TY - JOUR

T1 - Cellular plasticity in response to suppression of storage proteins in the brassica napus embryo

AU - Rolletschek, Hardy

AU - Schwender, Jörg

AU - König, Christina

AU - Chapman, Kent D

AU - Romsdahl, Trevor

AU - Lorenz, Christin

AU - Braun, Hans-Peter

AU - Denolf, Peter

AU - Audenhove, Katrien van

AU - Munz, Eberhard

AU - Heinzel, Nicolas

AU - Ortleb, Stefan

AU - Rutten, Twan

AU - McCorkle, Sean

AU - Borysyuk, Taras

AU - Gündel, André

AU - Shi, Hai

AU - Vander Auwermeulen, Michiel

AU - Bourot, Stéphane

AU - Borisjuk, Ljudmilla

N1 - Funding Information: We thank Julie Claeys (BASF) for the production of the plant transformation vectors, Volodymyr Radchuk (Leibniz Institute of Plant Genetics and Crop Plant Research [IPK]) and Anne Fiebig (IPK) for support in bioinformatics, Yudelsy A.T. Moya (IPK) for performing the inductively coupled plasma optical emission spectroscopy experiments, Henning Tschiersch (IPK) for helpwiththePAMimaging,andSteffenWagner(IPK)andSabineHerrmann (IPK) for technical support. This work was supported by the U.S. Department of Energy (grant DE-SC0012704 to J.S., H.S., and S.M. and grant DE-SC0016536 to K.D.C.) and by the Deutsche Forschungsgemein-schaft (grants 223207907 and 397750294 to H.R. and L.B.).

PY - 2020/4/30

Y1 - 2020/4/30

N2 - The tradeoff between protein and oil storage in oilseed crops has been tested here in oilseed rape (Brassica napus) by analyzing the effect of suppressing key genes encoding protein storage products (napin and cruciferin). The phenotypic outcomes were assessed using NMR and mass spectrometry imaging, microscopy, transcriptomics, proteomics, metabolomics, lipidomics, immunological assays, and flux balance analysis. Surprisingly, the profile of storage products was only moderately changed in RNA interference transgenics. However, embryonic cells had undergone remarkable architectural rearrangements. The suppression of storage proteins led to the elaboration of membrane stacks enriched with oleosin (sixfold higher protein abundance) and novel endoplasmic reticulum morphology. Protein rebalancing and amino acid metabolism were focal points of the metabolic adjustments to maintain embryonic carbon/nitrogen homeostasis. Flux balance analysis indicated a rather minor additional demand for cofactors (ATP and NADPH). Thus, cellular plasticity in seeds protects against perturbations to its storage capabilities and, hence, contributes materially to homeostasis. This study provides mechanistic insights into the intriguing link between lipid and protein storage, which have implications for biotechnological strategies directed at improving oilseed crops.

AB - The tradeoff between protein and oil storage in oilseed crops has been tested here in oilseed rape (Brassica napus) by analyzing the effect of suppressing key genes encoding protein storage products (napin and cruciferin). The phenotypic outcomes were assessed using NMR and mass spectrometry imaging, microscopy, transcriptomics, proteomics, metabolomics, lipidomics, immunological assays, and flux balance analysis. Surprisingly, the profile of storage products was only moderately changed in RNA interference transgenics. However, embryonic cells had undergone remarkable architectural rearrangements. The suppression of storage proteins led to the elaboration of membrane stacks enriched with oleosin (sixfold higher protein abundance) and novel endoplasmic reticulum morphology. Protein rebalancing and amino acid metabolism were focal points of the metabolic adjustments to maintain embryonic carbon/nitrogen homeostasis. Flux balance analysis indicated a rather minor additional demand for cofactors (ATP and NADPH). Thus, cellular plasticity in seeds protects against perturbations to its storage capabilities and, hence, contributes materially to homeostasis. This study provides mechanistic insights into the intriguing link between lipid and protein storage, which have implications for biotechnological strategies directed at improving oilseed crops.

UR - http://www.scopus.com/inward/record.url?scp=85089128913&partnerID=8YFLogxK

U2 - 10.1105/tpc.19.00879

DO - 10.1105/tpc.19.00879

M3 - Article

C2 - 32358071

VL - 32

SP - 2383

EP - 2401

JO - The plant cell

JF - The plant cell

SN - 1040-4651

IS - 7

ER -