Borniego MB, Heinlein M, García ML (2018) Citrus psorosis virus movement protein contains an aspartic protease required for autocleavage and the formation of tubule-like structures at plasmodesmata. J Virol 92(21):1–18.  https://doi.org/10.1128/jvi.00355-18 CrossRefGoogle Scholar
  56. Roistacher CN (1991) Graft-transmissible diseases of citrus: Handbook for detection and diagnosis. Rome: International Organization of Citrus Virologists. Food and Agriculture Organization of the United NationsGoogle Scholar
  57. Roistacher CN (1993) Psorosis—a review. 12th Conf International Organisation of Citrus Virologists. IOCV, Riverside, pp 139–162Google Scholar
  58. Singh K, Talla A, Qiu W (2012) Small RNA profiling of virus-infected grapevines: evidences for virus infection-associated and variety-specific miRNAs. Funct Integr Genomics 12:659–669.  https://doi.org/10.1007/s10142-012-0292-1 CrossRefPubMedGoogle Scholar
  59. Song C, Jia Q, Fang J, Li F, Wang C, Zhang Z (2010a) Computational identification of citrus microRNAs and target analysis in citrus expressed sequence tags. Plant Biol 12:927–934.  https://doi.org/10.1111/j.1438-8677.2009.00300.x CrossRefPubMedGoogle Scholar
  60. Song C, Wang C, Zhang C, Korir NK et al (2010b) Deep sequencing discovery of novel and conserved microRNAs in trifoliate orange (Citrus trifoliata). BMC Genomics 11:431.  https://doi.org/10.1186/1471-2164-11-431 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Tagami Y, Inaba N, Kutsuna N, Kurihara Y, Watanabe Y (2007) Specific enrichment of miRNAs in Arabidopsis thaliana infected with tobacco mosaic virus. DNA Res 14:227–233.  https://doi.org/10.1093/dnares/dsm022 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Tang G, Reinhart BJ, Bartel DP, Zamore PD (2003) A biochemical framework for RNA silencing in plants. Genes Dev 17:49–63.  https://doi.org/10.1101/gad.1048103 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Tong A, Yuan Q, Wang S, Peng J et al (2017) Altered accumulation of osa-miR171b contributes to rice stripe virus infection by regulating disease symptoms. J Exp Bot 68:4357–4367.  https://doi.org/10.1093/jxb/erx230 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687.  https://doi.org/10.1016/j.cell.2009.01.046 CrossRefPubMedGoogle Scholar
  65. Wang A (2015) Dissecting the molecular network of virus-plant interactions: the complex roles of host factors. Annu Rev Phytopathol.  https://doi.org/10.1146/annurev-phyto-080614-120001 CrossRefPubMedGoogle Scholar
  66. Warpeha KM, Upadhyay S, Yeh J, Adamiak J et al (2007) The GCR1, GPA1, PRN1, NF-Y signal chain mediates both blue light and abscisic acid responses in Arabidopsis. Plant Physiol 143:1590–1600.  https://doi.org/10.1104/pp.106.089904 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Wu XM, Liu MY, Xu Q, Guo WW (2010) Identification and characterization of microRNAs from citrus expressed sequence tags. Tree Gen Genome 7:117–133.  https://doi.org/10.1007/s11295-010-0319-5 CrossRefGoogle Scholar
  68. Xiao B, Yang X, Ye CY, Liu Y et al (2014) A diverse set of miRNAs responsive to begomovirus-associated betasatellite in Nicotiana benthamiana. BMC Plant Biol 14(1):60.  https://doi.org/10.1186/1471-2229-14-60 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Xu Q, Chen LL, Ruan X, Chen D et al (2013) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45:59–66.  https://doi.org/10.1038/ng.2472 CrossRefPubMedGoogle Scholar
  70. Xu D, Mou G, Wang K, Zhou G (2014) microRNAs responding to southern rice black-streaked dwarf virus infection and their target genes associated with symptom development in rice. Virus Res 190:60–68.  https://doi.org/10.1016/j.virusres.2014.07.007 CrossRefPubMedGoogle Scholar
  71. Yin Z, Murawska Z, Xie F, Pawelkowicz M et al (2018) microRNA response in potato virus Y infected tobacco shows strain-specificity depending on host and symptom severity. Virus Res 260:20–32.  https://doi.org/10.1016/j.virusres.2018.11.002 CrossRefPubMedGoogle Scholar
  72. Yu X, Willmann MR, Anderson SJ, Gregory BD (2016) Genome-wide mapping of uncapped and cleaved transcripts reveals a role for the nuclear mRNA ´cap-binding complex in co-translational RNA decay in Arabidopsis. Plant Cell 28:2385–2397.  https://doi.org/10.1105/tpc.16.00456 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Zanek MC, Peña EJ, Reyes CA, Figueroa J et al (2006) Detection of citrus psorosis virus in the northwestern citrus production area of Argentina by using an improved TAS-ELISA. J Virol Methods 137:245–251.  https://doi.org/10.1016/j.jviromet.2006.06.021 CrossRefPubMedGoogle Scholar
  74. Zhang JZ, Ai XY, Guo WW, Peng SA et al (2012) Identification of miRNAs and their target genes using deep sequencing and degradome analysis in trifoliate orange [Poncirus trifoliata L. Raf] [corrected]. Mol Biotechnol 51:44–57.  https://doi.org/10.1007/s12033-011-9439-x CrossRefPubMedGoogle Scholar
  75. Zhu QH, Helliwell CA (2011) Regulation of flowering time and floral patterning by miR172. J Exp Bot 62:487–495.  https://doi.org/10.1093/jxb/erq295 CrossRefPubMedGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Facundo E. Marmisolle
    • 1
  • Ailín Arizmendi
    • 1
  • Andrés Ribone
    • 2
  • Máximo Rivarola
    • 2
  • María L. García
    • 1
  • Carina A. Reyes
    • 1
    Email author
  1. 1.Instituto de Biotecnología y Biología Molecular, CCT-La Plata, CONICET-UNLPBuenos AiresArgentina
  2. 2.IABiMo, Conicet-INTA, CICVyA-INTABuenos AiresArgentina

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