{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,7]],"date-time":"2026-09-07T21:11:09Z","timestamp":1788815469589,"version":"build-2803163510"},"reference-count":43,"publisher":"MDPI AG","issue":"21","license":[{"start":{"date-parts":[[2021,10,22]],"date-time":"2021-10-22T00:00:00Z","timestamp":1634860800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Yunnan Applied Basic Research Project","award":["2017FB057"],"award-info":[{"award-number":["2017FB057"]}]},{"name":"Yunnan Applied Basic Research Project","award":["2017AB001"],"award-info":[{"award-number":["2017AB001"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>NUTCRACKER (NUC) is a transcription factor expressed in multiple tissues, but little is known about its physiological roles. In this study, we explored the physiological function of NUC with the Arabidopsis knockout, rescue, and overexpression lines. We found that NUC overexpression promoted development at the germination, seedling, and juvenile stages. NUC overexpression increased resistance to nitrogen (N) deficiency stress by increasing the chlorophyll content, suppressing anthocyanin accumulation, and increasing the biomass under N deficiency. In contrast, the absence of NUC did not affect such characteristics. N deficiency significantly increased the expression of NUC in leaves but did not affect the expression of NUC in roots. The overexpression of NUC promoted primary root length under both normal and N deficiency conditions. Furthermore, we found that the N-responsive and lateral-root-related genes TGA1 and NRT2.4 had NUC-binding sites in their promoter regions and that their expression was upregulated by NUC under N deficiency. The overexpression of the NUC increased the number and length of the lateral roots under N deficiency through inducible promotion. Multiple lines of investigation suggest that the regulatory function of the NUC could be bypassed through its redundant MAGPIE (MGP) when the NUC is absent. Our findings provide novel insight into NUC\u2019s functions and will assist efforts to improve plants\u2019 development and resistance to nutrient stresses.<\/jats:p>","DOI":"10.3390\/ijms222111413","type":"journal-article","created":{"date-parts":[[2021,10,22]],"date-time":"2021-10-22T09:18:09Z","timestamp":1634894289000},"page":"11413","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["The Overexpression of NUC Promotes Development and Increases Resistance to Nitrogen Deficiency in Arabidopsis thaliana"],"prefix":"10.3390","volume":"22","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8867-4760","authenticated-orcid":false,"given":"Jing","family":"Ling","sequence":"first","affiliation":[{"name":"Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China"},{"name":"University of the Chinese Academy of Sciences, Beijing 100049, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7087-6601","authenticated-orcid":false,"given":"Xing","family":"Huang","sequence":"additional","affiliation":[{"name":"Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yanxia","family":"Jia","sequence":"additional","affiliation":[{"name":"Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4988-4516","authenticated-orcid":false,"given":"Weiqi","family":"Li","sequence":"additional","affiliation":[{"name":"Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xudong","family":"Zhang","sequence":"additional","affiliation":[{"name":"Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,10,22]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"418","DOI":"10.1111\/j.1365-313X.2010.04432.x","article-title":"Modulation of sugar metabolism by an INDETERMINATE DOMAIN transcription factor contributes to photoperiodic flowering in Arabidopsis","volume":"65","author":"Seo","year":"2011","journal-title":"Plant J."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Jeong, E.Y., Seo, P.J., Woo, J.C., and Park, C.M. (2015). AKIN10 delays flowering by inactivating IDD8 transcription factor through protein phosphorylation in Arabidopsis. BMC Plant Biol., 15.","DOI":"10.1186\/s12870-015-0503-8"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1185","DOI":"10.1105\/tpc.114.132407","article-title":"Arabidopsis BIRD Zinc Finger Proteins Jointly Stabilize Tissue Boundaries by Confining the Cell Fate Regulator SHORT-ROOT and Contributing to Fate Specification","volume":"27","author":"Long","year":"2015","journal-title":"Plant Cell"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1126\/science.1139531","article-title":"An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants","volume":"316","author":"Cui","year":"2007","journal-title":"Science"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/j.pld.2020.08.001","article-title":"Flavonoid scutellarin positively regulates root length through NUTCRACKER","volume":"43","author":"Huang","year":"2021","journal-title":"Plant Divers."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Crawford, N.M., and Forde, B.G. (2002). Molecular and Developmental Biology of Inorganic Nitrogen Nutrition. Arabidopsis Book, 1.","DOI":"10.1199\/tab.0011"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"192","DOI":"10.1126\/science.1186120","article-title":"The Evolution and Future of Earth\u2019s Nitrogen Cycle","volume":"330","author":"Canfield","year":"2010","journal-title":"Science"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"5567","DOI":"10.1093\/jxb\/eru245","article-title":"The primary nitrate response: A multifaceted signalling pathway","volume":"65","author":"Medici","year":"2014","journal-title":"J. Exp. Bot."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"648","DOI":"10.1016\/j.semcdb.2012.01.004","article-title":"Nitrate sensing and signaling in plants","volume":"23","author":"Bouguyon","year":"2012","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1146\/annurev-arplant-042817-040056","article-title":"Nitrate Transport, Signaling, and Use Efficiency","volume":"69","author":"Wang","year":"2018","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1255","DOI":"10.1104\/pp.111.179838","article-title":"Arabidopsis Roots and Shoots Show Distinct Temporal Adaptation Patterns toward Nitrogen Starvation","volume":"157","author":"Krapp","year":"2011","journal-title":"Plant Physiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1080\/00380768.2017.1360128","article-title":"Molecular basis of the nitrogen response in plants","volume":"63","author":"Ueda","year":"2017","journal-title":"Soil Sci. Plant Nutr."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1111\/j.1365-3040.2005.01292.x","article-title":"Nitrate, a signal relieving seed dormancy in Arabidopsis","volume":"28","author":"Alboresi","year":"2005","journal-title":"Plant Cell Environ."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2553","DOI":"10.1093\/jxb\/erx062","article-title":"Signals and players in the transcriptional regulation of root responses by local and systemic N signaling in Arabidopsis thaliana","volume":"68","author":"Bellegarde","year":"2017","journal-title":"J. Exp. Bot."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"707","DOI":"10.1093\/pcp\/pcw052","article-title":"Plant Nitrogen Acquisition Under Low Availability: Regulation of Uptake and Root Architecture","volume":"57","author":"Kiba","year":"2016","journal-title":"Plant Cell Physiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"814","DOI":"10.1111\/nph.15812","article-title":"Nitrate acts at the Arabidopsis thaliana shoot apical meristem to regulate flowering time","volume":"223","author":"Olas","year":"2019","journal-title":"New Phytol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1016\/j.pbi.2018.10.004","article-title":"Nitrate signaling and the control of Arabidopsis growth and development","volume":"47","author":"Fredes","year":"2019","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1007\/s00425-020-03376-4","article-title":"The physiological mechanism underlying root elongation in response to nitrogen deficiency in crop plants","volume":"251","author":"Sun","year":"2020","journal-title":"Planta"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1136","DOI":"10.1038\/s41477-020-00756-2","article-title":"Auxin-mediated root branching is determined by the form of available nitrogen","volume":"6","author":"Meier","year":"2020","journal-title":"Nat. Plants"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1080\/01904167.2018.1554074","article-title":"Natural variation of Arabidopsis thaliana root architecture in response to nitrate availability","volume":"42","author":"Li","year":"2019","journal-title":"J. Plant Nutr."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1038\/s41586-018-0656-3","article-title":"Transcriptional regulation of nitrogen-associated metabolism and growth","volume":"563","author":"Gaudinier","year":"2018","journal-title":"Nature"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1569","DOI":"10.1038\/s41467-019-09522-1","article-title":"Network Walking charts transcriptional dynamics of nitrogen signaling by integrating validated and predicted genome-wide interactions","volume":"10","author":"Brooks","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1003","DOI":"10.1093\/pcp\/pcs050","article-title":"Overexpressing the ANR1 MADS-box gene in transgenic plants provides new insights into its role in the nitrate regulation of root development","volume":"53","author":"Gan","year":"2012","journal-title":"Plant Cell. Physiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"730","DOI":"10.1007\/s00425-005-0020-3","article-title":"Nutritional regulation of ANR1 and other root-expressed MADS-box genes in Arabidopsis thaliana","volume":"222","author":"Gan","year":"2005","journal-title":"Planta"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"2419","DOI":"10.1073\/pnas.1615676114","article-title":"Interacting TCP and NLP transcription factors control plant responses to nitrate availability","volume":"114","author":"Guan","year":"2017","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"15267","DOI":"10.1073\/pnas.1411375111","article-title":"Nitrate foraging by Arabidopsis roots is mediated by the transcription factor TCP20 through the systemic signaling pathway","volume":"111","author":"Guan","year":"2014","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1016\/j.bbrc.2015.01.009","article-title":"AtTGA4, a bZIP transcription factor, confers drought resistance by enhancing nitrate transport and assimilation in Arabidopsis thaliana","volume":"457","author":"Zhong","year":"2015","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/tpj.12618","article-title":"Systems approach identifies TGA1 and TGA4 transcription factors as important regulatory components of the nitrate response of Arabidopsis thaliana roots","volume":"80","author":"Alvarez","year":"2014","journal-title":"Plant J."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1111\/tpj.13656","article-title":"Nitrate induction of root hair density is mediated by TGA1\/TGA4 and CPC transcription factors in Arabidopsis thaliana","volume":"92","author":"Canales","year":"2017","journal-title":"Plant J."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1105\/tpc.15.00567","article-title":"The Arabidopsis NRG2 Protein Mediates Nitrate Signaling and Interacts with and Regulates Key Nitrate Regulators","volume":"28","author":"Xu","year":"2016","journal-title":"Plant Cell"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"3567","DOI":"10.1105\/tpc.109.067041","article-title":"Members of the LBD Family of Transcription Factors Repress Anthocyanin Synthesis and Affect Additional Nitrogen Responses in Arabidopsis","volume":"21","author":"Rubin","year":"2009","journal-title":"Plant Cell"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1023\/A:1010329902165","article-title":"The nutritional control of root development","volume":"232","author":"Forde","year":"2001","journal-title":"Plant Soil"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1104\/pp.113.218453","article-title":"Plasticity of the Arabidopsis Root System under Nutrient Deficiencies","volume":"163","author":"Gruber","year":"2013","journal-title":"Plant Physiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"W202","DOI":"10.1093\/nar\/gkp335","article-title":"MEME SUITE: Tools for motif discovery and searching","volume":"37","author":"Bailey","year":"2009","journal-title":"Nucleic Acids Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"485","DOI":"10.3389\/fpls.2017.00485","article-title":"Nitrate: A Crucial Signal during Lateral Roots Development","volume":"8","author":"Sun","year":"2017","journal-title":"Front. Plant Sci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1105\/tpc.111.092221","article-title":"The Arabidopsis Nitrate Transporter NRT2.4 Plays a Double Role in Roots and Shoots of Nitrogen-Straved Plants","volume":"24","author":"Kiba","year":"2012","journal-title":"Plant Cell"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Aoyanagi, T., Ikeya, S., Kobayashi, A., and Kozaki, A. (2020). Gene Regulation via the Combination of Transcription Factors in the INDETERMINATE DOMAIN and GRAS Families. Genes, 11.","DOI":"10.3390\/genes11060613"},{"key":"ref_38","first-page":"739","article-title":"Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis","volume":"4","author":"Levesque","year":"2006","journal-title":"PLoS Biol."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Kumar, M., Le, D.T., Hwang, S., Seo, P.J., and Kim, H.U. (2019). Role of the INDETERMINATE DOMAIN Genes in Plants. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20092286"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1007\/s11240-005-0515-4","article-title":"The effect of salt stress and abscisic acid on proline production, chlorophyll content and growth of in vitro propagated shoots of Eucalyptus camaldulensis","volume":"82","author":"Woodward","year":"2005","journal-title":"Plant Cell Tissue Organ Cult."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1104\/pp.118.1.27","article-title":"Genetic Interactions between Phytochrome A, Phytochrome B, and Cryptochrome 1 during Arabidopsis Development","volume":"118","author":"Neff","year":"1998","journal-title":"Plant Physiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"18506","DOI":"10.1073\/pnas.1108644108","article-title":"Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)-dependent acropetal auxin transport","volume":"108","author":"Sanz","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Yuan, J.S., Reed, A., Chen, F., and Stewart, C.N. (2006). Statistical analysis of real-time PCR data. BMC Bioinform., 7.","DOI":"10.1186\/1471-2105-7-85"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/21\/11413\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:21:16Z","timestamp":1760167276000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/21\/11413"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,10,22]]},"references-count":43,"journal-issue":{"issue":"21","published-online":{"date-parts":[[2021,11]]}},"alternative-id":["ijms222111413"],"URL":"https:\/\/doi.org\/10.3390\/ijms222111413","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,10,22]]}}}