Genome-wide investigation of glycoside hydrolase 9 (GH9) gene family unveils implications in orchestrating the mastication trait of Citrus sinensis fruits.
Bioinformatics analyses
Cellulose
Citrus
Fruit mastication
GH9 family
Journal
BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258
Informations de publication
Date de publication:
30 Sep 2024
30 Sep 2024
Historique:
received:
23
05
2024
accepted:
23
09
2024
medline:
1
10
2024
pubmed:
1
10
2024
entrez:
30
9
2024
Statut:
epublish
Résumé
Mastication trait of citrus significantly influences the fruit's overall quality and consumer preference. The accumulation of cellulose in fruits significantly impacts the mastication trait of citrus fruits, and the glycoside hydrolase 9 (GH9) family plays a crucial role in cellulose metabolism. In this study, we successfully identified 32 GH9 genes from the Citrus sinensis genome and subsequently conducted detailed bioinformatics analyses of the GH9 family. Additionally, we profiled the spatiotemporal expression patterns of CsGH9 genes across four distinct fruit tissue types and six crucial developmental stages of citrus fruits, leveraging transcriptome data. Parallel to this, we undertook a comparative analysis of transcriptome profiles and cellulose content among diverse fruit tissues spanning six developmental stages. Furthermore, to identify the pivotal genes involved in cellulose metabolism within the GH9 family during fruit maturity, we employed correlation analysis between cellulose content and gene expression in varying tissues across diverse citrus varieties. This analysis highlighted key genes such as CsGH9A2/6 and CsGH9B12/13/14/22. Collectively, this study provides an in-depth analysis of the GH9 gene family in citrus and offers novel molecular insights into the underlying mechanisms governing the mastication trait formation in citrus fruits.
Identifiants
pubmed: 39350029
doi: 10.1186/s12864-024-10826-w
pii: 10.1186/s12864-024-10826-w
doi:
Substances chimiques
Glycoside Hydrolases
EC 3.2.1.-
Cellulose
9004-34-6
Plant Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
905Subventions
Organisme : Natural Science Foundation of China
ID : 32302511
Organisme : Doctoral Initiating Project of Linyi University
ID : Z6122057
Informations de copyright
© 2024. The Author(s).
Références
Pedersen GB, et al. Cellulose synthesis in land plants. Mol Plant. 2023;16(7):1228.
doi: 10.1016/j.molp.2023.05.008
pubmed: 37339637
Xue Y, et al. The transcription factor PbrMYB24 regulates lignin and cellulose biosynthesis in stone cells of pear fruits. Plant Physiol. 2023;192(3):1997–2014.
doi: 10.1093/plphys/kiad200
pmcid: 10315299
pubmed: 37011145
Tao D. The Relationship between the activity of PG and cx with Dietary Fibre in Sweet Orange Fruit. Acta Horticulturae Sinica; 2007.
Li L, et al. Changes in Fruit Firmness, Cell Wall Composition, and Transcriptional Profile in the yellow fruit tomato 1 (yft1) mutant. J Agric Food Chem. 2019;67(1):463–72.
doi: 10.1021/acs.jafc.8b04611
pubmed: 30545217
Phakeenuya V, et al. A novel multifunctional GH9 enzyme from Paenibacillus curdlanolyticus B-6 exhibiting endo/exo functions of cellulase, mannanase and xylanase activities. Appl Microbiol Biotechnol. 2020;104(5):2079–96.
doi: 10.1007/s00253-020-10388-3
pubmed: 31980921
Guerriero G, et al. Callose and cellulose synthase gene expression analysis from the tight cluster to the full bloom stage and during early fruit development in Malus× Domestica. J Plant Res. 2014;127:173–83.
doi: 10.1007/s10265-013-0586-y
pubmed: 23934062
Houle A, Conklin-Brittain NL, Wrangham RW. Vertical stratification of the nutritional value of fruit: macronutrients and condensed tannins. Am J Primatol. 2014;76(12):1207–32.
doi: 10.1002/ajp.22305
pubmed: 24865650
Delpino-Rius A, et al. Characterisation of phenolic compounds in processed fibres from the juice industry. Food Chem. 2015;172:575–84.
doi: 10.1016/j.foodchem.2014.09.071
pubmed: 25442594
Shen YanHong SY et al. Isolation of ripening-related genes from ethylene/1-MCP treated papaya through RNA-seq. 2017.
Gong X et al. PbMC1a/1b regulates lignification during stone cell development in pear (Pyrus Bretschneideri) fruit. Hortic Res, 2020. 7.
Shani Z, et al. Expression of endo-1,4-β-glucanase (cel1) in Arabidopsis thaliana is associated with plant growth, xylem development and cell wall thickening. Plant Cell Rep. 2006;25(10):1067–74.
doi: 10.1007/s00299-006-0167-9
pubmed: 16758197
Wang Y, et al. Genome-wide identification of GH9 gene family and the assessment of its role during fruit abscission zone formation in Vaccinium ashei. Plant Cell Rep; 2023.
Shigeru S et al. Role of the putative membrane-bound endo-1,4-beta-glucanase KORRIGAN in cell elongation and cellulose synthesis in Arabidopsis thaliana. Plant Cell Physiol, 2001(3): p. 251.
Lane DR, et al. Temperature-sensitive alleles of RSW2 link the KORRIGAN Endo-1,4-beta-Glucanase to Cellulose Synthesis and Cytokinesis in Arabidopsis. Plant Physiol. 2001;126(1):278–88.
doi: 10.1104/pp.126.1.278
pmcid: 102302
pubmed: 11351091
Junko T et al. KORRIGAN1 and its Aspen Homolog PttCel9A1 decrease cellulose crystallinity in Arabidopsis stems. Plant Cell Physiol, 2009(6): pp. 1099–115.
Maloney VJ, Mansfield SD. Characterization and varied expression of a membrane-bound endo-β-1,4-glucanase in hybrid poplar. Plant Biotechnol J, 2010.
Waldron KW, Parker M, Smith AC. Plant cell walls and food quality. Compr Rev Food Sci Food Saf. 2003;2(4):128–46.
doi: 10.1111/j.1541-4337.2003.tb00019.x
pubmed: 33451229
Goulao LF, Oliveira CM. Cell wall modifications during fruit ripening: when a fruit is not the fruit. Trends Food Sci Technol. 2008;19(1):4–25.
doi: 10.1016/j.tifs.2007.07.002
Feng G et al. Genomic and transcriptomic analyses of Citrus sinensis varieties provide insights into Valencia orange fruit mastication trait formation. Hortic Res, 2021. 8.
Dong T, et al. Effect of pre-harvest application of calcium and boron on dietary fibre, hydrolases and ultrastructure in ‘Cara Cara’ navel orange (Citrus sinensis L. Osbeck) fruit. Sci Hort. 2009;121(3):272–7.
doi: 10.1016/j.scienta.2009.02.003
Lei Y, et al. Comparison of cell wall metabolism in the pulp of three cultivars of ‘Nanfeng’tangerine differing in mastication trait. J Sci Food Agric. 2012;92(3):496–502.
doi: 10.1002/jsfa.4554
pubmed: 21732384
Urbanowicz BR, et al. Structural organization and a standardized nomenclature for plant endo-1,4-beta-glucanases (cellulases) of glycosyl hydrolase family 9. Plant Physiol. 2007;144(4):1693–6.
doi: 10.1104/pp.107.102574
pmcid: 1949884
pubmed: 17687051
Xie G, et al. Global identification of multiple OsGH9 family members and their involvement in cellulose crystallinity modification in rice. PLoS ONE. 2013;8(1):e50171.
doi: 10.1371/journal.pone.0050171
pmcid: 3537678
pubmed: 23308094
Brummell DA, et al. Cell wall metabolism during maturation, ripening and senescence of peach fruit. J Exp Bot. 2004;55(405):2029–39.
doi: 10.1093/jxb/erh227
pubmed: 15286150
Lei Y, et al. Physicochemical and molecular analysis of cell wall metabolism between two navel oranges (Citrus sinensis) with different mastication traits. J Sci Food Agric. 2010;90(9):1479–84.
doi: 10.1002/jsfa.3970
pubmed: 20549800
Wu L-M, et al. Transcriptome analysis unravels metabolic and molecular pathways related to fruit sac granulation in a late-ripening navel orange (Citrus sinensis Osbeck). Plants. 2020;9(1):95.
doi: 10.3390/plants9010095
pmcid: 7020443
pubmed: 31940826
Llop-Tous I, et al. Characterization of two divergent endo-β-1, 4-glucanase cDNA clones highly expressed in the nonclimacteric strawberry fruit. Plant Physiol. 1999;119(4):1415–22.
doi: 10.1104/pp.119.4.1415
pmcid: 32027
pubmed: 10198101
Rose JK, Bennett AB. Cooperative disassembly of the cellulose–xyloglucan network of plant cell walls: parallels between cell expansion and fruit ripening. Trends Plant Sci. 1999;4(5):176–83.
doi: 10.1016/S1360-1385(99)01405-3
pubmed: 10322557
Fischer RL, Bennett AB. Role of cell wall hydrolases in fruit ripening. Annu Rev Plant Physiol Plant Mol Biol. 1991;42(1):675–703.
doi: 10.1146/annurev.pp.42.060191.003331
Mejía-Mendoza MA, et al. Identification in silico and expression analysis of a β-1-4-endoglucanase and β-galactosidase genes related to ripening in guava fruit. J Genetic Eng Biotechnol. 2022;20:1–11.
doi: 10.1186/s43141-021-00289-x
Xu Q, et al. The draft genome of sweet orange (Citrus sinensis). Nat Genet. 2013;45(1):59–66.
doi: 10.1038/ng.2472
pubmed: 23179022
El-Gebali S, et al. The pfam protein families database in 2019. Nucleic Acids Res. 2019;47(D1):D427–32.
doi: 10.1093/nar/gky995
pubmed: 30357350
Letunic I, Bork P. 20 years of the SMART protein domain annotation resource. Nucleic Acids Res. 2018;46(D1):D493–6.
doi: 10.1093/nar/gkx922
pubmed: 29040681
Lu S, et al. CDD/SPARCLE: the conserved domain database in 2020. Nucleic Acids Res. 2020;48(D1):D265–8.
doi: 10.1093/nar/gkz991
pubmed: 31777944
Gasteiger E, et al. Protein identification and analysis tools on the ExPASy server. Springer; 2005.
Chou KC, Shen HB. Cell-PLoc: a package of web servers for predicting subcellular localization of proteins in various organisms. Nat Protoc. 2008;3(2):153–62.
doi: 10.1038/nprot.2007.494
pubmed: 18274516
Xie J et al. Tree visualization by one table (tvBOT): a web application for visualizing, modifying and annotating phylogenetic trees. Nucleic Acids Res, 2023: p. gkad359.
Chen C, et al. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020;13(8):1194–202.
doi: 10.1016/j.molp.2020.06.009
pubmed: 32585190
Lescot M, et al. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002;30(1):325–7.
doi: 10.1093/nar/30.1.325
pmcid: 99092
pubmed: 11752327
Bailey TL, et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 2009;37(suppl2):W202–8.
doi: 10.1093/nar/gkp335
pmcid: 2703892
pubmed: 19458158
Marchler-Bauer A, Bryant SH. CD-Search: protein domain annotations on the fly. Nucleic Acids Res. 2004;32(suppl2):W327–31.
doi: 10.1093/nar/gkh454
pmcid: 441592
pubmed: 15215404
Feng G, et al. High-spatiotemporal-resolution transcriptomes provide insights into fruit development and ripening in Citrus sinensis. Plant Biotechnol J. 2021;19(7):1337–53.
doi: 10.1111/pbi.13549
pmcid: 8313135
pubmed: 33471410
Feng G, Wu J, Yi H. Global tissue-specific transcriptome analysis of Citrus sinensis fruit across six developmental stages. Sci Data. 2019;6(1):153.
doi: 10.1038/s41597-019-0162-y
pmcid: 6704135
pubmed: 31434903
Mafra V, et al. Reference genes for accurate transcript normalization in citrus genotypes under different experimental conditions. PLoS ONE. 2012;7(2):e31263.
doi: 10.1371/journal.pone.0031263
pmcid: 3276578
pubmed: 22347455
Wu J, et al. Selection of reliable reference genes for gene expression studies using quantitative real-time PCR in navel orange fruit development and pummelo floral organs. Sci Hort. 2014;176:180–8.
doi: 10.1016/j.scienta.2014.06.040