biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 59:491-496, 2015 | DOI: 10.1007/s10535-015-0511-4

Effect of sulfate availability on root traits and microRNA395 expression in sugar beet

P. Stevanato1,*, P. Fedito1, D. Trebbi1, M. Cagnin1, M. Saccomani1, G. Cacco1
1 DAFNAE, Dipartimento di Agronomia Animali Alimenti Risorse Naturali e Ambiente, Università degli Studi di Padova, Legnaro, Italy

Nutritional stress is one of the main limits to sugar beet yield. This study evaluated morphological and molecular responses of sugar beet to changes in sulfate availability. Morphological characteristics of the root system and the accumulation of microRNA395 (miR395) were examined in sulfate(S)-supplemented and S-deprived seedlings under hydroponic conditions. We also investigated the functional role of miR395 in regulating the expression of APS1 gene coding for ATP-sulfurylase in roots and leaves. The S-deprived seedlings showed a significant increase in the number of root tips, in the miR395 expression in leaves but not in roots, and in the expression of APS1 gene. Our results indicate that miR395 may be a useful biomarker for sulfate status in sugar beet.

Keywords: ATP-sulfurylase; Beta vulgaris; root morphology
Subjects: sulphur; microRNA; ATP-sulfurylase; root morphology; gene expression; sugar beet

Received: July 24, 2014; Revised: December 2, 2014; Accepted: December 22, 2014; Published: September 1, 2015  Show citation

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Stevanato, P., Fedito, P., Trebbi, D., Cagnin, M., Saccomani, M., & Cacco, G. (2015). Effect of sulfate availability on root traits and microRNA395 expression in sugar beet. Biologia plantarum59(3), 491-496. doi: 10.1007/s10535-015-0511-4
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References

  1. Arnon, D.I., Hoagland, D.R.: Crop production in artificial culture solution and in soils with special reference to factors influencing yields and absorption of inorganic nutrients. - Soil Sci. 50: 463-483, 1940.
  2. Axtell, M.J., Bartel, D.P.: Antiquity of microRNAs and their targets in land plants. - Plant Cell 17: 1658-1673, 2005. Go to original source...
  3. Baluska, F., Mancuso, S., Volkmann, D., Barlow, P.: Root apices as plant command centres: the unique brain-like status of the root apex transition zone. - Biológia 59: 1-13, 2004.
  4. Barberon, M., Berthomieu, P., Clairotte, M., Shibagaki, N., Davidian, J., Gosti, F.: Unequal functional redundancy between the two Arabidopsis thaliana high-affinity sulphate transporters SULTR1;1 and SULTR1;2. - New Phytol. 180: 608-619, 2008. Go to original source...
  5. Buchner, P., Stuiver, C.E.E., Westerman, S., Wirtz, M., Hell, R., Hawkesford, M.J., De Kok, L.J.: Regulation of sulphate uptake and expression of sulphate transporter genes in Brassica oleracea as affected by atmospheric Hn2S and pedospheric sulphate nutrition. - Plant Physiol. 136: 3396-3408, 2004. Go to original source...
  6. Buhtz, A., Pieritz, J., Springer, F., Kehr, J.: Phloem small RNAs, nutrient stress responses, and systemic mobility. - BMC Plant Biol. 10: 64, 2010. Go to original source...
  7. Chen, X., Zhang, J., Chen, Y., Li, Q., Chen, F., Yua, L., Mi, G.: Changes in root size and distribution in relation to nitrogen accumulation during maize breeding in China. - Plant Soil 374: 121-130, 2014. Go to original source...
  8. Davidian, J.C., Kopriva, S.: Regulation of sulfate uptake and assimilation - the same or not the same? - Mol. Plant. 3: 314-325, 2010. Go to original source...
  9. De Kok, L.J., Stuiver, C.E.E., Shahbaz, M., Koralewska, A.: Regulation of expression of sulfate transporters and APS reductase in leaf tissue of Chinese cabbage (Brassica pekinensis). - Proc. Int. Plant Sulfur Workshop 1: 47-52, 2012. Go to original source...
  10. Forieri, I., Wirtz, M., Hell, R.: Toward new perspectives on the interaction of iron and sulfur metabolism in plants. - Front. Plant Sci. 4: 357, 2013. Go to original source...
  11. Giehl R.F.H., Gruber B.D., Von Wiré, N.: It's time to make changes: modulation of root system architecture by nutrient signals. - J. exp. Bot. 65: 769-778, 2014. Go to original source...
  12. Jagadeeswaran, G., Li, Y.F., Sunkar, R.: Redox signaling mediates the expression of a sulfate-deprivation-inducible microRNA395 in Arabidopsis. - Plant J. 77: 85-96, 2014. Go to original source...
  13. Jones-Rhoades M.W., Bartel, D.P.: Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. - Mol. Cell 14: 787-799, 2004. Go to original source...
  14. Hajizadeh, H., Razavi, K, Mostofi, Y., Musavi, A., Cacco, G., Zamani, Z., Stevanato, P.: Identification and characterization of genes differentially displayed in Rosa hybrida petals during flower senescence. - Sci. Hort. 128: 320-324, 2011. Go to original source...
  15. Havecker, E.R., Wallbridge, L.M., Fedito, P., Hardcastle, T.J., Baulcombe, D.C.: Metastable differentially methylated regions within Arabidopsis inbred populations are associated with modified expression of non-coding transcripts. - PLoS One 7: e45242, 2012. Go to original source...
  16. Kataoka, T., Watanabe-Takahashi, A., Hayashi, N., Ohnishi, M., Mimura, T., Buchner, P., Hawkesford, M.J., Yamaya, T., Takahashi, H.: Vacuolar sulphate transporters are essential determinants controlling internal distribution of sulphate in Arabidopsis. - Plant Cell 16: 2693-2704, 2004. Go to original source...
  17. Kawashima, C.G., Yoshimoto, N., Maruyama-Nakashita, A., Tsuchiya, Y.N., Saito, K., Takahashi, H., Dalmay, T.: Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. - Plant J. 57: 313-321, 2009. Go to original source...
  18. Kawashima, C.G., Matthewman, C.A., Huang, S., Lee, B.R., Yoshimoto, N., Koprivova, A., Rubio-Somoza I., Todesco M., Rathjen T., Saito K., Takahashi H., Dalmay, T., Kopriva, S.: Interplay of SLIM1 and miR395 in the regulation of sulfate assimilation in Arabidopsis. - Plant J. 66: 863-876, 2011. Go to original source...
  19. Kopriva, S., Rennenberg, H.: Control of sulphate assimilation and glutathione synthesis: interaction with N and C metabolism. - J. exp. Bot. 55: 1831-1842, 2004. Go to original source...
  20. Kruszka, K., Pieczynskia, M., Windels, D., Bielewicz, D., Jarmolowski, A., Szweykowska-Kulinska, Z.: Role of microRNAs and other sRNAs of plants in their changing environments. - J. Plant Physiol. 169: 1664-1672, 2012. Go to original source...
  21. Lappartient, A.G., Touraine, B.: Demand-driven control of root ATP sulfurylase activity and sulfate uptake in intact Canola. - Plant Physiol. 111: 147-157, 1996. Go to original source...
  22. Liang, G., Yu, D.: Reciprocal regulation among miR395, APS, and SULTR2;1 in Arabidopsis thaliana. - Plant Signal Behav. 5: 1257-1259, 2010. Go to original source...
  23. Lynch, J.P., Joseph, G. Chimungu, J.G., Brown, K.M. Root anatomical phenes associated with water acquisition from drying soil: targets for crop improvement. - J. exp. Bot. 65: 6155-6166, 2014. Go to original source...
  24. Matts, J., Jagadeeswaran, G., Roe, B.A., Sunkar, R.: Identification of microRNAs and their targets in switchgrass, a model biofuel plant species. - J. Plant Physiol. 167: 896-904, 2010. Go to original source...
  25. Parmar, S., Buchner, P., Hawkesford, M.J.: Leaf developmental stage affects sulphate depletion and specific sulphate transporter expression during sulphur deprivation in Brassica napus L. - Plant Biol. 9: 647-653, 2007. Go to original source...
  26. Potters, G., Pasternak, T.P., Guisez, Y., Palme, K.J., Jansen, M.A.K.: Stress-induced morphogenic responses: growing out of trouble? - Trends Plant Sci. 12: 98-105, 2007. Go to original source...
  27. Saccomani, M., Stevanato, P., Trebbi, D., McGrath, M., Biancardi, E.: Molecular and morpho-physiological characterization of sea, ruderal and cultivated beets. - Euphytica 169: 19-29, 2009. Go to original source...
  28. Steven, G. Thomas, S.G., Bilsborrow, P.E., Hocking, T.J., Bennett, J.: Effect of sulphur deficiency on the growth and metabolism of sugar beet (Beta vulgaris cv Druid). - J. Sci. Food Agr. 80: 2057-2062, 2000. Go to original source...
  29. Watanabe, M., Hubberten, H.M., Hoefgen, R.: Plant response to mineral ion availability: transcriptome responses to sulfate, selenium and iron. - Proc. Int. Plant Sulfur Workshop 1: 123-134, 2012. Go to original source...
  30. Yoshimoto, N., Takahashi, H., Smith, F.W., Yamaya, T., Saito, K.: Two distinct high-affinity sulphate transporters with different inducibilities mediate uptake of sulphate in Arabidopsis roots. - Plant J. 29: 465-473, 2002. Go to original source...
  31. Zeng, H., Wang, G., Hu, X., Wang, H., Du, L., Zhu, Y.: Role of microRNAs in plant responses to nutrient stress. - Plant Soil 374: 1005-1021, 2014. Go to original source...
  32. Zhang, L., Zheng, Y., Jagadeeswaran, G., Li, Y., Gowdu, K., Sunkar, R.: Identification and temporal expression analysis of conserved and novel microRNAs in Sorghum. - Genomics 98: 460-468, 2011. Go to original source...
  33. Zhao, Q., Wu, Y., Gao, L., Ma, J., Li, C.Y., Xiang, C.B.: Sulfur nutrient availability regulates root elongation by affecting root IAA levels and the stem cell niche. - J. Integr. Plant Biol. 56: 1151-1163, 2014. Go to original source...