Triacylglycerol stability limits futile cycles and inhibition of carbon capture in oil-accumulating leaves

Johnson, Brandon S.; Allen, Doug K.; Bates, Philip D.

doi:10.1093/plphys/kiae121

Title: Triacylglycerol stability limits futile cycles and inhibition of carbon capture in oil-accumulating leaves

Journal Article · 02 March 2024 · Plant Physiology (Bethesda)

DOI: https://doi.org/10.1093/plphys/kiae121 · OSTI ID:2352469

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Washington State University, Pullman, WA (United States); Washington State University
Donald Danforth Plant Science Center, St. Louis, MO (United States)
Washington State University, Pullman, WA (United States)

Engineering plant vegetative tissue to accumulate triacylglycerols (TAG, e.g. oil) can increase the amount of oil harvested per acre to levels that exceed current oilseed crops. Engineered tobacco (Nicotiana tabacum) lines that accumulate 15% to 30% oil of leaf dry weight resulted in starkly different metabolic phenotypes. In-depth analysis of the leaf lipid accumulation and ¹⁴CO₂ tracking describe metabolic adaptations to the leaf oil engineering. An oil-for-membrane lipid tradeoff in the 15% oil line (referred to as HO) was surprisingly not further exacerbated when lipid production was enhanced to 30% (LEAFY COTYLEDON 2 (LEC2) line). The HO line exhibited a futile cycle that limited TAG yield through exchange with starch, altered carbon flux into various metabolite pools and end products, and suggested interference of the glyoxylate cycle with photorespiration that limited CO₂ assimilation by 50%. In contrast, inclusion of the LEC2 transcription factor in tobacco improved TAG stability, alleviated the TAG-to-starch futile cycle, and recovered CO₂ assimilation and plant growth comparable to wild type but with much higher lipid levels in leaves. Thus, the unstable production of storage reserves and futile cycling limit vegetative oil engineering approaches. The capacity to overcome futile cycles and maintain enhanced stable TAG levels in LEC2 demonstrated the importance of considering unanticipated metabolic adaptations while engineering vegetative oil crops.

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Research Organization:: Washington State University, Pullman, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0023142

OSTI ID:: 2352469

Journal Information:: Plant Physiology (Bethesda), Journal Name: Plant Physiology (Bethesda) Journal Issue: 2 Vol. 197; ISSN 0032-0889

Publisher:: American Society of Plant BiologistsCopyright Statement

Country of Publication:: United States

Language:: English

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