Skip to main content
SpringerLink
Log in

Darkness and low-light alter reserve mobilization during the initial growth of soybean (Glycine max (L.) Merrill)

  • Published:
Theoretical and Experimental Plant Physiology Aims and scope Submit manuscript

Abstract

Light is both a source of energy and a developmental signal, and therefore has a major impact upon initial seedling growth. This is particularly the case for species where photosynthesis in the cotyledons makes a significant contribution to carbon balance. In addition to containing reserves of proteins, lipids and carbohydrates the cotyledons of soybean (Glycine max (L.) Merrill) maintain sufficient photosynthetic activity to counterbalance respiratory carbon loss. Based on the hypothesis that altered light regime would affect seedling photosynthesis and development, we investigated the impact of shading and darkness on the reserves present in different soybean seedling organs. Plants were grown until the VC/V1 stage under normal light conditions (500 µmol m−2 s−1, 12/12 h) before being divided into three groups; normal light, low light (50 µmol m−2 s−1, 12/12 h) and darkness. After 3 days plants were harvested at three time points over the course of a day/night cycle and seedling organs analysed separately. Low light and darkness led to partial etiolation and the consumption of carbohydrates and fatty acids in several organs. Effects on cotyledon reserve mobilisation were modest, as darkness and low light did not lead to decreased cotyledon mass. However, metabolism in the epicotyl was more strongly perturbed, with the accumulation of branched chain and aromatic amino acids together with sugars that may be required to drive organ elongation. Darkness also served to abolish diurnal alterations in starch and asparagine concentrations detected in control plants. Overall, the data reinforce the flexibility of seedling metabolism, revealing similarities to the responses of adult plants to carbon starvation .

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

Similar content being viewed by others

References

  • Abrahamsen M, Sudia TW (1966) Studies on the soluble carbohydrates and carbohydrate precursors in germinating soybean seed. Am J Bot 53(2):108–114

    CAS  Google Scholar 

  • Agrawal GK, Hajduc M, Graham K, Thelen JJ (2008) In-depth investigation of the soybean seed-filling proteome and comparison with a parallel study of rapeseed. Plant Physiol 148:504–518

    CAS  PubMed  PubMed Central  Google Scholar 

  • Albrecht V, Ingenfeld A, Apel K (2008) Snowy cotyledon 2: the identification of a zinc finger domain protein essential for chloroplast development in cotyledons but not in true leaves. Plant Mol Biol 66:599–608

    CAS  PubMed  Google Scholar 

  • Amaral LIV, Gaspar M, Costa PMF, Aidar MPM, Buckeridge MS (2007) Novo método enzimático rápido e sensível de extração e dosagem de amido em materiais vegetais. Hoehnea 34(4):425–431

    Google Scholar 

  • Araújo WL et al (2011) Protein degradation—an alternative respiratory substrate for stressed plants. Trends Plant Sci 16(9):489–498

    PubMed  Google Scholar 

  • Araújo WL et al (2012) Metabolic control and regulation of the tricarboxylic acid cycle in photosynthetic and heterotrophic plant tissues. Plant Cell Environ 35:1–21

    PubMed  Google Scholar 

  • Armarego-Marriott T, Sandoval-Ibanes O, Kowalewska L (2020) Beyond the darkness: recent lessons from etiolation and de-etiolation studies. J Exp Bot 71:1215–1225

    CAS  PubMed  Google Scholar 

  • Artuzo FD et al (2018) Gestão de custos na produção de milho e soja. Rev Bras Gest Neg São Paulo 20:273–294

    Google Scholar 

  • Avin-Wittenberg T et al (2015) Global analysis of the role of autophagy in cellular metabolism and energy homeostasis in Arabidopsis seedlings under carbon starvation. Plant Cell 27:306–322

    CAS  PubMed  PubMed Central  Google Scholar 

  • Barros JAS et al (2017) Autophagy deficiency compromises alternative pathways of respiration following energy deprivation in Arabidopsis thaliana. Plant Physiol 175:62–76

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brouquisse R, Gaudillére JP, Raymond P (1998) Induction of a carbon-starvation-related proteolysis in whole maize plants submitted to light/dark cycles and to extended darkness. Plant Physiol 117:1281–1291

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brown CS, Huber SC (1987) Photosynthesis, reserve mobilization and enzymes of sucrose metabolism in soybean (Glycine max) cotyledons. Physiol Plant 70:537–543

    CAS  Google Scholar 

  • Brown CS, Huber SC (1988) Reserve mobilization and starch formation in soybean (Glycine max) cotyledons in relation to seedling growth. Physiol Plant 72:518–524

    CAS  Google Scholar 

  • Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin J-F, Wu S-H, Swidzinski J, Ishizaki K, Leaver CJ (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42:567–585

    CAS  PubMed  Google Scholar 

  • Buckeridge MS, Aidar MP, Santos HP, Tiné MA (2004) Acúmulo de reservas. In: Ferreira AG, Borghetti F (eds) Germinação do básico ao aplicado. Artmed, Porto Alegre, pp 31–50

    Google Scholar 

  • Chatterton HJ, Silvius JE (1979) Photosynthate partitioning into starch in soybean leaves. Plant Physiol 64:749–753

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Zhou B, Li J, Tang H, Tang J, Yang Z (2018) Formation and change of chloroplast-located plant metabolites in response to light conditions. Int J Mol Sci 19(654):2018

    Google Scholar 

  • Clemente TE, Cahoon EB (2009) Soybean oil: genetic approaches for modification of functionality and total content. Plant Physiol 151:1030–1040

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dalchau N, Baek SJ, Briggs HM, Robertson FC, Dodd AN, Gardner MJ, Stancombe MA, Haydon MJ, Stan G, Gonçalves JM, Webb AAR (2011) The circadian oscillator gene GIGANTEA mediates a long-term response of the Arabidopsis thaliana circadian clock to sucrose. PNAS 108:5104–5109. https://doi.org/10.1073/pnas.1015452108

    Article  PubMed  Google Scholar 

  • Dodd AN, Salathia N, Hall A, Kévei E, Tóth R, Nagy F, Hibberd JM, Millar AJ, Webb AA (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–633

    CAS  PubMed  Google Scholar 

  • Fan J, Yan C, Roston R, Shanklin J, Xu C (2014) Arabidopsis lipins, PDAT1 acyltransferase, and SDP1 triacylglycerol lipase synergistically direct fatty acids toward β-oxidation, thereby maintaining membrane lipid homeostasis. Plant Cell 26(10):4119–4134. https://doi.org/10.1105/tpc.114.130377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farré EM, Weise S (2012) The interactions between the circadian clock and primary metabolism. Curr Opin Plant Biol 15:293–300

    PubMed  Google Scholar 

  • Fehr WR, Caviness CE (1977) Stages of soybean development. Spec Rep 87:12

    Google Scholar 

  • Galili G, Amir R, Fernie R (2016) The regulation of essential amino acid synthesis and accumulation in plants. Annu Rev Plant Biol. https://doi.org/10.1146/annurev-arplant-043015-112213

    Article  PubMed  Google Scholar 

  • Gommers CMM, Monte E (2018) Seedling establishment: a dimmer switch-regulated process between dark and light signaling. Plant Physiol 176:1061–1074

    CAS  PubMed  Google Scholar 

  • Hanley ME, Fegan EL (2007) Timing of cotyledon damage affects growth and flowering in mature plants. Plant Cell Environ 30:812–819

    CAS  PubMed  Google Scholar 

  • Harris M, Mackender RO, Smith D (1986) Photosynthesis of cotyledons of soybean seedlings. New Phytol 104:319–329

    Google Scholar 

  • He C, Wang W, Dongfang Y, Zhang J, Gai J, Chen S (2002) Transcription regulation of soybean ribulose-1,5-bisphosphate carboxylase small subunit gene by external factors. Chin Sci Bull 47:38–43

    Google Scholar 

  • Hildebrant TM, Nesi AN, Araújo WL, Braun H-P (2015) Amino acid catabolism in plants. Mol Plant. https://doi.org/10.1016/j.molp.2015.09.005

    Article  Google Scholar 

  • Housley TL, Schrader LE, Miller M, Setter TL (1979) Partitioning of 14C-Photosynthate, and long distance translocation of amino acids in preflowering and flowering, nodulated and nonnodulated soybeans. Plant Physiol 64:94–98

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hust CJ, Sudia TW (1973) The effect of light on the use of the nitrogen reserves of germinating soybean seeds. Am J Bot 60:1034–1040

    Google Scholar 

  • Hymowitz T (1970) On the domestication of the soybean. Econ Bot 23:408–421

    Google Scholar 

  • Ishizaki K, Larson TR, Schauer N, Fernie AR, Graham IA, Leaver CJ (2005) The critical role of Arabidopsis electron-transfer flavoprotein: ubiquinone oxidoreductase during dark-induced starvation. Plant Cell 17:2587–2600

    CAS  PubMed  PubMed Central  Google Scholar 

  • Josse EM, Halliday K (2008) Skotomorphogenesis: the dark side of light signalling. Curr Biol 18:1144–1146

    Google Scholar 

  • Joshi V, Joung JG, Fei ZJ, Jander G (2010) Interdependence of threonine, methionine and isoleucine metabolism in plants: accumulation and transcriptional regulation under abiotic stress. Amino Acids 39:933–947

    CAS  PubMed  Google Scholar 

  • Junknischke A, Kutschera U (1998) The role of the cotyledons and primary leaves during seedling establishment in sunflower. J Plant Physiol 153:700–705

    Google Scholar 

  • Kamranfar I, Xue GP, Tohge T, Sedaghatmehr M, Fernie AR, Balazadeh S, Mueller-Roeber B (2018) Transcription factor RD26 is a key regulator of metabolic reprogramming during dark-induced senescence. New Phytol 218:1543–1557

    CAS  PubMed  Google Scholar 

  • Kerr PS, Rufty TW, Huber SC (1985) Changes in nonstructural carbohydrates in different parts of soybean (Glycine max [L.J Merr.) plants during a light/dark cycle and in extended darkness. Plant Physiol 78:576–581

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim J, Park SJ, Lee IH, Chu H, Penfold CA, Kim JH, Buchanan-Wollaston V, Nam HG, Woo HR, Lim PO (2018) Comparative transcriptome analysis in Arabidopsis ein2/ore3 and ahk3/ore12 mutants during dark-induced leaf senescence. J Exp Bot 69:3023–3036

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kunz HH, Scharnewski M, Feussner K, Feussner I, Flügge UI, Fulda M, Gierth M (2009) The ABC transporter PXA1 and peroxisomal beta-oxidation are vital for metabolism in mature leaves of Arabidopsis during extended darkness. Plant cell 21:2733–2749

    CAS  PubMed  PubMed Central  Google Scholar 

  • Laurens LML, Quinn M, van Wychen S, Templenton DW, Wolfrum EJ (2012) Accurate and reliable quantification of total microalgal fuel potential as fatty acid methyl esters by in situ transesterification. Anal Bioanal Chem 403(1):167–178

    CAS  PubMed  PubMed Central  Google Scholar 

  • Law SR, Chrobok D, Juvany M, Delhomme N, Linén P, Brouwer B, Ahad A, Moritz T, Jansson S, Gardestrom P, Keech O (2018) Darkened leaves use different metabolic strategies for senescence and survival. Plant Physiol. https://doi.org/10.1104/pp.18.00062

    Article  PubMed  PubMed Central  Google Scholar 

  • Lea PJ, Sodek L, Parry MAJ, Shewry PR, Halford NG (2006) Asparagine in plants. Ann Appl Biol 150:1–26

    Google Scholar 

  • Legris M, Inca YC, Fankhauser C (2019) Molecular mechanisms underlying phytochrome-controlled morphogenesis in plants. Nat Commun 10:5219

    CAS  PubMed  PubMed Central  Google Scholar 

  • Levan NA, Goggi AS, Mullen R (2008) Improving the reproducibility of soybean standard germination test. Crop Sci 48:1933–1940

    Google Scholar 

  • Lima JD, Sodek L (2003) N-stress alters aspartate and asparagine levels of xylem sap in soybean. Plant Sci 165:649–656

    CAS  Google Scholar 

  • Marek LF, Stewart CR (1992) Photosynthesis and photorespiration in presenescent, senescent, and rejuvenated soybean cotyledons. Plant Physiol 98:694–699

    CAS  PubMed  PubMed Central  Google Scholar 

  • Masuda T, Goldsmith PD (2009) World soybean production: area harvested, yield, and long-term projections. Int Food Agribus Manage Rev 12:1–20

    Google Scholar 

  • Melo FPL, Neto AVA, Simaburkuro EA, Tabarelli M (2004) Recrutamento e estabelecimento de plântulas. In: Ferreira AG, Borghetti F (eds) Germinação do básico ao aplicado. Porto Alegre, Artmed, pp 149–162

    Google Scholar 

  • Moore S, Stein WH (1954) A modified ninhydrin reagent for the photometric determination of amino acids and related compounds. J Biol Chem 211:907–913

    CAS  PubMed  Google Scholar 

  • Morais ÁA, Silva AL (1996). In: Morais AA, Silva AL (eds) Soja: suas aplicações. MDSI Editora Médica e Científica Ltda, Rio de Janeiro, p 259

    Google Scholar 

  • Moreira TB, Shaw R, Luo X, Ganguly O, Kim HS, Coelho LGF, Cheung CYM, Williams TCR (2019) A genome-scale metabolic model of soybean (Glycine max) highlights metabolic fluxes in seedlings. Plant Physiol 180:1912–1929

    CAS  PubMed  PubMed Central  Google Scholar 

  • Muntz K, Belozersky MA, Dunaevsky YE, Schlereth A, Tiedemann J (2001) Stored proteinases and the initiation of storage protein mobilization in seeds during germination and seedling growth. J Exp Bot 52:1741–1752

    Google Scholar 

  • Nielsen N (1996) Soybean seed composition. In: Verma D, Shoemaker R (eds) Soybean: genetics, molecular biology and biotechnology. CAB International, Willingford, p 270

    Google Scholar 

  • Obata T, Fernie AR (2012) The use of metabolomics to dissect plant responses to abiotic stresses. Cell Mol Life Sci 69:3225–3243

    CAS  PubMed  PubMed Central  Google Scholar 

  • Penny MG, Moore KG, Lovell PH (1976) The effects of inhibition of cotyledon photosynthesis on seedling development in Cucumis sativus L.. Ann Bot 40:815–824

    Google Scholar 

  • Pires MV et al (2016) The influence of alternative pathways of respiration that utilize branched-chain amino acids following water shortage in Arabidopsis. Plant Cell Environ 39:1304–1319

    CAS  PubMed  Google Scholar 

  • Praxedes SC et al (2006) Effects of long-term soil drought on photosynthesis and carbohydrate metabolism in mature robusta coffee (Coffea canephora Pierre var. kouillou) leaves. Environ Exp Bot 56(3):263–273

    CAS  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org. Accessed 20 Sept 2018

  • Rikin A, Dillwith JW, Bergman DK (1993) Correlation between the circadian rhythm of resistance to extreme temperatures and changes in fatty acid composition in cotton seedlings. Plant Physiol 101:31–36

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schippers JHM, Schmidt R, Wagstaff C, Jing H (2015) Living to die and dying to live: the survival strategy behind leaf senescence. Plant Physiol 169:914–930

    CAS  PubMed  PubMed Central  Google Scholar 

  • Slot M, Kitajima K (2015) Whole-plant respiration and its temperature sensitivity during progressive carbon starvation. Funct Plant Biol 42:579–588

    CAS  PubMed  Google Scholar 

  • Srivastava D, Shamim M, Kumar M, Mishra A, Maurya R, Sharma D, Pandey P, Singh KN (2019) Role of circadian rhythm in plant system: an update from development to stress response. Environ Exp Bot 162:256–271

    Google Scholar 

  • Stitt M, Zeeman SC (2012) Starch turnover: pathways, regulation and role in growth. Plant Biol 15:282–292

    CAS  Google Scholar 

  • Sweetlove LJ et al (2010) Not just a circle: flux modes in the plant TCA cycle. Trends Plant Sci 15:462–470

    CAS  PubMed  Google Scholar 

  • Tcherkez G, Boex-Fontvieille E, Mahé A, Hodges M (2012) Respiratory carbon fluxes in leaves. Curr Opin Plant Biol 15(3):308–314

    CAS  PubMed  Google Scholar 

  • Thomas AL, Costa JA (1993) Crescimento de plântulas de soja afetado pelo sombreamento dos cotilédones e suas reservas. Pesq Agropec bras 28(8):925–929

    Google Scholar 

  • Wang L, Liu P, Wu LM, Tan J, Peacock WJ, Dennis ES (2019) Cotyledons contribute to plant growth and hybrid vigor in Arabidopsis. Planta 249:1107–1118

    CAS  PubMed  Google Scholar 

  • Willms JR, Salon C, Layzell DB (1999) Evidence for light-stimulated fatty acid synthesis in soybean fruit. Plant Physiol 120:1117–1128

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Z, Ohlrogge JB (2009) Turnover of fatty acids during natural senescence of arabidopsis, brachypodium, and switchgrass and in Arabidopsis β-oxidation mutants. Plant Physiol 150:1981–1989

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yanovsky MJ (2001) Signaling networks in the plant circadian system. Plant Biol 4:429

    CAS  Google Scholar 

  • Yemm EW, Cocking EC (1955) The determination of amino acids with ninhydrin. Analyst 80:209–213

    CAS  Google Scholar 

  • Yin Y, Yang R, Han Y, Gu Z (2014) Comparative proteomic and physiological analyses reveal the protective effect of exogenous calcium on the germinating soybean response to salt stress. J Proteom 113:110–126

    Google Scholar 

  • Zheng W, Wang P, Zhang H, Zhou D (2011) Photosynthetic characteristics of the cotyledon and first true leaf of castor (Ricinus communis L.). Aust J Crop Sci 5:702–708

    Google Scholar 

Download references

Funding

Funding was provided by Fundação de Apoio à Pesquisa do Distrito Federal (FAPDF, Processo 193.000.193/2014) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001.

Author information

Authors and Affiliations

  1. Departament of Botany, University of Brasília, Campus Darcy Ribeiro, Asa Norte, Brasília, Brazil

    Karen Fernanda Oliveira e Silva, Bruno Costa Val Melo, Thiago Batista Moreira & Thomas Christopher Rhys Williams

Authors
  1. Karen Fernanda Oliveira e Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bruno Costa Val Melo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thiago Batista Moreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Thomas Christopher Rhys Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thomas Christopher Rhys Williams.

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.

Electronic supplementary material 1 (DOCX 3600 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Silva, K.F.O.e., Melo, B.C.V., Moreira, T.B. et al. Darkness and low-light alter reserve mobilization during the initial growth of soybean (Glycine max (L.) Merrill). Theor. Exp. Plant Physiol. 33, 55–68 (2021). https://doi.org/10.1007/s40626-020-00194-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40626-020-00194-7

Keywords

Search

Navigation