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Overexpression of microRNA395c or 395e affects differently the seed germination of Arabidopsis thaliana under stress conditions

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Abstract

The Arabidopsis genome encodes six members of microRNA395 (miR395) family previously determined to regulate the expression of ATP sulfurylase (APS) and the sulfate transporter SULTR2;1. However, the mRNA targets for the individual miR395 family members and the biological consequences produced by target gene regulation of each miR395 remain to be identified. In this study, a transgenic approach was employed to determine the mRNA targets for each miR395 family member as well as the role each member plays in plant growth under abiotic stress conditions. Overexpression of miR395c or miR395e retarded and accelerated, respectively, the seed germination of Arabidopsis under high salt or dehydration stress conditions. Despite a single nucleotide difference between miR395c and miR395e, the cleavage of mRNA targets, APS1, APS3, APS4 and SULTR2;1, was not same in miR395c- and miR395e-overexpressing plants. These results demonstrate that a given miRNA family containing a single nucleotide difference can guide the cleavage of various mRNA targets, thereby acting as a positive or negative regulator of seed germination under stress.

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Abbreviations

APS:

ATP sulfurylase

miRNA:

MicroRNA

SULTR2;1:

Sulfate transporter

References

  • Achard P, Herr A, Baulcombe DC, Harberd NP (2004) Modulation of floral development by a gibberellin-regulated microRNA. Development 131:3357–3365

    Article  CAS  PubMed  Google Scholar 

  • Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221

    Article  CAS  PubMed  Google Scholar 

  • Arenas-Huertero C, Pérez B, Rabanal F, Blanco-Melo D, De la Rosa C, Estrada-Navarrete G, Sanchez F, Covarrubias AA, Reyes JL (2009) Conserved and novel miRNAs in the legume Phaseolus vulgaris in response to stress. Plant Mol Biol 70:385–401

    Article  CAS  PubMed  Google Scholar 

  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297

    Article  CAS  PubMed  Google Scholar 

  • Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215–233

    Article  CAS  PubMed  Google Scholar 

  • Chiou T-J (2007) The role of microRNAs in sensing nutrient stress. Plant Cell Environ 30:323–332

    Article  CAS  PubMed  Google Scholar 

  • Chiou T-J, Aung K, Lin S-I, Wu C-C, Chiang S-F, Su C-L (2006) Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18:412–421

    Article  CAS  PubMed  Google Scholar 

  • Dan H, Yang G, Zheng Z-L (2007) A negative regulatory role for auxin in sulphate deficiency response in Arabidopsis thaliana. Plant Mol Biol 63:221–235

    Article  CAS  PubMed  Google Scholar 

  • Fujii H, Chiou T-J, Lin S-I, Aung K, Zhu J-K (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15:2038–2043

    Article  CAS  PubMed  Google Scholar 

  • Guddeti S, Zhang DC, Li AL, Leseberg CH, Kang H, Li XG, Zhai WX, Johns MA, Mao L (2005) Molecular evolution of the rice miR395 gene family. Cell Res 15:631–638

    Article  CAS  PubMed  Google Scholar 

  • Hirsch J, Lefort V, Vankersschaver M, Boualem A, Lucas A, Thermes C, d’Aubenton-Carafa Y, Crespi M (2006) Characterization of 43 non-protein-coding mRNA genes in Arabidopsis, including the MIR162a-derived transcripts. Plant Physiol 140:1192–1204

    Article  CAS  PubMed  Google Scholar 

  • Jagadeeswaran G, Saini A, Sunkar R (2009) Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta 229:1009–1014

    Article  CAS  PubMed  Google Scholar 

  • Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cells 14:787–799

    Article  CAS  Google Scholar 

  • Jung HJ, Kang H (2007) Expression and functional analyses of microRNA417 in Arabidopsis thaliana under stress conditions. Plant Physiol Biochem 45:805–811

    Article  CAS  PubMed  Google Scholar 

  • Kawashima CG, Yoshimoto N, Maruyama-Nakashita A, Tsuchiya YN, Saito K, Takahashi H, Dalmay T (2009) Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. Plant J 57:313–321

    Article  CAS  PubMed  Google Scholar 

  • Kim YO, Kim JS, Kang H (2005) Cold-inducible zinc finger-containing glycine-rich RNA-binding protein contributes to the enhancement of freezing tolerance in Arabidopsis thaliana. Plant J 42:890–900

    Article  CAS  PubMed  Google Scholar 

  • Kim JY, Park SJ, Jang B, Jung C-H, Ahn SJ, Goh C-H, Cho K, Han O, Kang H (2007) Functional characterization of a glycine-rich RNA-binding protein2 in Arabidopsis thaliana under abiotic stress conditions. Plant J 50:439–451

    Article  CAS  PubMed  Google Scholar 

  • Kim JS, Jung HJ, Lee HJ, Kim KA, Goh C-H, Woo Y, Oh SH, Han YS, Kang H (2008) Glycine-rich RNA-binding protein7 affects abiotic stress responses by regulating stomata opening and closing in Arabidopsis thaliana. Plant J 55:455–466

    Article  CAS  PubMed  Google Scholar 

  • Kim JY, Kwak KJ, Jung HJ, Lee HJ, Kang H (2010) MicroRNA402 affects seed germination of Arabidopsis thaliana under stress conditions via targeting DEMETER-LIKE protein3 mRNA. Plant Cell Physiol 51:1079–1083

    Article  CAS  PubMed  Google Scholar 

  • Koprivova A, North KA, Kopriva S (2008) Complex signaling network in regulation of adenosine 5′-phosphosulfate reductase by salt stress in Arabidopsis roots. Plant Physiol 146:1408–1420

    Article  CAS  PubMed  Google Scholar 

  • Lin SI, Chiang SF, Lin WY, Chen JW, Tseng CY, Wu PC, Chiou TJ (2008) Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147:732–746

    Article  CAS  PubMed  Google Scholar 

  • Liu Q, Zhang Y-C, Wang C-Y, Luo Y-C, Huang Q-J, Chen S-Y, Zhou H, Qu L-H, Chen Y-Q (2009) Expression analysis of phytohormone-regulated microRNAs in rice, implying their regulation roles in plant hormone signaling. FEBS Lett 583:723–728

    Article  CAS  PubMed  Google Scholar 

  • Lu S, Sun YH, Chiang VL (2008) Stress-responsive microRNAs in Populus. Plant J 55:131–151

    Article  CAS  PubMed  Google Scholar 

  • Mallory AC, Bartel DP, 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

    Article  CAS  PubMed  Google Scholar 

  • Mittova V, Theodoulou FL, Kiddle G, Gomez L, Volokita M, Tal M, Foyer CH, Guy M (2003) Coordinate induction of glutathione biosynthesis and glutathione-metabolizing enzymes is correlated with salt tolerance in tomato. FEBS Lett 554:417–421

    Article  CAS  PubMed  Google Scholar 

  • Ohkama N, Takei K, Sakakibara H, Hayashi H, Yoneyama T, Fujiwara T (2002) Regulation of sulfur-responsive gene expression by exogenously applied cytokinins in Arabidopsis thaliana. Plant Cell Physiol 43:1493–1501

    Article  CAS  PubMed  Google Scholar 

  • Pant BD, Buhtz A, Kehr J, Scheible WR (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53:731–738

    Article  CAS  PubMed  Google Scholar 

  • Schommer C, Palatnik JF, Aggarwal P, Chételat A, Cubas P, Farmer EE, Nath U, Weigel D (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol 6:e230

    Article  PubMed  Google Scholar 

  • Sunkar R (2010) MicroRNAs with macro effects on plant stress responses. Semin Cell Dev Biol. doi:10.1016/j.semcdb.2010.04.001

  • Sunkar R, Zhu J-K (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019

    Article  CAS  PubMed  Google Scholar 

  • Sunkar R, Kapoor A, Zhu J-K (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065

    Article  CAS  PubMed  Google Scholar 

  • Sunkar R, Chinnusamy V, Zhu J, Zhu J-K (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12:301–309

    Article  CAS  PubMed  Google Scholar 

  • Takahashi H, Yamazaki M, Sasakura N, Watanabe A, Leustek T, Engler JA, Engler G, Van Montagu M, Saito K (1997) Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana. Proc Natl Acad Sci USA 94:11102–11107

    Article  CAS  PubMed  Google Scholar 

  • Takahashi H, Watanabe-Takahashi A, Smith FW, Blake-Kalff M, Hawkesford MJ, Saito K (2000) The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. Plant J 23:171–182

    Article  CAS  PubMed  Google Scholar 

  • Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687

    Article  CAS  PubMed  Google Scholar 

  • Xie Z, Allen E, Fahlgren N, Calamar A, Givan SA, Carrington JC (2005) Expression of Arabidopsis miRNA genes. Plant Physiol 138:2145–2154

    Article  CAS  PubMed  Google Scholar 

  • Zhang BH, Pan XP, Cannon CH, Cobb GP, Anderson TA (2006) Conservation and divergence of plant microRNA genes. Plant J 46:243–259

    Article  CAS  PubMed  Google Scholar 

  • Zhang JF, Yuan LJ, Shao Y, Du W, Yan DW, Lu YT (2008) The disturbance of small-RNA pathways enhanced abscisic acid response and multiple stress responses in Arabidopsis. Plant Cell Environ 31:562–574

    Article  CAS  PubMed  Google Scholar 

  • Zhao B, Ge L, Liang R, Li W, Ruan K, Lin H, Jin Y (2009) Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Mol Biol 10:29

    Article  PubMed  Google Scholar 

  • Zhou G-K, Kubo M, Zhong R, Demura T, Ye Z-H (2007) Overexpression of miR165 affects apical meristem formation, organ polarity establishment, and vascular development in Arabidopsis. Plant Cell Physiol 48:391–404

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported in part by a grant from the National Research Foundation (NRF) of Korea to the Agricultural Plant Stress Research Center (APSRC, R11-2001-092-04002-0) of Chonnam National University and by World Class University program through the NRF of Korea funded by the Ministry of Education, Science and Technology (R32-20047-0).

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Authors and Affiliations

  1. Department of Plant Biotechnology, Agricultural Plant Stress Research Center and Biotechnology Research Institute, College of Agriculture and Life Sciences, Chonnam National University, 300 Yongbong-dong, Buk-gu, Gwangju, 500-757, Korea

    Joo Yeol Kim, Hwa Jung Lee, Hyun Ju Jung & Hunseung Kang

  2. Research Institute for Bioresources, Okayama University, 2-20-1 Chu-ou, Kurashiki, Okayama, 710-0046, Japan

    Kazuyuki Maruyama & Nobuhiro Suzuki

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  1. Joo Yeol Kim
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  2. Hwa Jung Lee
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  6. Hunseung Kang
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Correspondence to Hunseung Kang.

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Kim, J.Y., Lee, H.J., Jung, H.J. et al. Overexpression of microRNA395c or 395e affects differently the seed germination of Arabidopsis thaliana under stress conditions. Planta 232, 1447–1454 (2010). https://doi.org/10.1007/s00425-010-1267-x

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