{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,24]],"date-time":"2026-08-24T17:15:05Z","timestamp":1787591705475,"version":"build-2736575974"},"reference-count":56,"publisher":"Oxford University Press (OUP)","issue":"4","license":[{"start":{"date-parts":[[2023,5,22]],"date-time":"2023-05-22T00:00:00Z","timestamp":1684713600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"funder":[{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["2022YFD1602000"],"award-info":[{"award-number":["2022YFD1602000"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32202519"],"award-info":[{"award-number":["32202519"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["U22A20498"],"award-info":[{"award-number":["U22A20498"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32072596"],"award-info":[{"award-number":["32072596"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Science and Technology Innovation Team of Shaanxi","award":["2021TD-32"],"award-info":[{"award-number":["2021TD-32"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2023,8,3]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Light signals promote photomorphogenesis and photosynthesis, allowing plants to establish photoautotrophic growth. Chloroplasts are organelles responsible for photosynthesis in which light energy is converted into chemical energy and stored as organic matter. However, how light regulates chloroplast photomorphogenesis remains unclear. Here, we isolated a cucumber (Cucumis sativus L.) mutant albino seedling (as) from an ethyl methane sulfonate mutagenesis library with an albino phenotype. Map-based cloning revealed that the mutation occurred in a component of cucumber translocon at the inner membrane of chloroplasts (CsTIC21). Subsequently, virus-induced gene silencing and CRISPR\/Cas9 analyses confirmed the association between the mutant gene and the as phenotype. Loss-of-function of CsTIC21 induces malformation of chloroplast formation, leading to albinism and death in cucumber. Notably, CsTIC21 transcription was very low in etiolated seedlings grown in the dark and was upregulated by light, with expression patterns similar to those of Nuclear factor-YC (NF-YC) genes. Here, 7 cucumber NF-YC family genes (CsNF-YC) were identified, among which the expression of 4 genes (CsNF-YC1, -YC2, -YC9, and -YC13) responded to light. Gene silencing of all CsNF-YC genes in cucumber indicated that CsNF-YC2, -YC9, -YC11-1, and -YC11-2 induced distinct etiolated growth and decreased chlorophyll content. Interaction studies verified that CsNF-YC2 and CsNF-YC9 target the CsTIC21 promoter directly and promote gene transcription. These findings provide mechanistic insights on the role of the NF-YCs\u2013TIC21 module in chloroplast photomorphogenesis promoted by light in cucumber.<\/jats:p>","DOI":"10.1093\/plphys\/kiad296","type":"journal-article","created":{"date-parts":[[2023,5,22]],"date-time":"2023-05-22T18:08:46Z","timestamp":1684778926000},"page":"2822-2837","source":"Crossref","is-referenced-by-count":25,"title":["Cucumber NUCLEAR FACTOR-YC2\/-YC9 target translocon component\n                    <i>CsTIC21<\/i>\n                    in chloroplast photomorphogenesis"],"prefix":"10.1093","volume":"192","author":[{"ORCID":"https:\/\/orcid.org\/0009-0004-4740-4472","authenticated-orcid":false,"given":"Xubo","family":"Ke","sequence":"first","affiliation":[{"name":"College of Horticulture, Northwest A&F University , Yangling 712100, Shaanxi , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8321-1521","authenticated-orcid":false,"given":"Junjun","family":"Shen","sequence":"additional","affiliation":[{"name":"College of Horticulture, Northwest A&F University , Yangling 712100, Shaanxi , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2604-8622","authenticated-orcid":false,"given":"Yuqian","family":"Niu","sequence":"additional","affiliation":[{"name":"College of Horticulture, Northwest A&F University , Yangling 712100, Shaanxi , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0003-1129-4163","authenticated-orcid":false,"given":"Hongjiao","family":"Zhao","sequence":"additional","affiliation":[{"name":"College of Horticulture, Northwest A&F University , Yangling 712100, Shaanxi , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0004-1450-6843","authenticated-orcid":false,"given":"Yalu","family":"Guo","sequence":"additional","affiliation":[{"name":"College of Horticulture, Northwest A&F University , Yangling 712100, Shaanxi , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Piaoyun","family":"Sun","sequence":"additional","affiliation":[{"name":"College of Horticulture, Northwest A&F University , Yangling 712100, Shaanxi , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0004-2559-8130","authenticated-orcid":false,"given":"Tongwen","family":"Yang","sequence":"additional","affiliation":[{"name":"College of Horticulture, Northwest A&F University , Yangling 712100, Shaanxi , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0009-6539-2846","authenticated-orcid":false,"given":"Yanxin","family":"Jiang","sequence":"additional","affiliation":[{"name":"College of Horticulture, Northwest A&F University , Yangling 712100, Shaanxi , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0004-9502-8651","authenticated-orcid":false,"given":"Bosi","family":"Zhao","sequence":"additional","affiliation":[{"name":"College of Horticulture, Northwest A&F University , Yangling 712100, Shaanxi , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0003-6381-2831","authenticated-orcid":false,"given":"Zheng","family":"Wang","sequence":"additional","affiliation":[{"name":"College of Horticulture, Northwest A&F University , Yangling 712100, Shaanxi , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5595-8644","authenticated-orcid":false,"given":"Tao","family":"Wu","sequence":"additional","affiliation":[{"name":"College of Horticulture, Hunan Agricultural University , Changsha 410000 , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7327-282X","authenticated-orcid":false,"given":"Huasen","family":"Wang","sequence":"additional","affiliation":[{"name":"Engineering Laboratory of Genetic Improvement of Horticultural Crops of Shandong Province, College of Horticulture, Qingdao Agricultural University , Qingdao 266109 , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3188-8300","authenticated-orcid":false,"given":"Zheng","family":"Li","sequence":"additional","affiliation":[{"name":"College of Horticulture, Northwest A&F University , Yangling 712100, Shaanxi , China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2023,5,22]]},"reference":[{"issue":"2","key":"2023080319580167500_kiad296-B1","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1038\/nbt.2095","article-title":"Genome sequencing reveals agronomically important loci in rice using MutMap","volume":"30","author":"Abe","year":"2012","journal-title":"Nat Biotechnol"},{"issue":"419","key":"2023080319580167500_kiad296-B2","doi-asserted-by":"crossref","first-page":"2287","DOI":"10.1093\/jxb\/eri243","article-title":"Recognition and envelope translocation of chloroplast preproteins","volume":"56","author":"B\u00e9dard","year":"2005","journal-title":"J Exp Bot"},{"issue":"5","key":"2023080319580167500_kiad296-B3","doi-asserted-by":"crossref","first-page":"2000","DOI":"10.1111\/nph.17839","article-title":"Chloroplast development in green plant tissues: the interplay between light, hormone, and transcriptional regulation","volume":"233","author":"Cackett","year":"2021","journal-title":"New Phytol"},{"issue":"1","key":"2023080319580167500_kiad296-B4","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1186\/1471-2164-11-569","article-title":"Genome-wide characterization of simple sequence repeats in cucumber (Cucumis sativus L)","volume":"11","author":"Cavagnaro","year":"2010","journal-title":"BMC Genomics"},{"issue":"7734","key":"2023080319580167500_kiad296-B5","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1038\/s41586-018-0713-y","article-title":"TIC236 links the outer and inner membrane translocons of the chloroplast","volume":"564","author":"Chen","year":"2018","journal-title":"Nature"},{"issue":"1","key":"2023080319580167500_kiad296-B6","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1146\/annurev-arplant-043015-112252","article-title":"Light-mediated hormonal regulation of plant growth and development","volume":"67","author":"de Wit","year":"2016","journal-title":"Annu Rev Plant Biol"},{"issue":"9","key":"2023080319580167500_kiad296-B7","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pgen.1005479","article-title":"HANABA TARANU (HAN) bridges meristem and organ primordia boundaries through PINHEAD, JAGGED, BLADE-ON-PETIOLE2 and CYTOKININ OXIDASE 3 during flower development in Arabidopsis","volume":"11","author":"Ding","year":"2015","journal-title":"PLoS Genet"},{"key":"2023080319580167500_kiad296-B8","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1093\/plphys\/kiac050","article-title":"Transcriptomic and functional analysis provides molecular insights into multicellular trichome development","volume":"189","author":"Dong","year":"2022","journal-title":"Plant Physiol"},{"issue":"3","key":"2023080319580167500_kiad296-B9","doi-asserted-by":"crossref","first-page":"986","DOI":"10.1105\/tpc.106.047407","article-title":"PIC1, an ancient permease in Arabidopsis chloroplasts, mediates iron transport","volume":"19","author":"Duy","year":"2007","journal-title":"Plant Cell"},{"issue":"5668","key":"2023080319580167500_kiad296-B10","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1126\/science.1094884","article-title":"Ancient invasions: from endosymbionts to organelles","volume":"304","author":"Dyall","year":"2004","journal-title":"Science"},{"key":"2023080319580167500_kiad296-B11","doi-asserted-by":"crossref","first-page":"907","DOI":"10.3389\/fpls.2016.00907","article-title":"Overexpression of SlRBZ results in chlorosis and dwarfism through impairing chlorophyll, carotenoid, and gibberellin biosynthesis in tomato","volume":"7","author":"Fan","year":"2016","journal-title":"Front Plant Sci"},{"issue":"2","key":"2023080319580167500_kiad296-B12","doi-asserted-by":"crossref","first-page":"853","DOI":"10.1093\/plphys\/kiab146","article-title":"A tobacco ringspot virus-based vector system for gene and microRNA function studies in 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Arabidopsis","volume":"5","author":"Hou","year":"2014","journal-title":"Nat Commun"},{"issue":"4","key":"2023080319580167500_kiad296-B19","doi-asserted-by":"crossref","first-page":"1567","DOI":"10.1104\/pp.125.4.1567","article-title":"Arabidopsis genes encoding components of the chloroplastic protein import apparatus","volume":"125","author":"Jackson-Constan","year":"2001","journal-title":"Plant Physiol"},{"issue":"26","key":"2023080319580167500_kiad296-B20","first-page":"16583","article-title":"The hydrophilic domain of Tic110, an inner envelope membrane component of the chloroplastic protein translocation apparatus, faces the stromal compartment","volume":"273","author":"Jackson","year":"1998","journal-title":"J Cell Biol"},{"issue":"25","key":"2023080319580167500_kiad296-B21","doi-asserted-by":"crossref","first-page":"4788","DOI":"10.1016\/j.cell.2022.10.030","article-title":"Structure of a TOC-TIC supercomplex spanning two chloroplast envelope 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membrane","volume":"21","author":"Kikuchi","year":"2009","journal-title":"Plant Cell"},{"issue":"3","key":"2023080319580167500_kiad296-B25","doi-asserted-by":"crossref","first-page":"972","DOI":"10.1104\/pp.114.255562","article-title":"Characterization of chloroplast protein import without Tic56, a component of the 1-megadalton translocon at the inner envelope membrane of chloroplasts","volume":"167","author":"K\u00f6hler","year":"2015","journal-title":"Plant Physiol"},{"issue":"13","key":"2023080319580167500_kiad296-B26","doi-asserted-by":"crossref","first-page":"3501","DOI":"10.1093\/nar\/gkg502","article-title":"CLOURE: Clustal Output Reformatter, a program for reformatting ClustalX\/ClustalW outputs for SNP analysis and molecular systematics","volume":"31","author":"Kohli","year":"2003","journal-title":"Nucleic Acids Res"},{"issue":"4","key":"2023080319580167500_kiad296-B27","doi-asserted-by":"crossref","first-page":"991","DOI":"10.1083\/jcb.143.4.991","article-title":"Tic20 and 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