Abstract
We carried out a circadian characterization of non-structural carbohydrate dynamics in the different organs of Erythrina velutina seedlings at late establishment. Seeds were incubated under controlled conditions for 9 days and then seedlings were hydroponically grown in a greenhouse for 8 days. Carbon dioxide uptake was measured in the cordiform leaves every 2 h during the daytime (12 h) and every 4 h during the night-time (12 h); seedlings were harvested every 4 h during the day-night cycle (24 h) to assess the contents of non-structural carbohydrates and the activities of amylases and invertases. Diel patterns of non-structural carbohydrate content were identified in the photosynthetic organs, in which the turnover of starch operated far from its depletion at dawn. In the heterotrophic organs, however, changes in the starch content over 24 h may have maintained the supply of soluble sugars, buffering transient fluctuations in carbon availability. Although it seems that amylase activity was not influenced by the circadian rhythm in the different seedling organs, diel patterns of invertase activity were recognized in the photosynthetic organs.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- AINV:
-
Acid invertases
- DW:
-
Dry weight
- DNS:
-
3,5-Dinitrosalicylic acid
- NINV:
-
Neutral invertases
- NRS:
-
Non-reducing sugars
- NSC:
-
Non-structural carbohydrates
- PPFD:
-
Photosynthetic photon flux density
- RS:
-
Reducing sugars
- TSS:
-
Total soluble sugars
References
Asano Y, Imura YA, Shimojo M, Furuse M, Masud Y (2000) Diurnal variation of amylase activities and carbohydrate contents in root and stem of phasey bean (Macroptilium Tathyroides L. Urb). Grassl Sci 46:66–69. https://doi.org/10.14941/grass.46.66_1
Baber O, Slot M, Celis G, Kitajima K (2014) Diel patterns of leaf carbohydrate concentrations differ between seedlings and mature trees of two sympatric oak species. Botany 92:535–540. https://doi.org/10.1139/cjb-2014-0032
Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H (2013) Seeds: physiology of development, germination and dormancy, 3rd edn. Springer, New York
Cunha TJF, Petrere VG, Silva DJ, Mendes AMS, Melo RF, Oliveira-Neto MB, Silva MSL, Alvarez IA (2010) Principais solos do semiárido tropical brasileiro: caracterização, potencialidades, limitações, fertilidade e manejo. In: Sá IB, Silva PCG (eds) Semiárido brasileiro: pesquisa, desenvolvimento e inovação. Embrapa Semiárido, Petrolina, pp 50–87
Dong S, Beckles DM (2019) Dynamic changes in the starch-sugar interconversion within plant source and sink tissues promote a better abiotic stress response. J Plant Physiol 234–235:80–93. https://doi.org/10.1016/j.jplph.2019.01.007
Elarbi MB, Khemiri H, Jridi T, Hamida JB (2009) Purification and characterization of α-amylase from safflower (Carthamus tinctorius L.) germinating seeds. C R Biol 332:426–432. https://doi.org/10.1016/j.crvi.2009.01.002
Gessler A, Roy J, Kayler Z, Ferrio JP, Alday JG, Bahn M, Castillo J, Devidal S, García-Muñoz S, Landais D, Martín-Gomez P, Milcu A, Piel C, Pirhofer-Walzl K, Galiano L, Schaub M, Haeni M, Ravel O, Salekin S, Tissue DT, Tjoelker MG, Voltas J, Hoch G, Dios VR (2017) Night and day – circadian regulation of night-time dark respiration and light-enhanced dark respiration in plant leaves and canopies. Environ Exp Bot 137:14–25. https://doi.org/10.1016/j.envexpbot.2017.01.014
Gibon Y, Bläsing OE, Palacios-Rojas N, Pankovic D, Hendriks JH, Fisahn J, Höhne M, Günther M, Stitt M (2004) Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period. Plant J 39:847–862. https://doi.org/10.1111/j.1365-313X.2004.02173.x
Gommers CMM, Monte E (2018) Seedling establishment: a dimmer switch-regulated process between dark and light signaling. Plant Physiol 176:1061–1074. https://doi.org/10.1104/pp.17.01460
Hartmann H, Adams HD, Hammond WH, Hoch G, Landhäusser SM, Wiley E, Zaehle S (2018) Identifying differences in carbohydrate dynamics of seedlings and mature trees to improve carbon allocation in models for trees and forests. Environ Exp Bot 152:7–18. https://doi.org/10.1016/j.envexpbot.2018.03.011
Li J, Wu L, Foster R, Ruan Y-L (2017) Molecular regulation of sucrose catabolism and sugar transport for development, defence and phloem function. J Integr Plant Biol 59:322–335. https://doi.org/10.1111/jipb.12539
Li J, Zhou W, Francisco P, Wong R, Zhang D, Smith SM (2017) Inhibition of Arabidopsis chloroplast β-amylase BAM3 by maltotriose suggests a mechanism for the control of transitory leaf starch mobilisation. PLoS ONE 12:e0172504. https://doi.org/10.1371/journal.pone.0172504
MacNeill GJ, Mehrpouya S, Minow MAA, Patterson JA, Tetlow IJ, Emes MJ (2017) Starch as a source, starch as a sink: the bifunctional role of starch in carbon allocation. J Exp Bot 68:4433–4453. https://doi.org/10.1093/jxb/erx291
Martínez-Vilalta J, Sala A, Asensio D, Galiano L, Hoch G, Palacio S, Piper FI, Lloret F (2016) Dynamics of non-structural carbohydrates in terrestrial plants: a global synthesis. Ecol Monogr 86:495–516. https://doi.org/10.1002/ecm.1231
Mccready RM, Guggolz A, Silveira V, Owens HS (1950) Determination of starch and amylase in vegetables: application to peas. Anal Chem 22:1156–1158. https://doi.org/10.1021/ac60045a016
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428. https://doi.org/10.1021/ac60147a030
Morris DL (1948) Quantitative determination of carbohydrates with Dreywood’s anthrone reagent. Science 107:111–114. https://doi.org/10.1126/science.107.2775.254
Oliveira DP, Oliveira LEM, Delú-Filho N (2006) Optimization of invertase assay conditions in rubber tree plants (Hevea brasiliensis Muell. Arg). Rev Árvore 30:687–692. https://doi.org/10.1590/S0100-67622006000500001
Oren I, Mannerheim N, Dumbur R, Fangmeier A, Buchmann N, Grünzweig JM (2020) Patterns and dynamics of canopy-root coupling in tropical tree saplings vary with light intensity but not with root depth. New Phytol 225:727–739. https://doi.org/10.1111/nph.16153
Proels RK, Hückelhoven R (2014) Cell-wall invertases, key enzymes in the modulation of plant metabolism during defence responses. Mol Plant Pathol 15:858–864. https://doi.org/10.1111/mpp.12139
Rodrigues RD, Silva AF, Cavalcanti MIP, Escobar IEC, Fraiz ACR, Ribeiro PRA, Ferreira-Neto RA, Freitas ADS, Fernandes-Júnior PI (2018) Phenotypic, genetic and symbiotic characterization of Erythrina velutina rhizobia from Caatinga dry forest. Braz J Microbiol 39:503–512. https://doi.org/10.1016/j.bjm.2017.09.007
Santos MG, Oliveira MT, Figueiredo KV, Falcão HM, Arruda CP, Cortez-Almeida J, Sampaio EVS, Ometto JPHB, Menezes RSC, Oliveira AFM, Pompelli MF, Antonino ACD (2014) Caatinga, the Brazilian dry tropical forest: can it tolerate climate changes? Theor Exp Plant Physiol 26:83–99. https://doi.org/10.1007/s40626-014-0008-0
Sevanto S, McDowell NG, Dickman LT, Pangle R, Pockman WT (2014) How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant Cell Environ 37:153–161. https://doi.org/10.1111/pce.12141
Silva KB, Alves EU, Bruno RLA, Matos VP, Gonçalves EP (2008) Morphology of fruits, seeds and seedlings of Erythrina velutina willd., Leguminoseae – Papilionideae. J Seed Sci 30:104–114. https://doi.org/10.1590/S0101-31222008000300014
Skryhan K, Gurrieri L, Sparla F, Trost P, Blennow A (2018) Redox regulation of starch metabolism. Front Plant Sci 9:1344. https://doi.org/10.3389/fpls.2018.01344
Smirnova J, Fernie AR, Steup M (2015) Starch degradation. In: Nakamura Y (ed) Starch. Springer, Tokyo, pp 239–290
Soriano D, Huante P, Buen AG, Orozco-Segovia A (2013) Seed reserve translocation and early seedling growth of eight tree species in a tropical deciduous forest in Mexico. Plant Ecol 214:3161–3175. https://doi.org/10.1007/s11258-013-0257-z
Tixier A, Orozco J, Roxas AA, Earles JM, Zwieniecki MA (2018) Diurnal variation in nonstructural carbohydrate storage in trees: remobilization and vertical mixing. Plant Physiol 178:1602–1613. https://doi.org/10.1104/pp.18.00923
Van Handel E (1968) Direct microdetermination of sucrose. Anal Biochem 22:280–283. https://doi.org/10.1016/0003-2697(68)90317-5
Villar-Salvador P, Uscola M, Jacobs DF (2015) The role of stored carbohydrates and nitrogen in the growth and stress tolerance of planted forest trees. New For 46:813–839. https://doi.org/10.1007/s11056-015-9499-z
Wan H, Wu L, Yang Y, Zhou G, Ruan Y-L (2018) Evolution of sucrose metabolism: the dichotomy of invertases and beyond. Trends Plant Sci 23:163–177. https://doi.org/10.1016/j.tplants.2017.11.001
Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514. https://doi.org/10.1042/bj0570508
Acknowledgements
The authors thank to Universidade Federal do Rio Grande do Norte for supporting the research and Dr. Juliana Espada Lichston as she kindly provided the infrared gas analyser for the CO2 uptake measurements.
Funding
This work was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (fellowship granted to Maryelle Campos-Silva) and Universidade Federal do Rio Grande do Norte (fellowship granted to Herley Carlos Bezerra-de-Oliveira).
Author information
Authors and Affiliations
Contributions
ELV and DFAO conceived and designed the experiment; MCS, HCBO, JDFF, and TMF carried out the experiment and made CO2 uptake measurements, seedling harvests, and NSC quantification; MCS and DFAO carried out enzyme assays, calculated NSC contents and enzyme activities, and performed statistical analysis; ELV, MCS, and DFAO wrote the 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.
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
Campos-Silva, M., Alves-de-Oliveira, D.F., Bezerra-de-Oliveira, H.C. et al. Circadian characterization of non-structural carbohydrate dynamics in the Caatinga pioneer tree Erythrina velutina during late seedling establishment. New Forests (2023). https://doi.org/10.1007/s11056-023-10017-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11056-023-10017-7