Abstract
The impact of water deficit on sucrose metabolism in sink organs like the fruit remains poorly known despite the need to improve fruit crops resilience to drought in the face of climate change. The present study investigated the effects of water deficit on sucrose metabolism and related gene expression in tomato fruits, aiming to identify candidate genes for improving fruit quality upon low water availability. Tomato plants were subjected to irrigated control and water deficit (−60% water supply compared to control) treatments, which were applied from the first fruit set to first fruit maturity stages. The results have shown that water deficit significantly reduced fruit dry biomass and number, among other plant physiological and growth variables, but substantially increased the total soluble solids content. The determination of soluble sugars on the basis of fruit dry weight revealed an active accumulation of sucrose and concomitant reduction in glucose and fructose levels in response to water deficit. The complete repertoire of genes encoding sucrose synthase (SUSY1-7), sucrose-phosphate synthase (SPS1-4), and cytosolic (CIN1-8), vacuolar (VIN1-2) and cell wall invertases (WIN1-4) was identified and characterized, of which SlSUSY4, SlSPS1, SlCIN3, SlVIN2, and SlCWIN2 were shown to be positively regulated by water deficit. Collectively, these results show that water deficit regulates positively the expression of certain genes from different gene families related to sucrose metabolism in fruits, favoring the active accumulation of sucrose in this organ under water-limiting conditions.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Almadanim MC, Alexandre BM, Rosa MTG, Sapeta H, Leitão AE, Ramalho JC, Lam TT, Negrão S, Abreu IA, Oliveira MM (2017) Rice calcium-dependent protein kinase OsCPK17 targets plasma membrane intrinsic protein and sucrose-phosphate synthase and is required for a proper cold stress response. Plant Cell Environ 40:1197–1213. https://doi.org/10.1111/pce.12916
An X, Chen Z, Wang J, Ye M, Ji L, Wang J, Liao W, Ma H (2014) Identification and characterization of the Populus sucrose synthase gene family. Gene 539:58–67. https://doi.org/10.1016/j.gene.2014.01.062
Andersen CL, Jensen JL, Ørntoft TF (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64:5245–5250. https://doi.org/10.1158/0008-5472.CAN-04-0496
Bai C, Zuo J, Watkins CB, Wang Q, Liang H, Zheng Y, Liu M, Ji Y (2023) Sugar accumulation and fruit quality of tomatoes under water deficit irrigation. Postharvest Biol Technol 195:112112. https://doi.org/10.1016/j.postharvbio.2022.112112
Baud S, Vaultier MN, Rochat C (2004) Structure and expression profile of the sucrose synthase multigene family in Arabidopsis. J Exp Bot 55:397–409. https://doi.org/10.1093/jxb/erh047
Beckles DMB, Ong NH, Tamova LS, Uengwilai KL (2012) Biochemical factors contributing to tomato fruit sugar content: a review. Fruits 67:49–64. https://doi.org/10.1051/fruits/2011066
Bertin N, Guichard S, Leonardi C, Longuenesse JJ, Langlois D, Navez B (2000) Seasonal evolution of the quality of fresh glasshouse tomatoes under Mediterranean conditions, as affected by air vapour pressure deficit and plant fruit load. Ann Bot 85:741–750. https://doi.org/10.1006/anbo.2000.1123
Bilska-Kos A, Mytych J, Suski S, Magoń J, Ochodzki P, Zebrowski J (2020) Sucrose phosphate synthase (SPS), sucrose synthase (SUS) and their products in the leaves of Miscanthus × giganteus and Zea mays at low temperature. Planta 252:23. https://doi.org/10.1007/s00425-020-03421-2
Braun DM, Wang L, Ruan YL (2014) Understanding and manipulating sucrose phloem loading, unloading, metabolism, and signalling to enhance crop yield and food security. J Exp Bot 65:1713–1735. https://doi.org/10.1093/jxb/ert416
Castellarin SD, Pfeiffer A, Sivilotti P, Degan M, Peterlunger E, Di Gaspero G (2007) Transcriptional regulation of anthocyanin biosynthesis in ripening fruits of grapevine under seasonal water deficit. Plant Cell Environ 30:1381–1399. https://doi.org/10.1111/J.1365-3040.2007.01716.X
Castleden CK, Aoki N, Gillespie VJ, Macrae EA, Quick WP, Buchne P, Foyer CH, Furbank RT, Lunn JE (2004) Evolution and function of the sucrose-phosphate synthase gene families in wheat and other grasses. Plant Physiol 135:1753–1764. https://doi.org/10.1104/pp.104.042457
Dahiya DA, Saini R, Saini HS, Devi A (2017) Sucrose metabolism: controls the sugar sensing and generation of signalling molecules in plants. J Pharmacogn Phytochem 6:1563–1572
Eom SH, Rim Y, Hyun TK (2019) Genome-wide identification and evolutionary analysis of neutral/alkaline invertases in Brassica rapa. Biotechnol Biotec Eq 33:1158–1163. https://doi.org/10.1080/13102818.2019.1643784
Garchery C, Gest N, Do PT, Alhagdow M, Baldet P, Menard G, Rothan C, Massot C, Gautier H, Aarrouf J, Fernie AR, Stevens R (2013) A diminution in ascorbate oxidase activity affects carbonal location and improves yield in tomato under water deficit. Plant Cell Environ 36:159–175. https://doi.org/10.1111/j.1365-3040.2012.02564.x
Geigenberger P, Reimholz R, Deiting U, Sonnewald U, Stitt M (1999) Decreased expression of sucrose phosphate synthase strongly inhibits the water stress-induced synthesis of sucrose in growing potato tubers. Plant J 19:119–129. https://doi.org/10.1046/j.1365-313X.1999.00506.x
Godt DE, Roitsch T (1997) Regulation and tissue-specific distribution of mRNAs for three extracellular invertase isoenzymes of tomato suggests an important function in establishing and maintaining sink metabolism. Plant Physiol 115:273–282. https://doi.org/10.1104/pp.115.1.273
Granot D, Kelly G, Stein O, David-Schwartz R (2014) Substantial roles of hexokinase and fructokinase in the effects of sugars on plant physiology and development. J Exp Bot 65:809–819. https://doi.org/10.1093/jxb/ert400
Guo AY, Zhu QH, Chen X, Luo JC (2007) GSDS a gene structure display server. Hereditas 29:1023–1026. https://doi.org/10.1360/yc-007-1023
Hernandez-Garcia CM, Finer JJ (2014) Identification and validation of promoters and cis-acting regulatory elements. Plant Sci 217–218:109–119. https://doi.org/10.1016/j.plantsci.2013.12.007
Hirose T, Scofield GN, Terao T (2008) An expression analysis profile for the entire sucrose synthase gene family in rice. Plant Sci 174:534–543. https://doi.org/10.1016/j.plantsci.2008.02.009
Hockema BR, Etxeberria E (2001) Metabolic contributors to drought-enhanced accumulation of sugars and acids in oranges. J Am Soc Hortic Sci 126:599–605. https://doi.org/10.21273/jashs.126.5.599
Hou X, ZhangDuKangDavies WTSWJ (2020) Responses of water accumulation and solute metabolism in tomato fruit to water scarcity and implications for main fruit quality variables. J Exp Bot 71:1249–1264. https://doi.org/10.1093/jxb/erz526
Hyun TK, Eom SH, Kim J (2011) Genomic analysis and gene structure of the two invertase families in the domesticated apple (Malus × domestica Borkh). Plant Omics 4:391–399
Ji X, Van Den Ende W, Van Laere A, Cheng S, Bennett J (2005) Structure, evolution, and expression of the two invertase gene families of rice. J Mol Evol 60:615–634. https://doi.org/10.1007/s00239-004-0242-1
Jia H, Wang Y, Sun M, Li B, Han Y, Zhao Y, Li X, Ding N, Li C, Ji W, Jia W (2013) Sucrose functions as a signal involved in the regulation of strawberry fruit development and ripening. New Phytol 198:453–465. https://doi.org/10.1111/NPH.12176
Jia L, Zhang B, Mao C, Li J, Wu Y, Wu P, Wu Z (2008) OsCYT-INV1 for alkaline/neutral invertase is involved in root cell development and reproductivity in rice (Oryza sativa L.). Planta 228:51–59. https://doi.org/10.1007/s00425-008-0718-0
Jiang S, Chi Y, Wang J, Zhou J, Cheng Y, Zhang L, Ma A, Vanitha J, Ramachandran S (2015) Sucrose metabolism gene families and their biological functions. Sci Rep 5:17583. https://doi.org/10.1038/srep17583
Juárez-Colunga S, López-González C, Morales-Elías NC, Massange-Sánchez JA, Trachsel S, Tiessen A (2018) Genome-wide analysis of the invertase gene family from maize. Plant Mol Biol 97:385–406. https://doi.org/10.1007/s11103-018-0746-5
Kumar P, Rouphael Y, Cardarelli M, Cola G (2007) Vegetable grafting as a tool to improve drought resistance and water use efficiency. Front Plant Sci 8:1130. https://doi.org/10.3389/fpls.2017.01130
Le Roy K, Lammens W, Verhaest M, De Coninck B, Rabijns A, Van Laere A, Van Den Ende W (2007) Unraveling the difference between invertases and fructan exohydrolases: A single amino acid (Asp-239) substitution transforms Arabidopsis cell wall invertase1 into a fructan 1-exohydrolase. Plant Physiol 145:616–625. https://doi.org/10.1104/pp.107.105049
Li YC, Meng FR, Zhang CY, Zhang N, Sun MS, Ren JP, Niu HB, Wang X, Yin J (2012) Comparative analysis of water stress-responsive transcriptomes in drought-susceptible and -tolerant wheat (Triticum aestivum L.). J Plant Biol 55:349–360. https://doi.org/10.1007/s12374-011-0032-4
Liao WB, Li YY, Lu C, Peng M (2017) Expression of sucrose metabolism and transport genes in cassava petiole abscission zones in response to water stress. Biol Plant 61:219–226. https://doi.org/10.1007/s10535-016-0658-7
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Lunn JE, Macrae E (2003) New complexities in the synthesis of sucrose. Curr Opin Plant Biol 6:208–214. https://doi.org/10.1016/S1369-5266(03)00033-5
Lutfiyya LL, Xu N, Ordine RLD, Morrell JA, Miller PW, Duff SMG (2007) Phylogenetic and expression analysis of sucrose phosphate synthase isozymes in plants. J Plant Physiol 164:923–933. https://doi.org/10.1016/j.jplph.2006.04.014
Ma QJ, Sun MH, Lu J, Zhu XP, Gao WS, Hao YJ (2017) Ectopic expression of apple MdSUT2 gene influences development and abiotic stress resistance in tomato. Sci Hortic 220:259–266. https://doi.org/10.1016/j.scienta.2017.04.013
Meissner M, Orsini E, Ruschhaupt M, Melchinger AE, Hincha DK, Heyer AG (2013) Mapping quantitative trait loci for freezing tolerance in a recombinant inbred line population of Arabidopsis thaliana accessions Tenela and C24 reveals REVEILLE1 as negative regulator of cold acclimation. Plant Cell Environ 36:1256–1267. https://doi.org/10.1111/pce.12054
Mou W, Li D, Luo Z, Mao L, Ying T (2015) Transcriptomic analysis reveals possible influences of ABA on secondary metabolism of pigments, flavonoids and antioxidants in tomato fruit during ripening. PLoS ONE 10:e0129598. https://doi.org/10.1371/journal.pone.0129598
Nguyen-Quoc B, Foyer CH (2001) A role for “futile cycles” involving invertase and sucrose synthase in sucrose metabolism of tomato fruit. J Exp Bot 52:881–889. https://doi.org/10.1093/jexbot/52.358.881
Pagliuso D, Grandis A, Igarashi ES, Lam E, Buckeridge MS (2018) Correlation of apiose levels and growth rates in duckweeds. Front Chem 6:291. https://doi.org/10.3389/FCHEM.2018.00291
Prioul JL, Pelleschi S, Séne M, Thévenot C, Causse M, De Vienne D, Leonardi A (1999) From QTLs for enzyme activity to candidate genes in maize. J Exp Bot 50:1281–1288. https://doi.org/10.1093/jxb/50.337.1281
Qi X, Wu Z, Li J, Mo X, Wu S, Chu J, Wu P (2007) AtCYT-INV1, a neutral invertase, is involved in osmotic stress-induced inhibition on lateral root growth in Arabidopsis. Plant Mol Biol 64:575–587. https://doi.org/10.1007/s11103-007-9177-4
Ripoll J, Urban L, Brunel B, Bertin N (2016) Water deficit effects on tomato quality depend on fruit developmental stage and genotype. J Plant Physiol 190:26–35. https://doi.org/10.1016/j.jplph.2015.10.006
Ripoll J, Urban L, Staudt M, Lopez-Lauri F, Bidel LPR, Bertin N (2014) Water shortage and quality of fleshy fruits - making the most of the unavoidable. J Exp Bot 65:4097–4117. https://doi.org/10.1093/jxb/eru197
Roitsch T, González MC (2004) Function and regulation of plant invertases: sweet sensations. Trend Plant Sci 9:606–613. https://doi.org/10.1016/j.tplants.2004.10.009
Ruan Y (2014) Sucrose metabolism : gateway to diverse carbon use and sugar signaling. Ann Rev Plant Biol 65:33–67. https://doi.org/10.1146/annurev-arplant-050213-040251
Ruan YL, Llewellyn DJ, Liu Q, Xu SM, Wu LM, Wang L, Furbank RT (2008) Expression of sucrose synthase in the developing endosperm is essential for early seed development in cotton. Funct Plant Biol 35:382–393. https://doi.org/10.1071/FP08017
Saitou N, Nei M (1987) The neighbor-joining method: A new method for reconstruction of phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Scholander PF, Hammel HT, Bradstreet ED, Hemmingsen EA (1965) Sap pressure in vascular plants. Science 148:339–346. https://doi.org/10.1126/SCIENCE.148.3668.339
Seneweera SP, Basra AS, Barlow EW, Conroy JP (1995) Diurnal regulation of leaf blade elongation in rice by CO2. Is it related to sucrose-phosphate synthase activity. Plant Physiol 108:1471–1477. https://doi.org/10.1104/pp.108.4.1471
Siebeneichler TJ, Crizel RL, Camozatto GH, Paim BT, da Silva MR, Rombaldi CV, Galli V (2020) The postharvest ripening of strawberry fruits induced by abscisic acid and sucrose differs from their in vivo ripening. Food Chem 317:126407. https://doi.org/10.1016/j.foodchem.2020.126407
Stein O, Granot D (2018) Plant fructokinases: evolutionary, developmental, and metabolic aspects in sink tissues. Front Plant Sci 9:339. https://doi.org/10.3389/fpls.2018.00339
Sun J, Zhang J, Larue CT, Huber SC (2011) Decrease in leaf sucrose synthesis leads to increased leaf starch turnover and decreased RuBP regeneration-limited photosynthesis but not Rubisco-limited photosynthesis in Arabidopsis null mutants of SPSA1. Plant Cell Environ 34:592–604. https://doi.org/10.1111/j.1365-3040.2010.02265.x
Taylor P, Winter H, Huber SC (2000) Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. Crit Rev Plant Sci 1:31–67. https://doi.org/10.1080/07352680091139178
Terry LA, Chope GA, Bordonaba JG (2007) Effect of water deficit irrigation and inoculation with Botrytis cinerea on strawberry (Fragaria × ananassa) fruit quality. J Agr Food Chem 55:10812–10819. https://doi.org/10.1021/jf072101n
The Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641.
Thompson JD, Higgins DG, Gibson TJ (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680.
Tong X-l, Wang Z-y, Ma B-q, Zhang C-x, Zhu L-c, Ma F-w, Li M-j (2018) Structure and expression analysis of the sucrose synthase gene family in apple. J Integr Agr 17:847–856. https://doi.org/10.1016/S2095-3119(17)61755-6
Toroser D, Huber SC (1997) Protein phosphorylation as a mechanism for osmotic-stress activation of sucrose-phosphate synthase in spinach leaves. Plant Physiol 114:947–955. https://doi.org/10.1104/pp.114.3.947
Vargas WA, Pontis HG, Salerno GL (2007) Differential expression of alkaline and neutral invertases in response to environmental stresses: characterization of an alkaline isoform as a stress-response enzyme in wheat leaves. Planta 226:1535–1545. https://doi.org/10.1007/s00425-007-0590-3
Wan H, Wu L, Yang Y, Zhou G, Ruan Y (2018) Evolution of sucrose metabolism: the dichotomy of invertases and beyond. Trend Plant Sci 23:163–177. https://doi.org/10.1016/j.tplants.2017.11.001
Wang L, Ruan YL (2012) New insights into roles of cell wall invertase in early seed development revealed by comprehensive spatial and temporal expression patterns of GhCWIN1 in cotton. Plant Physiol 160:777–787. https://doi.org/10.1104/pp.112.203893
Wang Y, Liu L, Wang Y, Tao H, Fan J, Zhao Z, Guo Y (2019) Effects of soil water stress on fruit yield, quality and their relationship with sugar metabolism in ‘Gala’apple. Sci Hortic 258:108753. https://doi.org/10.1016/j.scienta.2019.108753
Wang Z, Wei P, Wu M, Xu Y, Li F, Luo Z, Zhang J, Chen A, Xie X, Cao P (2015) Analysis of the sucrose synthase gene family in tobacco: structure, phylogeny, and expression patterns. Planta 242:153–166. https://doi.org/10.1007/s00425-015-2297-1
Wei H, Chai S, Ru L, Pan L, Cheng Y, Ruan M, Ye Q, Wang R, Yao Z, Zhou G, Chen Y, Wan H (2020) New insights into the evolution and expression dynamics of invertase gene family in Solanum lycopersicum. Plant Growth Regul 92:205–217. https://doi.org/10.1007/s10725-020-00631-2
Welham T, Pike J, Horst I, Flemetakis E, Katinakis P, Kaneko T, Sato S, Tabata S, Perry J, Parniske M, Wang TL (2009) A cytosolic invertase is required for normal growth and cell development in the model legume, Lotus japonicus. J Exp Bot 60:3353–3365. https://doi.org/10.1093/jxb/erp169
Xiang L, Le Roy K, Bolouri-Moghaddam MR, Vanhaecke M, Lammens W, Rolland F, Van Den Ende W (2011) Exploring the neutral invertase-oxidative stress defence connection in Arabidopsis thaliana. J Exp Bot 62:3849–3862. https://doi.org/10.1093/jxb/err069
Xiao X, Tang C, Fang Y, Yang M, Zhou B, Qi J (2014) Structure and expression profile of the sucrose synthase gene family in the rubber tree: indicative of roles in stress response and sucrose utilization in the laticifers. FEBS J 281:291–305. https://doi.org/10.1111/febs.12595
Yoshida T, Anjos L, Medeiros DB, Araújo WL, Fernie AR, Daloso DM (2019) Insights into ABA-mediated regulation of guard cell primary metabolism revealed by systems biology approaches. Prog Biophys Mol Biol 146:37–49. https://doi.org/10.1016/j.pbiomolbio.2018.11.006
Zhang B, Tieman DM, Jiao C, Xu Y, Chen K, Fe Z, Giovannoni JJ, Klee HJ (2016) Chilling-induced tomato flavor loss is associated with altered volatile synthesis and transient changes in DNA methylation. P Natl Acad Sci USA 113:12580–12585. https://doi.org/10.1073/pnas.1613910113
Zhang C, Yu M, Ma R, Shen Z, Zhang B, Korir NK (2015) Structure, expression profile, and evolution of the sucrose synthase gene family in peach (Prunus persica). Acta Physiol Plant 37:81. https://doi.org/10.1007/s11738-015-1829-4
Zhang Y, Zeng D, Liu Y, Zhu W (2022) SlSPS, a sucrose phosphate synthase gene, mediates plant growth and thermotolerance in tomato. Horticulturae 8:491. https://doi.org/10.3390/horticulturae8060491
Zhu X, Wang M, Li X, Jiu S, Wang C, Fang J (2017) Genome-wide analysis of the sucrose synthase gene family in grape (Vitis vinifera): structure, evolution, and expression profiles. Genes 8:111. https://doi.org/10.3390/genes8040111
Zhu YJ, Komor E, Moore PH (1997) Sucrose accumulation in the sugarcane stem is regulated by the difference between the activities of soluble acid invertase and sucrose phosphate synthase. Plant Physiol 115:609–616. https://doi.org/10.1104/pp.115.2.609
Acknowledgements
We thank Dr. Marcos Silveira Buckeridge (IB-USP) for providing the HPAEC-PAD instrumental facilities.
Funding
This work was supported by research grant from CNPq (Process # 304878/2018–9). ACOB was recipient of a master's degree scholarship provided by CAPES Foundation (Brasília, DF, Brazil). MGMS was recipient of a Scientific initiation program (IC) scholarship provided by UESC. MGCC is a CNPq Research Fellow. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Author information
Authors and Affiliations
Contributions
ACOB, DSRJ and MGCC conceived and designed the experiments; ACOB, DSRJ, GCBS, MGMS, PHGAO, and AAC performed the experiments; ACOB, DSRJ, MGMS, LRC and AAC analyzed the experimental data; ACOB wrote the article; and LRC and MGCC revised the article. All the authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Barbosa, A.C.O., Rocha, D.S., Silva, G.C.B. et al. Dynamics of the sucrose metabolism and related gene expression in tomato fruits under water deficit. Physiol Mol Biol Plants 29, 159–172 (2023). https://doi.org/10.1007/s12298-023-01288-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12298-023-01288-7