Transitions in wheat endosperm metabolism upon transcriptional induction of oil accumulation by oat endosperm WRINKLED1

A - Papers appearing in refereed journals

Grimberg, A., Wilkinson, M. D., Snell, P., De Vos, R. P., Gonzalez-Thuillier, I., Tawfike, A., Ward, J. L., Carlsson, A. S., Shewry, P. R. and Hofvander, P. 2020. Transitions in wheat endosperm metabolism upon transcriptional induction of oil accumulation by oat endosperm WRINKLED1 . BMC Plant Biology. 20, p. 235.

AuthorsGrimberg, A., Wilkinson, M. D., Snell, P., De Vos, R. P., Gonzalez-Thuillier, I., Tawfike, A., Ward, J. L., Carlsson, A. S., Shewry, P. R. and Hofvander, P.
Abstract

Background: Cereal grains, including wheat (Triticum aestivum L.), are major sources of food and feed, with wheat being dominant in temperate zones. These end uses exploit the storage reserves in the starchy endosperm of the grain, with starch being the major storage component in most cereal species. However, oats (Avena sativa L.) differs in that the starchy endosperm stores significant amounts of oil. Understanding the control of carbon allocation between groups of storage compounds, such as starch and oil, is therefore important for understanding the composition and hence end use quality of cereals. WRINKLED1 is a transcription factor known to induce triacylglycerol (TAG; oil) accumulation in several plant storage tissues.
Results: An oat endosperm homolog of WRI1 (AsWRI1) expressed from the endosperm-specific HMW1Dx5 promoter resulted in drastic changes in carbon allocation in wheat grains, with reduced seed weight and a wrinkled seed phenotype. The starch content of mature grain endosperms of AsWRI1-wheat was reduced compared to controls (from 62 to 22% by dry weight (dw)), TAG was increased by up to nine-fold (from 0.7 to 6.4% oil by dw) and sucrose from 1.5 to 10% by dw. Expression of AsWRI1 in wheat grains also resulted in multiple layers of elongated peripheral aleurone cells. RNA-sequencing, lipid analyses, and pulse-chase experiments using 14C-sucrose indicated that futile cycling of fatty acids could be a limitation for oil accumulation.
Conclusions: Our data show that expression of oat endosperm WRI1 in the wheat endosperm results in changes in metabolism which could underpin the application of biotechnology to manipulate grain composition. In particular, the striking effect on starch synthesis in the wheat endosperm indicates that an important indirect role of WRI1 is to divert carbon allocation away from starch biosynthesis in plant storage tissues that accumulate oil.

KeywordsAleurone; Cereal endosperm; Oil biosynthesis; Transcriptional regulation; Triacylglycerol; Wheat; WRINKLED1
Year of Publication2020
JournalBMC Plant Biology
Journal citation20, p. 235
Digital Object Identifier (DOI)doi:10.1186/s12870-020-02438-9
Open accessPublished as bronze (free) open access
FunderBiotechnology and Biological Sciences Research Council
Funder project or codeDesigning Future Wheat (DFW) [ISPG]
Publisher's version
Output statusPublished
Publication dates
Online25 May 2020
Publication process dates
Accepted10 May 2020
PublisherBiomed Central Ltd
ISSN1471-2229

Permalink - https://repository.rothamsted.ac.uk/item/97vy1/transitions-in-wheat-endosperm-metabolism-upon-transcriptional-induction-of-oil-accumulation-by-oat-endosperm-wrinkled1

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