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NAC103, a NAC family transcription factor, regulates ABA response during seed germination and seedling growth in Arabidopsis

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Abstract

Main conclusion

The Arabidopsis transcription factor NAC103 is up-regulated and its encoding protein is stabilized by ABA treatment, which positively regulates several ABA-responsive downstream genes during seed germination and seedlings growth.

Abstract

The Arabidopsis transcription factor NAC103 was previously found to be involved in endoplasmic reticulum (ER) stress and DNA damage responses. In this study, we report the new biological function of NAC103 in abscisic acid (ABA) response during seed germination and seedling growth in Arabidopsis. The expression of NAC103 was up-regulated and the NAC103 protein was stabilized by ABA treatment. Both the loss-of-function mutants of NAC103, created by targeted gene-editing, and the over-expression plants of NAC103 have no obvious germination-related phenotype under normal growth conditions. However, under exogenous ABA treatment conditions, the NAC103 mutants were less sensitive to ABA during seed germination; in contrast, the NAC103 over-expression plants were more sensitive to ABA during seed germination and young seedling growth. Further, NAC103 regulated several ABA-responsive downstream genes including MYB78, MYB3, PLP3, AMY1, and RGL2. These results demonstrate that NAC103 positively regulates ABA response in Arabidopsis.

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References

  • Adam R, Cole T, Julie D, John LR, Lior P (2011) Improving RNA-Seq expression estimates by correcting for fragment bias. Genome Biol 12:R22

    Article  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 30:2114

    Article  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  Google Scholar 

  • Deng Y, Humbert S, Liu JX, Srivastava R, Rothstein SJ, Howell SH (2011) Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis. Proc Natl Acad Sci 108:7247–7252

    Article  CAS  Google Scholar 

  • Ernst HA, Olsen AN, Larsen S, Lo Leggio L (2004) Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors. EMBO Rep 5:297–303

    Article  CAS  Google Scholar 

  • Finkelstein RR (1994) Mutations at two new Arabidopsis ABA response loci are similar to the abi3 mutations. Plant J 5:765–771

    Article  Google Scholar 

  • Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609

    Article  CAS  Google Scholar 

  • Finkelstein RR, Ming LW, Lynch TJ, Goodman RHM (1998) The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA 2 domain protein. Plant Cell 10:1043–1054

    Article  CAS  Google Scholar 

  • Gao HB, Brandizzi F, Benning C, Larkin RM (2008) A membrane-tethered transcription factor defines a branch of the heat stress response in Arabidopsis thaliana. Proc Natl Acad Sci 105:16398–16403

    Article  CAS  Google Scholar 

  • Giraudat J, Hauge BM, Valon C, Smalle J, Parcy F, Goodman HM (1992) Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4:1251–1261

    CAS  PubMed  PubMed Central  Google Scholar 

  • Greve K, La Cour T, Jensen MK, Poulsen FM, Skriver K (2003) Interactions between plant RING-H2 and plant-specific NAC (NAM/ATAF1/2/CUC2) proteins: RING-H2 molecular specificity and cellular localization. Biochemical J 371:97–108

    Article  CAS  Google Scholar 

  • Humbert S, Zhong SH, Deng Y, Howell SH, Rothstein SJ (2012) Alteration of the bZIP60/IRE1 pathway affects plant response to ER stress in Arabidopsis thaliana. PLoS ONE 7:e39023

    Article  CAS  Google Scholar 

  • Jensen MK, Kjaersgaard T, Nielsen MM, Galberg P, Petersen K, O’Shea C, Skriver K (2010) The Arabidopsis thaliana NAC transcription factor family: structure–function relationships and determinants of ANAC019 stress signalling. Biochem J 426:183–196

    Article  CAS  Google Scholar 

  • Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360

    Article  CAS  Google Scholar 

  • Li X, Li X, Li M, Yan Y, Liu X, Li L (2016) Dual function of NAC072 in ABF3-mediated ABA-responsive gene regulation in Arabidopsis. Front Plant Sci 7:1075–1084

    PubMed  PubMed Central  Google Scholar 

  • Liu JX, Howell SH (2016) Managing the protein folding demands in the endoplasmic reticulum of plants. New Phytol 211:418–428

    Article  CAS  Google Scholar 

  • Liu JX, Srivastava R, Howell SH (2008) Stress-induced expression of an activated form of AtbZIP17 provides protection from salt stress in Arabidopsis. Plant Cell Environ 31:1735–1743

    Article  CAS  Google Scholar 

  • Liu X, Hu P, Huang M, Tang Y, Li Y, Li L, Hou X (2016) The NF-YC–RGL2 module integrates GA and ABA signalling to regulate seed germination in Arabidopsis. Nat Commun 7:12768–12782

    Article  CAS  Google Scholar 

  • Monika D, Sarika S, Sneha T, Rao R, Kishor G (2018) Transcriptome analysis reveals interplay between hormones, ROS metabolism and cell wall biosynthesis for drought-induced root growth in wheat. Plant Physiol Biochem 130:482–492

    Article  Google Scholar 

  • Niu F, Wang B, Wu F, Yan J, Li L, Wang C, Wang Y, Yang B, Jiang YQ (2014) Canola (Brassica napus L.) NAC103 transcription factor gene is a novel player inducing reactive oxygen species accumulation and cell death in plants. Biochem Biophys Res Commun 454:30–35

    Article  CAS  Google Scholar 

  • Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87

    Article  CAS  Google Scholar 

  • Pelagio-Flores R, Munoz-Parra E, Barrera-Ortiz S, Ortiz-Castro R, Saenz-Mata J, Ortega-Amaro MA, Jimenez-Bremont JF, Lopez-Bucio J (2019) The cysteine-rich receptor-like protein kinase CRK28 modulates Arabidopsis growth and development and influences abscisic acid responses. Planta 251:2

    Article  Google Scholar 

  • Roldán-Arjona T, Ariza RR (2009) Repair and tolerance of oxidative DNA damage in plants. Mutat Res 681:169–179

    Article  Google Scholar 

  • Ryu TH, Go YS, Choi SH, Kim JI, Chung BY, Kim JH (2019) SOG1-dependent NAC103 modulates the DNA damage response as a transcriptional regulator in Arabidopsis. Plant J 98:83–96

    Article  CAS  Google Scholar 

  • Seki M, Ishida J, Narusaka M, Fujita M, Nanjo T, Umezawa T, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Kazuko YS, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression pattern of around 7,000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray. Funct Integr Genomics 2:282–291

    Article  CAS  Google Scholar 

  • Seok HY, Woo DH, Nguyen LV, Tran HT, Tarte VN, Mehdi SM, Lee SY, Moon YH (2017) Arabidopsis AtNAP functions as a negative regulator via repression of AREB1 in salt stress response. Planta 245:329–341

    Article  CAS  Google Scholar 

  • Shahnejat-Bushehri S, Tarkowska D, Sakuraba Y, Balazadeh S (2016) Arabidopsis NAC transcription factor JUB1 regulates GA/BR metabolism and signalling. Nat Plants 2:16013

    Article  CAS  Google Scholar 

  • Sun L, Yang ZT, Song ZT, Wang MJ, Liu JX (2013) The plant-specific transcription factor NAC103 is induced by bZIP60 through a new cis-regulatory element to modulate the unfolded protein response in Arabidopsis. Plant J 76:274–286

    CAS  PubMed  Google Scholar 

  • Tran L-SP, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyam K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16:2481–2498

    Article  CAS  Google Scholar 

  • Wang J, Yu D, Guo XH, Liu X (2009) Arabidopsis AMY1 expressions and early flowering mutant phenotype. BMB Rep 42:101–105

    Article  CAS  Google Scholar 

  • Xian MJ, Zhang SS, Liu JX, Lu SJ (2016) Membrane-associated transcription factor, bZIP60, is activated by ABA and interacts with MYB7 to regulate seed germination in Arabidopsis. J Fudan Univ (Nat Sci) 55:632–641

    Google Scholar 

  • Xu ZY, Kim SY, Hyeon DY, Kim DH, Dong T, Park Y, Jin JB, Joo SH, Kim SK, Hong JC (2013) The Arabidopsis NAC transcription factor ANAC096 cooperates with bZIP-type transcription factors in dehydration and osmotic stress responses. Plant Cell 25:4708–4724

    Article  CAS  Google Scholar 

  • Yan L, Wei S, Wu Y, Hu R, Li H, Yang W, Xie Q (2015) High-efficiency genome editing in Arabidopsis using YAO Promoter-Driven CRISPR/Cas9 system. Mol Plant 8:1820–1823

    Article  CAS  Google Scholar 

  • Yang SD, Seo PJ, Yoon HK, Park CM (2011) The Arabidopsis NAC transcription factor VNI2 integrates abscisic acid signals into leaf senescence via the COR/RD genes. Plant Cell 23:2155–2168

    Article  CAS  Google Scholar 

  • Yang ZT, Lu SJ, Wang MJ, Bi DL, Sun L, Zhou SF, Song ZT, Liu JX (2014) A plasma membrane-tethered transcription factor, NAC062/ANAC062/NTL6, mediates the unfolded protein response in Arabidopsis. Plant J 79:1033–1043

    Article  CAS  Google Scholar 

  • Yang ZT, Wang MJ, Sun L, Lu SJ, Bi DL, Sun L, Song ZT, Zhang SS, Zhou SF, Liu JX (2014) The membrane-associated transcription factor NAC089 controls ER-stress-induced programmed cell death in plants. PLoS Genet 10:e1004243

    Article  Google Scholar 

  • Zhou SF, Sun L, Valdes AE, Engstrom P, Song ZT, Lu SJ, Liu JX (2015) Membrane-associated transcription factor peptidase, site-2 protease, antagonizes ABA signaling in Arabidopsis. New Phytol 208:188–197

    Article  CAS  Google Scholar 

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Acknowledgements

This study was financially supported by grants from the National Natural Science Foundation of China (31600197 and 32000374) and the Startup Scientific Research Fund from Jiangsu University for Advanced Professionals (14JDG158). The authors also thank Dr. Yu Wang, Jia-Jia Han and Sun-Jie Lu for their help in gene-editing.

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Authors and Affiliations

  1. School of Food and Biological Engineering, Jiangsu University, Zhenjiang, Jiangsu, China

    Ling Sun, Li-Ping Liu, Ya-Zhen Wang & Lei Yang

  2. State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, China

    Mei-Jing Wang & Jian-Xiang Liu

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  1. Ling Sun
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  2. Li-Ping Liu
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  3. Ya-Zhen Wang
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  4. Lei Yang
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  5. Mei-Jing Wang
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  6. Jian-Xiang Liu
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Correspondence to Ling Sun or Mei-Jing Wang.

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We declare that we have no financial and personal relationships with other people or organizations that can inappropriately influence our work, there is no professional or other personal interest of any nature or kind in any product, service and/or company that could be construed as influencing the position presented in, or the review of, the manuscript entitled, “NAC103, a NAC family transcription factor, regulates ABA response during seed germination and seedling growth in Arabidopsis”.

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Communicated by Fuminori Takahashi.

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Sun, L., Liu, LP., Wang, YZ. et al. NAC103, a NAC family transcription factor, regulates ABA response during seed germination and seedling growth in Arabidopsis. Planta 252, 95 (2020). https://doi.org/10.1007/s00425-020-03502-2

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