Skip to main content
SpringerLink
Log in

Sugar metabolic changes in protein expression associated with different light quality combinations in tomato fruit

  • Original Paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Light quality is an important environmental factor that drives photosynthesis and regulates plant growth and development. The purpose of this study was to investigate effects of light quality on sugar metabolism of tomato fruit. Tomato variety ‘Micro-Tom’ was used as the test material. After a 30-day cultivation period, seedlings were moved to an artificial climate chamber and grown under different light conditions: ratio of red and blue light, 1:1 (RB11), ratio of red and blue light, 3:1 (RB31), ratio of red and blue light, 5:1 (RB51), ratio of red and blue light, 7:1 (RB71), and white light as the control (CK). Fruit were harvested at the mature green, breaker, and ripe stages. The soluble sugar, total soluble solids, glucose, fructose, and sucrose contents in developing tomato fruit were highest under the RB31 condition. To further investigate effects of light quality on tomato fruit sugar metabolism, proteomic analysis using total proteins extracted from the CK and RB31-treated tomato fruit revealed that nine, three, and two proteins related to sugar metabolism were differentially accumulated between the CK and RB31-treated fruit at mature green, breaker, and ripe stages, respectively. Seven of them were up-regulated and the rest were down-regulated. The transcript abundances of these corresponding genes were analyzed by qRT-PCR. The expression levels of 12 genes were consistent with the protein abundances, but expression levels of xylose isomerase and l-iditol 2-dehydrogenase did not correlate with their protein abundances.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Centeno DC, Osorio S, Nunes-Nesi A, Bertolo ALF, Carneiro RT, Araujo WL, Steinhauser MC, Michalska J, Rohrmann J, Geigenberger P, Oliver SN, Stitt M, Carrari F, Rose JK, Fernie AR (2011) Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening. Plant Cell 23:162–184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho MH, Jang A, Bhoo SH, Jeon JS, Hahn TR (2012) Manipulation of triose phosphate/phosphate translocator and cytosolic fructose-1,6-bisphosphatase, the key components in photosynthetic sucrose synthesis, enhances the source capacity of transgenic Arabidopsis plant. Photosynth Res 111:261–268

    Article  CAS  PubMed  Google Scholar 

  • Cope KR, Bugbee B (2013) Spectral effects of three types of white light-emitting diodes on plant growth and development: absolute versus relative amounts of blue light. HortScience 48:504–509

    Article  CAS  Google Scholar 

  • Dobarro I, Valladares F, Peco B (2010) Light quality and not quantity segregates germination of grazing increasers from decreasers in Mediterranean grasslands. Acta Oecol 36:74–79

    Article  Google Scholar 

  • Fatima B, Aftab MN, Haq IU (2016) Cloning, purification, and characterization of xylose isomerase from Thermotoga naphthophila RKU-10. J Basic Microbiol 56:949–962

    Article  CAS  PubMed  Google Scholar 

  • Faurobert M, Mihr C, Bertin N, Pawlowski T, Negroni L, Sommerer N, Causse M (2007) Major proteome variations associated with cherry tomato pericarp development and ripening. J Plant Physiol 143:1327–1346

    Article  CAS  Google Scholar 

  • Gao B, Yang ZC, Li WQ, Wang XX, Ding JJ, Geng FZ, Cai H, Wang DF (2015) Effects of three different red and blue LED light ratio on growth and quality of celery. Acta Agric Boreali-occident Sin 24:125–132

    Google Scholar 

  • Giliberto L, Perrotta G, Pallara P, Weller JL, Fraser PD, Bramley PM, Fiore A, Tavazza M, Giuliano G (2005) Manipulation of the blue light photoreceptor cryptochrome 2 in tomato affects vegetative development, flowering time, and fruit antioxidant content. Plant Physiol 137:199–208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gómez-Anduro G, Ceniceros-Ojeda E, Casados-Vázquez L, Bencivenni C, Sierra- Beltrán A, Murillo-Amador B, Tiessen A (2011) Genome-wide analysis of the beta-glucosidase gene family in maize (Zea mays L. var B73). Plant Mol Biol 77:159–183

    Article  CAS  PubMed  Google Scholar 

  • Götz S, García-Gómez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talon M, Dopazo J, Conesa A (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36:3420–3435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo YL (2013) The isolation and expression analysis of loquat PFP gene. Dissertation, Zhejiang A&F University

  • Iacona C, Muleo R (2010) Light quality affects in vitro adventitious rooting and ex vitro performance of cherry rootstock Colt. Sci Hortic 125:630–636

    Article  Google Scholar 

  • Kopsell DA, Kopsell DE (2008) Genetic and environmental factors affecting plant lutein/zeaxanthin. Agro Food Industry Hi Tech 19:44–46

    CAS  Google Scholar 

  • Lee SH, Tewari RK, Hahn EJ, Peak KY (2007) Photon flux density and light quality induce changes in growth, stomatal development, photosynthesis and transpiration of Withania Somnifera (L.) Dunal. plantlets. Plant Cell Tiss Organ Cult 90:141–151

    Article  CAS  Google Scholar 

  • Li Q, Kubota C (2009) Effects of supplemental light quality on growth and phytochemicals of baby leaf lettuce. Environ Exp Bot 67:59–64

    Article  CAS  Google Scholar 

  • Li Y, Xin GF, Wei M, Shi QH, Yang FJ, Wang XF (2017) Carbohydrate accumulation and sucrose metabolism responses in tomato seedling leaves when subjected to different light qualities. Sci Hortic 225:490–497

    Article  CAS  Google Scholar 

  • Lin KH, Huang MY, Huang WD, Hsu MH, Yang ZW, Yang CM (2013) The effects of red, blue, and white light-emitting diodes on the growth, development, and edible quality of hydroponically grown lettuce (Lactuca sativa L. var. capitata). Sci Hortic 150:86–91

    Article  Google Scholar 

  • Liu XY, Chang TT, Guo SR, Xu ZG, Chen WH (2010) Effect of irradiation with blue and red LED on fruit quality of cherry tomato during growth period. China Veg 22:21–27

    Google Scholar 

  • Liu Y, Song LL, Yu WW, Hu YY, Ma XH, Wu JS, Ying YQ (2015a) Light quality modifies camptothecin production and gene expressionof biosynthesis in Camptotheca acuminata Decne seedlings. Ind Crop Prod 66:137–143

    Article  CAS  Google Scholar 

  • Liu SJ, Lan JX, Zhou BH, Qin YX, Zhou YH, Xiao XH, Yang JH, Gou JQ, Qi JY, Huang YC, Tang CR (2015b) HbNIN2, a cytosolic alkaline/neutral-invertase, is responsible for sucrose catabolism in rubber-producing laticifers of Hevea brasiliensis (para rubber tree). New Phytol 206:709–725

    Article  CAS  PubMed  Google Scholar 

  • Lu N, Maruo T, Johkan M, Hohjo M, Tsukagoshi S, Ito Y, Ichimura T, Shinohara Y (2012) Effects of supplemental lighting with light-emitting diodes (LEDs) on tomato yield and quality of single-truss tomato plants grown at high planting density. Environ Control Biol 50:63–67

    Article  CAS  Google Scholar 

  • Mohapatra PK, Patro L, Raval MK, Ramaswamy NK, Biswal UC, Biswal B (2010) Senescence-induced loss in photosynthesis enhances cell wall β-glucosidase activity. Physiol Plant 138:346–355

    Article  CAS  PubMed  Google Scholar 

  • Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:W182–W185

    Article  PubMed  PubMed Central  Google Scholar 

  • Pan XQ, Zhu BZ, Zhu HL, Chen YX, Tian HQ, Luo YB, Fu DQ (2014) iTRAQ protein profile analysis of tomato green-ripe mutant reveals new aspects critical for fruit ripening. J Proteome Res 13:1979–1993

    Article  CAS  PubMed  Google Scholar 

  • Qi XD, Wei JM, Zhao MW, Peng HL, Zhang HE (2015) Relationship between fruit softening and the metabolism of sugar and starch and their related-gene expression in post-harvest ‘Jingbaili’ fruits. Sci Agric Sin 48:2591–2599

    CAS  Google Scholar 

  • Qu L, Xu Y, Ji DH, Chen CS, Xie CT (2015) Cloning and expression analysis of the cytosolic fructose-1,6-bisphosphatase gene from Pyropia haitanensis. J Appl Oceanogr 34:402–410

    Google Scholar 

  • Ramalho JC, Marques NC, Semedo JN, Matos MC, Quartin VL (2002) Photosynthetic performance and pigment composition of leaves from two tropical species is determined by light quality. Plant Biol 4:112–120

    Article  CAS  Google Scholar 

  • Rossignol M, Peltier JB, Mock HP, Matros A, Maldonado AM, Jorrín JV (2006) Plant proteome analysis: a 2004–2006 update. Proteomics 6:5529–5548

    Article  CAS  PubMed  Google Scholar 

  • Rozanov AS, Zagrebelny SN, Beklemishev AB (2009) Cloning of Escherichia coli K12 xylose isomerase (glucose isomerase) gene and studying the enzymatic properties of its expression product. App Biochem Micro 45:31–37

    Article  CAS  Google Scholar 

  • Ruedell CM, Almeida MR, Schwambach J, Posenato CF, Fett-Neto AG (2013) Pre and post-severance effects of light quality on carbohydrate dynamics and microcutting adventitious rooting of two Eucalyptus species of contrasting recalcitrance. Plant Growth Regul 69:235–245

    Article  CAS  Google Scholar 

  • Sæbø A, Krekling T, Appelgren M (1995) Light quality affects photosynthesis and leaf anatomy of birch plantlets in vitro. Plant Cell Tiss Org 41:177–185

    Article  Google Scholar 

  • Smirnova J, Fernie AR, Spahn CMT, Steup M (2017) Photometric assay of maltose and maltose-forming enzyme activity by using 4-alpha-glucanotransferase (DPE2) from higher plants. Anal Biochem 532:72–82

    Article  CAS  PubMed  Google Scholar 

  • Strand S, Zrenner R, Trevanion S, Stitt M, Gustafsson P, Gardeatrm P (2000) Decreased expression of two key enzymes in the sucrose biosynthesis pathway, cytosolic fructose-1,6-bisphosphatase and sucrose phosphate synthase, has remarkably different consequences for photosynthetic carbon metabolism in transgenic Arabidopsis thaliana. Plant J 23:759–770

    Article  CAS  PubMed  Google Scholar 

  • Sun QQ, Zhang N, Wang JF, Cao YY, Li XS, Zhang HJ, Zhang L, Tan DX, Guo YD (2016) A label-free differential proteomics analysis reveals the effectof melatonin on promoting fruit ripening and anthocyanin accumulation upon postharvest in tomato. J Pineal Res 61:138–153

    Article  CAS  PubMed  Google Scholar 

  • Tandon KS, Baldwin EA, Scott JW, Shewfelt RL (2003) Linking sensory descriptors to volatile and nonvolatile components of fresh tomato flavor. J Food Sci 68:2366–2371

    Article  CAS  Google Scholar 

  • Taylor AR, Assmann SM (2001) Apparent absence of a redox requirement for blue light activation of pump current in broad bean guard cells. Plant Physiol 125:329–338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tripathy BC, Brown CS (1995) Root–shoot interaction in the greening of wheat seedlings grown under red light. Plant Physiol 107:407–411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tymowska-Lalanne Z, Kreis M (1998) The plant invertases: physiology, biochemistry and molecular biology. Adv Bot Res 28:71–117

    Article  CAS  Google Scholar 

  • Van der Maarel MJEC, Leemhuis H (2013) Starch modification with microbial alpha- glucanotranferase enzymes. Carbohyd Polym 93:116–121

    Article  CAS  Google Scholar 

  • Vieira MF, Vieira AMS, Zanin GM, Tardioli PW, Mateo C, Guisan JM (2011) β-Glucosidase immobilized and stabilized on agarose matrix functionalized with distinct reactive groups. J Mol Catal B Enzym 69:47–53

    Article  CAS  Google Scholar 

  • Watzl B, Bub A, Brandstetter BR, Rechkemmer G (1999) Modulation of human T- lymphocyte functions by the consumption of carotenoid-rich vegetables. Br J Nutr 82:383–389

    Article  CAS  PubMed  Google Scholar 

  • Willis JE, Sallach HJ (1962) Activation of mammalian glycerate dehydrogenase by inorganic salts. BBA 62:443–444

    CAS  PubMed  Google Scholar 

  • Wisniewski JR, Zougman A, Nagaraj N, Mann M (2009) Universal sample preparation method for proteome analysis. Nat Methods 6:359–362

    Article  CAS  PubMed  Google Scholar 

  • Yao K, Wu YY (2016) Phosphofructokinase and glucose-6-phosphate dehydrogenase in response to drought and bicarbonate stress at transcriptional and functional levels in mulberry. Russ J Plant Physl 63:235–242

    Article  CAS  Google Scholar 

  • Yin HX (2010) Studying of cloning, expression and bioactivity analysis of xylose isomerase and xylulokinase. Dissertation, Hainan University

  • Yu L, Liu HX, Shao XF, Yu F, Wei YZ, Ni ZM, Xu F, Wang HF (2016) Effects of hot air and methyl jasmonate treatment on the metabolism of soluble sugars in peach fruit during cold storage. Postharvest Biol Technol 113:8–16

    Article  CAS  Google Scholar 

  • Yu Y, Qin WQ, Li Y, Zhang CJ, Wang Y, Yang ZE, Ge XY, Li FG (2019) Red light promotes cotton embryogenic callus formation by influencing endogenous hormones, polyamines and antioxidative enzyme activities. Plant Growth Regul 87:187–199

    Article  CAS  Google Scholar 

  • Zeng JF (2016) The research of PCNA protein-ligand in the vein graft remodeling. Dissertation, Nanchang University

  • Zhang MQ, Zhuo XL, Wang JH, Yang CY, Powell CA, Rk Chen (2015) Phosphomannose isomerase affects the key enzymes of glycolysis and sucrose metabolism in transgenic sugarcane overexpressing the manA gene. Mol Breed 35:100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Wang YX, Gao QH, Duan K (2017) The phylogeney, expression patterns of alkaline/neutral invertase gene (Fa.A/N-Invs) family and their influence on sugar accumulation in strawberry fruit. Acta Hortic Sin 44:1049–1060

    Google Scholar 

  • Zhang XQ, Tian B, Fang YX, Tong T, Zheng JJ, Xue DW (2019) Proteome analysis and phenotypic characterization of the lesion mimic mutant bspl in barley. Plant Growth Regul 87:329–339

    Article  CAS  Google Scholar 

  • Zhao SJ, Shi GA, Dong XC (2002) Determination of soluble sugar and starch in plant tissues. In: Liu XS (ed) Techniques of plant physiological experiment, 1st edn. China Agricultural Science and Technology Press, Beijing, pp 84–85

    Google Scholar 

  • Zhao YF, Chen K, Zhang QH, Han YF, Han CG (2017) Effects of light quality on carbon and nitrogen assimilation and root activity of eggplant. Agric Sci Technol 18:2229–2231, 2235

    Google Scholar 

  • Zhou Y, Singh BR (2002) Red light stimulates flowering and anthocyanin biosynthesis in American cranberry. Plant Growth Regul 38:165–171

    Article  CAS  Google Scholar 

  • Zrenner R, Krause KP, Apel P, Sonnewald U (1996) Reduction of the cytosolic fructose-1,6-bisphosphatase in transgenic potato plants limits photosynthetic sucrose biosynthesis with no impact on plant growth and tuber yield. Plant J 9:671–681

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Special Fund for Agro-scientific Research in the Public Interest (Grant No. 201303108). We thank Margaret Biswas, PhD, from Liwen Bianji, Edanz Group China (www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript. We are very grateful to Shanghai applied protein technology co., ltd. for the proteomic data determination.

Author information

Authors and Affiliations

  1. College of Horticulture Science and Engineering, Shandong Agricultural University, 61 Daizong Street, Tai An, 271018, Shandong, China

    Fei Dong, Xiudong Sun, Zhilong Bao, Cuihui Sun, Yuqian Ren & Shiqi Liu

  2. State Key Laboratory of Crop Biology, Tai An, 271018, Shandong, China

    Fei Dong, Xiudong Sun, Zhilong Bao & Shiqi Liu

  3. Ministry of Agriculture Key Laboratory of Biology and Genetic Improvement of Horticultural Crops in Huanghuai Region, Tai An, Shandong, China

    Fei Dong, Xiudong Sun, Zhilong Bao & Shiqi Liu

  4. Shandong Academy of Agricultural Sciences, Jinan, 250000, Shandong, China

    Chuanzeng Wang

  5. Higher Education Evaluation Center Ministry of Education, Beijing, 100000, China

    Chen Dong

Authors
  1. Fei Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chuanzeng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiudong Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhilong Bao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chen Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Cuihui Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yuqian Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shiqi Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SL and FD planned and designed the experiments. XD and ZB helped in the design of the experiment. YQ and CD formatted and revised the manuscript. FD and CS conducted the experiments including date recording and analysis. SL and FD wrote the manuscript, and all authors contributed and revised the final version of the manuscript.

Corresponding author

Correspondence to Shiqi Liu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

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.

Supplementary material 1 (DOC 48 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dong, F., Wang, C., Sun, X. et al. Sugar metabolic changes in protein expression associated with different light quality combinations in tomato fruit. Plant Growth Regul 88, 267–282 (2019). https://doi.org/10.1007/s10725-019-00506-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-019-00506-1

Keywords

Search

Navigation