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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Identification and characterisation of ‘No apical meristem; Arabidopsis transcription activation factor; Cup-shape cotyledon’ (NAC) family transcription factors involved in sugar accumulation and abscisic acid signalling in grape (Vitis vinifera)

Shuang Xia A , Xinyuan Qi A , Jinli Yang A , Qiaoyun Deng A and Xiuqin Wang https://orcid.org/0000-0003-4764-835X A *
+ Author Affiliations
- Author Affiliations

A College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, People’s Republic of China.

* Correspondence to: wangxqbj@163.com

Handling Editor: Peter Bozhkov

Functional Plant Biology 51, FP24207 https://doi.org/10.1071/FP24207
Submitted: 14 August 2024  Accepted: 7 October 2024  Published: 25 October 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

The ‘No apical meristem; Arabidopsis transcription activation factor; Cup-shape cotyledon’ (NAC) transcription factors are pivotal in plant development and stress response. Sucrose-non-fermenting-related protein kinase 1.2 (SnRK1) is a key enzyme in glucose metabolism and ABA signalling. In this study, we used grape (Vitis vinifera) calli to explore NAC’s roles in sugar and ABA pathways and its relationship with VvSnRK1.2. We identified 19 VvNACs highly expressed at 90 days after blooming, coinciding with grape maturity and high sugar accumulation, and 11 VvNACs randomly selected from 19 were demonstrated in response to sugar and ABA treatments. VvNAC26 showed significant response to sugar and ABA treatments, and its protein, as a nucleus protein, had transcriptional activation in yeast. We obtained the overexpression (OE-VvNAC26) and RNA-inhibition (RNAi-VvNAC26) of VvNAC26 in transgenic calli by Agrobacterium tumefaciens-mediated transformation. We found that VvNAC26 negatively influenced fructose content. Under sugar and ABA treatments, VvNAC26 negatively influenced the expression of most sugar-related genes, while positively influencing the expression of most ABA pathway-related genes. Dual-luciferase reporter experiments demonstrated that VvNAC26 significantly upregulates VvSnRK1.2 promoter expression in tobacco (Nicotiana benthamiana) leaves, although this process in grape calli requires ABA. The levels of sugar content, sugar-related genes, and ABA-related genes fluctuated significantly in OE-VvNAC26 + RNAi-VvSnRK1.2 and OE-VvSnRK1.2 + RNAi-VvNAC26 transgenic calli. These findings indicated that VvNAC26 regulates sugar metabolism and ABA pathway, displaying synergistic interactions with VvSnRK1.2.

Keywords: ABA-related genes, ABA treatment, grape calli, NAC, sugar content, sugar-related genes, sugar treatment, VvNAC26, VvSnRK1.2.

References

Baena-González E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448, 938-942.
| Crossref | Google Scholar | PubMed |

Belda-Palazón B, Adamo M, Valerio C, Ferreira LJ, Confraria A, Reis-Barata D, Rodrigues A, Meyer C, Rodriguez PL, Baena-González E (2020) A dual function of SnRK2 kinases in the regulation of SnRK1 and plant growth. Nature Plants 6, 1345-1353.
| Crossref | Google Scholar | PubMed |

Borsani J, Budde CO, Porrini L, Lauxmann MA, Lombardo VA, Murray R, Andreo CS, Drincovich MF, Lara MV (2009) Carbon metabolism of peach fruit after harvest: changes in enzymes involved in organic acid and sugar level modifications. Journal of Experimental Botany 60, 1823-1837.
| Crossref | Google Scholar | PubMed |

Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annual Review of Plant Biology 61, 651-679.
| Crossref | Google Scholar | PubMed |

Du Z, You S, Yang D, Tao Y, Zhu Y, Sun W, Chen Z, Li J (2022) Comprehensive analysis of the NAC transcription factor gene family in Kandelia obovata reveals potential members related to chilling tolerance. Frontiers in Plant Science 13, 1048822.
| Crossref | Google Scholar | PubMed |

D’Incà E, Cazzaniga S, Foresti C, Vitulo N, Bertini E, Galli M, Gallavotti A, Pezzotti M, Battista Tornielli G, Zenoni S (2021) VviNAC33 promotes organ de-greening and represses vegetative growth during the vegetative-to-mature phase transition in grapevine. New Phytologist 231, 726-746.
| Crossref | Google Scholar | PubMed |

Fang L, Su L, Sun X, Li X, Sun M, Karungo SK, Fang S, Chu J, Li S, Xin H (2016) Expression of Vitis amurensis NAC26 in Arabidopsis enhances drought tolerance by modulating jasmonic acid synthesis. Journal of Experimental Botany 67, 2829-2845.
| Crossref | Google Scholar | PubMed |

Feng P, Sun X, Liu X, Li Y, Sun Q, Lu H, Li M, Ding X, Dong Y (2022) Epigenetic regulation of plant tolerance to salt stress by histone acetyltransferase GsMYST1 from wild soybean. Frontiers in Plant Science 13, 860056.
| Crossref | Google Scholar | PubMed |

Fichtner F, Lunn JE (2021) The role of trehalose 6-phosphate (Tre6P) in plant metabolism and development. Annual Review of Plant Biology 72, 737-760.
| Crossref | Google Scholar | PubMed |

Fields S, Song O-K (1989) A novel genetic system to detect protein-protein interactions. Nature 340, 245-246.
| Crossref | Google Scholar | PubMed |

Hamasaki H, Kurihara Y, Kuromori T, Kusano H, Nagata N, Yamamoto YY, Shimada H, Matsui M (2019) SnRK1 kinase and the NAC transcription factor SOG1 are components of a novel signaling pathway mediating the low energy response triggered by ATP depletion. Frontiers in Plant Science 10, 503.
| Crossref | Google Scholar | PubMed |

Hansey CN, Vaillancourt B, Sekhon RS, de Leon N, Kaeppler SM, Buell CR (2012) Maize (Zea mays L.) genome diversity as revealed by RNA-sequencing. PLoS ONE 7, e33071.
| Crossref | Google Scholar | PubMed |

Hu Y, Liu B, Ren H, Chen L, Watkins CB, Gan S-S (2021) The leaf senescence-promoting transcription factor AtNAP activates its direct target gene CYTOKININ OXIDASE 3 to facilitate senescence processes by degrading cytokinins. Molecular Horticulture 1, 12.
| Crossref | Google Scholar | PubMed |

Huang T, Yu D, Wang X (2021) VvWRKY22 transcription factor interacts with VvSnRK1.1/VvSnRK1.2 and regulates sugar accumulation in grape. Biochemical and Biophysical Research Communications 554, 193-198.
| Crossref | Google Scholar | PubMed |

Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Bioinformatics 8, 275-282.
| Crossref | Google Scholar | PubMed |

Jossier M, Bouly J-P, Meimoun P, Arjmand A, Lessard P, Hawley S, Grahame Hardie D, Thomas M (2009) SnRK1 (SNF1-related kinase 1) has a central role in sugar and ABA signalling in Arabidopsis thaliana. The Plant Journal 59, 316-328.
| Crossref | Google Scholar | PubMed |

Kou X, Zhou J, Wu CE, Yang S, Liu Y, Chai L, Xue Z (2021) The interplay between ABA/ethylene and NAC TFs in tomato fruit ripening: a review. Plant Molecular Biology 106, 223-238.
| Crossref | Google Scholar | PubMed |

Li L, Jiang W, Lu Y (2018) A modified gibson assembly method for cloning large DNA fragments with high GC contents. Methods in Molecular Biology 1671, 203-209.
| Crossref | Google Scholar | PubMed |

Mair A, Pedrotti L, Wurzinger B, Anrather D, Simeunovic A, Weiste C, Valerio C, Dietrich K, Kirchler T, Nägele T, Vicente Carbajosa J, Hanson J, Baena-González E, Chaban C, Weckwerth W, Dröge-Laser W, Teige M (2015) SnRK1-triggered switch of bZIP63 dimerization mediates the low-energy response in plants. eLife 4, e05828.
| Crossref | Google Scholar | PubMed |

Meng X, Liu S, Zhang C, He J, Ma D, Wang X, Dong T, Guo F, Cai J, Long T, Li Z, Zhu M (2023) The unique sweet potato NAC transcription factor IbNAC3 modulates combined salt and drought stresses. Plant Physiology 191, 747-771.
| Crossref | Google Scholar | PubMed |

Moine A, Pugliese M, Monchiero M, Gribaudo I, Gullino ML, Pagliarani C, Gambino G (2023) Effects of fungicide application on physiological and molecular responses of grapevine (Vitis vinifera L.): a comparison between copper and sulfur fungicides applied alone and in combination with novel fungicides. Pest Management Science 79, 4569-4588.
| Crossref | Google Scholar | PubMed |

Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods 5, 621-628.
| Crossref | Google Scholar | PubMed |

Nägele T, Gibon Y, Le Hir R (2022) Plant sugar metabolism, transport and signalling in challenging environments. Physiologia Plantarum 174, e13768.
| Crossref | Google Scholar | PubMed |

Peixoto B, Baena-González E (2022) Management of plant central metabolism by SnRK1 protein kinases. Journal of Experimental Botany 73, 7068-7082.
| Crossref | Google Scholar | PubMed |

Peng X, Wang Q, Wang Y, Cheng B, Zhao Y, Zhu S (2019) A maize NAC transcription factor, ZmNAC34, negatively regulates starch synthesis in rice. Plant Cell Reports 38, 1473-1484.
| Crossref | Google Scholar | PubMed |

R Core Team (2020) R: A language and environment for statistical computing. Version 3.6.3. (R Foundation for Statistical Computing: Vienna, Austria) Available at https://www.R-project.org/

Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annual Review of Plant Biology 57, 675-709.
| Crossref | Google Scholar | PubMed |

Ruan Y-L (2014) Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annual Review of Plant Biology 65, 33-67.
| Crossref | Google Scholar | PubMed |

Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406-425.
| Crossref | Google Scholar | PubMed |

Sakr S, Wang M, Dédaldéchamp F, Perez-Garcia M-D, Ogé L, Hamama L, Atanassova R (2018) The sugar-signaling hub: overview of regulators and interaction with the hormonal and metabolic network. International Journal of Molecular Sciences 19, 2506.
| Crossref | Google Scholar | PubMed |

Sami F, Yusuf M, Faizan M, Faraz A, Hayat S (2016) Role of sugars under abiotic stress. Plant Physiology and Biochemistry 109, 54-61.
| Crossref | Google Scholar | PubMed |

Seok H-Y, Woo D-H, Nguyen LV, Tran HT, Tarte VN, Mehdi SMM, Lee S-Y, Moon Y-H (2017) Arabidopsis AtNAP functions as a negative regulator via repression of AREB1 in salt stress response. Planta 245, 329-341.
| Crossref | Google Scholar | PubMed |

Sun H, Hu M, Li J, Chen L, Li M, Zhang S, Zhang X, Yang X (2018) Comprehensive analysis of NAC transcription factors uncovers their roles during fiber development and stress response in cotton. BMC Plant Biology 18, 150.
| Crossref | Google Scholar | PubMed |

Sun Z, Liu Q, Qu G, Feng Y, Reetz MT (2019) Utility of B-Factors in protein science: interpreting rigidity, flexibility, and internal motion and engineering thermostability. Chemical Reviews 119, 1626-1665.
| Crossref | Google Scholar | PubMed |

Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution 38, 3022-3027.
| Crossref | Google Scholar | PubMed |

Ueda H, Ito T, Inoue R, Masuda Y, Nagashima Y, Kozuka T, Kusaba M (2020) Genetic interaction among phytochrome, ethylene and abscisic acid signaling during dark-induced senescence in Arabidopsis thaliana. Frontiers in Plant Science 11, 564.
| Crossref | Google Scholar | PubMed |

Wang N, Zheng Y, Xin H, Fang L, Li S (2013) Comprehensive analysis of NAC domain transcription factor gene family in Vitis vinifera. Plant Cell Reports 32, 61-75.
| Crossref | Google Scholar | PubMed |

Wheeler S, Loveys B, Ford C, Davies C (2009) The relationship between the expression of abscisic acid biosynthesis genes, accumulation of abscisic acid and the promotion of Vitis vinifera L. berry ripening by abscisic acid. Australian Journal of Grape and Wine Research 15, 195-204.
| Crossref | Google Scholar |

Xing S, Chen K, Zhu H, Zhang R, Zhang H, Li B, Gao C (2020) Fine-tuning sugar content in strawberry. Genome Biology 21, 230.
| Crossref | Google Scholar | PubMed |

Yang T, Ma H, Li Y, Zhang Y, Zhang J, Wu T, Song T, Yao Y, Tian J (2021) Apple MPK4 mediates phosphorylation of MYB1 to enhance light-induced anthocyanin accumulation. The Plant Journal 106, 1728-1745.
| Crossref | Google Scholar | PubMed |

Yu W, Peng F, Wang W, Liang J, Xiao Y, Yuan X (2021) SnRK1 phosphorylation of SDH positively regulates sorbitol metabolism and promotes sugar accumulation in peach fruit. Tree Physiology 41, 1077-1086.
| Crossref | Google Scholar | PubMed |

Zhang K, Gan S-S (2012) An abscisic acid – AtNAP transcription factor – SAG113 protein phosphatase 2C regulatory chain for controlling dehydration in senescing Arabidopsis leaves. Plant Physiology 158, 961-969.
| Crossref | Google Scholar | PubMed |

Zhang X, Long Y, Chen X, Zhang B, Xin Y, Li L, Cao S, Liu F, Wang Z, Huang H, Zhou D, Xia J (2021) A NAC transcription factor OsNAC3 positively regulates ABA response and salt tolerance in rice. BMC Plant Biology 21, 546.
| Crossref | Google Scholar | PubMed |

Zhao Y, Wang X-Q (2021) The hot issue: TOR signalling network in plants. Functional Plant Biology 48, 1-7.
| Crossref | Google Scholar | PubMed |

Zhao Y, Wang X-Q (2022) VvTOR interacts with VvSnRK1.1 and regulates sugar metabolism in grape. Planta 256, 56.
| Crossref | Google Scholar | PubMed |