Abstract
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.
Similar content being viewed by others
Abbreviations
- APX:
-
ascorbate peroxidase
- Fv/Fm :
-
variable to maximum chlorophyll fluorescence ratio (the maximal photochemical efficiency of PS II)
- HSGs :
-
heat shock genes
- HSPs:
-
heat shock proteins
- H2O2 :
-
hydrogen peroxide
- MDA:
-
malondialdehyde
- O2 ·− :
-
superoxide anion radical
- P5CS:
-
pyrroline-5-carboxylate synthase
- PFD:
-
photon flux density
- PN :
-
net photosynthetic rate
- PS:
-
photosystem
- REC:
-
relative electric conductance
- ROS:
-
reactive oxygen species
- sHSPs:
-
small heat shock proteins
- TBA:
-
thiobarbituric acid
- TCA:
-
trichloroacetic acid
- WT:
-
wild type
References
Abdul-Baki, A.A.: Tolerance of tomato cultivars and selected germ plasm to heat stress. — J. amer. Soc. hort. Sci. 116: 1113–1116, 1991.
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.
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.
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.
Bokszczanin, K.L. Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. — Front. Plant Sci. 4: 1–20, 2013.
Boston, R.S., Viitanen, P.V., Vierling, E.: Molecular chaperones and protein folding in plants. — Plant mol. Biol. 32: 191–222, 1996.
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.
Chang, H.C., Tang, Y.C., Hayer-Hartl, M., Hartl, F.U.: SnapShot: molecular chaperones, part I. — Cell 128: 212–e1, 2007.
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.
Hartl, F.U., Bracher, A., Hayer-Hartl, M.: Molecular chaperones in protein folding and proteostasis. — Nature 475: 324–332, 2011.
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.
Jakob, U., Gaestel, M., Engel, K., Buchner, J.: Small heat shock proteins are molecular chaperones. — J. biol. Chem. 268: 1517–1520, 1993.
Janska, A., Marsik, P., Zelenkova, S., Ovesna, J.: Cold stress and acclimation: what is important for metabolic adjustment? — Plant Biol. 12: 395–405, 2010.
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.
Katiyar-Agarwal, S., Agarwal, M., Grover, A.: Heat tolerant basmati rice engineered by over-expression of hsp101. — Plant mol. Biol. 51: 677–686, 2003.
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.
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.
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.
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.
Lindquist, S., Craig, E.A.: The heat-shock proteins. — Annu. Rev. Genet. 22: 631–677, 1988.
Liu, X.Z., Huang, B.R.: Heat stress injury in relation to membrane lipid peroxidation in creeping bentgrass. — Crop Sci. 40: 503–510, 2000.
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.
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.
Morrow, G., Tanguay, R.M.: Small heat shock protein expression and functions during development. — Int. J. Biochem. Cell Biol. 44: 1613–1621, 2012.
Munns, R., Tester, M.: Mechanisms of salinity tolerance. — Annu. Rev. Plant Biol. 59: 651–681, 2008.
Nakano, Y., Asada, K.: Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplast. — Plant Cell Physiol. 22: 867–880, 1981.
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.
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.
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.
Rodríguez, M., Canales, E., Borrás-Hidalgo, O.: Molecular aspects of abiotic stress in plants. — Biotecnol. apl. 22: 1–10, 2005.
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.
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.
Valliyodan, B., Nguyen, H.T.: Understanding regulatory networks and engineering for enhanced drought tolerance in plants. — Curr. Opin. Plant Biol. 9: 189–195, 2006.
Van Kooten, O., Snel, J.F.: The use of chlorophyll fluorescence nomenclature in plant stress physiology. — Photosynth. Res. 25: 147–150, 1990.
Vierling, E: The roles of heat shock proteins in plants. — Annu. Rev. Plant Biol. 42: 579–620, 1991.
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.
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.
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.
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Acknowledgements: This research was supported by the State Key Basic Research and Development Plan of China (2009CB118505) and the Natural Science Foundation of China (31171474, 31371553). The first two authors contributed equally to this work.
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Liang, X.Q., Ma, N.N., Wang, G.D. et al. Suppression of SlNAC1 reduces heat resistance in tomato plants. Biol Plant 59, 92–98 (2015). https://doi.org/10.1007/s10535-014-0477-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10535-014-0477-7