Export of defensive glucosinolates is key for their accumulation in seeds

Deyang Xu (), Niels Christian Holm Sanden, Line Lykke Hansen, Zeinu Mussa Belew, Svend Roesen Madsen, Lasse Meyer, Morten Egevang Jørgensen, Pascal Hunziker, Dorottya Veres, Christoph Crocoll, Alexander Schulz, Hussam Hassan Nour-Eldin and Barbara Ann Halkier ()
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Deyang Xu: University of Copenhagen
Niels Christian Holm Sanden: University of Copenhagen
Line Lykke Hansen: University of Copenhagen
Zeinu Mussa Belew: University of Copenhagen
Svend Roesen Madsen: University of Copenhagen
Lasse Meyer: University of Copenhagen
Morten Egevang Jørgensen: Carlsberg Research Laboratory
Pascal Hunziker: University of Copenhagen
Dorottya Veres: University of Copenhagen
Christoph Crocoll: University of Copenhagen
Alexander Schulz: University of Copenhagen
Hussam Hassan Nour-Eldin: University of Copenhagen
Barbara Ann Halkier: University of Copenhagen

Nature, 2023, vol. 617, issue 7959, 132-138

Abstract: Abstract Plant membrane transporters controlling metabolite distribution contribute key agronomic traits1–6. To eliminate anti-nutritional factors in edible parts of crops, the mutation of importers can block the accumulation of these factors in sink tissues7. However, this often results in a substantially altered distribution pattern within the plant8–12, whereas engineering of exporters may prevent such changes in distribution. In brassicaceous oilseed crops, anti-nutritional glucosinolate defence compounds are translocated to the seeds. However, the molecular targets for export engineering of glucosinolates remain unclear. Here we identify and characterize members of the USUALLY MULTIPLE AMINO ACIDS MOVE IN AND OUT TRANSPORTER (UMAMIT) family—UMAMIT29, UMAMIT30 and UMAMIT31—in Arabidopsis thaliana as glucosinolate exporters with a uniport mechanism. Loss-of-function umamit29 umamit30 umamit31 triple mutants have a very low level of seed glucosinolates, demonstrating a key role for these transporters in translocating glucosinolates into seeds. We propose a model in which the UMAMIT uniporters facilitate glucosinolate efflux from biosynthetic cells along the electrochemical gradient into the apoplast, where the high-affinity H+-coupled glucosinolate importers GLUCOSINOLATE TRANSPORTERS (GTRs) load them into the phloem for translocation to the seeds. Our findings validate the theory that two differently energized transporter types are required for cellular nutrient homeostasis13. The UMAMIT exporters are new molecular targets to improve nutritional value of seeds of brassicaceous oilseed crops without altering the distribution of the defence compounds in the whole plant.

Date: 2023
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DOI: 10.1038/s41586-023-05969-x

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