Dual role of MdSND1 in the biosynthesis of lignin and in signal transduction in response to salt and osmotic stress in apple

Keqin Chen , Yunna Guo , Mengru Song , Lifu Liu , Hao Xue , Hongyan Dai , Zhihong Zhang

Horticulture Research ›› 2020, Vol. 7 ›› Issue (1) : 204

PDF (4388KB)
Horticulture Research ›› 2020, Vol. 7 ›› Issue (1) :204 DOI: 10.1038/s41438-020-00433-7
Article
research-article
Dual role of MdSND1 in the biosynthesis of lignin and in signal transduction in response to salt and osmotic stress in apple
Author information +
History +
PDF (4388KB)

Abstract

Clarifying the stress signal transduction pathway would be helpful for understanding the abiotic stress resistance mechanism in apple (Malus × domestica Borkh.) and could assist in the development of new varieties with high stress tolerance by genetic engineering. The key NAC transcription factor SND1, which is involved in the lignin biosynthesis process in apple, was functionally analyzed. The results of the stress treatments indicated that MdSND1 could be induced by salt, mannitol and ABA. Compared with wild-type GL-3 plants, MdSND1-overexpressing apple plants with greater antioxidant capacity and lignin were more resistant to salt and simulated osmotic stress, while RNAi plants were more vulnerable. Additionally, molecular experiments confirmed that MdSND1 could regulate the biosynthesis of lignin by activating the transcription of MdMYB46/83. Moreover, genes known to be involved in the stress signal transduction pathway (MdAREB1A, MdAREB1B, MdDREB2A, MdRD29A, and MdRD22) were screened for their close correlations with the expression of MdSND1 and the response to salt and osmotic stress. Multiple verification tests further demonstrated that MdSND1 could directly bind to these gene promoters and activate their transcription. The above results revealed that MdSND1 is directly involved in the regulation of lignin biosynthesis and the signal transduction pathway involved in the response to both salt and osmotic stress in apple.

Cite this article

Download citation ▾
Keqin Chen, Yunna Guo, Mengru Song, Lifu Liu, Hao Xue, Hongyan Dai, Zhihong Zhang. Dual role of MdSND1 in the biosynthesis of lignin and in signal transduction in response to salt and osmotic stress in apple. Horticulture Research, 2020, 7 (1) : 204 DOI:10.1038/s41438-020-00433-7

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Zhu, J. K. Abiotic stress signaling and responses in plants. Cell 167, 313-324 (2016).

[2]

Yamaguchi-Shinozaki, K. & Shinozaki, K. Organization of cis-acting regulatory elements in osmotic-and cold-stress-responsive promoters. Trends Plant Sci. 10, 88-94 (2005).

[3]

Yoshida, T., Mogami, J. & Yamaguchi-Shinozaki, K. ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr. Opin. Plant Biol. 21, 133-139 (2014).

[4]

Xie, Q. Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Gene. Dev. 14, 3024-3036 (2000).

[5]

Duval, M., Hsieh, T. F., Kim, S. Y. & Thomas, T. L. Molecular characterization of AtNAM: a member of the Arabidopsis NAC domain superfamily. Plant Mol. Biol. 50, 237-248 (2002).

[6]

Ernst, H. A., Nina Olsen, A., Skriver, K., Larsen, S. & Lo-Leggio, L. Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors. EMBO Rep. 5, 297-303 (2004).

[7]

Hu, H. et al. Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc. Natl Acad. Sci. USA 103, 12987-12992 (2006).

[8]

Souer, E., van 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).

[9]

Zhong, R., Demura, T. & Ye, Z. H. SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 18, 3158-3170 (2006).

[10]

Zhong, R., Richardson, E., Ye, Z. H. & Two, N. A. C. domain transcription factors, SND1 and NST1, function redundantly in regulation of secondary wall synthesis in fibers of Arabidopsis. Planta 225, 1603-1611 (2007).

[11]

Yang, S. D., Seo, P. J., Yoon, H. K. & Park, C. M. The Arabidopsis NAC transcription factor VNI2 integrates abscisic acid signals into leaf senescence via the COR/RD genes. Plant Cell 23, 2155-2168 (2011).

[12]

Zhong, R. & Ye, Z. H. Transcriptional regulation of lignin biosynthesis. Plant Signal. Behav. 4, 1028-1034 (2009).

[13]

Jeong, C. Y. et al. Dual role of SND1 facilitates efficient communication between abiotic stress signalling and normal growth in Arabidopsis. Sci. Rep. 8, 10114 (2018).

[14]

Mitsuda, N. et al. NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell 19, 270-280 (2007).

[15]

Nakashima, K., Takasaki, H., Mizoi, J., Shinozaki, K. & Yamaguchi-Shinozaki, K. NAC transcription factors in plant abiotic stress responses. Biochim. Biophys. Acta 1819, 97-103 (2012).

[16]

Sun, L., Li, D., Zhang, H. & Song, F. Functions of NAC transcription factors in biotic and abiotic stress responses in plants. Hereditas (Beijing) 34, 993-1002 (2012).

[17]

Ramegowda, V. et al. Expression of a finger millet transcription factor, EcNAC1, in tobacco confers abiotic stress-tolerance. PLoS ONE 7, e40397 (2012).

[18]

Nuruzzaman, M., Sharoni, A. M. & Kikuchi, S. Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Front. Microbiol. 4, 1-16 (2013).

[19]

Zhu, J. K. Plant salt tolerance. Trends Plant Sci. 6, 66-71 (2001).

[20]

Zhu, J. K. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247-273 (2002).

[21]

Ouyang, B. et al. Identification of early salt stress response genes in tomato root by suppression subtractive hybridization and microarray analysis. J. Exp. Bot. 58, 507-520 (2007).

[22]

Li, D., Su, Z., Dong, J. & Wang, T. An expression database for roots of the model legume Medicago truncatula under salt stress. BMC Genomics 10, 517 (2009).

[23]

Yadav, N. R., Taunk, J., Rani, A., Aneja, B. & Yadav, R. C. in Climate Change and Plant Abiotic Stress Tolerance (eds Narendra T. & Sarvajeet S. G.) 605-640 (Wiley Blackwell, 2013).

[24]

Agarwal, P. K., Agarwal, P., Reddy, M. K. & Sopory, S. K. Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep. 25, 1263-1274 (2006).

[25]

Shen, H. et al. OsWRKY30 is activated by MAP kinases to confer drought tolerance in rice. Plant Mol. Biol. 80, 241-253 (2012).

[26]

Nakashima, K. et al. Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant Mol. Biol. 42, 657-665 (2000).

[27]

Lee, S. J. et al. DREB2C interacts with ABF2, a bZIP protein regulating abscisic acid responsive gene expression, and its overexpression affects abscisic acid sensitivity. Plant Physiol. 153, 716-727 (2010).

[28]

Chen, M. et al. GmDREB2, a soybean DRE-binding transcription factor, conferred drought and high-salt tolerance in transgenic plants. Biochem. Bioph. Res. Commun. 353, 299-305 (2007).

[29]

Chen, J., Xia, X. & Yin, W. Expression profiling and functional characterization of a DREB2-type gene from Populus euphratica. Biochem. Bioph. Res. Commun. 378, 483-487 (2009).

[30]

Cui, M. et al. Induced over-expression of the transcription factor OsDREB2A improves drought tolerance in rice. Plant Physiol. Biochem. 49, 1384-1391 (2011).

[31]

Li, X. et al. EsDREB2B, a novel truncated DREB2-type transcription factor in the desert legume Eremosparton songoricum, enhances tolerance to multiple abiotic stresses in yeast and transgenic tobacco. BMC Plant Biol. 14, 44 (2014).

[32]

Hichri, I. et al. SlDREB2, a tomato dehydration-responsive element-binding 2 transcription factor, mediates salt stress tolerance in tomato and Arabidopsis. Plant Cell Environ. 39, 62-79 (2015).

[33]

Yoshida, T. et al. Four Arabidopsis AREB/ABF transcription factors function predominantly in gene expression downstream of SnRK2 kinases in abscisic acid signalling in response to osmotic stress. Plant Cell Environ. 38, 35-49 (2015).

[34]

Narusaka, Y. et al. Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J. 34, 137-148 (2003).

[35]

Yamaguchi-Shinozaki, K. & Shinozaki, K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 57, 781-803 (2006).

[36]

Chen, K. et al. MdMYB46 could enhance salt and osmotic stress tolerance in apple by directly activating stress responsive signals. Plant Biotechnol. J. 17, 2341-2355 (2019).

[37]

McCarthy, R. L., Zhong, R. & Ye, Z. H. MYB83 is a direct target of SND1 and acts redundantly with MYB46 in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell Physiol. 50, 1950-1964 (2009).

[38]

Shi, H., Lee, B. H., Wu, S. J. & Zhu, J. K. Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana . Nat. Biotechnol. 21, 81-85 (2003).

[39]

Yamaguchi-Shinozaki, K. & Shinozaki, K. A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6, 251-264 (1994).

[40]

Abe, H. et al. Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15, 63-78 (2003).

[41]

Thomashow, M. F. Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. Plant Physiol. 154, 571-577 (2010).

[42]

Lata, C. & Prasad, M. Role of DREBs in regulation of abiotic stress responses in plants. J. Exp. Bot. 62, 4731-4748 (2011).

[43]

Yamaguchi-Shinozaki, K. & Shinozaki, K. The plant hormone abscisic acid mediates the drought-induced expression but not the seed-specific expression of rd22, a gene responsive to dehydration stress in Arabidopsis thaliana. Mol. Gen. Genet. 238, 17-25 (1993).

[44]

Zhao, T., Liang, D., Wang, P., Liu, J. & Ma, F. Genome-wide analysis and expression profiling of the DREB transcription factor gene family in Malus under abiotic stress. Mol. Genet. Genomics 287, 423-436 (2012).

[45]

Ma, Q. et al. An apple CIPK protein kinase targets a novel residue of AREB transcription factor for ABA-dependent phosphorylation. Plant Cell Environ. 40, 2207-2219 (2017).

[46]

An, J. P. et al. An apple NAC transcription factor enhances salt stress tolerance by modulating the ethylene response. Physiol. Plant. 164, 279-289 (2018).

[47]

Shao, Y., Zhang, X., van Nocker, S., Gong, X. & Ma, F. Overexpression of a protein kinase gene MpSnRK2.10 from Malus prunifolia confers tolerance to drought stress in transgenic Arabidopsis thaliana and apple. Gene 692, 26-34 (2019).

[48]

Shao, H., Wang, H. & Tang, X. NAC transcription factors in plant multiple abiotic stress responses: progress and prospects. Front. Plant Sci. 6, 902 (2015).

[49]

Simpson, S. D. et al. Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. Plant J. 33, 259-270 (2003).

[50]

Kim, S. G., Kim, S. Y. & Park, C. M. A membrane-associated NAC transcription factor regulates salt-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Planta 226, 647-654 (2007).

[51]

Ogo, Y. et al. A novel NAC transcription factor, IDEF2, that recognizes the iron deficiency-responsive element 2 regulates the genes involved in iron homeostasis in plants. J. Biol. Chem. 283, 13407-13417 (2008).

[52]

Zhong, R., Lee, C. & Ye, Z. H. Global analysis of direct targets of secondary wall NAC master switches in Arabidopsis. Mol. Plant 3, 1087-1103 (2010).

[53]

Jensen, M. K. et al. Transcriptional regulation by an NAC (NAM-ATAF1,2-CUC2) transcription factor attenuates ABA signalling for efficient basal defence towards Blumeria graminis f. sp. hordei in Arabidopsis. Plant J. 56, 867-880 (2008).

[54]

Jensen, J. K., Johnson, N. & Wilkerson, C. G. Discovery of diversity in xylan biosynthetic genes by transcriptional profiling of a heteroxylan containing mucilaginous tissue. Front. Plant Sci. 4, 183 (2013).

[55]

Sakuraba, Y., Kim, Y. S., Han, S. H., Lee, B. D. & Paek, N. C. The Arabidopsis transcription factor NAC016 promotes drought stress responses by repressing AREB1 transcription through a trifurcate feed-forward regulatory loop involving NAP. Plant Cell 27, 1771-1787 (2015).

[56]

Dai, H. et al. Development of a seedling clone with high regeneration capacity and susceptibility to Agrobacterium in apple. Sci. Hortic. 164, 202-208 (2013).

PDF (4388KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/