Loading [MathJax]/extensions/tex2jax.js

Seed Architecture Shapes Embryo Metabolism in Oilseed Rape

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Ljudmilla Borisjuk
  • Thomas Neuberger
  • Jörg Schwender
  • Nicolas Heinzel
  • Hans Peter Braun

Research Organisations

External Research Organisations

  • Leibniz Institute of Plant Genetics and Crop Plant Research (IPK)
  • Pennsylvania State University
  • Brookhaven National Laboratory (BNL)
  • Julius Maximilian University of Würzburg
  • Bayer Corporation - USA
  • Research Center Magnetic Resonance Bavaria

Details

Original languageEnglish
Pages (from-to)1625-1640
Number of pages16
JournalPLANT CELL
Volume25
Issue number5
Publication statusPublished - May 2013

Abstract

Constrained to develop within the seed, the plant embryo must adapt its shape and size to fit the space available. Here, we demonstrate how this adjustment shapes metabolism of photosynthetic embryo. Noninvasive NMR-based imaging of the developing oilseed rape (Brassica napus) seed illustrates that, following embryo bending, gradients in lipid concentration became established. These were correlated with the local photosynthetic electron transport rate and the accumulation of storage products. Experimentally induced changes in embryo morphology and/or light supply altered these gradients and were accompanied by alterations in both proteome and metabolome. Tissue-specific metabolic models predicted that the outer cotyledon and hypocotyl/radicle generate the bulk of plastidic reductant/ATP via photosynthesis, while the inner cotyledon, being enclosed by the outer cotyledon, is forced to grow essentially heterotrophically. Under field-relevant highlight conditions, major contribution of the ribulose-1,5-bisphosphate carboxylase/oxygenase-bypass to seed storage metabolism is predicted for the outer cotyledon and the hypocotyl/radicle only. Differences between in vitro- versus in planta-grown embryos suggest that metabolic heterogeneity of embryo is not observable by in vitro approaches. We conclude that in vivo metabolic fluxes are locally regulated and connected to seed architecture, driving the embryo toward an efficient use of available light and space.

ASJC Scopus subject areas

Cite this

Seed Architecture Shapes Embryo Metabolism in Oilseed Rape. / Borisjuk, Ljudmilla; Neuberger, Thomas; Schwender, Jörg et al.
In: PLANT CELL, Vol. 25, No. 5, 05.2013, p. 1625-1640.

Research output: Contribution to journalArticleResearchpeer review

Borisjuk, L, Neuberger, T, Schwender, J, Heinzel, N, Sunderhaus, S, Fuchs, J, Hay, JO, Tschiersch, H, Braun, HP, Denolf, P, Lambert, B, Jakob, PM & Rolletschek, H 2013, 'Seed Architecture Shapes Embryo Metabolism in Oilseed Rape', PLANT CELL, vol. 25, no. 5, pp. 1625-1640. https://doi.org/10.1105/tpc.113.111740, https://doi.org/10.15488/11686
Borisjuk, L., Neuberger, T., Schwender, J., Heinzel, N., Sunderhaus, S., Fuchs, J., Hay, J. O., Tschiersch, H., Braun, H. P., Denolf, P., Lambert, B., Jakob, P. M., & Rolletschek, H. (2013). Seed Architecture Shapes Embryo Metabolism in Oilseed Rape. PLANT CELL, 25(5), 1625-1640. https://doi.org/10.1105/tpc.113.111740, https://doi.org/10.15488/11686
Borisjuk L, Neuberger T, Schwender J, Heinzel N, Sunderhaus S, Fuchs J et al. Seed Architecture Shapes Embryo Metabolism in Oilseed Rape. PLANT CELL. 2013 May;25(5):1625-1640. doi: 10.1105/tpc.113.111740, 10.15488/11686
Borisjuk, Ljudmilla ; Neuberger, Thomas ; Schwender, Jörg et al. / Seed Architecture Shapes Embryo Metabolism in Oilseed Rape. In: PLANT CELL. 2013 ; Vol. 25, No. 5. pp. 1625-1640.
Download
@article{c8661c614880486d8e4ec0a266de1cb0,
title = "Seed Architecture Shapes Embryo Metabolism in Oilseed Rape",
abstract = "Constrained to develop within the seed, the plant embryo must adapt its shape and size to fit the space available. Here, we demonstrate how this adjustment shapes metabolism of photosynthetic embryo. Noninvasive NMR-based imaging of the developing oilseed rape (Brassica napus) seed illustrates that, following embryo bending, gradients in lipid concentration became established. These were correlated with the local photosynthetic electron transport rate and the accumulation of storage products. Experimentally induced changes in embryo morphology and/or light supply altered these gradients and were accompanied by alterations in both proteome and metabolome. Tissue-specific metabolic models predicted that the outer cotyledon and hypocotyl/radicle generate the bulk of plastidic reductant/ATP via photosynthesis, while the inner cotyledon, being enclosed by the outer cotyledon, is forced to grow essentially heterotrophically. Under field-relevant highlight conditions, major contribution of the ribulose-1,5-bisphosphate carboxylase/oxygenase-bypass to seed storage metabolism is predicted for the outer cotyledon and the hypocotyl/radicle only. Differences between in vitro- versus in planta-grown embryos suggest that metabolic heterogeneity of embryo is not observable by in vitro approaches. We conclude that in vivo metabolic fluxes are locally regulated and connected to seed architecture, driving the embryo toward an efficient use of available light and space.",
author = "Ljudmilla Borisjuk and Thomas Neuberger and J{\"o}rg Schwender and Nicolas Heinzel and Stephanie Sunderhaus and Johannes Fuchs and Hay, {Jordan O.} and Henning Tschiersch and Braun, {Hans Peter} and Peter Denolf and Bart Lambert and Jakob, {Peter M.} and Hardy Rolletschek",
year = "2013",
month = may,
doi = "10.1105/tpc.113.111740",
language = "English",
volume = "25",
pages = "1625--1640",
journal = "PLANT CELL",
issn = "1040-4651",
publisher = "American Society of Plant Biologists",
number = "5",

}

Download

TY - JOUR

T1 - Seed Architecture Shapes Embryo Metabolism in Oilseed Rape

AU - Borisjuk, Ljudmilla

AU - Neuberger, Thomas

AU - Schwender, Jörg

AU - Heinzel, Nicolas

AU - Sunderhaus, Stephanie

AU - Fuchs, Johannes

AU - Hay, Jordan O.

AU - Tschiersch, Henning

AU - Braun, Hans Peter

AU - Denolf, Peter

AU - Lambert, Bart

AU - Jakob, Peter M.

AU - Rolletschek, Hardy

PY - 2013/5

Y1 - 2013/5

N2 - Constrained to develop within the seed, the plant embryo must adapt its shape and size to fit the space available. Here, we demonstrate how this adjustment shapes metabolism of photosynthetic embryo. Noninvasive NMR-based imaging of the developing oilseed rape (Brassica napus) seed illustrates that, following embryo bending, gradients in lipid concentration became established. These were correlated with the local photosynthetic electron transport rate and the accumulation of storage products. Experimentally induced changes in embryo morphology and/or light supply altered these gradients and were accompanied by alterations in both proteome and metabolome. Tissue-specific metabolic models predicted that the outer cotyledon and hypocotyl/radicle generate the bulk of plastidic reductant/ATP via photosynthesis, while the inner cotyledon, being enclosed by the outer cotyledon, is forced to grow essentially heterotrophically. Under field-relevant highlight conditions, major contribution of the ribulose-1,5-bisphosphate carboxylase/oxygenase-bypass to seed storage metabolism is predicted for the outer cotyledon and the hypocotyl/radicle only. Differences between in vitro- versus in planta-grown embryos suggest that metabolic heterogeneity of embryo is not observable by in vitro approaches. We conclude that in vivo metabolic fluxes are locally regulated and connected to seed architecture, driving the embryo toward an efficient use of available light and space.

AB - Constrained to develop within the seed, the plant embryo must adapt its shape and size to fit the space available. Here, we demonstrate how this adjustment shapes metabolism of photosynthetic embryo. Noninvasive NMR-based imaging of the developing oilseed rape (Brassica napus) seed illustrates that, following embryo bending, gradients in lipid concentration became established. These were correlated with the local photosynthetic electron transport rate and the accumulation of storage products. Experimentally induced changes in embryo morphology and/or light supply altered these gradients and were accompanied by alterations in both proteome and metabolome. Tissue-specific metabolic models predicted that the outer cotyledon and hypocotyl/radicle generate the bulk of plastidic reductant/ATP via photosynthesis, while the inner cotyledon, being enclosed by the outer cotyledon, is forced to grow essentially heterotrophically. Under field-relevant highlight conditions, major contribution of the ribulose-1,5-bisphosphate carboxylase/oxygenase-bypass to seed storage metabolism is predicted for the outer cotyledon and the hypocotyl/radicle only. Differences between in vitro- versus in planta-grown embryos suggest that metabolic heterogeneity of embryo is not observable by in vitro approaches. We conclude that in vivo metabolic fluxes are locally regulated and connected to seed architecture, driving the embryo toward an efficient use of available light and space.

UR - http://www.scopus.com/inward/record.url?scp=84879473895&partnerID=8YFLogxK

U2 - 10.1105/tpc.113.111740

DO - 10.1105/tpc.113.111740

M3 - Article

C2 - 23709628

AN - SCOPUS:84879473895

VL - 25

SP - 1625

EP - 1640

JO - PLANT CELL

JF - PLANT CELL

SN - 1040-4651

IS - 5

ER -

By the same author(s)