{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T07:01:13Z","timestamp":1790146873202,"version":"4.0.1"},"reference-count":45,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T00:00:00Z","timestamp":1790121600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Plant Sci."],"abstract":"\n Introduction<\/jats:title>\n \n The\n SnRK<\/jats:italic>\n (Sucrose Non-fermenting 1-Related Protein Kinase) gene family plays critical roles in plant stress responses and growth regulation.\n <\/jats:p>\n <\/jats:sec>\n \n Methods<\/jats:title>\n \n In this study, we performed a genome-wide identification of\n SnRK<\/jats:italic>\n genes across 49 plant species and and focused on functional characterization of key members in the halophyte\n Spartina alterniflora<\/jats:italic>\n .\n <\/jats:p>\n <\/jats:sec>\n \n Results<\/jats:title>\n \n A total of 1192\n SnRK<\/jats:italic>\n genes were identified across the 49 species, showing a progressive increase from algae to angiosperms. In\n S. alterniflora<\/jats:italic>\n , 55\n SaSnRK<\/jats:italic>\n genes were identified and classified into SaSnRK1 (9), SaSnRK2 (21), and SaSnRK3 (25) subfamilies. These genes are unevenly distributed across 22 chromosomes and exhibit distinct gene structures and conserved motifs. Synteny analysis revealed that segmental duplication events have predominantly driven the expansion of the\n SaSnRK<\/jats:italic>\n family. Codon usage analysis suggested that SaSnRK2 subfamily members are under stronger selective constraints and may represent highly expressed genes. Promoter\n cis<\/jats:italic>\n -element analysis indicated an enrichment of stress- and hormone-related regulatory motifs. Expression profiling under increasing salt concentrations revealed divergent response patterns among SaSnRK2 subfamily genes, including both constitutively upregulated and high-salinity-specific isoforms. Functional characterization of a salt-inducible\n SaSnRK2<\/jats:italic>\n gene,\n SaSnRK2.9<\/jats:italic>\n , demonstrated that it physically interacts with two SaPP2C proteins and, when overexpressed in\n Arabidopsis<\/jats:italic>\n , not only promotes earlier flowering by 4\u20136 days but also significantly enhances salt tolerance, with transgenic lines achieving a survival rate exceeding 50% following salt stress and recovery, compared to less than 20% in wild-type plants.\n <\/jats:p>\n <\/jats:sec>\n \n Discussion<\/jats:title>\n \n These findings, obtained primarily through heterologous overexpression in\n Arabidopsis<\/jats:italic>\n , provide mechanistic insights into how a halophytic SnRK2 kinase balances stress tolerance and developmental regulation. While direct\n in vivo<\/jats:italic>\n evidence in\n S. alterniflora<\/jats:italic>\n is still required, our results highlight\n SaSnRK2.9<\/jats:italic>\n as a promising candidate gene for improving salt tolerance and agronomic traits in crops.\n <\/jats:p>\n <\/jats:sec>","DOI":"10.3389\/fpls.2026.1957301","type":"journal-article","created":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T06:16:08Z","timestamp":1790144168000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":0,"title":["Evolutionary expansion of the SnRK gene family in the halophyte Spartina alterniflora and functional characterization of salt-tolerant SaSnRK2.9"],"prefix":"10.3389","volume":"17","author":[{"given":"Chenxi","family":"Wei","sequence":"first","affiliation":[{"name":"Key Laboratory of Plant Molecular & Developmental Biology, College of Life Sciences, Yantai University","place":["Yantai, Shandong, China"]},{"name":"State Key Laboratory of Crop Gene Resources and Breeding, National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences","place":["Beijing, China"]},{"name":"National Nanfan Research Institute, Chinese Academy of Agricultural Sciences (CAAS)","place":["Sanya, Hainan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shoukun","family":"Chen","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Crop Gene Resources and Breeding, National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences","place":["Beijing, China"]},{"name":"National Nanfan Research Institute, Chinese Academy of Agricultural Sciences (CAAS)","place":["Sanya, Hainan, China"]},{"name":"Guangxi Key Laboratory of Rice Genetics and Breeding, Rice Research Institute, Guangxi Academy of Agricultural Sciences","place":["Nanning, Guangxi, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qin","family":"Shu","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Crop Gene Resources and Breeding, National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences","place":["Beijing, China"]},{"name":"National Nanfan Research Institute, Chinese Academy of Agricultural Sciences (CAAS)","place":["Sanya, Hainan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiahui","family":"Geng","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Crop Gene Resources and Breeding, National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences","place":["Beijing, China"]},{"name":"National Nanfan Research Institute, Chinese Academy of Agricultural Sciences (CAAS)","place":["Sanya, Hainan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shihua","family":"Chen","sequence":"additional","affiliation":[{"name":"Key Laboratory of Plant Molecular & Developmental Biology, College of Life Sciences, Yantai University","place":["Yantai, Shandong, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lei","family":"Chen","sequence":"additional","affiliation":[{"name":"Key Laboratory of Plant Molecular & Developmental Biology, College of Life Sciences, Yantai University","place":["Yantai, Shandong, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huihui","family":"Li","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Crop Gene Resources and Breeding, National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences","place":["Beijing, China"]},{"name":"National Nanfan Research Institute, Chinese Academy of Agricultural Sciences (CAAS)","place":["Sanya, Hainan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2026,9,23]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"572","DOI":"10.21203\/rs.3.rs-1772837\/v1","article-title":"Comprehensive identification and expression analyses of the SnRK gene family in Casuarina equisetifolia in response to salt stress","volume":"22","author":"Ai","year":"2022","journal-title":"BMC Plant Biol."},{"key":"B2","doi-asserted-by":"publisher","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":"B3","doi-asserted-by":"publisher","DOI":"10.1126\/sciadv.adn0895","article-title":"Molecular mechanism of trehalose 6-phosphate inhibition of the plant metabolic sensor kinase SnRK1","volume":"10","author":"Blanford","year":"2024","journal-title":"Sci. Adv."},{"key":"B4","doi-asserted-by":"publisher","first-page":"1071","DOI":"10.1038\/s41558-024-02113-z","article-title":"Climate change will exacerbate land conflict between agriculture and timber production","volume":"14","author":"Bousfield","year":"2024","journal-title":"Nat. Clim. Change"},{"key":"B5","doi-asserted-by":"publisher","first-page":"1194","DOI":"10.1016\/j.molp.2020.06.009","article-title":"TBtools: An integrative toolkit developed for interactive analyses of big biological data","volume":"13","author":"Chen","year":"2020","journal-title":"Mol. Plant"},{"key":"B6","doi-asserted-by":"publisher","first-page":"2558","DOI":"10.1111\/pbi.14368","article-title":"The Spartina alterniflora genome sequence provides insights into the salt-tolerance mechanisms of exo-recretohalophytes","volume":"22","author":"Chen","year":"2024","journal-title":"Plant Biotechnol. J."},{"key":"B7","doi-asserted-by":"publisher","DOI":"10.1002\/advs.202417560","article-title":"Unveiling salt tolerance mechanisms in plants: integrating the KANMB machine learning model with metabolomic and transcriptomic analysis","volume":"12","author":"Chen","year":"2025","journal-title":"Adv. Sci. (Weinh)"},{"key":"B8","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1111\/jipb.13061","article-title":"Protein kinases in plant responses to drought, salt, and cold stress","volume":"63","author":"Chen","year":"2021","journal-title":"J. Integr. Plant Biol."},{"key":"B9","doi-asserted-by":"publisher","DOI":"10.3390\/ijms23073560","article-title":"Protein kinases: function, substrates, and implication in diseases","volume":"23","author":"Cipak","year":"2022","journal-title":"Int. J. Mol. Sci."},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-313x.1998.00343.x","article-title":"Floral dip: a simplified method for Agrobacterium -mediated transformation of Arabidopsis thaliana","volume":"16","author":"Clough","year":"1998","journal-title":"Plant J"},{"key":"B11","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2022.1087839","article-title":"Genome-wide identification of sucrose non-fermenting-1-related protein kinase genes in maize and their responses to abiotic stresses","volume":"13","author":"Feng","year":"2022","journal-title":"Front. Plant Sci."},{"key":"B12","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2018.02003","article-title":"TaSnRK2.9, a sucrose non-fermenting 1-related protein kinase gene, positively regulates plant response to drought and salt stress in transgenic tobacco","volume":"9","author":"Feng","year":"2018","journal-title":"Front. Plant Sci."},{"key":"B13","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1007\/s42994-023-00125-5","article-title":"Mining salt stress-related genes in Spartina alterniflora via analyzing co-evolution signal across 365 plant species using phylogenetic profiling","volume":"4","author":"Gao","year":"2023","journal-title":"aBIOTECH"},{"key":"B14","doi-asserted-by":"publisher","first-page":"D1178","DOI":"10.1093\/nar\/gkr944","article-title":"Phytozome: a comparative platform for green plant genomics","volume":"40","author":"Goodstein","year":"2012","journal-title":"Nucleic Acids Res."},{"key":"B15","doi-asserted-by":"publisher","DOI":"10.1080\/15592324.2022.2071024","article-title":"ABA activated SnRK2 kinases: an emerging role in plant growth and physiology","volume":"17","author":"Hasan","year":"2022","journal-title":"Plant Signal. Behav."},{"key":"B16","doi-asserted-by":"publisher","first-page":"4634","DOI":"10.1093\/jxb\/erab182","article-title":"The role of amino acid metabolism in signaling and metabolic adaptation to stress-induced energy deficiency in plants","volume":"72","author":"Heinemann","year":"2021","journal-title":"J. Exp. Bot."},{"key":"B17","doi-asserted-by":"publisher","first-page":"666","DOI":"10.1104\/pp.102.011999","article-title":"The Arabidopsis CDPK-SnRK superfamily of protein kinases","volume":"132","author":"Hrabak","year":"2003","journal-title":"Plant Physiol."},{"key":"B18","doi-asserted-by":"publisher","first-page":"2917","DOI":"10.1093\/jxb\/erae046","article-title":"AMPK activator 991 specifically activates SnRK1 and thereby affects seed germination in rice","volume":"75","author":"Hu","year":"2024","journal-title":"J. Exp. Bot."},{"key":"B19","doi-asserted-by":"publisher","first-page":"2239","DOI":"10.1093\/jxb\/erz107","article-title":"Evolution of TOR-SnRK dynamics in green plants and its integration with phytohormone signaling networks","volume":"70","author":"Jamsheer","year":"2019","journal-title":"J. Exp. Bot."},{"key":"B20","doi-asserted-by":"publisher","first-page":"1592211","DOI":"10.1186\/s12870-017-1038-y","article-title":"Characterization and expression analysis of transcription factors in Spartina alterniflora unveil their critical roles in salt stress resistance","volume":"16","author":"Jiang","year":"2025","journal-title":"Front. Plant Sci."},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2022.934226","article-title":"Mining the roles of wheat (Triticum aestivum) SnRK genes in biotic and abiotic responses","volume":"13","author":"Jiang","year":"2022","journal-title":"Front. Plant Sci."},{"key":"B22","doi-asserted-by":"publisher","first-page":"W78","DOI":"10.1093\/nar\/gkae268","article-title":"Interactive Tree of Life (iTOL) v6: recent updates to the phylogenetic tree display and annotation tool","volume":"52","author":"Letunic","year":"2024","journal-title":"Nucleic Acids Res."},{"key":"B23","doi-asserted-by":"publisher","first-page":"1423","DOI":"10.1016\/j.devcel.2024.12.036","article-title":"Calcium-dependent protein kinases CPK3\/4\/6\/11 and 27 respond to osmotic stress and activate SnRK2s in Arabidopsis","volume":"60","author":"Li","year":"2025","journal-title":"Dev. Cell"},{"key":"B24","doi-asserted-by":"publisher","first-page":"2823","DOI":"10.1105\/tpc.20.00352","article-title":"A SnRK1-ZmRFWD3-Opaque2 signaling axis regulates diurnal nitrogen accumulation in maize seeds","volume":"32","author":"Li","year":"2020","journal-title":"Plant Cell"},{"key":"B25","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2316011120","article-title":"TORC pathway intersects with a calcium sensor kinase network to regulate potassium sensing in Arabidopsis","volume":"120","author":"Li","year":"2023","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B26","doi-asserted-by":"publisher","DOI":"10.3390\/plants13070994","article-title":"Genome-wide identification and expression analysis of sucrose nonfermenting 1-related protein kinase (SnRK) genes in Salvia miltiorrhiza in response to hormone","volume":"13","author":"Liu","year":"2024","journal-title":"Plants (Basel)"},{"key":"B27","doi-asserted-by":"publisher","first-page":"1179","DOI":"10.1016\/j.tplants.2020.09.003","article-title":"Plant osmotic stress signaling: MAPKKKs meet SnRK2s","volume":"25","author":"Lozano-Juste","year":"2020","journal-title":"Trends Plant Sci."},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.1111\/ppl.14543","article-title":"The multifaceted role of different SnRK gene family members in regulating multiple abiotic stresses in plants","volume":"176","author":"Mondal","year":"2024","journal-title":"Physiol. Plant"},{"key":"B29","doi-asserted-by":"publisher","first-page":"959","DOI":"10.1007\/s00299-013-1418-1","article-title":"ABA signaling in stress-response and seed development","volume":"32","author":"Nakashima","year":"2013","journal-title":"Plant Cell Rep."},{"key":"B30","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2023.1285485","article-title":"The rice SnRK family: biological roles and cell signaling modules","volume":"14","author":"Son","year":"2023","journal-title":"Front. Plant Sci."},{"key":"B31","doi-asserted-by":"publisher","first-page":"3022","DOI":"10.1093\/molbev\/msab120","article-title":"MEGA11: molecular evolutionary genetics analysis version 11","volume":"38","author":"Tamura","year":"2021","journal-title":"Mol. Biol. Evol."},{"key":"B32","doi-asserted-by":"publisher","DOI":"10.1016\/j.stress.2024.100652","article-title":"Integrative mechanisms of plant salt tolerance: Biological pathways, phytohormonal regulation, and technological innovations","volume":"14","author":"Waheed","year":"2024","journal-title":"Plant Stress"},{"key":"B33","doi-asserted-by":"publisher","DOI":"10.7717\/peerj.14463","article-title":"Genome-wide identification and expression pattern of SnRK gene family under several hormone treatments and its role in floral scent emission in Hedychium coronarium","volume":"9","author":"Wang","year":"2021","journal-title":"PeerJ"},{"key":"B34","doi-asserted-by":"publisher","first-page":"1784","DOI":"10.1016\/j.modpat.2023.100354","article-title":"Comprehensive genomic analysis of SnRK in Rosaceae and expression analysis of RoSnRK2 in response to abiotic stress in Rubus occidentalis","volume":"12","author":"Wang","year":"2023","journal-title":"Plants (Basel)"},{"key":"B35","doi-asserted-by":"publisher","first-page":"1094","DOI":"10.1038\/s41477-022-01236-5","article-title":"Regulatory functions of cellular energy sensor SnRK1 for nitrate signalling through NLP7 repression","volume":"8","author":"Wang","year":"2022","journal-title":"Nat. Plants"},{"key":"B36","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkr1293","article-title":"MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity","volume":"40","author":"Wang","year":"2012","journal-title":"Nucleic Acids Res."},{"key":"B37","doi-asserted-by":"publisher","first-page":"531","DOI":"10.1385\/1-59259-584-7:531","article-title":"Protein identification and analysis tools in the ExPASy server","volume":"112","author":"Wilkins","year":"1999","journal-title":"Methods Mol. Biol."},{"key":"B38","doi-asserted-by":"publisher","first-page":"1390461","DOI":"10.5220\/0014348500004918","article-title":"Comprehensive analysis of the Spartina alterniflora WD40 gene family reveals the regulatory role of SaTTG1 in plant development","volume":"15","author":"Yang","year":"2024","journal-title":"Front. Plant Sci."},{"key":"B39","doi-asserted-by":"publisher","first-page":"690","DOI":"10.1111\/tpj.16397","article-title":"Deep learning-enabled discovery and characterization of HKT genes in Spartina alterniflora","volume":"116","author":"Yang","year":"2023","journal-title":"Plant J."},{"key":"B40","doi-asserted-by":"publisher","first-page":"743","DOI":"10.1002\/1873-3468.13350","article-title":"AaPP2C1 negatively regulates the expression of genes involved in artemisinin biosynthesis through dephosphorylating AaAPK1","volume":"593","author":"Zhang","year":"2019","journal-title":"FEBS Lett."},{"key":"B41","doi-asserted-by":"publisher","first-page":"1198","DOI":"10.23860\/diss-1847","article-title":"Functional characterization of TaSnRK2.8 promoter in response to abiotic stresses by deletion analysis in transgenic Arabidopsis","volume":"8","author":"Zhang","year":"2017","journal-title":"Front. Plant Sci."},{"key":"B42","doi-asserted-by":"publisher","first-page":"1109","DOI":"10.1093\/jxb\/erx444","article-title":"ARTEMISININ BIOSYNTHESIS PROMOTING KINASE 1 positively regulates artemisinin biosynthesis through phosphorylating AabZIP1","volume":"69","author":"Zhang","year":"2018","journal-title":"J. Exp. Bot."},{"key":"B43","doi-asserted-by":"publisher","DOI":"10.1016\/j.xinn.2020.100017","article-title":"Mechanisms of plant responses and adaptation to soil salinity","volume":"1","author":"Zhao","year":"2020","journal-title":"Innovation"},{"key":"B44","doi-asserted-by":"publisher","DOI":"10.1016\/j.plantsci.2019.110373","article-title":"Rice SnRK protein kinase OsSAPK8 acts as a positive regulator in abiotic stress responses","volume":"292","author":"Zhong","year":"2020","journal-title":"Plant Sci."},{"key":"B45","doi-asserted-by":"publisher","DOI":"10.1186\/s12870-020-02484-3","article-title":"Genome-wide identification and characterization of SnRK family genes in Brassica napus","volume":"20","author":"Zhu","year":"2020","journal-title":"BMC Plant Biol."}],"container-title":["Frontiers in Plant Science"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2026.1957301\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T06:16:09Z","timestamp":1790144169000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2026.1957301\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,23]]},"references-count":45,"alternative-id":["10.3389\/fpls.2026.1957301"],"URL":"https:\/\/doi.org\/10.3389\/fpls.2026.1957301","relation":{},"ISSN":["1664-462X"],"issn-type":[{"value":"1664-462X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,23]]},"article-number":"1957301"}}