Metabolomic and transcriptomic analyses reveal new insights into the role of abscisic acid in modulating mango fruit ripening

Shibo Wu , Di Wu , Juan Song , Yanyu Zhang , Qing Tan , Tianquan Yang , Jingya Yang , Songbiao Wang , Jianchu Xu , Wei Xu , Aizhong Liu

Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) : uhac102

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Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) :uhac102 DOI: 10.1093/hr/uhac102
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Metabolomic and transcriptomic analyses reveal new insights into the role of abscisic acid in modulating mango fruit ripening
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Abstract

Mango (Mangifera indica L.) is a climacteric tropical fruit consumed around the world. Although ethylene and abscisic acid (ABA) have been considered to be stimulators that trigger mango fruit ripening, their regulation mechanisms in modulating mango fruit ripening remain uncertain. In this study, we performed integrative analyses of metabolome and transcriptome data combined with a series of physiological and experimental analyses in the ‘Keitt’ mango, and we characterized changes in accumulation of specific metabolites at different stages during fruit development and ripening, which were strongly correlated with transcriptional changes and embodied physiological changes as well as taste formation. Specifically, we found that ABA, rather than ethylene, was highly associated with mango ripening, and exogenous ABA application promoted mango fruit ripening. Transcriptomic analysis identified diverse ripening-related genes involved in sugar and carotenoid biosynthesis and softening-related metabolic processes. Furthermore, networks of ABA- and ripening-related genes (such as MiHY5, MiGBF4, MiABI5, and MibZIP9) were constructed, and the direct regulation by the key ABA-responsive transcription factor MiHY5 of ripening-related genes was experimentally confirmed by a range of evidence. Taken together, our results indicate that ABA plays a key role in directly modulating mango fruit ripening through MiHY5, suggesting the need to reconsider how we understand ABA function in modulating climacteric fruit ripening.

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Shibo Wu, Di Wu, Juan Song, Yanyu Zhang, Qing Tan, Tianquan Yang, Jingya Yang, Songbiao Wang, Jianchu Xu, Wei Xu, Aizhong Liu. Metabolomic and transcriptomic analyses reveal new insights into the role of abscisic acid in modulating mango fruit ripening. Horticulture Research, 2022, 9 (1) : uhac102 DOI:10.1093/hr/uhac102

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References

[1]

Giovannoni JJ . Genetic regulation of fruit development and ripening. Plant Cell. 2004; 16: S170-80.

[2]

Seymour GB, Østergaard L, Chapman NH et al. Fruit development and ripening. Annu Rev Plant Biol. 2013; 64: 219-41.

[3]

Forlani S, Masiero S, Mizzotti C . Fruit ripening: the role of hormones, cell wall modifications, and their relationship with pathogens. J Exp Bot. 2019; 70: 2993-3006.

[4]

Chen T, Qin G, Tian S . Regulatory network of fruit ripening: current understanding and future challenges. New Phytol. 2020; 228: 1219-26.

[5]

Tang D, Gallusci P, Lang Z . Fruit development and epigenetic modifications. New Phytol. 2020; 228: 839-44.

[6]

Pereira L, Domingo MS, Ruggieri V et al. Genetic dissection of climacteric fruit ripening in a melon population segregating for ripening behavior. Hortic Res. 2020; 7: 187.

[7]

Liu S, Huang H, Huber DJ et al. Delay of ripening and softening in ‘Guifei’ mango fruit by postharvest application of melatonin. Postharvest Biol Technol. 2020; 163: 111136.

[8]

Kuang J, Wu C, Guo Y et al. Deciphering transcriptional regulators of banana fruit ripening by regulatory network analysis. Plant Biotechnol J. 2021; 19: 477-89.

[9]

Cherian S, Figueroa CR, Nair H . ‘Movers and shakers’ in the regulation of fruit ripening: a cross-dissection of climacteric versus non-climacteric fruit. J Exp Bot. 2014; 65: 4705-22.

[10]

Cheng J, Niu Q, Zhang B et al. Downregulation of RdDM during strawberry fruit ripening. Genome Biol. 2018; 19: 212.

[11]

McMurchie EJ, McGlasson WB, Eaks IL . Treatment of fruit with propylene gives information about the biogenesis of ethylene. Nature. 1972; 237: 235-6.

[12]

Qiao H, Zhang H, Wang Z et al. Fig fruit ripening is regulated by the interaction between ethylene and abscisic acid. J Integr Plant Biol. 2021; 63: 553-69.

[13]

Alexander L, Grierson D . Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot. 2002; 53: 2039-55.

[14]

Liu M, Pirrello J, Chervin C et al. Ethylene control of fruit ripening: revisiting the complex network of transcriptional regulation. Plant Physiol. 2015; 169: 2380-90.

[15]

Nicolas P, Lecourieux D, Kappel C et al. The basic leucine zipper transcription factor ABSCISIC ACID RESPONSE ELEMENT-BINDING FACTOR2 is an important transcriptional regulator of abscisic acid-dependent grape berry ripening processes. Plant Physiol. 2014; 164: 365-83.

[16]

Jia H, Chai Y, Li C et al. Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiol. 2011; 157: 188-99.

[17]

Leng P, Yuan B, Guo Y . The role of abscisic acid in fruit ripening and responses to abiotic stress. J Exp Bot. 2014; 65: 4577-88.

[18]

Liao X, Li M, Liu B et al. Interlinked regulatory loops of ABA catabolism and biosynthesis coordinate fruit growth and ripening in woodland strawberry. Proc Natl Acad Sci USA. 2018; 115: E11542-50.

[19]

Hobo T, Kowyama Y, Hattori T . A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc Natl Acad Sci USA. 1999; 96: 15348-53.

[20]

Finkelstein RR, Gampala SSL, Rock CD . Abscisic acid signaling in seeds and seedlings. Plant Cell. 2002; 14: S15-45.

[21]

Wu R, Duan L, Pruneda-Paz JL et al. The 6xABRE synthetic promoter enables the spatiotemporal analysis of ABA-mediated transcriptional regulation. Plant Physiol. 2018; 177: 1650-65.

[22]

Pilati S, Bagagli G, Sonego P et al. Abscisic acid is a major regulator of grape berry ripening onset: new insights into ABA signaling network. Front Plant Sci. 2017; 8: 1093.

[23]

Liang B, Zheng Y, Wang J et al. Overexpression of the persimmon abscisic acid beta-glucosidase gene (DkBG1) alters fruit ripening in transgenic tomato . Plant J. 2020; 102: 1220-33.

[24]

Wang X, Zeng W, Ding Y et al. PpERF3 positively regulates ABA biosynthesis by activating PpNCED2/3 transcription during fruit ripening in peach. Hortic Res. 2019; 6: 19.

[25]

Zhang M, Yuan B, Leng P . The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit. J Exp Bot. 2009; 60: 1579-88.

[26]

Carrari F, Baxter C, Usadel B et al. Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior. Plant Physiol. 2006; 142: 1380-96.

[27]

Wang R, Shu P, Zhang C et al. Integrative analyses of metabolome and genome-wide transcriptome reveal the regulatory network governing flavor formation in kiwifruit (Actinidia chinensis) . New Phytol. 2022; 233: 373-89.

[28]

Zhang Q, Wang L, Liu Z et al. Transcriptome and metabolome profiling unveil the mechanisms of Ziziphus jujuba Mill. Peel coloration. Food Chem. 2020; 312: 125903.

[29]

Wang M, Chen L, Liang Z et al. Metabolome and transcriptome analyses reveal chlorophyll and anthocyanin metabolism pathway associated with cucumber fruit skin color. BMC Plant Biol. 2020; 20: 386.

[30]

Serrano A, Espinoza C, Poblete E et al. Omics approaches for understanding grapevine berry development: regulatory networks associated with endogenous processes and environmental responses. Front Plant Sci. 2017; 8: 1486.

[31]

Lin Q, Wang C, Dong W et al. Transcriptome and metabolome analyses of sugar and organic acid metabolism in Ponkan (Citrus reticulata) fruit during fruit maturation . Gene. 2015; 554: 64-74.

[32]

Ma X, Zheng B, Ma Y et al. Carotenoid accumulation and expression of carotenoid biosynthesis genes in mango flesh during fruit development and ripening. Sci Hortic. 2018; 237: 201-6.

[33]

Vasquez-Caicedo AL, Heller A, Neidhart S et al. Chromoplast morphology and beta-carotene accumulation during postharvest ripening of mango cv. ’Tommy Atkins’. J Agric Food Chem. 2006; 54: 5769-76.

[34]

Pott I, Breithaupt DE, Carle R . Detection of unusual carotenoid esters in fresh mango (Mangifera indica L. cv. ’Kent’) . Phytochemistry. 2003; 64: 825-9.

[35]

Li L, Wu H, Ma X et al. Transcriptional mechanism of differential sugar accumulation in pulp of two contrasting mango (Mangifera indica L.) cultivars . Genomics. 2020; 112: 4505-15.

[36]

Vithana MDK, Singh Z, Johnson SK . Regulation of the levels of health promoting compounds: lupeol, mangiferin and phenolic acids in the pulp and peel of mango fruit: a review. J Sci Food Agric. 2019; 99: 3740-51.

[37]

Gómez-Lim MA . Mango fruit ripening: physiology and molecular biology. Acta Hortic. 1993; 341: 484-99.

[38]

Tharanathan RN, Yashoda HM, Prabha TN . Mango (Mangifera indica L.), ‘the king of fruits’-an overview . Food Rev Int. 2006; 22: 95-123.

[39]

Kondo S, Sungcome K, Setha S et al. ABA catabolism during development and storage in mangoes: influence of jasmonates. J Hortic Sci Biotechnol. 2004; 79: 891-6.

[40]

Zaharah SS, Singh Z . Abscisic acid modulates mango fruit ripening. Acta Hortic. 2012; 934: 913-9.

[41]

Hinai TZSA, Vreeburg RAM, Mackay CL et al. Fruit softening: evidence for pectate lyase action in vivo in date (Phoenix dactylifera) and rosaceous fruit cell walls . Ann Bot. 2021; 128: 511-25.

[42]

Jarvis MC, Briggs SPH, Knox JP . Intercellular adhesion and cell separation in plants. Plant Cell Environ. 2003; 26: 977-89.

[43]

Brummell DA . Cell wall disassembly in ripening fruit. Funct Plant Biol. 2006; 33: 103-19.

[44]

Krinsky NI, Johnso EJ . Carotenoid actions and their relation to health and disease. Mol Asp Med. 2005; 26: 459-516.

[45]

Davies KM . Genetic modification of plant metabolism for human health benefits. Mutat Res. 2007; 622: 122-37.

[46]

Della Penna D, Pogson BJ . Vitamin synthesis in plants: tocopherols and carotenoids. Annu Rev Plant Biol. 2006; 57: 711-38.

[47]

Li Y, Chen Y, Zhou L et al. MicroTom metabolic network: rewiring tomato metabolic regulatory network throughout the growth cycle. Mol Plant. 2020; 13: 1203-18.

[48]

Mercadante AZ, Rodriguez-Amaya DB, Britton G . HPLC and mass spectrometric analysis of carotenoids from mango. J Agric Food Chem. 1997; 45: 120-3.

[49]

Lee J, He K, Stolc V et al. Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell. 2007; 19: 731-49.

[50]

Gangappa SN, Botto JF . The multifaceted roles of HY5 in plant growth and development. Mol Plant. 2016; 9: 1353-65.

[51]

White PJ . Recent advances in fruit development and ripening: an overview. J Exp Bot. 2002; 53: 1995-2000.

[52]

Medlicott AP, Sigrist JMM, Reynolds SB et al. Effects of ethylene and acetylene on mango fruit ripening. Ann Appl Biol. 1987; 111: 439-44.

[53]

Reddy YV, Srivastava GC . Ethylene biosynthesis and respiration in mango fruits during ripening. Indian J Plant Physiol. 1999; 4: 32-5.

[54]

Ngamchuachit P, Barrett DM, Mitcham EJ . Effects of 1-methylcyclopropene and hot water quarantine treatment on quality of ‘Keitt’ mangos. J Food Sci. 2014; 79: C505-9.

[55]

Zaharah SS, Singh Z, Symons GM et al. Mode of action of abscisic acid in triggering ethylene biosynthesis and softening during ripening in mango fruit. Postharvest Biol Technol. 2013; 75: 37-44.

[56]

Zaharah SS, Singh Z, Symons GM et al. Role of brassinosteroids, ethylene, abscisic acid, and indole-3-acetic acid in mango fruit ripening. J Plant Growth Regul. 2012; 31: 363-72.

[57]

Silva APFB, Nascimento JROD, Lajolo FM et al. Starch mobilization and sucrose accumulation in the pulp of Keitt mangoes during postharvest ripening. J Food Biochem. 2008; 32: 384-95.

[58]

Candelario-Rodríguez HE, Zavala-García F, León JAR-D et al. Effect of high pressure processing on postharvest physiology of ‘Keitt’ mango. Postharvest Biol Technol. 2014; 94: 35-40.

[59]

Mitcham EJ, McDonald RE . Cell wall modification during ripening of ‘Keitt’ and ‘Tommy Atkins’ mango fruit. J Am Soc Hortic Sci. 1992; 117: 919-24.

[60]

Xin M, Li C, Khoo HE et al. Dynamic analyses of transcriptome and metabolic profiling: revealing molecular insight of aroma synthesis of mango (Mangifera indica L. var. Tainong) . Front Plant Sci. 2021; 12: 666805.

[61]

Tan L, Jin Z, Ge Y et al. Comprehensive ESI-Q TRAP-MS/MS based characterization of metabolome of two mango (Mangifera indica L.) cultivars from China . Sci Rep. 2020; 10: 20017.

[62]

Llorente B, D’Andrea L, Rodríguez-Concepción M . Evolutionary recycling of light signaling components in fleshy fruits: new insights on the role of pigments to monitor ripening. Front Plant Sci. 2016; 7: 263.

[63]

Wang W, Wang P, Li X et al. The transcription factor SlHY5 regulates the ripening of tomato fruit at both the transcriptional and translational levels. Hortic Res. 2021; 8: 83.

[64]

Zhao Y, Chen K, Dong W et al. Differential sensitivity of fruit pigmentation to ultraviolet light between two peach cultivars. Front Plant Sci. 2017; 8: 1552.

[65]

Zhang H, Li W, Wang H et al. Transcriptome profiling of light-regulated anthocyanin biosynthesis in the pericarp of litchi. Front Plant Sci. 2016; 7: 963.

[66]

An J, Qu F, Yao J et al. The bZIP transcription factor MdHY5 regulates anthocyanin accumulation and nitrate assimilation in apple. Hortic Res. 2017; 4: 17023.

[67]

Camacho-Vázquez C, Ruiz-May E, Guerrero-Analco JA et al. Filling gaps in our knowledge on the cuticle of mangoes (Mangifera indica) by analyzing six fruit cultivars: architecture/structure, postharvest physiology and possible resistance to fruit fly (Tephritidae) attack . Postharvest Biol Technol. 2019; 148: 83-96.

[68]

Carella A, Gianguzzi G, Scalisi A et al. Fruit growth stage transitions in two mango cultivars grown in a Mediterranean environment. Plants. 2021; 10: 1332.

[69]

Zhang Y, Gao Z, Hu M et al. Delay of ripening and senescence in mango fruit by 6-benzylaminopurine is associated with inhibition of ethylene biosynthesis and membrane lipid catabolism. Postharvest Biol Technol. 2022; 185: 111797.

[70]

Song J, Bian J, Xue N et al. Inter-species mRNA transfer among green peach aphids, dodder parasites, and cucumber host plants. Plant Divers. 2022; 44: 1-10.

[71]

Chen W, Xiong L, Gong L et al. A novel integrated method for large-scale detection, identification, and quantification of widely targeted metabolites: application in the study of rice metabolomics. Mol Plant. 2013; 6: 1769-80.

[72]

Fraga CG, Clowers BH, Moore RJ et al. Signature-discovery approach for sample matching of a nerve-agent precursor using liquid chromatography-mass spectrometry, XCMS, and chemometrics. Anal Chem. 2010; 82: 4165-73.

[73]

Zou S, Wu J, Shahid MQ et al. Identification of key taste components in loquat using widely targeted metabolomics. Food Chem. 2020; 323: 126822.

[74]

Chen C, Chen H, Zhang Y et al. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020; 13: 1194-202.

[75]

Li W, Zhu X, Zhang Q et al. SMRT sequencing generates the chromosome-scale reference genome of tropical fruit mango, Mangifera indica . bioRxiv. 2020. https://doi.org/10.1101/2020.02.22.960880.

[76]

Dobin A, Davis CA, Schlesinger F et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013; 29: 15-21.

[77]

Li B, Dewey CN . RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011; 12: 323.

[78]

Love MI, Huber W, Anders S . Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014; 15: 550-71.

[79]

Walvoort DJJ, Brus DJ, Gruijter JJ . An R package for spatial coverage sampling and random sampling from compact geographical strata by k-means. Comput Geosci. 2010; 36: 1261-7.

[80]

Langfelder P, Horvath S . WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics. 2008; 9: 559.

[81]

Shannon P, Markiel A, Ozier O et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003; 13: 2498-504.

[82]

Scholtz JJ, Visser B . Reference gene selection for qPCR gene expression analysis of rust-infected wheat. Physiol Mol Plant Pathol. 2013; 81: 22-5.

[83]

Kapila J, Rycke RD, Montagu MV et al. An Agrobacterium-mediated transient gene expression system for intact leaves. Plant Sci. 1997; 122: 101-8.

[84]

Abel S, Theologis A . Transient transformation of Arabidopsis leaf protoplasts: a versatile experimental system to study gene expression. Plant J. 1994; 5: 421-7.

[85]

Hellens RP, Allan AC, Friel EN et al. Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods. 2005; 1: 13.

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