Biochemical, transcriptome and metabolome analysis of the pulp of Citrus sinensis (L.) Osbeck ‘Hong Jiang’ and its two variants reveal pathways regulating pulp taste, mastication, and color

Li, 2017, Citrus fruit-cracking: Causes and occurrence, Hortic Plant J, 3, 255, 10.1016/j.hpj.2017.08.002 Xu, 2013, The draft genome of sweet orange (Citrus sinensis), Nat Genet, 45, 59, 10.1038/ng.2472 Foster, 2018, Attention sports fans! The far-reaching contributions of bud sport mutants to horticulture and plant biology, Hort Res, 5, 44, 10.1038/s41438-018-0062-x Zhang, 2020, Chimerism Evaluation of ‘Hongrou Huyou’, a Grafted Chimera between Citrus changshan-huyou and Citrus unshiu, Horticult Sci Technol, 38, 107, 10.7235/HORT.20200011 Zhang, 2007, Characterization of a new natural periclinal navel–Satsuma chimera of Citrus: ‘Zaohong’navel orange, J Am Soc Hort Sci, 132, 374, 10.21273/JASHS.132.3.374 Chen, 2019, Cit 1, 2RhaT and two novel CitdGlcTs participate in flavor-related flavonoid metabolism during citrus fruit development, J Exp Bot, 70, 2759, 10.1093/jxb/erz081 Feng, 2018, Differentiation between flavors of sweet orange (Citrus sinensis) and mandarin (Citrus reticulata), J Agric Food Chem, 66, 203, 10.1021/acs.jafc.7b04968 Le Lievre, 2021, Modifying Carbohydrate Supply to Fruit during Development Changes the Composition and Flavour of Actinidia chinensis var. chinensis ‘Zesy002’ Kiwifruit, Plants, 10, 1328, 10.3390/plants10071328 Arena, 2013, Berberis buxifolia fruit growth and ripening: Evolution in carbohydrate and organic acid contents, Sci Hortic, 158, 52, 10.1016/j.scienta.2013.04.026 Lado, 2018, Key determinants of citrus fruit quality: Metabolites and main changes during maturation, Sci Hortic, 233, 238, 10.1016/j.scienta.2018.01.055 Goldenberg, 2018, Mandarin fruit quality: A review, J Sci Food Agri, 98, 18, 10.1002/jsfa.8495 Xiong, 2020, Nutritional component analyses of kiwifruit in different development stages by metabolomic and transcriptomic approaches, J Sci Food Agri, 100, 2399, 10.1002/jsfa.10251 Chen, 2015, Pigments in citrus, 165 Rodrigo, 2013, Biochemical bases and molecular regulation of pigmentation in the peel of Citrus fruit, Sci Hortic, 163, 46, 10.1016/j.scienta.2013.08.014 Lu, 2016, Comparative transcriptome analysis reveals a global insight into molecular processes regulating citrate accumulation in sweet orange (Citrus sinensis), Physiol Plantarum, 158, 463, 10.1111/ppl.12484 Tian, 2018, Single-molecule long-read sequencing of Zanthoxylum bungeanum Maxim. transcriptome: identification of aroma-related genes, Forests, 9, 765, 10.3390/f9120765 Liew, 2018, Phytochemical composition and in vitro antioxidant activities of Citrus sinensis peel extracts, PeerJ, 6, 5331, 10.7717/peerj.5331 Grintzalis, 2015, An accurate and sensitive Coomassie Brilliant Blue G-250-based assay for protein determination, Analyt Biochem, 480, 28, 10.1016/j.ab.2015.03.024 Wu, 2020, Transcriptome analysis unravels metabolic and molecular pathways related to fruit sac granulation in a late-ripening navel orange (Citrus sinensis Osbeck), Plants, 9, 95, 10.3390/plants9010095 Chen, 2019, Combined De Novo Transcriptome and Metabolome Analysis of Common Bean Response to Fusarium oxysporum f. sp. phaseoli Infection, Int J Mol Sci, 20, 6278, 10.3390/ijms20246278 Kim, 2019, Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype, Nature Biotechnol, 37, 907, 10.1038/s41587-019-0201-4 Gel, 2017, karyoploteR: an R/Bioconductor package to plot customizable genomes displaying arbitrary data, Bioinformatics, 33, 3088, 10.1093/bioinformatics/btx346 Liao, 2014, featureCounts: an efficient general purpose program for assigning sequence reads to genomic features, Bioinformatics, 30, 923, 10.1093/bioinformatics/btt656 Benjamini, 1995, Controlling the false discovery rate: a practical and powerful approach to multiple testing, J Roy Stat Soc: Ser B (Methodol), 57, 289 Love, 2014, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2, Genome Biol, 15, 550, 10.1186/s13059-014-0550-8 Kukurba, 2015, RNA sequencing and analysis, Cold Spring Harbor Protocols, 2015, 951, 10.1101/pdb.top084970 Chong, 2018, MetaboAnalystR: an R package for flexible and reproducible analysis of metabolomics data, Bioinformatics, 34, 4313, 10.1093/bioinformatics/bty528 Xie, 2011, KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases, Nucleic Acids Res, 39, W316, 10.1093/nar/gkr483 Fukushima, 2013, DiffCorr: an R package to analyze and visualize differential correlations in biological networks, Gene, 518, 209, 10.1016/j.gene.2012.11.028 Frydman, 2013, The molecular and enzymatic basis of bitter/non-bitter flavor of citrus fruit: evolution of branch-forming rhamnosyltransferases under domestication, The Plant J, 73, 166, 10.1111/tpj.12030 Etienne, 2013, What controls fleshy fruit acidity? A review of malate and citrate accumulation in fruit cells, J Exp Bot, 64, 1451, 10.1093/jxb/ert035 Forlani, 2019, Fruit ripening: the role of hormones, cell wall modifications, and their relationship with pathogens, J Exp Bot, 70, 2993, 10.1093/jxb/erz112 Colodel, 2018, Cell wall polysaccharides from Ponkan mandarin (Citrus reticulata Blanco cv. Ponkan) peel, Carbohyd Polym, 195, 120, 10.1016/j.carbpol.2018.04.066 Nawaz, 2017, Systems identification and characterization of cell wall reassembly and degradation related genes in Glycine max (L.) Merill, a bioenergy legume, Sci Rep, 7, 10862, 10.1038/s41598-017-11495-4 Nawaz, 2019, Characterization of cellulose synthase A (CESA) gene family in eudicots, Biochem Genet, 57, 248, 10.1007/s10528-018-9888-z Little, 2018, Revised phylogeny of the Cellulose synthase gene superfamily: Insights into cell wall evolution, Plant Physiol, 177, 1124, 10.1104/pp.17.01718 Gyawali, 2014, Anticancer phytochemicals of citrus fruits—A review, J Animal Res, 4, 85, 10.5958/2277-940X.2014.00079.5 Baldwin, 2014, Citrus fruit quality assessment; producer and consumer perspectives, Stewart Postharvest Rev, 10 Li, 2019, Citrus taste modification potentials by genetic engineering, Int J Mol Sci, 20, 6194, 10.3390/ijms20246194 Carvalho, 2020, Determination of organic acids and carbohydrates in ‘Salustiana’ orange fruit from different rootstocks. Brazilian, J Food Technol, 23 Decker, 2019, UDP-sugar producing pyrophosphorylases: Distinct and essential enzymes with overlapping substrate specificities, providing de novo precursors for glycosylation reactions, Front Plant Sci, 9, 1822, 10.3389/fpls.2018.01822 Sharabi, 2015, Molecular pathophysiology of hepatic glucose production, Mol Aspects Med, 46, 21, 10.1016/j.mam.2015.09.003 Sharma, 2019, Naringin: Biosynthesis and pharmaceutical applications, Indian J Pharmac Sci, 81, 988 Liu, 2011, Isolation of a polygalacturonase gene from Citrus sinensis fruit and its expression relative to fruit mastication trait, fruit development, and calcium or boron treatments, Plant Mol Biol Rep, 29, 51, 10.1007/s11105-010-0206-0 Lei, 2012, Comparison of cell wall metabolism in the pulp of three cultivars of ‘Nanfeng’ tangerine differing in mastication trait, J Sci Food Agri, 92, 496, 10.1002/jsfa.4554 Molinett, 2021, Postharvest treatment of hydrogen sulfide delays the softening of Chilean strawberry fruit by downregulating the expression of key genes involved in pectin catabolism, Int J Mol Sci, 22, 10008, 10.3390/ijms221810008 Wang, 2018, Transcriptomic insights into citrus segment membrane’s cell wall components relating to fruit sensory texture, BMC Genomics, 19, 280, 10.1186/s12864-018-4669-y Yao, 2020, Molecular basis of postharvest granulation in orange fruit revealed by metabolite, transcriptome and methylome profiling, Postharvest Biol Technol, 166, 111205, 10.1016/j.postharvbio.2020.111205 Zhong, 2008, A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis, Plant Cell, 20, 2763, 10.1105/tpc.108.061325 Napiroon, 2018, Scopoletin from Lasianthus lucidus Blume (Rubiaceae): a potential antimicrobial against multidrug-resistant Pseudomonas aeruginosa, J Appl Pharmaceut Sci, 8, 1, 10.7324/JAPS.2018.8901 Lado, 2015, Fruit shading enhances peel color, carotenes accumulation and chromoplast differentiation in red grapefruit, Physiol Plantarum, 154, 469, 10.1111/ppl.12332 Dautermann, 2017, A functional zeaxanthin epoxidase from red algae shedding light on the evolution of light-harvesting carotenoids and the xanthophyll cycle in photosynthetic eukaryotes, Plant J, 92, 879, 10.1111/tpj.13725 Buaban, 2020, Lycopene accumulation in pummelo (Citrus Maxima [Burm.] Merr.) is influenced by growing temperature, Int J Fruit Sci, 20, 149, 10.1080/15538362.2019.1605559 Khoo, 2017, Anthocyanidins and anthocyanins: colored pigments as food, pharmaceutical ingredients, and the potential health benefits, Food Nut Res, 61, 1361779, 10.1080/16546628.2017.1361779 Fabroni, 2016, Anthocyanins in different Citrus species: an UHPLC-PDA-ESI/MSn-assisted qualitative and quantitative investigation, J Sci Food & Agri, 96, 4797, 10.1002/jsfa.7916 Zhang, 2016, The Reaumuria trigyna leucoanthocyanidin dioxygenase (RtLDOX) gene complements anthocyanidin synthesis and increases the salt tolerance potential of a transgenic Arabidopsis LDOX mutant, Plant Physiol Biochem, 106, 278, 10.1016/j.plaphy.2016.05.005