Abstract
Sugar content and composition are critical to fruit development. Sucrose, a photosynthate unloaded to the fruit, is metabolized by sucrose synthase, which might play a dominant role in sucrose accumulation during strawberry fruit ripening. However, substantial evidence regarding the molecular mechanism underlying sucrose accumulation in strawberry fruit development is lacking. Here, a strawberry sucrose synthase gene, FaSS1, was cloned and identified. Its 2421-bp cDNA includes an intact open reading frame and encodes an 806 amino acid protein, in which sucrose synthase-related conserved domains were predicted by a homology analysis. Using tobacco rattle virus-induced gene silencing, the downregulation of FaSS1 transcripts significantly delayed fruit ripening, as evidenced by the changes of firmness, and soluble sugar and anthocyanin contents, as well as the transcripts of several ripening-related genes, including PE1, PL1, XYL2, CHS, CHI, and DFR. Furthermore, the mRNA expression level of FaSS1 was inhibited by abscisic acid or sucrose, but not by glucose after fruit disc incubation in vitro. In conclusion, FaSS1 plays an important role in the regulation of strawberry fruit ripening, and its expression could be inhibited by abscisic acid and sucrose.
Abbreviations
- SS/Sus:
-
Sucrose synthase
- ABA:
-
Abscisic acid
- SqRT-PCR:
-
Semiquantitative RT-PCR
- TRV:
-
Tobacco rattle virus
- PG1:
-
Polygalacturonase 1
- PL1:
-
Pectate lyase 1
- XYL2:
-
Xylitol dehydrogenase 2
- CHS:
-
Chalcone synthase
- CHI:
-
Chalcone isomerase
- DFR:
-
Dihydroflavonol 4-reductase
References
Angeles-Núñez JG, Tiessen A (2010) Arabidopsis sucrose synthase 2 and 3 modulate metabolic homeostasis and direct carbon towards starch synthesis in developing seeds. Planta 232:701–718
Angeles-Núñez JG1, Tiessen A (2012) Regulation of AtSUS2 and AtSUS3 by glucose and the transcription factor LEC2 in different tissues and at different stages of Arabidopsis seed development. Plant Mol Biol 78:377–392
Asano T, Kunieda N, Omura Y, Ibe H, Kawasaki T, Takano M, Sato M, Furuhashi H, Mujin T, Takaiwa F, Wu CY, Tada Y, Satozawa T, Sakamoto M, Shimada H (2002) Rice SPK, a calmodulin-like domain protein kinase, is required for storage product accumulation during seed development: phosphorylation of sucrose synthase is a possible factor. Plant Cell 14:619–628
Bastías A, López-Climent M, Valcárcel M, Rosello S, Gómez-Cadenas A, Casaretto JA (2011) Modulation of organic acids and sugar content in tomato fruits by an abscisic acid-regulated transcription factor. Physiol Plant 141(3):215–226
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
Ben L, Salzberg SL (2012) Fast gapped-read alignment with bowtie 2. Nat Method 9:357–359
Benjamini Yoav YD (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188
Borisjuk L, Walenta S, Rolletschek H, Mueller-Klieser W, Wobus U, Weber H (2002) Spatial analysis of plant metabolism: sucrose imaging within Vicia faba cotyledons reveals specific developmental patterns. Plant J 29:521–530
Chai YM, Zhang Q, Tian L, Li CL, Xing Y, Qin L, Shen YY (2013) Brassinosteroid is involved in strawberry fruit ripening. Plant Growth Regul 69:63–69
D’Aoust MA, Yelle S, Nguyen-Quoc B (1999) Antisense inhibition of tomato fruit sucrose synthase decreases fruit setting and the sucrose unloading capacity of young fruit. Plant Cell 11:2407–2418
Fallahi H, Scofield GN, Badger MR, Chow WS, Furbank RT, Ruan YL (2008) Localization of sucrose synthase in developing seed and siliques of Arabidopsis thaliana reveals diverse roles for SUS during development. J Exp Bot 59:3283–3295
Fu DQ, Zhu BZ, Zhu HL, Jiang WB, Luo YB (2005) Virus-induced gene silencing in tomato fruit. Plant J 43:299–308
Hou J, Jiang Q, Hao C, Wang Y, Zhang H, Zhang X (2014) Global selection on sucrose synthase haplotypes during a century of wheat breeding. Plant Physiol 164:1918–1929
Huber SC, Akazawa T (1986) A nove1 sucrose synthase pathway for sucrose degradation in cultured sycamore cells. Plant Physiol 81:1008–1013
Islam MZ, Hu XM, Jin LF, Liu YZ, Peng SA (2014) Genome-wide identification and expression profile analysis of citrus sucrose synthase genes: investigation of possible roles in the regulation of sugar accumulation. PLoS One 9(11):e113623
Jia HF, Chai YM, Li CL, Lu D, Luo JJ, Qin L, Shen YYY (2011) Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiol 157:188–199
Jia HF, Wang YH, Sun MZ, Li BB, Han Y, Zhan YX, Li XL, Ding N, Li C, Ji WS (2013) Sucrose functions as a signal involved in the regulation of strawberry fruit development and ripening. New Phytol 198:453–465
Jiang Y, Guo W, Zhu H, Ruan YL, Zhang T (2012) Overexpression of GhSusA1 increases plant biomass and improves cotton fiber yield and quality. Plant Biotechnol J 10(3):301–312
Karrer EE, Rodriguez RL (1992) Metabolic regulation of rice alpha-amylase and sucrose synthase genes in planta. Plant J 2:517–523
Kortstee AJ, Appeldoorn NJ, Oortwijn ME, Visser RG (2007) Differences in regulation of carbohydrate metabolism during early fruit development between domesticated tomato and two wild relatives. Planta 226:929–939
Li CL, Fang KF, Lei H, Xing Y, Shen YY (2012) Phloem unloading follows an extensive apoplastic pathway in developing strawberry fruit. J Hortic Sci Biotechnol 87:470–477
Li J, Baroja-Fernández E, Bahaji A, Muñoz FJ, Ovecka M, Montero M, Sesma MT, Alonso-Casajús N, Almagro G, Sánchez-López AM, Hidalgo M, Zamarbide M, Pozueta-Romero J (2013) Enhancing sucrose synthase activity results in increased levels of starch and ADP-glucose in maize (Zea mays L.) seed endosperms. Plant Cell Physiol 54:282–294
Liu Y, Schiff M, Dinesh-Kumar SP (2002) Virus-induced gene silencing in tomato. Plant J 31:777–786
Martínez-Esteso MJ, Sellés-Marchart S, Lijavetzky D, Pedreño MA, Bru-Martínez R (2011) A DIGE-based quantitative proteomic analysis of grape berry flesh development and ripening reveals key events in sugar and organic acid metabolism. J Exp Bot 62:2521–2569
Ming YL, Gui RQ, Jing J, Hui QY, Li HX, Jin ZX, Ren YZ (2012) Transcriptome sequencing and de novo analysis for bamboo using the illumina platform. Plos one 7:1–11
Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-SEq. Nat Method 5:621–628
Núñez JG, Kronenberger J, Wuillème S, Lepiniec L, Rochat C (2008) Study of AtSUS2 localization in seeds reveals a strong association with plastids. Plant Cell Physiol 49:1621–1626
Sreenivasulu N, Altschmied L, Radchuk V, Gubatz S, Wobus U, Weschke W (2004) Transcript profiles and deduced changes of metabolic pathways in maternal and filial tissues of developing barley grains. Plant J 37:539–553
Sun JH, Dong YH, Li CL, Shen YY (2015) Transcription and enzymatic analysis of beta-glucosidase VvBG1 in grape berry ripening. Plant Growth Regul 75:67–73
Sung SJ, Xu DP, Gelloway CM, Black CC (1988) A reassessment of glycolysis and gluconeogenesis in higher plants. Physiol Plant 72:650–654
Tian L, Jia HF, Li CL, Fan PG, Xing Y, Shen YY (2012) Sucrose accumulation during grape berry and strawberry fruit ripening is controlled predominantly by sucrose synthase activity. J Hortic Sci Biotechnol 87:661–667
Villarreal NM, Bustamante CA, Civello PM (2010) Effect of ethylene and 1-MCP treatments on strawberry fruit ripening. J Sci Food Agric 90:683–689
Wang Z, Fang B, Chen J, Zhang X, Luo Z, Huang L, Chen X, Li Y (2010) De novo assembly and characterization of root transcriptome using Illumina paired-end sequencing and development of SSR markers in sweet potato (Ipomoea batatas). BMC Genomic 11:726
Wang X, Peng F, Li M, Yang L, Li G (2012) Expression of a heterologous SnRK1 in tomato increases carbon assimilation, nitrogen uptake and modifies fruit development. J Plant Physiol 169:1173–1182
Wang XQ, Li LM, Yang PP, Gong CL (2014) The role of hexokinases from grape berries (Vitis vinifera L.) in regulating the expression of cell wall invertase and sucrose synthase genes. Plant Cell Rep 33:337–347
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
Yang Z, Wang T, Wang H, Huang X, Qin Y, Hu G (2013) Patterns of enzyme activities and gene expressions in sucrose metabolism in relation to sugar accumulation and composition in the aril of litchi chinensis sonn. J Plant Physiol 170:731–740
Zhang XM, Wang W, Du LQ, Xie JH, Yao YL, Sun GM (2012) Expression patterns, activities and carbohydrate-metabolizing regulation of sucrose phosphate synthase, sucrose synthase and neutral invertase in pineapple fruit during development and ripening. Int J Mol Sci 13:9460–9477
Acknowledgments
This work was supported the China National Science Foundation (Project 31471837, 31272144, 41473004) and the National Key Technology Supported Program of China (Project 2011BAD32B03), the Project of Construction of Innovative Teams and Teacher Career Development for Universities and Colleges under Beijing Municipality (Grant No. IDHT20140509), One Hundred Talent Program of Beijing Science and Technology (Grant No. LIRC201612), and Beijing Municipal Education Commission (Grant No. CEFF-PXM2016-014207-000038).
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Cheng Zhao, Li-Na Hua and Xiao-Feng Liu contributed equally to this work.
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Zhao, C., Hua, LN., Liu, XF. et al. Sucrose synthase FaSS1 plays an important role in the regulation of strawberry fruit ripening. Plant Growth Regul 81, 175–181 (2017). https://doi.org/10.1007/s10725-016-0189-4
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DOI: https://doi.org/10.1007/s10725-016-0189-4