Export of defensive glucosinolates is key for their accumulation in seeds

Xu, Deyang; Sanden, Niels Christian; Hansen, Line Lykke; Belew, Zeinu Mussa; Madsen, Svend Roesen; Meyer, Lasse; Jørgensen, Morten; Hunziker, Pascal; Veres, Dorottya; Crocoll, Christoph; Schulz, Alexander; Nour-Eldin, Hussam Hassan; Halkier, Barbara Ann

doi:10.1038/s41586-023-05969-x

Cited by 29 publications

(12 citation statements)

References 63 publications

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“…However, being an anti-nutritional factor, it can significantly impinge on the taste and nutritional value of the plant's edible tissues. As a result, the use of metabolic engineering strategies aimed at enriching rice seeds with glucosinolates would not be considered an optimal choice either (Xu et al 2023 ). In recent years, the strong activity against rice leaf blast of sakuranetin has been revealed by many studies (Kodama et al 1992 ; Hasegawa et al 2014 ; Murata et al 2020 ).…”

Section: Discussionmentioning

confidence: 99%

Biofortified Rice Provides Rich Sakuranetin in Endosperm

Zhao,

Hu,

Zhou

et al. 2024

Rice

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Sakuranetin plays a key role as a phytoalexin in plant resistance to biotic and abiotic stresses, and possesses diverse health-promoting benefits. However, mature rice seeds do not contain detectable levels of sakuranetin. In the present study, a transgenic rice plant was developed in which the promoter of an endosperm-specific glutelin gene OsGluD-1 drives the expression of a specific enzyme naringenin 7-O-methyltransferase (NOMT) for sakuranetin biosynthesis. The presence of naringenin, which serves as the biosynthetic precursor of sakuranetin made this modification feasible in theory. Liquid chromatography tandem mass spectrometry (LC–MS/MS) validated that the seeds of transgenic rice accumulated remarkable sakuranetin at the mature stage, and higher at the filling stage. In addition, the panicle blast resistance of transgenic rice was significantly higher than that of the wild type. Specially, the matrix-assisted laser desorption/ionization mass spectrometry (MALDI-MS) imaging was performed to detect the content and spatial distribution of sakuranetin and other nutritional metabolites in transgenic rice seeds. Notably, this genetic modification also did not change the nutritional and quality indicators such as soluble sugars, total amino acids, total flavonoids, amylose, total protein, and free amino acid content in rice. Meanwhile, the phenotypes of the transgenic plant during the whole growth and developmental periods and agricultural traits such as grain width, grain length, and 1000-grain weight exhibited no significant differences from the wild type. Collectively, the study provides a conceptual advance on cultivating sakuranetin-rich biofortified rice by metabolic engineering. This new breeding idea may not only enhance the disease resistance of cereal crop seeds but also improve the nutritional value of grains for human health benefits.

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Section: Discussionmentioning

confidence: 99%

Biofortified Rice Provides Rich Sakuranetin in Endosperm

Zhao,

Hu,

Zhou

et al. 2024

Rice

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“…Glucosinolates are the major defence compounds in species belonging to the Brassicaceae family, including the Brassica species belonging to the U's triangle that are cultivated globally as oilseed and vegetable crops. It is now well‐established that seed lacks the glucosinolates biosynthesis machinery and most of the seed‐bound glucosinolates are synthesized in reproductive organs including silique walls and rosette (Jørgensen et al ., 2015 ; Xu et al ., 2023 ). The most involved work on the glucosinolate transport mechanism has been carried out on the model plant A. thaliana where two genes, GTR1 and GTR2 , were shown to be involved with the transport of glucosinolates from source tissues to the seeds (Nour‐Eldin et al ., 2012 ).…”

Section: Discussionmentioning

confidence: 99%

“…Nonetheless, studies in both Arabidopsis and polyploid B. juncea strengthen the fact that the GTR1 and GTR2 genes play a critical role in transporting glucosinolates from source tissues (silique walls and flag leaves) to the seeds (sink). Further, our findings are in agreement with a recent study in Arabidopsis which suggests that de novo synthesis and transport within the reproductive tissues are sufficient to supply the seeds with glucosinolates (Xu et al ., 2023 ).…”

Section: Discussionmentioning

confidence: 99%

“…The conventionally bred Canola quality lines of rapeseed have become increasingly susceptible to generalist pests in Europe and elsewhere leading to increased use of pesticides for crop protection (Zheng et al ., 2020 ). The recent discovery of glucosinolate exporters (UMAMIT29, UMAMIT30, and UMAMIT31) in Arabidopsis could provide new opportunities to improve the seed meal quality of the Brassica oilseed crops, without disturbing the distribution of defence compounds in the whole plant (Xu et al ., 2023 ).…”

Section: Discussionmentioning

confidence: 99%

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Targeted editing of multiple homologues of GTR1 and GTR2 genes provides the ideal low‐seed, high‐leaf glucosinolate oilseed mustard with uncompromised defence and yield

Mann

Kumari

Kumar

et al. 2023

Plant Biotechnology Journal

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SummaryGlucosinolate content in the two major oilseed Brassica crops—rapeseed and mustard has been reduced to the globally accepted Canola quality level (<30 μmoles/g of seed dry weight, DW), making the protein‐rich seed meal useful as animal feed. However, the overall lower glucosinolate content in seeds as well as in the other parts of such plants renders them vulnerable to biotic challenges. We report CRISPR/Cas9‐based editing of glucosinolate transporter (GTR) family genes in mustard (Brassica juncea) to develop ideal lines with the desired low seed glucosinolate content (SGC) while maintaining high glucosinolate levels in the other plant parts for uncompromised plant defence. Use of three gRNAs provided highly efficient and precise editing of four BjuGTR1 and six BjuGTR2 homologues leading to a reduction of SGC from 146.09 μmoles/g DW to as low as 6.21 μmoles/g DW. Detailed analysis of the GTR‐edited lines showed higher accumulation and distributional changes of glucosinolates in the foliar parts. However, the changes did not affect the plant defence and yield parameters. When tested against the pathogen Sclerotinia sclerotiorum and generalist pest Spodoptera litura, the GTR‐edited lines displayed a defence response at par or better than that of the wild‐type line. The GTR‐edited lines were equivalent to the wild‐type line for various seed yield and seed quality traits. Our results demonstrate that simultaneous editing of multiple GTR1 and GTR2 homologues in mustard can provide the desired low‐seed, high‐leaf glucosinolate lines with an uncompromised defence and yield.

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“…GRA and GER are aliphatic GSLs derived from methionine and transplanted from biosynthesis cells to seeds [ 17 , 18 ]. In plants, GER can be catalyzed by a subclade of flavin-monooxygenases into GRA [ 19 ].…”

Section: Introductionmentioning

confidence: 99%

Unravelling Glucoraphanin and Glucoerucin Metabolism across Broccoli Sprout Development: Insights from Metabolite and Transcriptome Analysis

Wang,

Shen,

Sheng

et al. 2024

Plants

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Variations in the concentration of glucoraphanin (GRA) and glucoerucin (GER), as well as the corresponding breakdown products, isothiocyanates (ITCs) and nitriles, were investigated during the growth of broccoli sprouts. The concentrations of GRA and GER decreased sharply from 33.66 µmol/g to 11.48 µmol/g and 12.98 µmol/g to 8.23 µmol/g, respectively, after seed germination. From the third to the seventh day, both GRA and GER were maintained as relatively stable. The highest concentrations of sulforaphane (17.16 µmol/g) and erucin (12.26 µmol/g) were observed on the first day. Hereafter, the concentrations of nitrile hydrolyzed from GRA or GER were higher than those of the corresponding ITCs. Moreover, the ratio of sulforaphane to sulforaphane nitrile decreased from 1.35 to 0.164 from 1 d to 5 d, with a similar trend exhibited for erucin/erucin nitrile after 2 d. RNA-seq analysis showed that BolMYB28 and BolCYP83A1, involved in aliphatic glucosinolate (GSL) biosynthesis, remained largely unexpressed until the third day. In contrast, the genes operating within the GSL-myrosinase hydrolysis pathway were highly expressed right from the beginning, with their expression levels increasing significantly after the third day. Additionally, we identified two BolESPs and six BolNSPs that might play important roles in promoting the production of nitriles during the development of broccoli sprouts.

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Export of defensive glucosinolates is key for their accumulation in seeds

Cited by 29 publications

References 63 publications

Biofortified Rice Provides Rich Sakuranetin in Endosperm

Biofortified Rice Provides Rich Sakuranetin in Endosperm

Targeted editing of multiple homologues of GTR1 and GTR2 genes provides the ideal low‐seed, high‐leaf glucosinolate oilseed mustard with uncompromised defence and yield

Unravelling Glucoraphanin and Glucoerucin Metabolism across Broccoli Sprout Development: Insights from Metabolite and Transcriptome Analysis

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