Key message
The first transcriptome coupled to metabolite analyses reveals major trends during acerola fruit ripening and shed lights on ascorbate, ethylene signalling, cellular respiration, sugar accumulation, and softening key regulatory genes.
Abstract
Acerola is a fast growing and ripening fruit that exhibits high amounts of ascorbate. During ripening, the fruit experience high respiratory rates leading to ascorbate depletion and a quickly fragile and perishable state. Despite its growing economic importance, understanding of its developmental metabolism remains obscure due to the absence of genomic and transcriptomic data. We performed an acerola transcriptome sequencing that generated over 600 million reads, 40,830 contigs, and provided the annotation of 25,298 unique transcripts. Overall, this study revealed the main metabolic changes that occur in the acerola ripening. This transcriptional profile linked to metabolite measurements, allowed us to focus on ascorbate, ethylene, respiration, sugar, and firmness, the major metabolism indicators for acerola quality. Our results suggest a cooperative role of several genes involved in AsA biosynthesis (PMM, GMP1 and 3, GME1 and 2, GGP1 and 2), translocation (NAT3, 4, 6 and 6-like) and recycling (MDHAR2 and DHAR1) pathways for AsA accumulation in unripe fruits. Moreover, the association of metabolites with transcript profiles provided a comprehensive understanding of ethylene signalling, respiration, sugar accumulation and softening of acerola, shedding light on promising key regulatory genes. Overall, this study provides a foundation for further examination of the functional significance of these genes to improve fruit quality traits.
Similar content being viewed by others
Data availability
The sequencing project has been deposited at the SRA database under the accession number PRJNA473364. The acerola reference transcriptome has been deposited at DDBJ/EMBL/GenBank under the accession GHDH00000000.1.
References
Abeles FB, Takeda F (1990) Cellulase activity and ethylene in ripening strawberry and apple fruits. Sci Hortic (Amsterdam) 42:269–275. https://doi.org/10.1016/0304-4238(90)90050-O
Aboobucker SI, Suza WP, Lorence A (2017) Characterization of two Arabidopsis l-Gulono-1,4-lactone oxidases, AtGulLO3 and AtGulLO5, involved in ascorbate biosynthesis. React Oxyg Species 4:1–29. https://doi.org/10.20455/ros.2017.861
Abu-Sarra AF, Abu-Goukh AA (1992) Changes in pectinesterase, polygalacturonase and cellulase activity during mango fruit ripening. J Hort Sci 67:561–568. https://doi.org/10.1080/00221589.1992.11516284
Agius F, González-Lamothe R, Caballero JL et al (2003) Engineering increased vitamin C levels in plants by overexpression of a d-galacturonic acid reductase. Nat Biotechnol 21:177–181. https://doi.org/10.1038/nbt777
Alos E, Martinez-Fuentes A, Reig C et al (2017) Ethylene biosynthesis and perception during ripening of loquat fruit (Eriobotrya japonica Lindl.). J Plant Physiol 210:64–71. https://doi.org/10.1016/j.jplph.2016.12.008
Alós E, Rodrigo MJ, Zacarías L (2013) Transcriptomic analysis of genes involved in the biosynthesis, recycling and degradation of l-ascorbic acid in pepper fruits (Capsicum annuum L.). Plant Sci 207:2–11. https://doi.org/10.1016/j.plantsci.2013.02.007
Alós E, Rodrigo MJ, Zacarías L (2014) Differential transcriptional regulation of l-ascorbic acid content in peel and pulp of citrus fruits during development and maturation. Planta 239:1113–1128. https://doi.org/10.1007/s00425-014-2044-z
Altschul SF, Madden TL, Schäffer AA et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402. https://doi.org/10.1093/nar/25.17.3389
Alves Filho EG, Almeida FDL, Cavalcante RS et al (2016) 1H NMR spectroscopy and chemometrics evaluation of non-thermal processing of orange juice. Food Chem 204:102–107. https://doi.org/10.1016/j.foodchem.2016.02.121
Alves RE, Chitarra AB, Chitarra MIF (1995) Postharvest physiology of acerola (Malpighia emarginata D.C.) fruits: maturation changes, respiration activity and refrigerated storage at ambient and modified atmospheres. Acta Hortic 370:223–229. https://doi.org/10.17660/actahortic.1995.370.35
Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. In: Babraham Bioinforma. http://www.bioinformatics.babraham.ac.uk/projects/fastqc
Asif MH, Lakhwani D, Pathak S et al (2014) Transcriptome analysis of ripe and unripe fruit tissue of banana identifies major metabolic networks involved in fruit ripening process. BMC Plant Biol 14:316. https://doi.org/10.1186/s12870-014-0316-1
Atkinson RG, Johnston SL, Yauk YK et al (2009) Analysis of xyloglucan endotransglucosylase/hydrolase (XTH) gene families in kiwifruit and apple. Postharvest Biol Technol 51:149–157. https://doi.org/10.1016/j.postharvbio.2008.06.014
Badejo AA, Esaka M, Jeong ST, Goto-Yamamoto N (2007a) Molecular cloning and expression of GDP-d-mannose-3,5-epimerase during fruit ripening in acerola. Acta Hortic 763:91–98. https://doi.org/10.17660/actahortic.2007.763.12
Badejo AA, Jeong ST, Goto-Yamamoto N, Esaka M (2007b) Cloning and expression of GDP-d-mannose pyrophosphorylase gene and ascorbic acid content of acerola (Malpighia glabra L.) fruit at ripening stages. Plant Physiol Biochem 45:665–672. https://doi.org/10.1016/j.plaphy.2007.07.003
Badejo AA, Tanaka N, Esaka M (2008) Analysis of GDP-d-mannose pyrophosphorylase gene promoter from acerola (Malpighia glabra) and increase in ascorbate content of transgenic tobacco expressing the acerola gene. Plant Cell Physiol 49:126–132. https://doi.org/10.1093/pcp/pcm164
Badejo AA, Fujikawa Y, Esaka M (2009) Gene expression of ascorbic acid biosynthesis related enzymes of the Smirnoff-Wheeler pathway in acerola (Malpighia glabra). J Plant Physiol 166:652–660. https://doi.org/10.1016/j.jplph.2008.09.004
Badejo AA, Wada K, Gao Y et al (2012) Translocation and the alternative d-galacturonate pathway contribute to increasing the ascorbate level in ripening tomato fruits together with the d-mannose/l-galactose pathway. J Exp Bot 63:229–239. https://doi.org/10.1093/jxb/err275
Bairoch A, Boeckmann B (1991) The SWISS-PROT protein sequence data bank. Nucleic Acids Res 19:2247–2249. https://doi.org/10.1093/nar/19.suppl.2247
Balibrea ME, Martínez-Andújar C, Cuartero J et al (2006) The high fruit soluble sugar content in wild Lycopersicon species and their hybrids with cultivars depends on sucrose import during ripening rather than on sucrose metabolism. Funct Plant Biol 33:279–288. https://doi.org/10.1071/FP05134
Barry CS, Llop-Tous MI, Grierson D (2000) The regulation of 1-aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from system-1 to system-2 ethylene synthesis in tomato. Plant Physiol 123:979–986. https://doi.org/10.1104/pp.123.3.979
Biais B, Benard C, Beauvoit B et al (2014) Remarkable reproducibility of enzyme activity profiles in tomato fruits grown under contrasting environments provides a roadmap for studies of fruit metabolism. Plant Physiol 164:1204–1221. https://doi.org/10.1104/pp.113.231241
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Bower J, Holford P, Latché A, Pech JC (2002) Culture conditions and detachment of the fruit influence the effect of ethylene on the climacteric respiration of melon. Postharvest Biol Technol 26:135–146. https://doi.org/10.1016/S0925-5214(02)00007-8
Brummell DA, Labavitch JM (1997) Effect of antisense suppression of endopolygalacturonase activity on polyuronide molecular weight in ripening tomato fruit and in fruit homogenates. Plant Physiol 115:717–725. https://doi.org/10.1104/pp.115.2.717
Bulley S, Laing W (2016) The regulation of ascorbate biosynthesis. Curr Opin Plant Biol 33:15–22. https://doi.org/10.1016/j.pbi.2016.04.010
Bulley SM, Rassam M, Hoser D et al (2009) Gene expression studies in kiwifruit and gene over-expression in Arabidopsis indicates that GDP-l-galactose guanyltransferase is a major control point of vitamin C biosynthesis. J Exp Bot 60:765–778. https://doi.org/10.1093/jxb/ern327
Cação SM, Leite TF, Budzinski IG et al (2012) Gene expression and enzymatic activity of pectin methylesterase during fruit development and ripening in Coffea arabica L. Genet Mol Res 11:3186–3197. https://doi.org/10.4238/2012.September.3.7
Carrari F, Baxter C, Usadel B et al (2006) 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 142:1380–1396. https://doi.org/10.1104/pp.106.088534
Carrington CMS, King RAG (2002) Fruit development and ripening in Barbados cherry, Malpighia emarginata DC. Sci Hortic (Amsterdam) 92:1–7. https://doi.org/10.1016/S0304-4238(01)00268-0
Chardon F, Bedu M, Calenge F et al (2013) Leaf fructose content is controlled by the vacuolar transporter SWEET17 in Arabidopsis. Curr Biol 23:697–702. https://doi.org/10.1016/j.cub.2013.03.021
Chen H, Boutros PC (2011) VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R. BMC Bioinformatics 12:35. https://doi.org/10.1186/1471-2105-12-35
Christoffersen RE, Tucker ML, Laties GG (1984) Cellulase gene expression in ripening avocado fruit: the accumulation of cellulase mRNA and protein as demonstrated by cDNA hybridization and immunodetection. Plant Mol Biol 3:385–391. https://doi.org/10.1007/BF00033386
Colombié S, Beauvoit B, Nazaret C et al (2017) Respiration climacteric in tomato fruits elucidated by constraint-based modelling. New Phytol 213:1726–1739. https://doi.org/10.1111/nph.14301
Conesa A, Madrigal P, Tarazona S et al (2016) A survey of best practices for RNA-seq data analysis. Genome Biol 17:13. https://doi.org/10.1186/s13059-016-0881-8
Cordenunsi BR, Lajolo FM (1995) Starch breakdown during banana ripening: sucrose synthase and sucrose phosphate synthase. J Agric Food Chem 43:347–351. https://doi.org/10.1021/jf00050a016
Cruz-Hernández A, Gómez-Lim MA (1995) Alternative oxidase from mango (Mangifera indica, L.) is differentially regulated during fruit ripening. Planta 197:569–576. https://doi.org/10.1007/BF00191562
Cruz-Rus E, Amaya I, Sánchez-Sevilla JF et al (2011) Regulation of l-ascorbic acid content in strawberry fruits. J Exp Bot 62:4191–4201. https://doi.org/10.1093/jxb/err122
Da Silva Nunes W, De Oliveira CS, Alcantara GB (2016) Ethanol determination in frozen fruit pulps: an application of quantitative nuclear magnetic resonance. Magn Reson Chem 54:334–340. https://doi.org/10.1002/mrc.4383
Das P, Majumder AL (2018) Transcriptome analysis of grapevine under salinity and identification of key genes responsible for salt tolerance. Funct Integr Genomics 19(1):61–73. https://doi.org/10.1007/s10142-018-0628-6
Dautt-Castro M, Ochoa-Leyva A, Contreras-Vergara CA et al (2015) Mango (Mangifera indica L.) cv. Kent fruit mesocarp de novo transcriptome assembly identifies gene families important for ripening. Front Plant Sci 6:1–12. https://doi.org/10.3389/fpls.2015.00062
de Assis SA, Pedro Fernandes F, Martins ABG, de Faria Oliveira OMM (2008) Acerola: importance, culture conditions, production and biochemical aspects. Fruits 63:93–101. https://doi.org/10.1051/fruits:2007051
de Ong W, Voo LYC, Kumar VS (2012) De novo assembly, characterization and functional annotation of pineapple fruit transcriptome through massively parallel sequencing. PLoS ONE. https://doi.org/10.1371/journal.pone.0046937
Del-Saz NF, Ribas-Carbo M, McDonald AE et al (2018) An in vivo perspective of the role(s) of the alternative oxidase pathway. Trends Plant Sci 23:206–219. https://doi.org/10.1016/j.tplants.2017.11.006
Delva L, Schneider RG (2013) Acerola (Malpighia emarginata DC): production, postharvest handling, nutrition, and biological activity. Food Rev Int 29:107–126. https://doi.org/10.1080/87559129.2012.714433
Di Matteo A, Giovane A, Raiola A et al (2005) Structural basis for the interaction between pectin methylesterase and a specific inhibitor protein. Plant Cell Online 17:849–858. https://doi.org/10.1105/tpc.104.028886
Do Nascimento JR, Cordenunsi BR, Lajolo FM, Alcocer MJC (1997) Banana sucrose-phosphate synthase gene expression during fruit ripening. Planta 203:283–288. https://doi.org/10.1007/s004250050193
Do Nascimento JRO, Júnior AV, Bassinello PZ et al (2006) Beta-amylase expression and starch degradation during banana ripening. Postharvest Biol Technol 40:41–47. https://doi.org/10.1016/j.postharvbio.2005.11.008
Eltelib HA, Badejo AA, Fujikawa Y, Esaka M (2011) Gene expression of monodehydroascorbate reductase and dehydroascorbate reductase during fruit ripening and in response to environmental stresses in acerola (Malpighia glabra). J Plant Physiol 168:619–627. https://doi.org/10.1016/j.jplph.2010.09.003
Eltelib HA, Fujikawa Y, Esaka M (2012) Overexpression of the acerola (Malpighia glabra) monodehydroascorbate reductase gene in transgenic tobacco plants results in increased ascorbate levels and enhanced tolerance to salt stress. S Afr J Bot 78:295–301. https://doi.org/10.1016/j.sajb.2011.08.005
Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2:953–971. https://doi.org/10.1038/nprot.2007.131
Etienne A, Génard M, Lobit P et al (2013) What controls fleshy fruit acidity? A review of malate and citrate accumulation in fruit cells. J Exp Bot 64:1451–1469. https://doi.org/10.1093/jxb/ert035
Fabi JP, Broetto SG, Da Silva SLGL et al (2014) Analysis of papaya cell wall-related genes during fruit ripening indicates a central role of polygalacturonases during pulp softening. PLoS ONE. https://doi.org/10.1371/journal.pone.0105685
Fan H, Xiao Y, Yang Y et al (2013) RNA-Seq analysis of Cocos nucifera: transcriptome sequencing and de novo assembly for subsequent functional genomics approaches. PLoS ONE 8:1–10. https://doi.org/10.1371/journal.pone.0059997
Feng C, Chen M, Xu CJ et al (2012) Transcriptomic analysis of Chinese bayberry (Myrica rubra) fruit development and ripening using RNA-Seq. BMC Genomics 13:19. https://doi.org/10.1186/1471-2164-13-19
Ferreira DF (2014) Sisvar: a guide for its bootstrap procedures in multiple comparisons. Cienc Agrotecnol 38:109–112. https://doi.org/10.1590/S1413-70542014000200001
Freitas VS, de Souza Miranda R, Costa JH et al (2018) Ethylene triggers salt tolerance in maize genotypes by modulating polyamine catabolism enzymes associated with H2O2 production. Environ Exp Bot 145:75–86. https://doi.org/10.1016/j.envexpbot.2017.10.022
Gillaspy GE (2011) The cellular language of myo-inositol signaling. New Phytol 92:823–839. https://doi.org/10.1111/j.1469-8137.2011.03939.x
Giovannoni J, Nguyen C, Ampofo B et al (2017) The epigenome and transcriptional dynamics of fruit ripening. Annu Rev Plant Biol 68:61–84. https://doi.org/10.1146/annurev-arplant-042916-040906
Gómez-García MDR, Ochoa-Alejo N (2016) Predominant role of the l-galactose pathway in l-ascorbic acid biosynthesis in fruits and leaves of the Capsicum annuum L. chili pepper. Rev Bras Bot 39:157–168. https://doi.org/10.1007/s40415-015-0232-0
Goodenough PW, Prosser IM, Young K (1985) Nadp-linked malic enzyme and malate metabolism in aging tomato fruit. Phytochemistry 24:1157–1162. https://doi.org/10.1016/S0031-9422(00)81093-6
Grabherr MG, Haas BJ, Yassour M et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652. https://doi.org/10.1038/nbt.1883
Hanamura T, Uchida E, Aoki H (2008) Changes of the composition in acerola (Malpighia emarginata DC.) fruit in relation to cultivar, growing region and maturity. J Sci Food Agric 88:1813–1820. https://doi.org/10.1002/jsfa.3285
Hellemans J, Mortier G, De Paepe A et al (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8:R19. https://doi.org/10.1186/gb-2007-8-2-r19
Holtzapffel RC, Finnegan PM, Millar AH et al (2002) Mitochondrial protein expression in tomato fruit during on-vine ripening and cold storage. Funct Plant Biol 29:827–834. https://doi.org/10.1071/PP01245
Horemans N, Szarka A, De Bock M et al (2009) Dehydroascorbate and glucose are taken up into Arabidopsis thaliana cell cultures by two distinct mechanisms. FEBS Lett 6:247–253. https://doi.org/10.1111/j.1743-6109.2008.01122.x.Endothelial
Horton P, Park K-J, Obayashi T, Fujita N et al (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587. https://doi.org/10.1093/nar/gkm259
Hotelling H (1933) Analysis of a complex of statistical variables into principal components. J Educ Psychol 24:417–441. https://doi.org/10.1037/h0071325
Hu XM, Shi CY, Liu X et al (2015) Genome-wide identification of citrus ATP-citrate lyase genes and their transcript analysis in fruits reveals their possible role in citrate utilization. Mol Genet Genomics 290:29–38. https://doi.org/10.1007/s00438-014-0897-2
Huang M, Xu Q, Deng XX (2014) l-Ascorbic acid metabolism during fruit development in an ascorbate-rich fruit crop chestnut rose (Rosa roxburghii Tratt). J Plant Physiol 171:1205–1216. https://doi.org/10.1016/j.jplph.2014.03.010
Hunter S, Apweiler R, Attwood TK et al (2009) InterPro: the integrative protein signature database. Nucleic Acids Res 37:211–215. https://doi.org/10.1093/nar/gkn785
Jimenez-Bermudez S, Redondo-Nevado J, Munoz-Blanco J et al (2002) Manipulation of strawberry fruit softening by antisense expression of a pectate lyase gene. Plant Physiol 128:751–759. https://doi.org/10.1104/pp.010671
Karlova R, Rosin FM, Busscher-Lange J et al (2011) Transcriptome and metabolite profiling show that APETALA2a is a major regulator of tomato fruit ripening. Plant Cell 23:923–941. https://doi.org/10.1105/tpc.110.081273
Kevany BM, Tieman DM, Taylor MG et al (2007) Ethylene receptor degradation controls the timing of ripening in tomato fruit. Plant J 51:458–467. https://doi.org/10.1111/j.1365-313X.2007.03170.x
Klann EM, Chetelat RT, Bennett AB (1993) Expression of acid invertase gene controls sugar composition in tomato (Lycopersicon) fruit. Plant Physiol 103:863–870. https://doi.org/10.1104/pp.103.3.863
Klann EM, Hall B, Bennett AB (1994) Antisense acid invertase (TW 7) gene alters soluble sugar composition and size in transgenic tomato fruit. Plant Physiol 11:330. https://doi.org/10.1104/pp.112.3.1321
Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 45:41–59. https://doi.org/10.1146/annurev-genet-110410-132507
Klemens PAW, Patzke K, Trentmann O et al (2014) Overexpression of a proton-coupled vacuolar glucose exporter impairs freezing tolerance and seed germination. New Phytol 202:188–197. https://doi.org/10.1111/nph.12642
Klosterhoff RR, Bark JM, Glänzel NM et al (2018) Structure and intracellular antioxidant activity of pectic polysaccharide from acerola (Malpighia emarginata). Int J Biol Macromol 106:473–480. https://doi.org/10.1016/j.ijbiomac.2017.08.032
Koch JL, Nevins DJ (1989) Tomato fruit cell wall: use of purified tomato polygalacturonase and pectinmethylesterase to identify developmental changes in pectins. Plant Physiol 91:816–822
Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. https://doi.org/10.1186/gb-2009-10-3-r25
Lazan H, Selamat MK, Ali ZM (1995) β-Galactosidase, polygalacturonase and pectinesterase in differential softening and cell wall modification during papaya fruit ripening. Physiol Plant 95:106–112. https://doi.org/10.1111/j.1399-3054.1995.tb00815.x
Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform. https://doi.org/10.1186/1471-2105-12-323
Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659. https://doi.org/10.1093/bioinformatics/btl158
Li T, Jiang Z, Zhang L et al (2016) Apple (Malus domestica) MdERF2 negatively affects ethylene biosynthesis during fruit ripening by suppressing MdACS1 transcription. Plant J 88:735–748. https://doi.org/10.1111/tpj.13289
Lima LCO, Chitarra BA, Chitarra MIF (2001) Changes in amylase activity starch and sugars contents in mango fruits pulp Cv. Tommy Atkins with spongy tissue. Braz Arch Biol Technol 59:59–62. https://doi.org/10.1590/S1516-89132001000100008
Linster CL, Clarke SG (2008) l-Ascorbate biosynthesis in higher plants: the role of VTC2. Trends Plant Sci 13(11):567–573. https://doi.org/10.1016/j.tplants.2008.08.005
Liu M, Pirrello J, Chervin C et al (2015) Ethylene control of fruit ripening: revisiting the complex network of transcriptional regulation. Plant Physiol 169:2380–2390. https://doi.org/10.1104/pp.15.01361
Liu M, Lima Gomes B, Mila I et al (2016) Comprehensive profiling of ethylene response factors expression identifies ripening-associated ERF genes and their link to key regulators of fruit ripening in tomato (Solanum lycopersicum). Plant Physiol 170:1732–1744. https://doi.org/10.1104/pp.15.01859
Loewus FA, Murthy PPN (2000) myo-Inositol metabolism in plants. Plant Sci 150:1–19. https://doi.org/10.1016/S0168-9452(99)00150-8
Lorence A, Chevone BI, Mendes P, Nessler CL (2004) myo-Inositol oxygenase offers a possible entry point into plant ascorbate biosynthesis. Plant Physiol 134:1200–1205. https://doi.org/10.1104/pp.103.033936
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:1–21. https://doi.org/10.1186/s13059-014-0550-8
Maria T, Tsaniklidis G, Delis C et al (2016) Gene transcript accumulation and enzyme activity of β-amylases suggest involvement in the starch depletion during the ripening of cherry tomatoes. Plant Gene 5:8–12. https://doi.org/10.1016/j.plgene.2015.10.004
Marshall OJ (2004) PerlPrimer: cross-platform, graphical primer design for standard, bisulphite and real-time PCR. Bioinformatics 20:2471–2472. https://doi.org/10.1093/bioinformatics/bth254
Martínez-López LA, Ochoa-Alejo N, Martínez O (2014) Dynamics of the chili pepper transcriptome during fruit development. BMC Genomics 15:1–18. https://doi.org/10.1186/1471-2164-15-143
Mathooko FM, Tsunashima Y, Owino WZO et al (2001) Regulation of genes encoding ethylene biosynthetic enzymes in peach (Prunus persica L.) fruit by carbon dioxide and 1-methylcyclopropene. Postharvest Biol Technol 21:265–281. https://doi.org/10.1016/S0925-5214(00)00158-7
Maurino VG, Grube E, Zielinski J et al (2006) Identification and expression analysis of twelve members of the nucleobase-ascorbate transporter (NAT) gene family in Arabidopsis thaliana. Plant Cell Physiol 47:1381–1393. https://doi.org/10.1093/pcp/pcl011
McGettigan PA (2013) Transcriptomics in the RNA-seq era. Curr Opin Chem Biol 17:4–11. https://doi.org/10.1016/j.cbpa.2012.12.008
Miao H, Sun P, Liu W et al (2014) Identification of genes encoding granule-bound starch synthase involved in amylose metabolism in banana fruit. PLoS ONE 9:1–9. https://doi.org/10.1371/journal.pone.0088077
Miao H, Sun P, Liu Q et al (2017) Soluble starch synthase III-1 in amylopectin metabolism of banana fruit: characterization, expression, enzyme activity, and functional analyses. Front Plant Sci 8:1–12. https://doi.org/10.3389/fpls.2017.00454
Minoia S, Boualem A, Marcel F et al (2015) Induced mutations in tomato SlExp1 alter cell wall metabolism and delay fruit softening. Plant Sci 242:195–202. https://doi.org/10.1016/j.plantsci.2015.07.001
Moriya Y, Itoh M, Okuda S et al (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:182–185. https://doi.org/10.1093/nar/gkm321
Muñoz-Bertomeu J, Miedes E, Lorences EP (2013) Expression of xyloglucan endotransglucosylase/hydrolase (XTH) genes and XET activity in ethylene treated apple and tomato fruits. J Plant Physiol 170:1194–1201. https://doi.org/10.1016/j.jplph.2013.03.015
Nakatsuka A, Murachi S, Okunishi H et al (1998) Differential expression and internal feedback regulation of 1-aminocyclopropane-1-carboxylate synthase, 1-aminocyclopropane-1-carboxylate oxidase, and ethylene receptor genes in tomato fruit during development and ripening. Plant Physiol 118:1295–1305. https://doi.org/10.1104/pp.118.4.1295
Nardi CF, Villarreal NM, Opazo MC et al (2014) Expression of FaXTH1 and FaXTH2 genes in strawberry fruit. Cloning of promoter regions and effect of plant growth regulators. Sci Hortic (Amsterdam) 165:111–122. https://doi.org/10.1016/j.scienta.2013.10.035
Nguyen-Quoc B, N’Tchobo H, Foyer CH, Yelle S (1999) Overexpression of sucrose phosphate synthase increases sucrose unloading in transformed tomato fruit. J Exp Bot 50:785–791. https://doi.org/10.1093/jxb/50.335.785
Nishikimi M, Koshizaka T, Ozawa T, Yagi K (1988) Occurrence in humans and guinea pigs of the gene related to their missing enzyme l-gulono-y-lactone oxidase. Arch Biochem Biophys 267:842–846
Nordey T, Léchaudel M, Génard M, Joas J (2016) Factors affecting ethylene and carbon dioxide concentrations during ripening: incidence on final dry matter, total soluble solids content and acidity of mango fruit. J Plant Physiol 196–197:70–78. https://doi.org/10.1016/j.jplph.2016.03.008
Ogata H, Goto S, Sato K et al (1999) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 27:29–34. https://doi.org/10.1093/nar/27.1.29
Oliveira LDS, Moura CFH, De Brito ES et al (2012) Antioxidant metabolism during fruit development of different acerola (Malpighia emarginata D.C) clones. J Agric Food Chem 60:7957–7964. https://doi.org/10.1021/jf3005614
Oliveira MG, Mazorra LM, Souza AF et al (2015) Involvement of AOX and UCP pathways in the post-harvest ripening of papaya fruits. J Plant Physiol 189:42–50. https://doi.org/10.1016/j.jplph.2015.10.001
Osorio S, Fernie AR (2013) Biochemistry of fruit ripening. In: Seymour GB, Poole M, Giovannoni JJ, Tucker GA (eds) The molecular biology and biochemistry of fruit ripening. Wiley-Blackwell, Oxford, pp 1–13
Paniagua C, Posé S, Morris VJ et al (2014) Fruit softening and pectin disassembly: an overview of nanostructural pectin modifications assessed by atomic force microscopy. Ann Bot 114:1375–1383. https://doi.org/10.1093/aob/mcu149
Paull RE, Chen NJ, Turano H et al (2011) Tropical fruit genomes and postharvest technology. Acta Hortic 875:237–244. https://doi.org/10.17660/actahortic.2011.906.30
Plaza L, Crespo I, de Pascual-Teresa S et al (2011) Impact of minimal processing on orange bioactive compounds during refrigerated storage. Food Chem 124:646–651. https://doi.org/10.1016/j.foodchem.2010.06.089
Powell ALT, Kalamaki MS, Kurien PA et al (2003) Simultaneous transgenic suppression of LePG and LeExp1 influences fruit texture and juice viscosity in a fresh market tomato variety. J Agric Food Chem 51:7450–7455. https://doi.org/10.1021/jf034165d
Prakash A, Baskaran R (2018) Acerola, an untapped functional superfruit: a review on latest frontiers. J Food Sci Technol 55:3373–3384. https://doi.org/10.1007/s13197-018-3309-5
Prasanna V, Prabha TN, Tharanathan RN (2007) Fruit ripening phenomena-an overview. Crit Rev Food Sci Nutr 47:1–19. https://doi.org/10.1080/10408390600976841
Pruitt KD, Tatusova T, Maglott DR (2007) NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 35:501–504. https://doi.org/10.1093/nar/gkl842
Quesada MA, Blanco-Portales R, Pose S et al (2009) Antisense down-regulation of the FaPG1 gene reveals an unexpected central role for polygalacturonase in strawberry fruit softening. Plant Physiol 150:1022–1032. https://doi.org/10.1104/pp.109.138297
Radzio JA, Lorence A, Chevone BI, Nessler CL (2003) l-Gulono-1,4-lactone oxidase expression rescues vitamin C-deficient Arabidopsis (vtc) mutants. Plant Mol Biol 53:837–844. https://doi.org/10.1023/B:PLAN.0000023671.99451.1d
Renato M, Pateraki I, Boronat A, Azcon-Bieto J (2014) Tomato fruit chromoplasts behave as respiratory bioenergetic organelles during ripening. Plant Physiol 166:920–933. https://doi.org/10.1104/pp.114.243931
Rigano MM, Lionetti V, Raiola A et al (2018) Pectic enzymes as potential enhancers of ascorbic acid production through the d-galacturonate pathway in Solanaceae. Plant Sci 266:55–63. https://doi.org/10.1016/j.plantsci.2017.10.013
Robinson MD, McCarthy DJ, Smyth GK (2009) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. https://doi.org/10.1093/bioinformatics/btp616
Roe B, Bruemmer JH (1981) Changes in pectic substances and enzymes during ripening and storage of “Keitt” mangos. J Food Sci 46:186–189. https://doi.org/10.1111/j.1365-2621.1981.tb14560.x
Ruan Y-L (2014) Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol 65:33–67. https://doi.org/10.1146/annurev-arplant-050213-040251
Ruggieri V, Bostan H, Barone A et al (2016) Integrated bioinformatics to decipher the ascorbic acid metabolic network in tomato. Plant Mol Biol 91:397–412. https://doi.org/10.1007/s11103-016-0469-4
Schaffer AA, Petreikov M (1997) Sucrose-to-starch metabolism in tomato fruit undergoing transient starch accumulation. Plant Physiol 113:739–746. https://doi.org/10.1104/pp.113.3.739
Schultz J, Copley RR, Doerks T et al (2000) SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res 28:231–234
Sheehy RE, Kramer M, Hiatt WR (1988) Reduction of polygalacturonase activity in tomato fruit by antisense RNA. Proc Natl Acad Sci 85:8805–8809. https://doi.org/10.1073/pnas.85.23.8805
Shellie KC, Saltveit ME (1993) The lack of a respiratory rise in muskmelon fruit ripening on the plant challenges the definition of climacteric behaviour. J Exp Bot 44:1403–1406. https://doi.org/10.1093/jxb/44.8.1403
Shi T, Sun J, Wu X et al (2018) Transcriptome analysis of Chinese bayberry (Myrica rubra Sieb. et Zucc.) fruit treated with heat and 1-MCP. Plant Physiol Biochem 133:40–49. https://doi.org/10.1016/j.plaphy.2018.10.022
Slewinski TL (2011) Diverse functional roles of monosaccharide transporters and their homologs in vascular plants: a physiological perspective. Mol Plant 4:641–662. https://doi.org/10.1093/mp/ssr051
Spraul M, Schütz B, Humpfer E et al (2009) Mixture analysis by NMR as applied to fruit juice quality control. Magn Reson Chem 47:S130–S137. https://doi.org/10.1002/mrc.2528
Sweetman C, Deluc LG, Cramer GR et al (2009) Regulation of malate metabolism in grape berry and other developing fruits. Phytochemistry 70:1329–1344. https://doi.org/10.1016/j.phytochem.2009.08.006
Tian T, Liu Y, Yan H et al (2017) AgriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res 45:W122–W129. https://doi.org/10.1093/nar/gkx382
Truffault V, Fry SC, Stevens RG, Gautier H (2017) Ascorbate degradation in tomato leads to accumulation of oxalate, threonate and oxalyl threonate. Plant J 89:996–1008. https://doi.org/10.1111/tpj.13439
Tucker GA (1993) Introduction. In: Seymour GB, Taylor JE, Tucker GA (eds) Biochemistry of fruit ripening, 1st edn. Chapman and Hall, London, pp 1–51
Uluisik S, Chapman NH, Smith R et al (2016) Genetic improvement of tomato by targeted control of fruit softening. Nat Biotechnol 34:950–952. https://doi.org/10.1038/nbt.3602
Van de Poel B, Van Der Straeten D (2014) 1-Aminocyclopropane-1-carboxylic acid (ACC) in plants: more than just the precursor of ethylene! Front Plant Sci 5:1–11. https://doi.org/10.3389/fpls.2014.00640
Van de Poel B, Bulens I, Markoula A et al (2012) Targeted systems biology profiling of tomato fruit reveals coordination of the yang cycle and a distinct regulation of ethylene biosynthesis during postclimacteric ripening. Plant Physiol 160:1498–1514. https://doi.org/10.1104/pp.112.206086
Vandesompele J, De Preter K, Pattyn F et al (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. https://doi.org/10.1186/gb-2002-3-7-research0034
Vimolmangkang S, Zheng H, Peng Q et al (2016) Assessment of sugar components and genes involved in the regulation of sucrose accumulation in peach fruit. J Agric Food Chem 64:6723–6729. https://doi.org/10.1021/acs.jafc.6b02159
Wang D, Yeats TH, Uluisik S et al (2018) Fruit softening: revisiting the role of pectin. Trends Plant Sci 23:302–310. https://doi.org/10.1016/j.tplants.2018.01.006
Wegrzyn T, MacRae E (1995) Alpha-amylase and starch degradation in kiwifruit. J Plant Physiol 147:19–28. https://doi.org/10.1016/S0176-1617(11)81407-0
Wei X, Liu F, Chen C et al (2014) The Malus domestica sugar transporter gene family: identifications based on genome and expression profiling related to the accumulation of fruit sugars. Front Plant Sci 5:1–15. https://doi.org/10.3389/fpls.2014.00569
Wen X, Zhang W, Feng Y, Yu X (2010) Cloning and characterization of a sucrose synthase-encoding gene from muskmelon. Mol Biol Rep 37:695–702. https://doi.org/10.1007/s11033-009-9539-x
Wheeler GL, Jones MA, Smirnoff N (1998) The biosynthetic pathway of vitamin C in higher plants. Nature 393:365–369
Winter H, Huber SC (2000) Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. Crit Rev Plant Sci 35:253–289. https://doi.org/10.1080/07352680091139178
Wishart DS, Jewison T, Guo AC et al (2013) HMDB 3.0—the human metabolome database in 2013. Nucleic Acids Res 41:801–807. https://doi.org/10.1093/nar/gks1065
Wolucka BA, Van Montagu M (2003) GDP-mannose 3′,5′-epimerase forms GDP-l-gulose, a putative intermediate for the de novo biosynthesis of vitamin C in plants. J Biol Chem 278:47483–47490. https://doi.org/10.1074/jbc.M309135200
Wu HX, Jia HM, Ma XW et al (2014) Transcriptome and proteomic analysis of mango (Mangifera indica Linn) fruits. J Proteomics 105:19–30. https://doi.org/10.1016/j.jprot.2014.03.030
Xiao YY, Chen JY, Kuang JF et al (2013) Banana ethylene response factors are involved in fruit ripening through their interactions with ethylene biosynthesis genes. J Exp Bot 64:2499–2510. https://doi.org/10.1093/jxb/ert108
Xu F, Yuan S, Zhang D-W, Lv XLH-H (2012) The role of alternative oxidase in tomato fruit ripening and its regulatory interaction with ethylene. J Exp Bot 63:5705–5716. https://doi.org/10.1093/jxb/ers226
Yang X, Song J, Campbell-Palmer L et al (2013) Effect of ethylene and 1-MCP on expression of genes involved in ethylene biosynthesis and perception during ripening of apple fruit. Postharvest Biol Technol 78:55–66. https://doi.org/10.1016/j.postharvbio.2012.11.012
Yang L, Huang W, Xiong F et al (2017) Silencing of SlPL, which encodes a pectate lyase in tomato, confers enhanced fruit firmness, prolonged shelf-life and reduced susceptibility to grey mould. Plant Biotechnol J 15:1544–1555. https://doi.org/10.1111/pbi.12737
Yang H, Liu J, Dang M et al (2018) Analysis of β-galactosidase during fruit development and ripening in two different texture types of apple cultivars. Front Plant Sci 9:1–13. https://doi.org/10.3389/fpls.2018.00539
Yu CS, Chen YC, Lu CH, Hwang JK (2006) Prediction of protein subcellular localizations. Proteins 64:643–651. https://doi.org/10.1109/ISDA.2008.306
Yuan XY, Wang RH, Zhao XD et al (2016) Role of the tomato non-ripening mutation in regulating fruit quality elucidated using iTRAQ protein profile analysis. PLoS ONE 11:1–21. https://doi.org/10.1371/journal.pone.0164335
Zeeman SC (2015) Carbohydrate metabolism. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants, 2nd edn. American Society of Plant Physiologists, Rockville
Zhang Q, Moore CS, Soole KL, Wiskich JT (2003) Over-reduction of cultured tobacco cells mediates changes in respiratory activities. Physiol Plant 119:183–191. https://doi.org/10.1034/j.1399-3054.2003.00182.x
Zhang C, Huang J, Li X (2016) Transcriptomic analysis reveals the metabolic mechanism of l-ascorbic acid in Ziziphus jujuba Mill. Front Plant Sci 7:1–11. https://doi.org/10.3389/fpls.2016.00122
Zhang Z, Wang N, Jiang S et al (2017) Analysis of the xyloglucan endotransglucosylase/hydrolase gene family during apple fruit ripening and softening. J Agric Food Chem 65:429–434. https://doi.org/10.1021/acs.jafc.6b04536
Zhu Q, Gao P, Liu S et al (2017) Comparative transcriptome analysis of two contrasting watermelon genotypes during fruit development and ripening. BMC Genomics 18:1–20. https://doi.org/10.1186/s12864-016-3442-3
Funding
This research was supported by CNPq, CAPES, FUNCAP and INCT- Frutos Tropicais (4653352014-4). CPS acknowledge doctoral grants from CNPq. JHC is grateful to CNPq for the Researcher fellowship (CNPq grant 309795/2017-6).
Author information
Authors and Affiliations
Contributions
This study was performed by the help of all authors. CPS and JHC conceived, designed and drafted the manuscript. CPS performed the experiments with help of KDCS, ALMR, RSM and LMAS. CPS performed the bioinformatics analysis of the transcriptomic data with the help of MCB. EGAF carried out the chemometrics analysis on 1H NMR data. CFHM helped with scientific advices in the design of field experiments. KMC helped in the design of 1H NMR assays, and with critical review of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflicts of interest to declare.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
dos Santos, C.P., Batista, M.C., da Cruz Saraiva, K.D. et al. Transcriptome analysis of acerola fruit ripening: insights into ascorbate, ethylene, respiration, and softening metabolisms. Plant Mol Biol 101, 269–296 (2019). https://doi.org/10.1007/s11103-019-00903-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-019-00903-0