Biologia plantarum 59:92-98, 2015 | DOI: 10.1007/s10535-014-0477-7

Suppression of SlNAC1 reduces heat resistance in tomato plants

X.-Q. Liang1, N.-N. Ma1, G.-D. Wang1, X. Meng1, X.-Z. Ai1, Q.-W. Meng1,*
1 College of Life Science, State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai'an, Shandong, P.R. China

NAC (NAM, ATAF1,2, and CUC2) transcription factors play an important role in the responses of plants to various environmental stresses. To investigate the function of SlNAC1, which was found to be a member of the ATAF subfamily in tomato (Solanum lycopersicum L.) plants under heat stress conditions, transgenic tomato plants were generated using an antisense technology. After a treatment at 40 °C for 48 h, in comparison with wild-type (WT) plants, the transgenic plants were severely wilted and exhibited a lower net photosynthetic rate and a maximal photochemical efficiency of photosystem II. Moreover, the transgenic plants displayed a higher ion leakage and malondialdehyde content and a lower proline content. The content of reactive oxygen species (superoxide anion radicals and hydrogen peroxide) were higher, and activities of ascorbate peroxidase and superoxide dismutase lower in the transgenic plants than in the WT plants. The transgenic plants also exhibited a lower accumulation of the transcripts of some heat shock protein genes (Hsp70, Hsp90, sHsp17.4, and sHsp17.6). All of these results suggest that the suppression of SlNAC1 could obviously reduce heat resistance in the tomato plants, and this indicates that SlNAC1 played an important role in the thermal tolerance of the tomato plants.

Keywords: ascorbate peroxidase; chlorophyll fluorescence; heat shock proteins; high temperature; net photosynthetic rate; reactive oxygen species; Solanum lycopersicum; superoxide dismutase; transgenic plants
Subjects: gene suppression; heat tolerance; temperature - high; transgenic plants; net photosynthetic rate; chlorophyll fluorescence; malondialdehyde; proline; superoxide anion; hydrogen peroxide; superoxide dismutase; ascorbate peroxidase; gene expression; tomato
Species: Solanum lycopersicum

Received: April 27, 2014; Revised: August 1, 2014; Accepted: September 2, 2014; Published: January 1, 2015Show citation

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Liang, X.-Q., Ma, N.-N., Wang, G.-D., Meng, X., Ai, X.-Z., & Meng, Q.-W. (2015). Suppression of SlNAC1 reduces heat resistance in tomato plants. Biologia plantarum59(1), 92-98. doi: 10.1007/s10535-014-0477-7.
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References

  1. Abdul-Baki, A.A.: Tolerance of tomato cultivars and selected germ plasm to heat stress. - J. amer. Soc. hort. Sci. 116: 1113-1116, 1991. Go to original source...
  2. Aida, M., Ishida, T., Fukaki, H., Fujisawa, H., Tasaka, M.: Genes involved in organ separation in Arabidopsis: analysis of the cup-shaped cotyledon mutant. - Plant Cell 9: 841-857, 1997. Go to original source...
  3. Almeselmani, M., Deshmukh, P.S., Sairam, R.K.: High temperature stress tolerance in wheat genotypes: role of antioxidant defence enzymes. - Acta agron. hung. 57: 1-14, 2009. Go to original source...
  4. Baniwal, S.K., Bharti, K., Chan, K.Y., Fauth, M., Ganguli, A., Kotak, S., Mishra, S.K., Nover, L., Port, M., Scharf, K.D.: Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. - J. Biosci. 29: 471-487, 2004. Go to original source...
  5. Bokszczanin, K.L. Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. - Front. Plant Sci. 4: 1-20, 2013. Go to original source...
  6. Boston, R.S., Viitanen, P.V., Vierling, E.: Molecular chaperones and protein folding in plants. - Plant mol. Biol. 32: 191-222, 1996. Go to original source...
  7. Camejo, D., Jiménez, A., Alarcón, J.J., Torres, W., Gómez, J.M., Sevilla, F.: Changes in photosynthetic parameters and antioxidant activities following hea-shock treatment in tomato plants. - Funct. Plant Biol. 33: 177-187, 2006. Go to original source...
  8. Chang, H.C., Tang, Y.C., Hayer-Hartl, M., Hartl, F.U.: SnapShot: molecular chaperones, part I. - Cell 128: 212-e1, 2007. Go to original source...
  9. Delessert, C., Kazan, K., Wilson, I.W., Van Der Straeten, D., Manners, J., Dennis, E.S.: The transcription factor ATAF2 represses the expression of pathogenesis-related genes in Arabidopsis. - Plant J. 43: 745-757, 2005. Go to original source...
  10. Hartl, F.U., Bracher, A., Hayer-Hartl, M.: Molecular chaperones in protein folding and proteostasis. - Nature 475: 324-332, 2011. Go to original source...
  11. Hu, W.H., Xiao, Y.A., Zeng J.J., Hu, X.H.: Photosynthesis, respiration and antioxidant enzymes in pepper leaves under drought and heat stresses. - Biol. Plant. 54: 761-765, 2010. Go to original source...
  12. Jakob, U., Gaestel, M., Engel, K., Buchner, J.: Small heat shock proteins are molecular chaperones. - J. biol. Chem. 268: 1517-1520, 1993.
  13. Janska, A., Marsik, P., Zelenkova, S., Ovesna, J.: Cold stress and acclimation: what is important for metabolic adjustment? - Plant Biol. 12: 395-405, 2010. Go to original source...
  14. Jeong, J.S., Kim, Y.S., Baek, K.H., Jung, H., Ha, S.H., Do, C., Kim, M.: Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. - Plant Physiol. 153: 185-197, 2010. Go to original source...
  15. Katiyar-Agarwal, S., Agarwal, M., Grover, A.: Heat tolerant basmati rice engineered by over-expression of hsp101. - Plant mol. Biol. 51: 677-686, 2003. Go to original source...
  16. Kim, J.H., Woo, H.R., Kim, J., Lim, P.O., Lee, I.C., Choi, S.H.: Trifurcate feed-forward regulation of age dependent cell death involving miR164 in Arabidopsis. - Science 323: 1053-1057, 2009. Go to original source...
  17. Kong, F.Y., Deng, Y.S., Z, B., Wang, G.D., Wang, Y., Meng, Q.W.: A chloroplast-targeted DnaJ protein contributes to maintenance of photosystem II under chilling stress. - J. exp. Bot. 65: 143-158, 2013.
  18. Li, Z.J., Zhang, L.L., Wang, A.X., Xu, X.Y., Li, J.F.: Ectopic overexpression of SlHsfA3, a heat stress transcription factor from tomato, confers increased thermotolerance and salt hypersensitivity in germination in transgenic Arabidopsis. - PloS one 8: e54880, 2013. Go to original source...
  19. Liming, Y., Qian, Y., Pigang, L., Sen, L.: Expression of the HSP24 gene from Trichoderma harzianum in Saccharomyces cerevisiae. - J. Therm. Biol. 33: 1-6, 2008. Go to original source...
  20. Lindquist, S., Craig, E.A.: The heat-shock proteins. - Annu. Rev. Genet. 22: 631-677, 1988. Go to original source...
  21. Liu, X.Z., Huang, B.R.: Heat stress injury in relation to membrane lipid peroxidation in creeping bentgrass. - Crop Sci. 40: 503-510, 2000. Go to original source...
  22. Lu, P.L., Chen, N.Z., An, R., Su, Z., Qi, B.S., Ren, F., Chen, J., Wang, X.C.: A novel drought-inducible gene, ATAF1, encodes a NAC family protein that negatively regulates the expression of stress-responsive genes in Arabidopsis. - Plant mol. Biol. 63: 289-305, 2007.
  23. Ma, N.N., Zuo, Y.Q., Liang, X.Q., Yin, B., Wang, G.D., Meng, Q.W.: The multiple stress-responsive transcription factor SlNAC1 improves the chilling tolerance of tomato. - Physiol. Plant. 149: 474-486, 2013. Go to original source...
  24. Morrow, G., Tanguay, R.M.: Small heat shock protein expression and functions during development. - Int. J. Biochem. Cell Biol. 44: 1613-1621, 2012. Go to original source...
  25. Munns, R., Tester, M.: Mechanisms of salinity tolerance. - Annu. Rev. Plant Biol. 59: 651-681, 2008. Go to original source...
  26. Nakano, Y., Asada, K.: Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplast. - Plant Cell Physiol. 22: 867-880, 1981.
  27. Nakashima, K., Ito, Y., Yamaguchi-Shinozaki, K.: Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. - Plant Physiol. 149: 88-95, 2009. Go to original source...
  28. Puranik, S., Bahadur, R.P., Srivastava, P.S., Prasad, M.: Molecular cloning and characterization of a membrane associated NAC family gene, SiNAC from foxtail millet [Setaria italica (L.) P.Beauv]. - Mol. Biotechnol. 49: 138-150, 2011. Go to original source...
  29. Rizhsky, L., Liang, H.J., Shuman, J., Shulaev, V., Davletova, S., Mittler, R.: When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. - Plant Physiol. 134: 1683-1696, 2004. Go to original source...
  30. Rodríguez, M., Canales, E., Borrás-Hidalgo, O.: Molecular aspects of abiotic stress in plants. - Biotecnol. apl. 22: 1-10, 2005.
  31. Souer, E., Houwelingen, A., Kloos, D., Mol, J., Koes, R.: The no apical meristem gene of Petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. - Cell 85: 159-170, 1996. Go to original source...
  32. Swindell, W.R., Huebner, M., Weber, A.P.: Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. - BMC Genom. 8: 125, 2007. Go to original source...
  33. Valliyodan, B., Nguyen, H.T.: Understanding regulatory networks and engineering for enhanced drought tolerance in plants. - Curr. Opin. Plant Biol. 9: 189-195, 2006. Go to original source...
  34. Van Kooten, O., Snel, J.F.: The use of chlorophyll fluorescence nomenclature in plant stress physiology. - Photosynth. Res. 25: 147-150, 1990. Go to original source...
  35. Vierling, E: The roles of heat shock proteins in plants. - Annu. Rev. Plant Biol. 42: 579-620, 1991. Go to original source...
  36. Wang, J.Z., Cui, L.J., Wang, Y., Li, J.L.: Growth, lipid peroxidation and photosynthesis in two tall fescue cultivars differing in heat tolerance. - Biol. Plant. 53: 237-242, 2009. Go to original source...
  37. Wang, W., Vinocur, B., Shoseyov, O., Altman, A.: Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. - Trends Plant Sci. 9: 244-252, 2004. Go to original source...
  38. Waters, E.R., Lee, G.J., Vierling, E.: Evolution, structure and function of the small heat shock proteins in plants. - J. exp. Bot. 47: 325-338, 1996. Go to original source...
  39. Wu, Y., Deng, Z., Lai, J., Zhang, Y., Yang, C., Yin, B., Zhao, Q., Zhang, L., Li, Y., Xie, Q.: Dual function of Arabidopsis ATAF1 in abiotic and biotic stress responses. - Cell. Res. 19: 1279-1290, 2009. Go to original source...