Skip to main content
SpringerLink
Log in

Light induces gene expression to enhance the synthesis of storage reserves in Brassica napus L. embryos

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Key message

In this manuscript, we disclosed the influence of light on the accumulation of storage reserves in B. napus embryos.

  1. 1.

    Light induced the gene expression in the developing embryos of B. napus.

  2. 2.

    Light promoted the starch synthesis in chloroplasts of B. napus embryos.

  3. 3.

    Light enhanced the metabolic activity of storage reserve synthesis in B. napus embryos.

Abstract

Light influences the accumulation of storage reserves in embryos, but the molecular mechanism was not fully understood. Here, we monitored the effects of light on reserve biosynthesis in Brassica napus by comparing embryos from siliques grown in normal light conditions to those that were shaded or masked (i.e., darkened completely). Masked embryos developed more slowly, weighed less, and contained fewer proteins and lipids than control embryos. They also had fewer and smaller oil bodies than control embryos and lacked chloroplasts, where starch grains are usually synthesized. The levels of most amino acids, carbohydrates, and fatty acids were higher in masked embryos than in control or shaded embryos, whereas the levels of these metabolites in the masked endosperms were lower than those in control and shaded endosperm. Transcriptome analysis indicated that genes involved in photosynthesis (42 genes), amino acid biosynthesis (51 genes), lipid metabolism (61 genes), and sugar transport (13 genes) were significantly repressed in masked embryos. Our results suggest that light contributes to reserve accumulation in embryos by inducing the expression of metabolic genes, thereby enhancing the biosynthesis of storage reserves.

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

Similar content being viewed by others

References

  • Allen DK, Ohlrogge JB, Shachar-Hill Y (2009) The role of light in soybean seed filling metabolism. Plant J 58:220–234

    Article  CAS  PubMed  Google Scholar 

  • Allorent G, Courtois F, Chevalier F, Lerbs-Mache S (2013) Plastid gene expression during chloroplast differentiation and dedifferentiation into non-photosynthetic plastids during seed formation. Plant Mol Biol 82:59–70

    Article  CAS  PubMed  Google Scholar 

  • Andriotis VM, Pike MJ, Kular B, Rawsthorne S, Smith AM (2010) Starch turnover in developing oilseed embryos. New Phytol 187:791–804

    Article  CAS  PubMed  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta Vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Batz O, Neuhaus SR (1995) Purification of chloroplasts from fruits of green pepper (Capsicum annum L.) and characterization of starch synthesis. Planta 196:50–57

    Article  CAS  Google Scholar 

  • Baud S, Lepiniec L (2010) Physiological and developmental regulation of seed oil production. Prog Lipid Res 49:235–249

    Article  CAS  PubMed  Google Scholar 

  • Browse J, Slack CR (1985) Fatty-acid synthesis in plastids from maturing safflower and linseed cotyledons. Planta 166:74–80

    Article  CAS  PubMed  Google Scholar 

  • Bylesjo M, Rantalainen M, Cloarec O, Nicholson JK, Holmes E, Trygg J (2006) OPLS discriminant analysis: combining the strengths of PLS-DA and SIMCA classification. J Chemom 20:341–351

    Article  CAS  Google Scholar 

  • daSilva PMFR, Eastmond PJ, Hill LM, Smith AM, Rawsthorne S (1997) Starch metabolism in developing embryos of oilseed rape. Planta 203:480–487

    Article  CAS  Google Scholar 

  • Denyer K, Smith AM (1988) The capacity of plastids from developing pea cotyledons to synthesize acetyl coa. Planta 173:172–182

    Article  CAS  PubMed  Google Scholar 

  • Derek BJ, Black M (1994) Seed development and maturation. Seeds: physiology of development and germination. Springer, Boston, pp 35–115

    Google Scholar 

  • Eastmond PJ, Rawsthorne S (2000) Coordinate changes in carbon partitioning and plastidial metabolism during the development of oilseed rape embryos. Plant Physiol 122:767–774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eastmond P, Kolacna L, Rawsthorne S (1996) Photosynthesis by developing embryos of oilseed rape (Brassica napus L). J Exp Bot 47:1763–1769

    Article  CAS  Google Scholar 

  • Entwistle G, Aprees T (1990) Lack of fructose-1,6-bisphosphatase in a rnge of higher-plants that store starch. Biochem J 271:467–472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fluhr R, Kuhlemeier C, Nagy F, Chua NH (1986) Organ-specific and light-induced expression of plant genes. Science 232:1106–1112

    Article  CAS  PubMed  Google Scholar 

  • Goffman FD, Alonso AP, Schwender J, Shachar-Hill Y, Ohlrogge JB (2005) Light enables a very high efficiency of carbon storage in developing embryos of rapeseed. Plant Physiol 138:2269–2279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hua W, Li RJ, Zhan GM, Liu J, Li J, Wang XF, Liu GH, Wang HZ (2012) Maternal control of seed oil content in Brassica napus: the role of silique wall photosynthesis. Plant J 69:432–444

    Article  CAS  PubMed  Google Scholar 

  • Jia HJ, Araki A, Okamoto G (2005) Influence of fruit bagging on aroma volatiles and skin coloration of 'Hakuho' peach (Prunus persica Batsch). Postharvest Biol Tec 35:61–68

    Article  CAS  Google Scholar 

  • Kang F, Rawsthorne S (1994) Starch and fatty-acid synthesis in plastids from developing embryos of oilseed rape (Brassica napus L). Plant J 6:795–805

    Article  CAS  Google Scholar 

  • Kazusato O, Shigeru M, Shoji M, Maki K, Kenji Y, Makoto H, Takatoshi K, Akeo K, Wataru S, Shoichi H, Masakatsu W, Toshiaki M, Akinori S, Takanori I, Yoichiroh H, Mikio N (2015) Physical interaction between peroxisomes and chloroplasts elucidated by in situ laser analysis. Nat Plants 1:15035

    Article  CAS  Google Scholar 

  • King SP, Badger MR, Furbank RT (1998) CO2 refixation characteristics of developing canola seeds and silique wall. Aus J Plant Physiol 25:377–386

    CAS  Google Scholar 

  • Kropat J, Oster U, Rudiger W, Beck CF (1997) Chlorophyll precursors are signals of chloroplast origin involved in light induction of nuclear heat-shock genes. Proc Natl Acad Sci 94:14168–14172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuno N, Furuya M (2000) Phytochrome regulation of nuclear gene expression in plants. Semin Cell Dev Biol 11:485–493

    Article  CAS  PubMed  Google Scholar 

  • Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Le BH, Cheng C, Bui AQ, Wagmaister JA, Henry KF, Pelletier J, Kwong L, Belmonte M, Kirkbride R, Horvath S, Drews GN, Fischer RL, Okamuro JK, Harada JJ, Goldberg RB (2010) Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc Natl Acad Sci 107:8063–8070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H, Wang X, Ren K, Li K, Wei M, Wang W, Sheng X (2017) Light deprivation-induced inhibition of chloroplast biogenesis does not arrest embryo morphogenesis but strongly reduces the accumulation of storage reserves during embryo maturation in Arabidopsis. Front Plant Sci 8:1287

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma LG, Li JM, Qu LJ, Hager J, Chen ZL, Zhao HY, Deng XW (2001) Light control of Arabidopsis development entails coordinated regulation of genome expression and cellular pathways. Plant Cell 13:2589–2607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mansfield S, Briarty L (1991) Early embryogenesis in Arabidopsis thaliana. II. The developing embryo. Can J Bot 69:461–476

    Article  Google Scholar 

  • Moutot F, Huet JC, Morot-Gaudry JF, Pernollet JC (1986) Relationship between photosynthesis and protein synthesis in maize: I. Kinetics of translocation of the photoassimilated carbon from the ear leaf to the seed. Plant Physiol 80:211–215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muller LL, Jacks TJ (1975) Rapid chemical dehydration of samples for electron microscopic examinations. J Histochem Cytochem 23:107–110

    Article  CAS  PubMed  Google Scholar 

  • Oster UBH, Rtidiger W (1996) The greening process in cress seedlings. V. Possible interference of chlorophyll precursors, accumulated after thujaplicin treatment, with light-regulated expression of Lhc genes. J Photochem Photobiol 36:255–261

    Article  CAS  Google Scholar 

  • Patel RK, Jain M (2012) NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PLoS ONE 7:e30619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Periappuram C, Steinhauer L, Barton DL, Taylor DC, Chatson B, Zou JT (2000) The plastidic phosphoglucomutase from Arabidopsis. A reversible enzyme reaction with an important role in metabolic control. Plant Physiol 122:1193–1199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piippo M, Allahverdiyeva Y, Paakkarinen V, Suoranta UM, Battchikova N, Aro EM (2006) Chloroplast-mediated regulation of nuclear genes in Arabidopsis thaliana in the absence of light stress. Physiol Genomics 25:142–152

    Article  CAS  PubMed  Google Scholar 

  • Rolletschek H, Radchuk R, Klukas C, Schreiber F, Wobus U, Borisjuk L (2005) Evidence of a key role for photosynthetic oxygen release in oil storage in developing soybean seeds. New Phytol 167:777–786

    Article  CAS  PubMed  Google Scholar 

  • Ruban AVWR, Horton P (1992) The molecular mechanism of the control of excitation energy dissipation in chloroplast membranes Inhibition of ΔpH-dependent quenching of chlorophyll fluorescence by dicyclohexylcarbodiimide. FEBS Lett 309:175–179

    Article  CAS  PubMed  Google Scholar 

  • Ruuska SA, Schwender J, Ohlrogge JB (2004) The capacity of green oilseeds to utilize photosynthesis to drive biosynthetic processes. Plant Physiol 136:2700–2709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakamoto T, Morinaka Y, Ohnishi T, Sunohara H, Fujioka S, Ueguchi-Tanaka M, Mizutani M, Sakata K, Takatsuto S, Yoshida S, Tanaka H, Kitano H, Matsuoka M (2006) Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice. Nat Biotechnol 24:105–109

    Article  CAS  PubMed  Google Scholar 

  • Schwender J, Ohlrogge JB (2002) Probing in vivo metabolism by stable isotope labeling of storage lipids and proteins in developing Brassica napus embryos. Plant Physiol 130:347–361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith AM, Quintontulloch J, Denyer K (1990) Characteristics of plastids responsible for starch synthesis in developing pea embryos. Planta 180:517–523

    Article  CAS  PubMed  Google Scholar 

  • Streb S, Delatte T, Umhang M, Eicke S, Schorderet M, Reinhardt D, Zeeman SC (2008) Starch granule biosynthesis in arabidopsis is abolished by Rremoval of all debranching enzymes but restored by the subsequent removal of an endoamylase. Plant Cell 20:3448–3466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tan HL, Yang XH, Zhang FX, Zheng X, Qu CM, Mu JY, Fu FY, Li JA, Guan RZ, Zhang HS, Wang GD, Zuo JR (2011) Enhanced seed oil production in canola by conditional expression of Brassica napus LEAFY COTYLEDON1 and LEC1-LIKE in developing seeds. Plant Physiol 156:1577–1588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tan H, Xie Q, Xiang X, Li J, Zheng S, Xu X, Guo H, Ye W (2015) Dynamic metabolic profiles and tissue-specific source effects on the metabolome of developing seeds of Brassica napus. PLoS ONE 10:e0124794

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tan HL, Xiang XE, Tang J, Wang XC (2016) Nutritional functions of the funiculus in Brassica napus seed maturation revealed by transcriptome and dynamic metabolite profile analyses. Plant Mol Biol 92:539–553

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tan HL, Zhang JH, Qi X, Shi XL, Zhou JG, Wang XC, Xiang XE (2018) Correlation analysis of the transcriptome and metabolome reveals the regulatory network for lipid synthesis in developing Brassica napus embryos. Plant Mol Biol. https://doi.org/10.1007/s11103-018-0800-3

    Article  PubMed  Google Scholar 

  • Thomson WWWJ (1980) Development of nongreen plastids. Annu Rev Plant Physiol 31:375–394

    Article  Google Scholar 

  • Vigeolas H, Mohlmann T, Martini N, Neuhaus HE, Geigenberger P (2004) Embryo-specific reduction of ADP-Glc pyrophosphorylase leads to an inhibition of starch synthesis and a delay in oil accumulation in developing seeds of oilseed rape. Plant Physiol 136:2676–2686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the NSFC project (31671730), the National Key R&D Program of China (2016YFD0100506), and the Fundamental Research Funds for the Central Universities (KYZ201301 and KJSY201510).

Author information

Authors and Affiliations

  1. State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, 210095, China

    Helin Tan & Wenxue Ye

  2. College of Life Sciences, Shanxi Agricultural University, Taigu, 030801, China

    Xiao Qi, Yan Li & Xingchun Wang

  3. Animal Sciences National Teaching Demonstration Center, Nanjing Agricultural University, Nanjing, 210095, China

    Jianguo Zhou, Xiuhong Liu, Xiaoli Shi & Xiaoe Xiang

Authors
  1. Helin Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiao Qi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xingchun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jianguo Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiuhong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiaoli Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Wenxue Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Xiaoe Xiang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

TH, XX, QX, JZ, XS, XL, WY, WX and LY carried out the experiments. TH drafted the manuscript. TH and XX conceived and designed the study and finalized the manuscript. All the authors have read and approved the final manuscript.

Corresponding author

Correspondence to Helin Tan.

Ethics declarations

Conflict of interest

The authors declare that there are 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.

11103_2020_1003_MOESM1_ESM.tif

Supplementary file1 (TIF 3048 kb). Supplemental Figure 1 Starch content in embryo. The starch content of the fresh embryos removed from masked and untreated control siliques at 25D, 28D, and 35D was analyzed with a Total Starch (AA/AMG) Assay Kit. All values are means ± SE of three biological replicates; the asterisks indicate statistically significant differences, Student’s t-test: * P < 0.05

11103_2020_1003_MOESM2_ESM.tif

Supplementary file2 (TIF 3011 kb). Supplemental Figure 2 OPLS analysis of endosperm metabolite profiles. (A) Comparison of metabolite profiles of the control (1–6) and shaded endosperms (7–12). (B) Comparison of metabolite profiles of the control (1–6) and masked endosperms (13–18)

11103_2020_1003_MOESM3_ESM.tif

Supplementary file3 (TIF 1177 kb). Supplemental Figure 3 PCA analysis of embryo metabolite profiles of shade, control, and darkness at different stages. PCA analysis of embryo metabolite profiles in SIMCA 14.0. The red frame represents the metabolite profiles of the darkened embryos at different stages, and the blue frame represents the metabolite profiles of the embryos of control and shade conditions at different stages

11103_2020_1003_MOESM4_ESM.tif

Supplementary file4 (TIF 115544 kb). Supplemental Figure 4 Relative expression of genes. The relative expression of genes involved in photosynthesis, lipid metabolism, and nutrient transport was analyzed by qRT-PCR. The developing embryo samples were collected from the Darkness, Shade, and Control siliques at 28D. The relative expression level of each gene was normalized using BnACTIN2 as an internal control. Data presented are mean values of three experiments, and standard deviations are indicated by bars. The expression level of each gene in darkness embryos is set as 1.0

Supplementary file5 (XLSX 40 kb)

Supplementary file6 (XLSX 125 kb)

Supplementary file7 (XLSX 72 kb)

Supplementary file8 (XLSX 70 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tan, H., Qi, X., Li, Y. et al. Light induces gene expression to enhance the synthesis of storage reserves in Brassica napus L. embryos. Plant Mol Biol 103, 457–471 (2020). https://doi.org/10.1007/s11103-020-01003-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-020-01003-0

Keywords

Search

Navigation