Abstract
Main conclusion
The potential biotechnological application of NAC overexpression has been challenged by meta-analysis, establishing a correlation between the magnitudes of several physiological and biochemical parameters and the enhanced tolerance to cold.
Abstract
Overexpression of various NAC (NAM/ATAF/CUC) transcription factors in different plant systems was shown to confer enhanced tolerance to low temperatures by inducing both common and distinctive stress response pathways. However, lack of consensus on the type of parameters evaluated, their magnitudes, and direction of the responses complicates drawing general conclusions on the effects of NAC expression in plant physiology. We report herein a meta-analysis summarizing the most critical response variables used to study the effect of overexpressing NAC regulators on cold stress tolerance. We found that NAC overexpression affected all of the outcome parameters in stressed plants, and one response in control conditions. Transformed plants displayed an increase of at least 40% in positive responses, while negative outcomes were reduced by at least 30%. The most reported parameters included survival, electrolyte leakage, and malondialdehyde contents, whereas the most sensitive to the treatments were the Fv/Fm parameter, survival, and the activity of catalases. We also explored how different experimental arrangements affected the magnitudes of the responses. NAC-mediated improvements were best observed after severe stress episodes and during brief treatments (ranging from 5 to 24 h), especially in terms of antioxidant activities, accumulation of free proline, and parameters related to membrane integrity. Use of heterologous expression also favored several indicators of plant fitness. Our findings should help both basic and applied research on the influence of NAC expression on enhanced tolerance to cold.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article and its supplementary information files.
Abbreviations
- CAT:
-
Catalase
- EL:
-
Electrolyte leakage
- LT:
-
Low temperature
- MDA:
-
Malondialdehyde
- NT:
-
Non-transformed plants
- POD:
-
Peroxidase
- SOD:
-
Superoxide dismutase
- TF:
-
Transcription factor
References
Borenstein M, Hedges LV, Higgins J, Rothstein H (2009) Introduction to meta-analysis. Wiley, Hoboken
Campos PS, Quartin V, Ramalho JC, Nunes MA (2003) Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. plants. J Plant Physiol 160:283–292. https://doi.org/10.1078/0176-1617-00833
Cao H, Wang L, Nawaz MA, Niu M, Sun J, Xie J, Kong Q, Huang Y, Cheng F, Bie Z (2017) Ectopic expression of pumpkin NAC transcription factor CmNAC1 improves multiple abiotic stress tolerance in Arabidopsis. Front Plant Sci 8:2052. https://doi.org/10.3389/fpls.2017.02052
Chen X, Wang Y, Lv B, Li J, Luo L, Lu S, Zhang X, Ma H, Ming F (2014) The NAC family transcription factor OsNAP confers abiotic stress response through the ABA pathway. Plant Cell Physiol 55:604–619. https://doi.org/10.1093/pcp/pct204
Chinnusamy V, Ohta M, Kanrar S, Lee B-H, Hong X, Agarwal M, Zhu J-K (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17:1043–1054. https://doi.org/10.1101/gad.1077503
Diao P, Chen C, Zhang Y, Meng Q, Lv W, Ma N (2020) The role of NAC transcription factor in plant cold response. Plant Signal Behav 15:9. https://doi.org/10.1080/15592324.2020.1785668
Ding A, Li S, Li W, Hao Q, Wan X, Wang K, Liu Q, Liu Q, Jiang X (2019a) RhNAC31, a novel rose NAC transcription factor, enhances tolerance to multiple abiotic stresses in Arabidopsis. Acta Physiol Plant 41:75. https://doi.org/10.1007/s11738-019-2866-1
Ding Y, Shi Y, Yang S (2019b) Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants. New Phytol 222:1690–1704. https://doi.org/10.1111/nph.15696
Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634. https://doi.org/10.1136/bmj.315.7109.629
Farooq M, Aziz T, Wahid A, Lee D-J, Siddique KHM (2009) Chilling tolerance in maize: agronomic and physiological approaches. Crop Pasture Sci 60:501–516. https://doi.org/10.1071/CP08427
Figueroa N, Lodeyro AF, Carrillo N, Gómez R (2021) Meta-analysis reveals key features of the improved drought tolerance of plants overexpressing NAC transcription factors. Environ Exp Bot 186:104449. https://doi.org/10.1016/j.envexpbot.2021.104449
Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690. https://doi.org/10.1105/tpc.003483
Foyer CH, Hanke G (2022) Abiotic stress and adaptation of electron transport: regulation of the production and processing of ROS signals in chloroplasts. In: Ruban A, Foyer CH, Murchie EH (eds) Photosynthesis in action. Academic Press, Cambridge, pp 85–102. https://doi.org/10.1016/B978-0-12-823781-6.00010-1
Gómez R, Vicino P, Carrillo N, Lodeyro AF (2019) Manipulation of oxidative stress responses as a strategy to generate stress-tolerant crops. From damage to signaling to tolerance. Crit Rev Biotechnol 39:693–708. https://doi.org/10.1080/07388551.2019.1597829
Guo Y, Ping W, Chen J, Zhu L, Zhao Y, Guo J, Huang Y (2019) Meta-analysis of the effects of overexpression of WRKY transcription factors on plant responses to drought stress. BMC Genet 20:63. https://doi.org/10.1186/s12863-019-0766-4
Han D, Du M, Zhou Z, Wang S, Li T, Han J, Xu T, Yang G (2020a) An NAC transcription factor gene from Malus baccata, MbNAC29, increases cold and high salinity tolerance in Arabidopsis. Vitro Cell Dev Biol Plant 56:588–599. https://doi.org/10.1007/s11627-020-10105-9
Han D, Du M, Zhou Z, Wang S, Li T, Han J, Xu T, Yang G (2020b) Overexpression of a Malus baccata NAC transcription factor gene MbNAC25 increases cold and salinity tolerance in Arabidopsis. Int J Mol Sci 21:1198. https://doi.org/10.3390/ijms21041198
Hao Y-J, Wei W, Song Q-X, Chen H-W, Zhang Y-Q, Wang F, Zou H-F, Lei G, Tian A-G, Zhang W-K, Ma B, Zhang J-S, Chen S-Y (2011) Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. Plant J 68:302–313. https://doi.org/10.1111/j.1365-313X.2011.04687.x
He M, Dijkstra FA (2014) Drought effect on plant nitrogen and phosphorus: a meta-analysis. New Phytol 204:924–931. https://doi.org/10.1111/nph.12952
Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156. https://doi.org/10.1890/0012-9658(1999)080[1150:TMAORR]2.0.CO;2
Hénanff GL, Profizi C, Courteaux B, Rabenoelina F, Gérard C, Clément C, Baillieul F, Cordelier S, Dhondt-Cordelier S (2013) Grapevine NAC1 transcription factor as a convergent node in developmental processes, abiotic stresses, and necrotrophic/biotrophic pathogen tolerance. J Exp Bot 64:4877–4893. https://doi.org/10.1093/jxb/ert277
Hou X-M, Zhang H-F, Liu S-Y, Wang X-K, Zhang Y-M, Meng Y-C, Luo D, Chen R-G (2020) The NAC transcription factor CaNAC064 is a regulator of cold stress tolerance in peppers. Plant Sci 291:110346. https://doi.org/10.1016/j.plantsci.2019.110346
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. https://doi.org/10.1007/s11103-008-9309-5
Huang G-T, Ma S-L, Bai L-P, Zhang L, Ma H, Jia P, Liu J, Zhong M, Guo Z-F (2012) Signal transduction during cold, salt, and drought stresses in plants. Mol Biol Rep 39:969–987. https://doi.org/10.1007/s11033-011-0823-1
Hussain HA, Hussain S, Khaliq A, Ashraf U, Anjum SA, Men S, Wang L (2018) Chilling and drought stresses in crop plants: implications, cross talk, and potential management opportunities. Front Plant Sci 9:393. https://doi.org/10.3389/fpls.2018.00393
Jeong JS, Kim YS, Baek KH, Jung H, Ha S-H, Do Choi Y, Kim M, Reuzeau C, Kim J-K (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153:185–197. https://doi.org/10.1104/pp.110.154773
Jin C, Li K-Q, Xu X-Y, Zhang H-P, Chen H-X, Chen Y-H, Hao J, Wang Y, Huang X-S, Zhang S-L (2017) A novel NAC transcription factor, PbeNAC1, of Pyrus betulifolia confers cold and drought tolerance via interacting with pbeDREBs and activating the expression of stress-responsive genes. Front Plant Sci 8:1049. https://doi.org/10.3389/fpls.2017.01049
Ju Y-L, Yue X-F, Min Z, Wang X-H, Fang Y-L, Zhang J-X (2020) VvNAC17, a novel stress-responsive grapevine (Vitis vinifera L.) NAC transcription factor, increases sensitivity to abscisic acid and enhances salinity, freezing, and drought tolerance in transgenic Arabidopsis. Plant Physiol Biochem 146:98–111. https://doi.org/10.1016/j.plaphy.2019.11.002
Kalaji HM, Schansker G, Ladle RJ et al (2014) Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynth Res 122:121–158. https://doi.org/10.1007/s11120-014-0024-6
Knight H, Zarka DG, Okamoto H, Thomashow MF, Knight MR (2004) Abscisic acid induces CBF gene transcription and subsequent induction of cold-regulated genes via the CRT promoter element. Plant Physiol 135:1710–1717. https://doi.org/10.1104/pp.104.043562
Li X-L, Yang X, Hu Y-X, Yu X-D, Li Q-L (2014) A novel NAC transcription factor from Suaeda liaotungensis K. enhanced transgenic Arabidopsis drought, salt, and cold stress tolerance. Plant Cell Rep 33:767–778. https://doi.org/10.1007/s00299-014-1602-y
Li X-D, Zhuang K-Y, Liu Z-M, Yang D-Y, Ma N-N, Meng Q-W (2016) Overexpression of a novel NAC-type tomato transcription factor, SlNAM1, enhances the chilling stress tolerance of transgenic tobacco. J Plant Physiol 204:54–65. https://doi.org/10.1016/j.jplph.2016.06.024
Li P, Peng Z, Xu P, Tang G, Ma C, Zhu J, Shan L, Wan S (2021) Genome-wide identification of NAC transcription factors and their functional prediction of abiotic stress response in peanut. Front Genet 12:630292. https://doi.org/10.3389/fgene.2021.630292
Liang J, Zheng J, Wu Z, Wang H (2020) Strawberry FaNAC2 enhances tolerance to abiotic stress by regulating proline metabolism. Plants 9:1–17. https://doi.org/10.3390/plants9111417
Lin J, Liu D, Wang X, Ahmed S, Li M, Kovinich N, Sui S (2021) Transgene CpNAC68 from wintersweet (Chimonanthus praecox) improves Arabidopsis survival of multiple abiotic stresses. Plants 10:1403. https://doi.org/10.3390/plants10071403
Ling L, Song L, Wang Y, Guo C (2017) Genome-wide analysis and expression patterns of the NAC transcription factor family in Medicago truncatula. Physiol Mol Biol Plants 23:343–356. https://doi.org/10.1007/s12298-017-0421-3
Liu W, Yu K, He T, Li F, Zhang D, Liu J (2013) The low temperature induced physiological responses of Avena nuda L., a cold-tolerant plant species. Sci World J 2013:658793. https://doi.org/10.1155/2013/658793
Liu Y, Jiang Y, Lan J, Zou Y, Gao J (2014) Comparative transcriptomic analysis of the response to cold acclimation in Eucalyptus dunnii. PLoS One 9:e113091. https://doi.org/10.1371/journal.pone.0113091
Liu X, Zhou Y, Xiao J, Bao F (2018) Effects of chilling on the structure, function and development of chloroplasts. Front Plant Sci 9:1715. https://doi.org/10.3389/fpls.2018.01715
Ma N-N, Zuo Y-Q, Liang X-Q, Yin B, Wang G-D, Meng Q-W (2013) The multiple stress-responsive transcription factor SlNAC1 improves the chilling tolerance of tomato. Physiol Plant 149:474–486. https://doi.org/10.1111/ppl.12049
Mao X, Zhang H, Qian X, Li A, Zhao G, Jing R (2012) TaNAC2, a NAC-type wheat transcription factor conferring enhanced multiple abiotic stress tolerances in Arabidopsis. J Exp Bot 63:2933–2946. https://doi.org/10.1093/jxb/err462
Mao X, Chen S, Li A, Zhai C, Jing R (2014) Novel NAC transcription factor TaNAC67 confers enhanced multi-abiotic stress tolerances in Arabidopsis. PLoS One 9:e84359. https://doi.org/10.1371/journal.pone.0084359
Min X, Jin X, Zhang Z, Wei X, Ndayambaza B, Wang Y, Liu W (2020) Genome-wide identification of NAC transcription factor family and functional analysis of the abiotic stress-responsive genes in Medicago sativa L. J Plant Growth Regul 39:324–337. https://doi.org/10.1007/s00344-019-09984-z
Murugesan AK, Somasundaram S, Mohan H, Parida AK, Alphonse V, Govindan G (2020) Ectopic expression of AmNAC1 from Avicennia marina (Forsk.) Vierh. confers multiple abiotic stress tolerance in yeast and tobacco. Plant Cell Tissue Organ Cult 142:51–68. https://doi.org/10.1007/s11240-020-01830-5
Nuruzzaman M, Manimekalai R, Sharoni AM, Satoh K, Kondoh H, Ooka H, Kikuchi S (2010) Genome-wide analysis of NAC transcription factor family in rice. Gene 465:30–44. https://doi.org/10.1016/j.gene.2010.06.008
Nuruzzaman M, Sharoni AM, Kikuchi S (2013) Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Front Microbiol 4:248. https://doi.org/10.3389/fmicb.2013.00248
Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87. https://doi.org/10.1016/j.tplants.2004.12.010
Pang X, Xue M, Ren M, Nan D, Wu Y, Guo H (2019) Ammopiptanthus mongolicus stress-responsive NAC gene enhances the tolerance of transgenic Arabidopsis thaliana to drought and cold stresses. Genet Mol Biol 42:624–634. https://doi.org/10.1590/1678-4685-gmb-2018-0101
Pearce RS (2001) Plant freezing and damage. Ann Bot 87:417–424. https://doi.org/10.1006/anbo.2000.1352
Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17:369–381. https://doi.org/10.1016/j.tplants.2012.02.004
Qu Y, Duan M, Zhang Z, Dong J, Wang T (2016) Overexpression of the Medicago falcata NAC transcription factor MfNAC3 enhances cold tolerance in Medicago truncatula. Environ Exp Bot 129:67–76. https://doi.org/10.1016/j.envexpbot.2015.12.012
Rankenberg T, Geldhof B, van Veen H, Holsteens K, Van de Poel B, Sasidharan R (2021) Age-dependent abiotic stress resilience in plants. Trends Plant Sci 26:692–705. https://doi.org/10.1016/j.tplants.2020.12.016
Rihan HZ, Al-Issawi M, Fuller MP (2017) Advances in physiological and molecular aspects of plant cold tolerance. J Plant Interact 12:143–157. https://doi.org/10.1080/17429145.2017.1308568
Rosenberg MS (2005) The file-drawer problem revisited: a general weighted method for calculating fail-safe numbers in meta-analysis. Evolution 59:464–468. https://doi.org/10.1111/j.0014-3820.2005.tb01004.x
Rosenthal R (1979) The file drawer problem and tolerance for null results. Psychol Bull 86:638–641. https://doi.org/10.1037/0033-2909.86.3.638
Sanghera GS, Wani SH, Hussain W, Singh NB (2011) Engineering cold stress tolerance in crop plants. Curr Genom 12:30–43. https://doi.org/10.2174/138920211794520178
Seo PJ, Kim MJ, Park J-Y, Kim S-Y, Jeon J, Lee Y-H, Kim J, Park C-M (2010) Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis. Plant J 61:661–671. https://doi.org/10.1111/j.1365-313X.2009.04091.x
Shan W, Kuang J-F, Lu W-J, Chen J-Y (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. https://doi.org/10.1111/pce.12303
Singh AK, Sharma V, Pal AK, Acharya V, Ahuja PS (2013) Genome-wide organization and expression profiling of the NAC transcription factor family in potato (Solanum tuberosum L.). DNA Res 20:403–423. https://doi.org/10.1093/dnares/dst019
Singh S, Koyama H, Bhati KK, Alok A (2021) The biotechnological importance of the plant-specific NAC transcription factor family in crop improvement. J Plant Res 134:475–495. https://doi.org/10.1007/s10265-021-01270-y
Song S-Y, Chen Y, Chen J, Dai X-Y, Zhang W-H (2011) Physiological mechanisms underlying OsNAC5-dependent tolerance of rice plants to abiotic stress. Planta 234:331–345. https://doi.org/10.1007/s00425-011-1403-2
Su H, Zhang S, Yin Y, Zhu D, Han L (2015) Genome-wide analysis of NAM-ATAF1,2-CUC2 transcription factor family in Solanum lycopersicum. J Plant Biochem Biotechnol 24:176–183. https://doi.org/10.1007/s13562-014-0255-9
Tarkowski ŁP, Van den Ende W (2015) Cold tolerance triggered by soluble sugars: a multifaceted countermeasure. Front Plant Sci 6:203. https://doi.org/10.3389/fpls.2015.00203
Thomashow MF (1999) PLANT COLD ACCLIMATION: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599. https://doi.org/10.1146/annurev.arplant.50.1.571
Tran L-SP, Nishiyama R, Yamaguchi-Shinozaki K, Shinozaki K (2010) Potential utilization of NAC transcription factors to enhance abiotic stress tolerance in plants by biotechnological approach. GM Crops 1:32–39. https://doi.org/10.4161/gmcr.1.1.10569
Viechtbauer W (2005) Bias and efficiency of meta-analytic variance estimators in the random-effects model. J Educ Behav Stat 30:261–293. https://doi.org/10.3102/10769986030003261
Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. J Stat SoftW 36:1–48. https://doi.org/10.18637/jss.v036.i03
Wang G-D, Liu Q, Shang X-T, Chen C, Xu N, Guan J, Meng Q-W (2018) Overexpression of transcription factor SlNAC35 enhances the chilling tolerance of transgenic tomato. Biol Plant 62:479–488. https://doi.org/10.1007/s10535-018-0770-y
Wang H-F, Shan H-Y, Shi H, Wu D-D, Li T-T, Li Q-L (2021) Characterization of a transcription factor SlNAC7 gene from Suaeda liaotungensis and its role in stress tolerance. J Plant Res 134:1105–1120. https://doi.org/10.1007/s10265-021-01309-0
Wei Y, Chen H, Wang L, Zhao Q, Wang D, Zhang T (2022) Cold acclimation alleviates cold stress-induced PSII inhibition and oxidative damage in tobacco leaves. Plant Signal Behav 17:2013638. https://doi.org/10.1080/15592324.2021.2013638
Yadav SK (2010) Cold stress tolerance mechanisms in plants. A review. Agron Sustain Dev 30:515–527. https://doi.org/10.1051/agro/2009050
Yang S-D, Seo PJ, Yoon H-K, Park C-M (2011) The Arabidopsis NAC transcription factor VNI2 integrates abscisic acid signals into leaf senescence via the COR/RD genes. Plant Cell 23:2155–2168. https://doi.org/10.1105/tpc.111.084913
Yang X, Wang X, Ji L, Yi Z, Fu C, Ran J, Hu R, Zhou G (2015) Overexpression of a Miscanthus lutarioriparius NAC gene MlNAC5 confers enhanced drought and cold tolerance in Arabidopsis. Plant Cell Rep 34:943–958. https://doi.org/10.1007/s00299-015-1756-2
Yarra R, Wei W (2021) The NAC-type transcription factor GmNAC20 improves cold, salinity tolerance, and lateral root formation in transgenic rice plants. Funct Integr Genom 21:473–487. https://doi.org/10.1007/s10142-021-00790-z
Yong Y, Zhang Y, Lyu Y (2019) A stress-responsive NAC transcription factor from Tiger Lily (LlNAC2) interacts with LlDREB1 and LlZHFD4 and enhances various abiotic stress tolerance in Arabidopsis. Int J Mol Sci 20:3225. https://doi.org/10.3390/ijms20133225
Yoo SY, Kim Y, Kim SY, Lee JS, Ahn JH (2007) Control of flowering time and cold response by a NAC-domain protein in Arabidopsis. PLoS One 2:e642. https://doi.org/10.1371/journal.pone.0000642
You J, Chan Z (2015) ROS regulation during abiotic stress responses in crop plants. Front Plant Sci 6:1092. https://doi.org/10.3389/fpls.2015.01092
Zhan P-L, Ke S-W, Zhang P-Y, Zhou C-C, Fu B-L, Zhang X-Q, Zhong T-X, Chen S, Xie X-M (2018) Overexpression of two cold-responsive ATAF-like NAC transcription factors from fine-stem stylo (Stylosanthes guianensis var. intermedia) enhances cold tolerance in tobacco plants. Plant Cell Tissue Organ Cult 135:545–558. https://doi.org/10.1007/s11240-018-1486-6
Zhang L, Zhang L, Xia C, Zhao G, Jia J, Kong X (2016) The novel wheat transcription factor TaNAC47 enhances multiple abiotic stress tolerances in transgenic plants. Front Plant Sci 6:1174. https://doi.org/10.3389/fpls.2015.01174
Zhang H, Ma F, Wang X, Liu S, Saeed UH, Hou X, Zhang Y, Luo D, Meng Y, Zhang W, Abid K, Chen R (2020) Molecular and functional characterization of CaNAC035, an NAC transcription factor from pepper (Capsicum annuum L.). Front Plant Sci 11:14. https://doi.org/10.3389/fpls.2020.00014
Zhao X, Yang X, Pei S, He G, Wang X, Tang Q, Jia C, Lu Y, Hu R, Zhou G (2016) The Miscanthus NAC transcription factor MlNAC9 enhances abiotic stress tolerance in transgenic Arabidopsis. Gene 586:158–169. https://doi.org/10.1016/j.gene.2016.04.028
Zhao Y, Han Q, Ding C, Huang Y, Liao J, Chen T, Feng S, Zhou L, Zhang Z, Chen Y, Yuan S, Yuan M (2020) Effect of low temperature on chlorophyll biosynthesis and chloroplast biogenesis of rice seedlings during greening. Int J Mol Sci 21:1390. https://doi.org/10.3390/ijms21041390
Zhou P, Li X, Liu X, Wen X, Zhang Y, Zhang D (2021) Transcriptome profiling of Malus sieversii under freezing stress after being cold-acclimated. BMC Genomics 22:681. https://doi.org/10.1186/s12864-021-07998-0
Funding
The authors declare that the present research received no external funds or other financial support.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Communicated by Dorothea Bartels.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Figueroa, N., Gómez, R. Bolstered plant tolerance to low temperatures by overexpressing NAC transcription factors: identification of critical variables by meta-analysis. Planta 256, 92 (2022). https://doi.org/10.1007/s00425-022-04007-w
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-022-04007-w