{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,12]],"date-time":"2026-09-12T02:16:12Z","timestamp":1789179372213,"version":"build-2803163510"},"reference-count":115,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2024,5,7]],"date-time":"2024-05-07T00:00:00Z","timestamp":1715040000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Modern Agriculture Project of Jiangsu Province","award":["BE2021307"],"award-info":[{"award-number":["BE2021307"]}]},{"name":"Modern Agriculture Project of Jiangsu Province","award":["202306003"],"award-info":[{"award-number":["202306003"]}]},{"name":"Modern Agriculture Project of Jiangsu Province","award":["2023-SJ-009"],"award-info":[{"award-number":["2023-SJ-009"]}]},{"name":"Modern Agriculture Project of Jiangsu Province","award":["LYKJ[2021]07"],"award-info":[{"award-number":["LYKJ[2021]07"]}]},{"name":"Science and Technology Development Plan Project of Nanjing City","award":["BE2021307"],"award-info":[{"award-number":["BE2021307"]}]},{"name":"Science and Technology Development Plan Project of Nanjing City","award":["202306003"],"award-info":[{"award-number":["202306003"]}]},{"name":"Science and Technology Development Plan Project of Nanjing City","award":["2023-SJ-009"],"award-info":[{"award-number":["2023-SJ-009"]}]},{"name":"Science and Technology Development Plan Project of Nanjing City","award":["LYKJ[2021]07"],"award-info":[{"award-number":["LYKJ[2021]07"]}]},{"name":"Jiangsu Provincial Innovation and Extension Project of Agricultural Science and Technology","award":["BE2021307"],"award-info":[{"award-number":["BE2021307"]}]},{"name":"Jiangsu Provincial Innovation and Extension Project of Agricultural Science and Technology","award":["202306003"],"award-info":[{"award-number":["202306003"]}]},{"name":"Jiangsu Provincial Innovation and Extension Project of Agricultural Science and Technology","award":["2023-SJ-009"],"award-info":[{"award-number":["2023-SJ-009"]}]},{"name":"Jiangsu Provincial Innovation and Extension Project of Agricultural Science and Technology","award":["LYKJ[2021]07"],"award-info":[{"award-number":["LYKJ[2021]07"]}]},{"name":"Jiangsu Provincial Innovation and Extension Project of Forestry Science and Technology","award":["BE2021307"],"award-info":[{"award-number":["BE2021307"]}]},{"name":"Jiangsu Provincial Innovation and Extension Project of Forestry Science and Technology","award":["202306003"],"award-info":[{"award-number":["202306003"]}]},{"name":"Jiangsu Provincial Innovation and Extension Project of Forestry Science and Technology","award":["2023-SJ-009"],"award-info":[{"award-number":["2023-SJ-009"]}]},{"name":"Jiangsu Provincial Innovation and Extension Project of Forestry Science and Technology","award":["LYKJ[2021]07"],"award-info":[{"award-number":["LYKJ[2021]07"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Plants"],"abstract":"<jats:p>Ilex \u00d7 attenuata \u2018Sunny Foster\u2019 represents a yellow leaf mutant originating from I. \u00d7 attenuata \u2018Foster#2\u2019, a popular ornamental woody cultivar. However, the molecular mechanisms underlying this leaf color mutation remain unclear. Using a comprehensive approach encompassing cytological, physiological, and transcriptomic methodologies, notable distinctions were discerned between the mutant specimen and its wild type. The mutant phenotype displayed aberrant chloroplast morphology, diminished chlorophyll content, heightened carotenoid\/chlorophyll ratios, and a decelerated rate of plant development. Transcriptome analysis identified differentially expressed genes (DEGs) related to chlorophyll metabolism, carotenoid biosynthesis and photosynthesis. The up-regulation of CHLD and CHLI subunits leads to decreased magnesium chelatase activity, while the up-regulation of COX10 increases heme biosynthesis\u2014both impair chlorophyll synthesis. Conversely, the down-regulation of HEMD hindered chlorophyll synthesis, and the up-regulation of SGR enhanced chlorophyll degradation, resulting in reduced chlorophyll content. Additionally, genes linked to carotenoid biosynthesis, flavonoid metabolism, and photosynthesis were significantly down-regulated. We also identified 311 putative differentially expressed transcription factors, including bHLHs and GLKs. These findings shed light on the molecular mechanisms underlying leaf color mutation in I. \u00d7 attenuata \u2018Sunny Foster\u2019 and provide a substantial gene reservoir for enhancing leaf color through breeding techniques.<\/jats:p>","DOI":"10.3390\/plants13101284","type":"journal-article","created":{"date-parts":[[2024,5,7]],"date-time":"2024-05-07T09:03:38Z","timestamp":1715072618000},"page":"1284","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["Molecular Mechanisms of Chlorophyll Deficiency in Ilex \u00d7 attenuata \u2018Sunny Foster\u2019 Mutant"],"prefix":"10.3390","volume":"13","author":[{"given":"Yiping","family":"Zou","sequence":"first","affiliation":[{"name":"College of Forestry, Nanjing Forestry University, Nanjing 210037, China"},{"name":"Institute of Botany, Jiangsu Province and Chinese Academy of Sciences (Nanjing Botanical Garden Mem. Sun Yat-Sen), Nanjing 210014, China"},{"name":"Jiangsu Qinghao Landscape Horticulture Co., Ltd., Nanjing 211225, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yajian","family":"Huang","sequence":"additional","affiliation":[{"name":"College of Forestry, Nanjing Forestry University, Nanjing 210037, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Donglin","family":"Zhang","sequence":"additional","affiliation":[{"name":"Department of Horticulture, University of Georgia, Athens, GA 30602, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7376-172X","authenticated-orcid":false,"given":"Hong","family":"Chen","sequence":"additional","affiliation":[{"name":"Institute of Botany, Jiangsu Province and Chinese Academy of Sciences (Nanjing Botanical Garden Mem. Sun Yat-Sen), Nanjing 210014, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Youwang","family":"Liang","sequence":"additional","affiliation":[{"name":"College of Forestry, Nanjing Forestry University, Nanjing 210037, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mingzhuo","family":"Hao","sequence":"additional","affiliation":[{"name":"College of Forestry, Nanjing Forestry University, Nanjing 210037, China"},{"name":"Jiangsu Qinghao Landscape Horticulture Co., Ltd., Nanjing 211225, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yunlong","family":"Yin","sequence":"additional","affiliation":[{"name":"College of Forestry, Nanjing Forestry University, Nanjing 210037, China"},{"name":"Institute of Botany, Jiangsu Province and Chinese Academy of Sciences (Nanjing Botanical Garden Mem. Sun Yat-Sen), Nanjing 210014, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,5,7]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"3125","DOI":"10.1093\/jxb\/erz128","article-title":"Loss of GLK1 Transcription Factor Function Reveals New Insights in Chlorophyll Biosynthesis and Chloroplast Development","volume":"70","author":"Gang","year":"2019","journal-title":"J. Exp. Bot."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Shim, K.-C., Kang, Y., Song, J.-H., Kim, Y.J., Kim, J.K., Kim, C., Tai, T.H., Park, I., and Ahn, S.-N. (2023). A Frameshift Mutation in the Mg-Chelatase I Subunit Gene OsCHLI Is Associated with a Lethal Chlorophyll-Deficient, Yellow Seedling Phenotype in Rice. Plants, 12.","DOI":"10.3390\/plants12152831"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1427","DOI":"10.1111\/pce.13180","article-title":"Leaf and Canopy Photosynthesis of a Chlorophyll Deficient Soybean Mutant","volume":"41","author":"Sakowska","year":"2018","journal-title":"Plant Cell Environ."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"233","DOI":"10.21273\/JASHS05025-20","article-title":"Photosynthetic Pigments Profiled in Capsicum Lutescens Mutants","volume":"146","author":"McKenzie","year":"2021","journal-title":"J. Am. Soc. Hortic. Sci."},{"key":"ref_5","first-page":"74","article-title":"Uncovering the mechanisms of novel foliar variegation patterns caused by structures and pigments","volume":"65","author":"Pao","year":"2020","journal-title":"Taiwania"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Zhao, M.-H., Li, X., Zhang, X.-X., Zhang, H., and Zhao, X.-Y. (2020). Mutation Mechanism of Leaf Color in Plants: A Review. Forests, 11.","DOI":"10.3390\/f11080851"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"2658","DOI":"10.1016\/j.ygeno.2020.02.019","article-title":"Pigment Variation and Transcriptional Response of the Pigment Synthesis Pathway in the S2309 Triple-Color Ornamental Kale (Brassica oleracea L. var. acephala) Line","volume":"112","author":"Liu","year":"2020","journal-title":"Genomics"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"153669","DOI":"10.1016\/j.jplph.2022.153669","article-title":"Effects of Reduced Chlorophyll Content on Photosystem Functions and Photosynthetic Electron Transport Rate in Rice Leaves","volume":"272","author":"Wang","year":"2022","journal-title":"J. Plant Physiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"111925","DOI":"10.1016\/j.plantsci.2023.111925","article-title":"Disruption of the Rice ALS1 Localized in Chloroplast Causes Seedling-Lethal Albino Phenotype","volume":"338","author":"Xu","year":"2024","journal-title":"Plant Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1007\/s00122-023-04343-9","article-title":"Melon Yellow-Green Plant (Cmygp) Encodes a Golden2-like Transcription Factor Regulating Chlorophyll Synthesis and Chloroplast Development","volume":"136","author":"Yang","year":"2023","journal-title":"Theor. Appl. Genet."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"117388","DOI":"10.1016\/j.indcrop.2023.117388","article-title":"GhFP Positively Regulates Chlorophyll Content and Seedling Biomass in Upland Cotton","volume":"204","author":"Wang","year":"2023","journal-title":"Ind. Crops Prod."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1104\/pp.111.1.1","article-title":"Regulation of Chlorophyll Biosynthesis in Angiosperms","volume":"111","author":"Reinbothe","year":"1996","journal-title":"Plant Physiol."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Wang, Y., Wang, J., Chen, L., Meng, X., Zhen, X., Liang, Y., Han, Y., Li, H., and Zhang, B. (2022). Identification and Function Analysis of Yellow-Leaf Mutant (YX-Yl) of Broomcorn Millet. BMC Plant Biol., 22.","DOI":"10.1186\/s12870-022-03843-y"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Lin, N., Gao, Y., Zhou, Q., Ping, X., Li, J., Liu, L., and Yin, J. (2022). Genetic Mapping and Physiological Analysis of Chlorophyll-Deficient Mutant in Brassica napus L.. BMC Plant Biol., 22.","DOI":"10.1186\/s12870-022-03630-9"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1038\/s41438-018-0015-4","article-title":"Cytological, Physiological, and Transcriptomic Analyses of Golden Leaf Coloration in Ginkgo biloba L.","volume":"5","author":"Li","year":"2018","journal-title":"Hortic. Res."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"968","DOI":"10.1016\/j.bbabio.2015.05.007","article-title":"Regulation and Function of Tetrapyrrole Biosynthesis in Plants and Algae","volume":"1847","author":"Brzezowski","year":"2015","journal-title":"Biochim. Biophys. Acta BBA Bioenerg."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"2487","DOI":"10.1007\/s11033-020-05323-8","article-title":"The Identification of Key Candidate Genes Mediating Yellow Seedling Lethality in a Lilium Regale Mutant","volume":"47","author":"Du","year":"2020","journal-title":"Mol. Biol. Rep."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1007\/s11103-006-9024-z","article-title":"Rice Chlorina-1 and Chlorina-9 Encode ChlD and ChlI Subunits of Mg-Chelatase, a Key Enzyme for Chlorophyll Synthesis and Chloroplast Development","volume":"62","author":"Zhang","year":"2006","journal-title":"Plant Mol. Biol."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Wang, Q., Zhang, H., Wei, L., Guo, R., Liu, X., Zhang, M., Fan, J., Liu, S., Liao, J., and Huang, Y. (2023). Yellow-Green Leaf 19 Encoding a Specific and Conservative Protein for Photosynthetic Organisms Affects Tetrapyrrole Biosynthesis, Photosynthesis, and Reactive Oxygen Species Metabolism in Rice. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms242316762"},{"key":"ref_20","first-page":"100015","article-title":"Research Progresses on Rice Leaf Color Mutants","volume":"1","author":"Li","year":"2022","journal-title":"Crop Des."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1961","DOI":"10.1007\/s00122-016-2752-9","article-title":"The Chlorophyll-Deficient Golden Leaf Mutation in Cucumber Is Due to a Single Nucleotide Substitution in CsChlI for Magnesium Chelatase I Subunit","volume":"129","author":"Gao","year":"2016","journal-title":"Theor. Appl. Genet."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Zhang, Q., Huang, J., Zhou, P., Hao, M., and Zhang, M. (2021). Cytological and Transcriptomic Analysis Provide Insights into the Formation of Variegated Leaves in Ilex \u00d7 Altaclerensis \u2018Belgica Aurea\u2019. Plants, 10.","DOI":"10.3390\/plants10030552"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1047090","DOI":"10.3389\/fpls.2022.1047090","article-title":"Cytological, Genetic and Transcriptomic Characterization of a Cucumber Albino Mutant","volume":"13","author":"Yan","year":"2022","journal-title":"Front. Plant Sci."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"113033","DOI":"10.1016\/j.scienta.2024.113033","article-title":"Molecular Insights into a Non-Lethal Yellow Bud Mutant in Ilex \u00d7 \u2018Nellie R. Stevens\u2019","volume":"329","author":"Zou","year":"2024","journal-title":"Sci. Hortic."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1313","DOI":"10.1105\/tpc.106.049270","article-title":"The Balance between Protein Synthesis and Degradation in Chloroplasts Determines Leaf Variegation in Arabidopsis Yellow Variegated Mutants","volume":"19","author":"Miura","year":"2007","journal-title":"Plant Cell"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"9647","DOI":"10.1038\/s41598-023-36656-6","article-title":"Physiological and Transcriptomic Analysis of a Yellow Leaf Mutant in Watermelon","volume":"13","author":"Xu","year":"2023","journal-title":"Sci. Rep."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Guo, P., Huang, Z., Zhao, W., Lin, N., Wang, Y., and Shang, F. (2023). Mechanisms for Leaf Color Changes in Osmanthus Fragrans \u2018Ziyan Gongzhu\u2019 Using Physiology, Transcriptomics and Metabolomics. BMC Plant Biol., 23.","DOI":"10.1186\/s12870-023-04457-8"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Sun, Y., Bai, P.-P., Gu, K.-J., Yang, S.-Z., Lin, H.-Y., Shi, C.-G., and Zhao, Y.-P. (2022). Dynamic Transcriptome and Network-Based Analysis of Yellow Leaf Mutant Ginkgo biloba. BMC Plant Biol., 22.","DOI":"10.1186\/s12870-022-03854-9"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Han, H., Zhou, Y., Liu, H., Chen, X., Wang, Q., Zhuang, H., Sun, X., Ling, Q., Zhang, H., and Wang, B. (2023). Transcriptomics and Metabolomics Analysis Provides Insight into Leaf Color and Photosynthesis Variation of the Yellow-Green Leaf Mutant of Hami Melon (Cucumis melo L.). Plants, 12.","DOI":"10.3390\/plants12081623"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Wang, F., Chen, N., and Shen, S. (2022). iTRAQ-Based Quantitative Proteomics Analysis Reveals the Mechanism of Golden-Yellow Leaf Mutant in Hybrid Paper Mulberry. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23010127"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"256","DOI":"10.3389\/fpls.2020.00256","article-title":"From Chloroplast Biogenesis to Chlorophyll Accumulation: The Interplay of Light and Hormones on Gene Expression in Camellia Sinensis Cv. Shuchazao Leaves","volume":"11","author":"Liu","year":"2020","journal-title":"Front. Plant Sci."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1111\/j.1399-3054.2012.01604.x","article-title":"Effect of Low Temperature on Chlorophyll Biosynthesis in Albinism Line of Wheat (Triticum aestivum) FA85","volume":"145","author":"Liu","year":"2012","journal-title":"Physiol. Plant."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"103796","DOI":"10.1016\/j.envexpbot.2019.06.009","article-title":"Effects of Light Intensity on Metabolism of Light-Harvesting Pigment and Photosynthetic System in Camellia sinensis L. Cultivar \u2018Huangjinya\u2019","volume":"166","author":"Yangen","year":"2019","journal-title":"Environ. Exp. Bot."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1867","DOI":"10.1104\/pp.113.217604","article-title":"A Rice Virescent-Yellow Leaf Mutant Reveals New Insights into the Role and Assembly of Plastid Caseinolytic Protease in Higher Plants","volume":"162","author":"Dong","year":"2013","journal-title":"Plant Physiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1007\/s10725-020-00633-0","article-title":"Characterization and Fine Mapping of a Leaf Yellowing Mutant in Common Wheat","volume":"92","author":"Zhang","year":"2020","journal-title":"Plant Growth Regul."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Guo, Y., Wang, T., Fu, F.-F., El-Kassaby, Y.A., and Wang, G. (2021). Metabolome and Transcriptome Analyses Reveal the Regulatory Mechanisms of Photosynthesis in Developing Ginkgo biloba Leaves. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22052601"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Dong, X., Huang, L., Chen, Q., Lv, Y., Sun, H., and Liang, Z. (2020). Physiological and Anatomical Differences and Differentially Expressed Genes Reveal Yellow Leaf Coloration in Shumard Oak. Plants, 9.","DOI":"10.3390\/plants9020169"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Zuo, L., Zhang, S., Liu, Y., Huang, Y., Yang, M., and Wang, J. (2019). The Reason for Growth Inhibition of Ulmus pumila \u2018Jinye\u2019: Lower Resistance and Abnormal Development of Chloroplasts Slow Down the Accumulation of Energy. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20174227"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"970023","DOI":"10.3389\/fpls.2022.970023","article-title":"Decoding the Formation of Diverse Petal Colors of Lagerstroemia indica by Integrating the Data from Transcriptome and Metabolome","volume":"13","author":"Hong","year":"2022","journal-title":"Front. Plant Sci."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Zhu, L., Wen, J., Ma, Q., Yan, K., Du, Y., Chen, Z., Lu, X., Ren, J., Wang, Y., and Li, S. (2022). Transcriptome Profiling Provides Insights into Leaf Color Changes in Two Acer palmatum Genotypes. BMC Plant Biol., 22.","DOI":"10.1186\/s12870-022-03979-x"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Yao, X., Zhang, F., and Corlett, R.T. (2022). Utilization of the Hollies (Ilex L. spp.): A Review. Forests, 13.","DOI":"10.3390\/f13010094"},{"key":"ref_42","unstructured":"Bailes, C., and Andrews, S. (2006). Hollies for Gardeners, Timber Press."},{"key":"ref_43","unstructured":"Galle, F.C. (1997). Hollies: The Genus Ilex, Timber Press."},{"key":"ref_44","unstructured":"(2023, December 10). Beyond Galle: A Compilation of Cultivated Ilex Not Included in Fred Galle\u2019s \u201cHollies: The Genus Ilex\u201d. Available online: https:\/\/www.hollysocam.org\/untitled\/memberindex\/PDF\/Beyond-Galle.pdf."},{"key":"ref_45","unstructured":"(2023, December 25). Holly of the Year 2006. Available online: https:\/\/www.hollysocam.org\/holly-year-6.htm."},{"key":"ref_46","unstructured":"(2024, March 02). Application of Ilex Plants in Urban Greening. Available online: https:\/\/www.proquest.com\/openview\/eb1962677c6ccfe6e2efcede33267740\/1?pq-origsite=gscholar&cbl=1596366."},{"key":"ref_47","unstructured":"Veil, J.M. (2015). Ilex at the University of Delaware Botanic Gardens: A Template for Measuring Collection Relevance at Small University Gardens. [Ph.D. Thesis, University of Delaware]."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"724","DOI":"10.32615\/ps.2019.049","article-title":"The Anatomical, Physiological, and Molecular Analysis of a Chlorophyll-Deficient Mutant in Tree Peony (Paeonia suffruticosa)","volume":"57","author":"Chang","year":"2019","journal-title":"Photosynthetica"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"845662","DOI":"10.3389\/fpls.2022.845662","article-title":"Comparative Transcriptome Profiling Analysis Reveals the Adaptive Molecular Mechanism of Yellow-Green Leaf in Rosa Beggeriana \u201cAurea\u201d","volume":"13","author":"Gan","year":"2022","journal-title":"Front. Plant Sci."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1007\/s11099-016-0214-x","article-title":"A Novel Method for the Estimation of Soybean Chlorophyll Content Using a Smartphone and Image Analysis","volume":"54","author":"Rigon","year":"2016","journal-title":"Photosynthetica"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1034\/j.1399-3054.1996.970214.x","article-title":"Partial Blocks in the Early Steps of the Chlorophyll Synthesis Pathway: A Common Feature of Chlorophyll b-Deficient Mutants","volume":"97","author":"Falbel","year":"1996","journal-title":"Physiol. Plant."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"103942","DOI":"10.1016\/j.jprot.2020.103942","article-title":"Label-Free Comparative Proteomic and Physiological Analysis Provides Insight into Leaf Color Variation of the Golden-Yellow Leaf Mutant of Lagerstroemia indica","volume":"228","author":"Li","year":"2020","journal-title":"J. Proteom."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"484","DOI":"10.1016\/j.tplants.2020.12.005","article-title":"Connecting Chlorophyll Metabolism with Accumulation of the Photosynthetic Apparatus","volume":"26","author":"Wang","year":"2021","journal-title":"Trends Plant Sci."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1146\/annurev-biochem-072711-162943","article-title":"Chlorophyll Modifications and Their Spectral Extension in Oxygenic Photosynthesis","volume":"83","author":"Chen","year":"2014","journal-title":"Annu. Rev. Biochem."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1016\/j.envexpbot.2019.02.006","article-title":"Photosynthesis and Organization of Maize Mesophyll and Bundle Sheath Thylakoids of Plants Grown in Various Light Intensities","volume":"162","author":"Rogowski","year":"2019","journal-title":"Environ. Exp. Bot."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"817","DOI":"10.1016\/j.tplants.2020.03.003","article-title":"Chloroplast Transition Metal Regulation for Efficient Photosynthesis","volume":"25","author":"Schmidt","year":"2020","journal-title":"Trends Plant Sci."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Feng, Y., Li, Y., Zhao, Y., and Shi, H. (2023). Physiological, Transcriptome and Co-Expression Network Analysis of Chlorophyll-Deficient Mutants in Flue-Cured Tobacco. BMC Plant Biol., 23.","DOI":"10.1186\/s12870-023-04169-z"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1016\/j.plaphy.2019.11.036","article-title":"Pale Green Mutant Analyses Reveal the Importance of CsGLKs in Chloroplast Developmental Regulation and Their Effects on Flavonoid Biosynthesis in Tea Plant","volume":"146","author":"Hao","year":"2020","journal-title":"Plant Physiol. Biochem."},{"key":"ref_59","first-page":"291","article-title":"Integrated Transcriptome and Metabolic Analyses Reveals Novel Insights into Free Amino Acid Metabolism in Huangjinya Tea Cultivar","volume":"8","author":"Zhang","year":"2017","journal-title":"Front. Plant Sci."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Dong, S., Fan, M., Qin, Q., Zhang, Z., Duan, K., \u0106osi\u0107, T., Raspor, M., and Ni, D. (2024). Natural Albino Mutant of Daylily (Hemerocallis spp.) Reveals a Link between Drought Sensitivity and Photosynthetic Pigments Metabolism. Front. Biosci., 29.","DOI":"10.31083\/j.fbl2902060"},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Chen, J., Li, Y., He, D., Bai, M., Li, B., Zhang, Q., and Luo, L. (2022). Cytological, Physiological and Transcriptomic Analysis of Variegated Leaves in Primulina pungentisepala Offspring. BMC Plant Biol., 22.","DOI":"10.1186\/s12870-022-03808-1"},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Zhang, X., Zhao, Z., Zhang, M., Wang, J., Cheng, T., Zhang, Q., and Pan, H. (2023). FsHemF Is Involved in the Formation of Yellow Forsythia Leaves by Regulating Chlorophyll Synthesis in Response to Light Intensity. Plant Physiol. Biochem., 200.","DOI":"10.1016\/j.plaphy.2023.107746"},{"key":"ref_63","first-page":"2419","article-title":"Identification and Characterization of a Novel Yellow Leaf Mutant Yl1 in Rice","volume":"91","author":"Zeng","year":"2022","journal-title":"Phyton Int. J. Exp. Bot."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/j.tplants.2005.05.005","article-title":"Green Genes Gleaned","volume":"10","author":"Beale","year":"2005","journal-title":"Trends Plant Sci."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"612","DOI":"10.1016\/S2095-3119(19)62710-3","article-title":"OsHemA Gene, Encoding Glutamyl-tRNA Reductase (GluTR) Is Essential for Chlorophyll Biosynthesis in Rice (Oryza Sativa)","volume":"19","author":"Zeng","year":"2020","journal-title":"J. Integr. Agric."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1146\/annurev.arplant.57.032905.105448","article-title":"Tetrapyrrole Biosynthesis in Higher Plants","volume":"58","author":"Tanaka","year":"2007","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Liu, Y., Feng, X., Zhang, Y., Zhou, F., and Zhu, P. (2021). Simultaneous Changes in Anthocyanin, Chlorophyll, and Carotenoid Contents Produce Green Variegation in Pink\u2013Leaved Ornamental Kale. BMC Genom., 22.","DOI":"10.1186\/s12864-021-07785-x"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1039\/b110549n","article-title":"Biosynthesis of Chlorophylls from Protoporphyrin IX","volume":"20","author":"Willows","year":"2003","journal-title":"Nat. Prod. Rep."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1016\/j.tibs.2006.01.001","article-title":"Chelatases: Distort to Select?","volume":"31","author":"Franco","year":"2006","journal-title":"Trends Biochem. Sci."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"2737","DOI":"10.1093\/plphys\/kiad247","article-title":"A Point Mutation in the Gene Encoding Magnesium Chelatase I Subunit Influences Strawberry Leaf Color and Metabolism","volume":"192","author":"Ma","year":"2023","journal-title":"Plant Physiol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"147712","DOI":"10.1016\/j.gene.2023.147712","article-title":"Characterization and Fine Mapping of a Yellow Leaf Gene Regulating Chlorophyll Biosynthesis and Chloroplast Development in Cotton (Gossypium arboreum)","volume":"885","author":"Fan","year":"2023","journal-title":"Gene"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1104\/pp.119.1.143","article-title":"Feedback Inhibition of Chlorophyll Synthesis in the Phytochrome Chromophore-Deficient Aurea Andyellow-Green-2 Mutants of Tomato","volume":"119","author":"Terry","year":"1999","journal-title":"Plant Physiol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"326","DOI":"10.1007\/s12374-013-0180-9","article-title":"Green-Revertible Chlorina 1 (Grc1) Is Required for the Biosynthesis of Chlorophyll and the Early Development of Chloroplasts in Rice","volume":"56","author":"Li","year":"2013","journal-title":"J. Plant Biol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"432","DOI":"10.1111\/tpj.16382","article-title":"Mutation to a Cytochrome P450-like Gene Alters the Leaf Color by Affecting the Heme and Chlorophyll Biosynthesis Pathways in Brassica napus","volume":"116","author":"Yang","year":"2023","journal-title":"Plant J."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.jplph.2018.01.010","article-title":"Mg-Dechelation of Chlorophyll a by Stay-Green Activates Chlorophyll b Degradation through Expressing Non-Yellow Coloring 1 in Arabidopsis thaliana","volume":"222","author":"Sato","year":"2018","journal-title":"J. Plant Physiol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"1649","DOI":"10.1105\/tpc.106.044891","article-title":"The Senescence-Induced Staygreen Protein Regulates Chlorophyll Degradation","volume":"19","author":"Park","year":"2007","journal-title":"Plant Cell"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1111\/j.1365-313X.2008.03447.x","article-title":"Biosynthesis of Plant Pigments: Anthocyanins, Betalains and Carotenoids","volume":"54","author":"Tanaka","year":"2008","journal-title":"Plant J."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.abb.2004.03.018","article-title":"Water-Soluble Carotenoid Proteins of Cyanobacteria","volume":"430","author":"Kerfeld","year":"2004","journal-title":"Arch. Biochem. Biophys."},{"key":"ref_79","doi-asserted-by":"crossref","unstructured":"Chen, X., Yang, X., Xie, J., Ding, W., Li, Y., Yue, Y., and Wang, L. (2020). Biochemical and Comparative Transcriptome Analyses Reveal Key Genes Involved in Major Metabolic Regulation Related to Colored Leaf Formation in Osmanthus Fragrans \u2018Yinbi Shuanghui\u2019 during Development. Biomolecules, 10.","DOI":"10.3390\/biom10040549"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1007\/s11120-005-0998-1","article-title":"LHC II Protein Phosphorylation in Leaves of Arabidopsis thaliana Mutants Deficient in Non-Photochemical Quenching","volume":"84","author":"Breitholtz","year":"2005","journal-title":"Photosynth. Res."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"21796","DOI":"10.1073\/pnas.2004405117","article-title":"Synthetic Conversion of Leaf Chloroplasts into Carotenoid-Rich Plastids Reveals Mechanistic Basis of Natural Chromoplast Development","volume":"117","author":"Llorente","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_82","doi-asserted-by":"crossref","unstructured":"Liu, H., and Blankenship, R.E. (2019). On the Interface of Light-Harvesting Antenna Complexes and Reaction Centers in Oxygenic Photosynthesis. Biochim. Biophys. Acta BBA Bioenerg., 1860.","DOI":"10.1016\/j.bbabio.2019.148079"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"e436","DOI":"10.1002\/pld3.436","article-title":"PALE-GREEN LEAF 1, a Rice cpSRP54 Protein, Is Essential for the Assembly of the PSI-LHCI Supercomplex","volume":"6","author":"Gao","year":"2022","journal-title":"Plant Direct"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"108709","DOI":"10.1016\/j.scienta.2019.108709","article-title":"Leaf-Color Mutation Induced by Ethyl Methane Sulfonate and Genetic and Physio-Biochemical Characterization of Leaf-Color Mutants in Pepper (Capsicum annuum L.)","volume":"257","author":"Cheng","year":"2019","journal-title":"Sci. Hortic."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"111763","DOI":"10.1016\/j.plantsci.2023.111763","article-title":"Studying the Effect of Light Intensity on the Photosynthetic Mechanism of Pepper Leaf Yellowing Mutants by Proteomics and Phosphoproteomics","volume":"334","author":"Mao","year":"2023","journal-title":"Plant Sci."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1046\/j.1365-313X.2003.01811.x","article-title":"Absence of the Lhcb1 and Lhcb2 Proteins of the Light-Harvesting Complex of Photosystem II\u2014Effects on Photosynthesis, Grana Stacking and Fitness","volume":"35","author":"Jenny","year":"2003","journal-title":"Plant J."},{"key":"ref_87","doi-asserted-by":"crossref","unstructured":"Koyama, T. (2023). Regulatory Mechanisms of Transcription Factors in Plant Morphology and Function. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms24087039"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1111\/tpj.14914","article-title":"WRKY42 Transcription Factor Positively Regulates Leaf Senescence through Modulating SA and ROS Synthesis in Arabidopsis thaliana","volume":"104","author":"Niu","year":"2020","journal-title":"Plant J."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"2699","DOI":"10.1093\/jxb\/erz095","article-title":"Rice Transcription Factor OsMYB102 Delays Leaf Senescence by Down-Regulating Abscisic Acid Accumulation and Signaling","volume":"70","author":"Piao","year":"2019","journal-title":"J. Exp. Bot."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"uhad098","DOI":"10.1093\/hr\/uhad098","article-title":"A Multi-Omics Approach Identifies bHLH71-like as a Positive Regulator of Yellowing Leaf Pepper Mutants Exposed to High-Intensity Light","volume":"10","author":"Liu","year":"2023","journal-title":"Hortic. Res."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1111\/nph.15766","article-title":"Multiple Transcriptional Factors Control Stomata Development in Rice","volume":"223","author":"Wu","year":"2019","journal-title":"New Phytol."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"23609","DOI":"10.1038\/srep23609","article-title":"The NAC Transcription Factor ANAC046 Is a Positive Regulator of Chlorophyll Degradation and Senescence in Arabidopsis Leaves","volume":"6","author":"Mitsuda","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.plaphy.2019.12.035","article-title":"Transcript Profiling for Regulation of Sweet Potato Skin Color in Sushu8 and Its Mutant Zhengshu20","volume":"148","author":"Yang","year":"2020","journal-title":"Plant Physiol. Biochem."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1007\/s00425-020-03426-x","article-title":"Involvement of CsERF2 in Leaf Variegation of Cymbidium Sinense \u2018Dharma\u2019","volume":"252","author":"Gao","year":"2020","journal-title":"Planta"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1007\/s11240-006-9182-3","article-title":"Chloroplast Genome Aberration in Micropropagation-Derived Albino Bambusa Edulis Mutants, Ab1 and Ab2","volume":"88","author":"Liu","year":"2007","journal-title":"Plant Cell Tissue Organ Cult."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"9433","DOI":"10.1073\/pnas.0803611105","article-title":"PIF1 Directly and Indirectly Regulates Chlorophyll Biosynthesis to Optimize the Greening Process in Arabidopsis","volume":"105","author":"Moon","year":"2008","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"1509","DOI":"10.3389\/fpls.2016.01509","article-title":"GOLDEN 2-LIKE Transcription Factors of Plants","volume":"7","author":"Chen","year":"2016","journal-title":"Front. Plant Sci."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"713","DOI":"10.1046\/j.1365-313X.2002.01390.x","article-title":"GLK Gene Pairs Regulate Chloroplast Development in Diverse Plant Species","volume":"31","author":"Fitter","year":"2002","journal-title":"Plant J."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"1933","DOI":"10.1093\/pcp\/pcp138","article-title":"Ectopic Overexpression of The Transcription Factor OsGLK1 Induces Chloroplast Development in Non-Green Rice Cells","volume":"50","author":"Nakamura","year":"2009","journal-title":"Plant Cell Physiol."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"1109","DOI":"10.1105\/tpc.108.065250","article-title":"GLK Transcription Factors Coordinate Expression of the Photosynthetic Apparatus in Arabidopsis","volume":"21","author":"Waters","year":"2009","journal-title":"Plant Cell"},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"778","DOI":"10.1007\/s00344-018-9889-5","article-title":"Functional Identification of Apple MdGLK1 Which Regulates Chlorophyll Biosynthesis in Arabidopsis","volume":"38","author":"An","year":"2019","journal-title":"J. Plant Growth Regul."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1016\/S0308-8146(01)00221-7","article-title":"Colour Effects of Co-Pigmentation of Anthocyanin Revisited\u20143. A Further Description Using CIELAB Differences and Assessment of Matched Colours Using the CMC Model","volume":"75","author":"Gonnet","year":"2001","journal-title":"Food Chem."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1016\/j.tifs.2005.03.019","article-title":"Tracking Color and Pigment Changes in Anthocyanin Products","volume":"16","author":"Wrolstad","year":"2005","journal-title":"Trends Food Sci. Technol."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1016\/0076-6879(87)48036-1","article-title":"[34] Chlorophylls and Carotenoids: Pigments of Photosynthetic Biomembranes","volume":"Volume 148","author":"Lichtenthaler","year":"1987","journal-title":"Methods in Enzymology"},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"675","DOI":"10.1111\/j.1469-8137.2007.02133.x","article-title":"Coordination of Anthocyanin Decline and Photosynthetic Maturation in Juvenile Leaves of Three Deciduous Tree Species","volume":"175","author":"Hughes","year":"2007","journal-title":"New Phytol."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1071\/FP02226","article-title":"Exposed Red (Anthocyanic) Leaves of Quercus Coccifera Display Shade Characteristics","volume":"30","author":"Manetas","year":"2003","journal-title":"Funct. Plant Biol."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1016\/j.plaphy.2014.03.024","article-title":"Expression of Flavonoid Biosynthesis Genes and Accumulation of Flavonoid in Wheat Leaves in Response to Drought Stress","volume":"80","author":"Ma","year":"2014","journal-title":"Plant Physiol. Biochem."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"4946","DOI":"10.1074\/jbc.M111.308239","article-title":"Structure of the Cyanobacterial Magnesium Chelatase H Subunit Determined by Single Particle Reconstruction and Small-Angle X-Ray Scattering","volume":"287","author":"Qian","year":"2012","journal-title":"J. Biol. Chem."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1007\/s40011-021-01244-z","article-title":"Leaf Epidermis in Rosaceae: Diversity of the Cuticular Folding and Microstructure","volume":"91","author":"Kumachova","year":"2021","journal-title":"Proc. Natl. Acad. Sci. India Sect. B Biol. Sci."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1016\/j.jprot.2019.03.001","article-title":"Transcriptomic and Proteomic Analyses Reveal New Insight into Chlorophyll Synthesis and Chloroplast Structure of Maize Leaves under Zinc Deficiency Stress","volume":"199","author":"Zhang","year":"2019","journal-title":"J. Proteom."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1080\/09291016.2018.1518206","article-title":"Effect Street Light Pollution on the Photosynthetic Efficiency of Different Plants","volume":"51","author":"Meravi","year":"2020","journal-title":"Biol. Rhythm Res."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1038\/168167a0","article-title":"A Colorimetric Method for the Determination of Sugars","volume":"168","author":"Dubois","year":"1951","journal-title":"Nature"},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/0003-2697(76)90527-3","article-title":"A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding","volume":"72","author":"Bradford","year":"1976","journal-title":"Anal. Biochem."},{"key":"ref_114","doi-asserted-by":"crossref","unstructured":"Chong, X., Wang, Y., Xu, X., Zhang, F., Wang, C., Zhou, Y., Zhou, T., Li, Y., Lu, X., and Chen, H. (2023). Efficient Virus-Induced Gene Silencing in Ilex Dabieshanensis Using Tobacco Rattle Virus. Forests, 14.","DOI":"10.3390\/f14030488"},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2\u2212\u0394\u0394CT Method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"}],"container-title":["Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2223-7747\/13\/10\/1284\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:40:58Z","timestamp":1760107258000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2223-7747\/13\/10\/1284"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,5,7]]},"references-count":115,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2024,5]]}},"alternative-id":["plants13101284"],"URL":"https:\/\/doi.org\/10.3390\/plants13101284","relation":{},"ISSN":["2223-7747"],"issn-type":[{"value":"2223-7747","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,5,7]]}}}