RhNAC31, a novel rose NAC transcription factor, enhances tolerance to multiple abiotic stresses in Arabidopsis

• Autorzy: Ding A. , Li S. , Li W. , Hao Q. , Wan X. , Wang K. , Liu Q. , Liu Q. , Jiang X.
• Języki publikacji: EN

Abstrakty

EN

Plant-specific NAM, ATAF1/2, and CUC (NAC) transcription factors serve essential functions in plant development and plant responses to environmental cues. Yet, transcription factors specific to the rose (Rosa hybrida) NAM/CUC3 subfamily are poorly understood. Here, we identify a novel NAM/CUC3-subfamily transcription factor, RhNAC31, that is associated with flower opening and can be induced by increased salt, cold, and dehydration stress treatment. RhNAC31 has a transactivation region in its C-terminal region, and its overexpression is associated with enhanced cold tolerance in Arabidopsis, conferring a higher survival rate and reduced reactive oxygen (H₂O₂ and O₂⁻) levels. Under salt stress conditions, plants overexpressing RhNAC31 displayed increased germination rates and lower levels of H₂O₂, malondiadehyde (MDA), peroxidase (POD), and superoxide dismutase (SOD). Moreover, RhNAC31 conferred enhanced drought resistance by reducing the rate of water loss through leaves. Further characterization revealed a higher sensitivity of RhNAC31 transgenic plants to abscisic acid (ABA) both during and post-germination, causing lower germination and root inhibition rates under ABA treatment. Quantitative PCR experiments showed that numerous abiotic stress-related genes were activated by RhNAC31 overexpression. Our results highlight RhNAC31 as a positive transcriptional regulator of tolerance to multiple abiotic pressures, and we conclude that RhNAC31 has potential for use in the molecular breeding of stress-tolerant crops.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2019
• Tom: 41
• Numer: 06
• Opis fizyczny: Article 75 [16p.], fig.,ref.

Twórcy

autor

Ding A.

• College of Landscape Architecture and Forestry, Qingdao Agricultural University, Qingdao 266109, Shandong, China

autor

Li S.

• College of Landscape Architecture and Forestry, Qingdao Agricultural University, Qingdao 266109, Shandong, China

autor

Li W.

• College of Landscape Architecture and Forestry, Qingdao Agricultural University, Qingdao 266109, Shandong, China

autor

Hao Q.

• College of Landscape Architecture and Forestry, Qingdao Agricultural University, Qingdao 266109, Shandong, China

autor

Wan X.

• College of Landscape Architecture and Forestry, Qingdao Agricultural University, Qingdao 266109, Shandong, China

autor

Wang K.

• College of Landscape Architecture and Forestry, Qingdao Agricultural University, Qingdao 266109, Shandong, China

autor

Liu Q.

• College of Landscape Architecture and Forestry, Qingdao Agricultural University, Qingdao 266109, Shandong, China

autor

Liu Q.

• College of Landscape Architecture and Forestry, Qingdao Agricultural University, Qingdao 266109, Shandong, China

autor

Jiang X.

• College of Landscape Architecture and Forestry, Qingdao Agricultural University, Qingdao 266109, Shandong, China

Bibliografia

• Balazadeh S, Siddiqui H, Allu AD, Matallana-Ramirez LP, Caldana C, Mehrnia M, Zanor MI, Köhler B, Mueller-Roeber B (2010) A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence. Plant J 62:250–264
• Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287
• Benjamin JG, Nielsen DC (2006) Water deficit effects on root distribution of soybean, field pea and chickpea. Field Crops Res 97:248–253
• Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompon JD (2003) Multiple sequence alignment with the clustal series of programs. Nucleic Acids Res 31:3497–3500
• Choudhury S, Panda P, Sahoo L, Panda SK (2013) Reactive oxygen species signaling in plants under abiotic stress. Plant Signal Behav 8:e23681
• Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90:856–867
• Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
• Cruz de Carvalho MH (2008) Drought stress and reactive oxygen species: production, scavenging and signaling. Plant Signal Behav 3:156–165
• Dai F, Zhang C, Jiang X, Kang M, Yin X, Lu P, Zhang X, Zheng Y, Gao J (2012) RhNAC2 and RhEXPA4 are involved in the regulation of dehydration tolerance during the expansion of rose petals. Plant Physiol 160:2064–2082
• 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
• Fang Y, Liao K, Du H, Xu Y, Song H, Li X, Xiong L (2015) A stress-responsive NAC transcription factor SNAC3 confers heat and drought tolerance through modulation of reactive oxygen species in rice. J Exp Bot 66:6803–6817
• Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Taraqi M, Tran LS, Yamaquchi-Shinozaki K, Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39:863–876
• Haake V, Cook D, Riechmann JL, Pineda O, Thomashow MF, Zhang JZ (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol 130:639–648
• Hanin M, Brini F, Ebel C, Toda Y, Takeda S, Masmoudi K (2011) Plant dehydrins and stress tolerance: versatile proteins for complex mechanisms. Plant Signal Behav 6:1503–1509
• Hu H, You J, Fang Y, Zhu X, Qi Z, Xiong L (2008) Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol Biol 67:169–181
• Hu R, Qi G, Kong Y, Kong D, Gao Q, Zhou G (2010) Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa. BMC Plant Biol 10:145
• Jiang X, Zhang C, Lv P, Jiang G, Liu X, Dai F, Gao J (2014) RhNAC3, a stress-associated NAC transcription factor, has a role in dehydration tolerance through regulating osmotic stress-related genes in rose petals. Plant Biotechnol J 12:38–48
• Jouve L, Jacques D, Douglas GC, Hoffmann L, Hausman JF (2007) Biochemical characterization of early and late bud flushing in common ash (Fraxinus excelsior L.). Plant Sci 172:962–969
• Kim KN, Cheong YH, Grant JJ, Pandey GK, Luan S (2003) CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell 15:411–423
• Kim JH, Woo HR, Kim J, Lim PO, Lee IC, Choi SH, Hwang D, Nam HG (2009) Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science 323:1053–1057
• Lång V, Palva ET (1992) The expression of a rab-related gene, rab18, is induced by abscisic acid during the cold acclimation process of Arabidopsis thaliana (L.) Heynh. Plant Mol Biol 20:951–962
• Lee S, Seo PJ, Lee HJ, Park CM (2012) A NAC transcription factor NTL4 promotes reactive oxygen species production during drought-induced leaf senescence in Arabidopsis. Plant J 70:831–844
• Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327
• Leung J, Merlot S, Giraudat J (1997) The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9:759–771
• Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136
• Liu Y, Chen Y (2007) High-efficiency thermal asymmetric interlaced PCR for amplification of unknown flanking sequences. Biotechniques 43:649–656
• Liu M, Ma Z, Sun W, Huang L, Wu Q, Tang Z, Bu T, Li C, Chen H (2019) Genome-wide analysis of the NAC transcription factor family in Tartary buckwheat (Fagopyrum tataricum). BMC Genom 20:113
• Ma N, Tan H, Liu X, Xue J, Li Y, Gao J (2006) Transcriptional regulation of ethylene receptor and CTR genes involved in ethylene-induced flower opening in cut rose (Rosa hybrida) cv. Samantha. J Exp Bot 57:2763–2773
• Mao C, Lu S, Lv B, Zhang B, Shen J, He J, Luo L, Xi D, Chen X, Ming F (2017) A rice NAC transcription factor promotes leaf senescence via ABA biosynthesis. Plant Physiol 174:1747–1763
• Meng JF, Xu TF, Wang ZZ, Fang YL, Xi ZM, Zhang ZW (2014) The ameliorative effects of exogenous melatonin on grape cuttings under water-deficient stress: antioxidant metabolites, leaf anatomy, and chloroplast morphology. J Pineal Res 57:200–212
• Merlot S, Gosti F, Guerrier D, Vavasseur A, Giraudat J (2001) The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signaling pathway. Plant J 25:295–303
• Msanne J, Lin J, Stone JM, Awada T (2011) Characterization of abiotic stress-responsive Arabidopsis thaliana RD29A and RD29B genes and evaluation of transgenes. Planta 234:97–107
• Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
• Nakashima K, Tran LS, Van Ngunan D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shiniozaki K (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51:617–630
• Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) NAC transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:97–103
• Nordin K, Vahala T, Palva ET (1993) Differential expression of two related, low-temperature-induced genes in Arabidopsis thaliana (L.) Heynh. Plant Mol Biol 21:641–653
• Nuruzzaman M, Manimekalai R, Sharoni A, Satoh K, Kondoh H, Ooka H, Kikuchi S (2010) Genome-wide analysis of NAC transcription factor family in rice. Gene 465:30–44
• Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87
• Pei H, Ma N, Tian J, Luo J, Chen J, Li J, Zheng Y, Chen X, Fei Z, Gao J (2013) An NAC transcription factor controls ethylene-regulated cell expansion in flower petals. Plant Physiol 163:775–791
• Pinheiro GL, Marques CS, Costa MD, Reis PA, Alves MS, Carvalho CM, Fietto LG, Fontes EP (2009) Complete inventory of soybean NAC transcription factor: sequence conservation and expression analysis uncover their distinct roles in stress response. Gene 444:10–23
• Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17:369–381
• Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na⁺/H⁺ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA 99:8436–8441
• Shan W, Kuang JF, Lu WJ, Chen JY (2014) Banana fruit NAC transcription factor MaNAC1 is a direct target of MaICE1 and involved in cold stress through interacting with MaCBF1. Plant Cell Environ 37:2116–2127
• Shi J, Fu XZ, Peng T, Huang XS, Fan QJ, Liu JH (2010) Spermine pretreatment confers dehydration tolerance of citrus in vitro plants via modulation of antioxidative capacity and stomatal response. Tree Physiol 30:914–922
• Souer E, van Houwelingen A, Kloos D, Mol J, Koes R (1996) 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
• Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
• Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama 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
• Wang K, Zhong M, Wu Y, Bai Z, Liang Q, Liu Q, Pan Y, Zhang L, Jiang B, Jia Y, Liu G (2017) Overexpression of a chrysanthemum transcription factor gene DgNAC1 improves the salinity tolerance in chrysanthemum. Plant Cell Rep 36:571–581
• Yokoi S, Quintero FJ, Cubero B, Ruiz MT, Bressan RA, Haseqawa PM, Pardo JM (2002) Differential expression and function of Arabidopsis thaliana NHX Na⁺/H⁺ antiporters in the salt stress response. Plant J 30:529–539
• Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaquchi-Shinozaki K (2010) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J 61:672–685
• Yu S, Huang A, Li J, Gao L, Feng Y, Pemberton E, Chen C (2018) OsNAC45 plays complex roles by mediating POD activity and the expression of development-related genes under various abiotic stress in rice root. Plant Growth Regul 84:519–531
• Zhang J, Huang GQ, Zou D, Yan JQ, Li Y, Hu S, Li XB (2018) The cotton (Gossypium hirsutum) NAC transcription factor (FSN1) as a positive regulator participates in controlling secondary cell wall biosynthesis and modification of fibers. New Phytol 217:625–640

Identyfikatory

DOI

10.1007/s11738-019-2866-1