Molecular Mechanisms of Albino Leaves in Brassica napus
YE Shen-hua, MA Xiao-wei, YANG Jie, LI Jia-xin, ZHAO Lun, YI Bin, MA Chao-zhi, TU Jin-xing, SHEN Jin-xiong, FU Ting-dong, WEN Jing
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College of Plant Science and Technology of Huazhong Agricultural University, National Research Center of Rapeseed Engineering and Technology, Wuhan 430070
Leaf-color mutants are crucial germplasms for deciphering the mechanisms of pigment metabolism and chloroplast development. In this study, to uncover the mechanisms of temperature-sensitive albino phenotype in Brassica napus, the physiological assessment and transcriptome analysis were performed in two resynthesized B. napus inbred lines, the white-leaf line W7105 and its green-leaf sibling line G7097. Under low temperature in field conditions, in albino leaves of W7105, the chlorophyll and carotenoid content were dramatically decreased and chloroplast structure was abnormal. Compared with green leaves, albino leaves showed significantly lower net photosynthetic rate (Pn) and significantly higher intercellular CO2 concentration (Ci). Transcriptome analysis of leaves at three different developing stages was performed in G7097 and W7105 lines. After pairwise comparisons, a total of 1532 differentially expressed genes (DEGs) associated with leaf color phenotype were identified, including 540 and 992 genes that were up-regulated and down-regulated, respectively. GO and KEGG enrichment analysis showed that the up-regulated DEGs in albino leaves of W7105 were significantly enriched in proteasome, translation process, carbohydrate and energy metabolism pathways; while the down-regulated DEGs were significantly enriched in chloroplasts, photosynthesis and electron transport chain. Moreover, several DEGs in chlorophyll and carotenoid biosynthesis were significantly down-regulated in albino leaves, suggesting that chlorophyll and carotenoid metabolisms were also impaired. Collectively, these findings provide references for further delimiting the candidate genes and uncovering the molecular mechanisms of albino leaves in B. napus.
YE Shen-hua,MA Xiao-wei,YANG Jie,LI Jia-xin,ZHAO Lun,YI Bin,MA Chao-zhi,TU Jin-xing,SHEN Jin-xiong,FU Ting-dong,WEN Jing.
Molecular Mechanisms of Albino Leaves in Brassica napus. Journal of Plant Genetic Resources. 2023, 24(3): 875-888 https://doi.org/10.13430/j.cnki.jpgr.20221215002
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参考文献
[1] Hayashi-Tsugane M, Takahara H, Ahmed N, Himi E, Takagi K, Iida S, Tsugane K, Maekawa M. A mutable albino allele in rice reveals that formation of thylakoid membranes requires the SNOW-WHITE LEAF1 gene. Plant and Cell Physiology, 2014, 55: 3-15
[2] Yu B, Gruber M Y, Khachatourians G G, Zhou R, Epp D J, Hegedus D D, Parkin I A, Welsch R, Hannoufa A. Arabidopsis cpSRP54 regulates carotenoid accumulation in Arabidopsis and Brassica napus. Journal of Experimental Botany, 2012, 63: 5189-5202
[3] Sandhu D, Atkinson T, Noll A, Johnson C, Espinosa K, Boelter J, Abel S, Dhatt B K, Barta T, Singsaas E, Sepsenwol S, Goggi A S, Palmer R G. Soybean proteins GmTic110 and GmPsbP are crucial for chloroplast development and function. Plant Science, 2016, 252: 76-87
[4] Gao M, Hu L, Li Y, Weng Y. The chlorophyll-deficient golden leaf mutation in cucumber is due to a single nucleotide substitution in CsChlI for magnesium chelatase I subunit. Theoretical and Applied Genetics, 2016, 129: 1961-1973
[5] Zhao M H, Li X, Zhang X X, Zhang H, Zhao X Y. Mutation mechanism of leaf color in plants: A review. Forests, 2020, 11: 851
[6] Glick R E, Sears B B. Genetically programmed chloroplast dedifferentiation as a consequence of plastome-genome incompatibility in Oenothera. Plant Physiology, 1994, 106: 367-373
[7] Chen L J, Li H M. Stable megadalton TOC-TIC supercomplexes as major mediators of protein import into chloroplasts. Plant Journal, 2017, 92: 178-188
[8] Bauer J, Chen K, Hiltbunner A, Wehrli E, Eugster M, Schnell D, Kessler F. The major protein import receptor of plastids is essential for chloroplast biogenesis. Nature, 2000, 403: 203-207
[9] Kohler D, Montandon C, Hause G, Majovsky P, Kessler F, Baginsky S, Agne B. Characterization of chloroplast protein import without Tic56, a component of the 1-megadalton translocon at the inner envelope membrane of chloroplasts. Plant Physiology, 2015, 167: 972-990
[10] Hedtke B, B?rner T, Weihe A. Mitochondrial and chloroplast phage-type RNA polymerases in Arabidopsis. Science, 1997, 277: 809-811
[11] Weihe A, B?rner T. Transcription and the architecture of promoters in chloroplasts. Trends in Plant Science, 1999, 4: 169-170
[12] Arsova B, Hoja U, Wimmelbacher M, Greiner E, Ustun S, Melzer M, Petersen K, Lein W, Bornke F. Plastidial thioredoxin z interacts with two fructokinase-like proteins in a thiol-dependent manner: Evidence for an essential role in chloroplast development in Arabidopsis and Nicotiana benthamiana. Plant Cell, 2010, 22: 1498-1515
[13] Wimmelbacher M, Bornke F. Redox activity of thioredoxin z and fructokinase-like protein 1 is dispensable for autotrophic growth of Arabidopsis thaliana. Journal of Experimental Botany, 2014, 65: 2405-2413
[14] Lv Y, Shao G, Qiu J, Jiao G, Sheng Z, Xie L, Wu Y, Tang S, Wei X, Hu P. White Leaf and Panicle 2, encoding a PEP-associated protein, is required for chloroplast biogenesis under heat stress in rice. Journal of Experimental Botany, 2017, 68: 5147-5160
[15] Song J, Wei X, Shao G, Sheng Z, Chen D, Liu C, Jiao G, Xie L, Tang S, Hu P. The rice nuclear gene WLP1 encoding a chloroplast ribosome L13 protein is needed for chloroplast development in rice grown under low temperature conditions. Plant Molecular Biology, 2014, 84: 301-314
[16] Wang W J, Zheng K L, Gong X D, Xu J L, Huang J R, Lin D Z, Dong Y J. The rice TCD11 encoding plastid ribosomal protein S6 is essential for chloroplast development at low temperature. Plant Science, 2017, 259: 1-11
[17] Waters M T, Wang P, Korkaric M, Capper R G, Saunders N J, Langdale J A. GLK transcription factors coordinate expression of the photosynthetic apparatus in Arabidopsis. Plant Cell, 2009, 21: 1109-1128
[18] Woodson J D. Chloroplast quality control-balancing energy production and stress. New Phytologist, 2016, 212: 36-41
[19] Woodson J D. Chloroplast stress signals: Regulation of cellular degradation and chloroplast turnover. Current Opinion in Plant Biology, 2019, 52: 30-37
[20] Zhu L X, Yang Z H, Zeng X H, Gao J, Liu J, Yi B, Ma C Z, Shen J X, Tu J X, Fu T D, Wen J. Heme oxygenase 1 defects lead to reduced chlorophyll in Brassica napus. Plant Molecular Biology, 2017, 93:579-592
[21]江莹芬, 吴新杰, 费维新, 李强生, 荣松柏, 初明光, 陈凤祥. 甘蓝型油菜角果特异白化种质的遗传和生理特性. 植物遗传资源学报, 2020, 21 (1): 113-120Jiang Y F, Wu X J, Fei W X, Li Q S, Rong S B, Chu M G, Chen F X. Genetic and physiological characteristics of Brassica napus germplasm resources showing albino silique. Journal of Plant Genetic Resources, 2020, 21 (1): 113-120
[22] Lichtenthaler H K. Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods in Enzymology, 1987, 148C: 350-382
[23] Yi B, Zeng F, Lei S, Chen Y, Yao X, Zhu Y, Wen J, Shen J, Ma C, Tu J, Fu T. Two duplicate CYP704B1-homologous genes BnMs1 and BnMs2 are required for pollen exine formation and tapetal development in Brassica napus. Plant Journal, 2010, 63: 925-938
[24] Sahraeian S M E, Mohiyuddin M, Sebra R, Tilgner H, Afshar P T, Au K F, Bani Asadi N, Gerstein M B, Wong W H, Snyder M P, Schadt E, Lam H Y K. Gaining comprehensive biological insight into the transcriptome by performing a broad-spectrum RNA-seq analysis. Nature Communication, 2017, 8: 59
[25] Pertea M, Kim D, Pertea G M, Leek J T, Salzberg S L. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nature Protocols, 2016, 11: 1650-1667
[26] Love M I, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 2014, 15: 550
[27] Jones P, Binns D, Chang H Y, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn A F, Sangrador-Vegas A, Scheremetjew M, Yong S Y, Lopez R, Hunter S. InterProScan 5: Genome-scale protein function classification. Bioinformatics, 2014, 30: 1236-1240
[28] Yu G, Wang L G, Han Y, He Q Y. clusterProfiler: An R package for comparing biological themes among gene clusters. Omics-A Journal of Integrative Biology, 2012, 16: 284-287
[29] Lu K, Li T, He J, Chang W, Zhang R, Liu M, Yu M, Fan Y, Ma J, Sun W, Qu C, Liu L, Li N, Liang Y, Wang R, Qian W, Tang Z, Xu X, Lei B, Zhang K, Li J. qPrimerDB: A thermodynamics-based gene-specific qPCR primer database for 147 organisms. Nucleic Acids Research, 2018, 46: D1229-D1236
[30] Li M, Lee K P, Liu T, Dogra V, Duan J, Li M, Xing W, Kim C. Antagonistic modules regulate photosynthesis-associated nuclear genes via GOLDEN2-LIKE transcription factors. Plant Physiology, 2022, 188: 2308-2324
[31] Ling Q, Broad W, Tr?sch R, T?pel M, Demiral Sert T, Lymperopoulos P, Baldwin A, Jarvis R P. Ubiquitin-dependent chloroplast-associated protein degradation in plants. Science, 2019, 363: eaav4467
[32] Beale S I. Green genes gleaned. Trends in Plant Science, 2005, 10: 309-312
[33] Shalygo N, Czarnecki O, Peter E, Grimm B. Expression of chlorophyll synthase is also involved in feedback-control of chlorophyll biosynthesis. Plant Molecular Biology, 2009, 71: 425-436
[34] Yamasato A, Nagata N, Tanaka R, Tanaka A. The N-terminal domain of chlorophyllide a oxygenase confers protein instability in response to chlorophyll B accumulation in Arabidopsis. Plant Cell, 2005, 17: 1585-1597
[35] Oster U, Tanaka R, Tanaka A, Rüdiger W. Cloning and functional expression of the gene encoding the key enzyme for chlorophyll b biosynthesis (CAO) from Arabidopsis thaliana. Plant Journal, 2000, 21: 305-310
[36] Lee S, Kim J H, Yoo E S, Lee C H, Hirochika H, An G. Differential regulation of chlorophyll a oxygenase genes in rice. Plant Molecular Biology, 2005, 57: 805-818
[37] Ruiz-Sola M A, Rodriguez-Concepcion M. Carotenoid biosynthesis in Arabidopsis: A colorful pathway. Arabidopsis Book, 2012, 10: e0158
[38] Rodriguez-Villalon A, Gas E, Rodriguez-Concepcion M. Phytoene synthase activity controls the biosynthesis of carotenoids and the supply of their metabolic precursors in dark-grown Arabidopsis seedlings. Plant Journal, 2009, 60: 424-435
[39] Zhang L, Ma G, Kato M, Yamawaki K, Takagi T, Kiriiwa Y, Ikoma Y, Matsumoto H, Yoshioka T, Nesumi H. Regulation of carotenoid accumulation and the expression of carotenoid metabolic genes in citrus juice sacs in vitro. Journal of Experimental Botany, 2012, 63: 871-886
[40] Ma F, Hu Y, Ju Y, Jiang Q, Cheng Z, Zhang Q, Sodmergen. A novel tetratricopeptide repeat protein, WHITE TO GREEN1, is required for early chloroplast development and affects RNA editing in chloroplasts. Journal of Experimental Botany, 2017, 68: 5829-5843
[41] Zhou S, Hu Z, Zhu M, Zhang B, Deng L, Pan Y, Chen G. Biochemical and molecular analysis of a temperature-sensitive albino mutant in kale named “White Dove”. Plant Growth Regulation, 2013, 71: 281-294
[42] Wu H, Shi N, An X, Liu C, Fu H, Cao L, Feng Y, Sun D, Zhang L. Candidate genes for yellow leaf color in common wheat (Triticum aestivum L.) and major related metabolic pathways according to transcriptome profiling. International Journal of Molecular Sciences, 2018, 19: 1594
[43] Yang X, Li Y, Qi M, Liu Y, Li T. Targeted control of chloroplast quality to improve plant acclimation: From protein import to degradation. Frontiers in Plant Science, 2019, 10: 958
[44] Begue H, Mounier A, Rosnoblet C, Wendehenne D. Toward the understanding of the role of CDC48, a major component of the protein quality control, in plant immunity. Plant Science, 2019, 279: 34-44
[45] Rottet S, Besagni C, Kessler F. The role of plastoglobules in thylakoid lipid remodeling during plant development. Biochimica et Biophysica Acta (BBA)?-Bioenergetics, 2015, 1847: 889-899
[46] Hall L N, Rossini L, Cribb L, Langdale J A. GOLDEN 2: A novel transcriptional regulator of cellular differentiation in the maize leaf. Plant Cell, 1998, 10: 925-936
[47] Tokumaru M, Adachi F, Toda M, Ito-Inaba Y, Yazu F, Hirosawa Y, Sakakibara Y, Suiko M, Kakizaki T, InabaT, Ubiquitin-proteasome dependent regulation of the GOLDEN2-LIKE 1 transcription factor in response to plastid signals. Plant Physiology, 2017, 173(1): 524-535
[48] Gang H, Li R, Zhao Y, Liu G, Chen S, Jiang J. Loss of GLK1 transcription factor function reveals new insights in chlorophyll biosynthesis and chloroplast development. Journal of Experimental Botany, 2019, 70: 3125-3138