May 5, 2024
Export of defensive glucosinolates is key for their accumulation in seeds – Nature

Export of defensive glucosinolates is key for their accumulation in seeds – Nature

  • Schroeder, J. I. et al. Using membrane transporters to improve crops for sustainable food production. Nature 497, 60–66 (2013).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Moore, J. W. et al. A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nat. Genet. 47, 1494–1498 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Krattinger, S. G. et al. The wheat durable, multipathogen resistance gene Lr34 confers partial blast resistance in rice. Plant Biotechnol. J. 14, 1261–1268 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Oliva, R. et al. Broad-spectrum resistance to bacterial blight in rice using genome editing. Nat. Biotechnol. 37, 1344–1350 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nour-Eldin, H. H. et al. Reduction of antinutritional glucosinolates in Brassica oilseeds by mutation of genes encoding transporters. Nat. Biotechnol. 35, 377–382 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zhang, J. et al. NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nat. Biotechnol. 37, 676–684 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Nour-Eldin, H. H. et al. NRT/PTR transporters are essential for translocation of glucosinolate defence compounds to seeds. Nature 488, 531–534 (2012).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Andersen, T. G. et al. Integration of biosynthesis and long-distance transport establish organ-specific glucosinolate profiles in vegetative Arabidopsis. Plant Cell 25, 3133–3145 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jørgensen, M. E. et al. Origin and evolution of transporter substrate specificity within the NPF family. eLife 6, e19466 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Xu, D. et al. Rhizosecretion of stele-synthesized glucosinolates and their catabolites requires GTR-mediated import in Arabidopsis. J. Exp. Bot. 68, 3205–3214 (2016).

    PubMed Central 

    Google Scholar
     

  • Madsen, S. R., Olsen, C. E., Nour-Eldin, H. H. & Halkier, B. A. Elucidating the role of transport processes in leaf glucosinolate distribution. Plant Physiol. 166, 1450–1462 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Xu, D. et al. GTR-mediated radial import directs accumulation of defensive glucosinolates to sulfur-rich cells in the phloem cap of Arabidopsis inflorescence stem. Mol. Plant 12, 1474–1484 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Dreyer, I. Nutrient cycling is an important mechanism for homeostasis in plant cells. Plant Physiol. 187, 2246–2261 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Feeny, P. in Biochemical Interaction Between Plants and Insects (eds Wallace, J. W. & Mansell, R. L.) 1–40 (Springer, 1976); https://doi.org/10.1007/978-1-4684-2646-5_1.

  • Hunziker, P. et al. Herbivore feeding preference corroborates optimal defence theory for specialized metabolites within plants. Proc. Natl Acad. Sci. USA 118, e2111977118 (2021).

  • Sánchez-Pérez, R. et al. Mutation of a bHLH transcription factor allowed almond domestication. Science 364, 1095–1098 (2019).

    Article 
    ADS 
    PubMed 

    Google Scholar
     

  • Itkin, M. et al. Biosynthesis of antinutritional alkaloids in solanaceous crops is mediated by clustered genes. Science 341, 175–179 (2013).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Khazaei, H. et al. Eliminating vicine and convicine, the main anti-nutritional factors restricting faba bean usage. Trends Food Sci. Technol. 91, 549–556 (2019).

    Article 
    CAS 

    Google Scholar
     

  • Alseekh, S. et al. Domestication of crop metabolomes: desired and unintended consequences. Trends Plant Sci. 26, 650–661 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Inglis, I. R., Wadsworth, J. T., Meyer, A. N. & Feare, C. J. Vertebrate damage to 00 and 0 varieties of oilseed rape in relation to SMCO and glucosinolate concentrations in the leaves. Crop Prot. 11, 64–68 (1992).

    Article 
    CAS 

    Google Scholar
     

  • Mithen, R. in Breeding for Disease Resistance (eds Johnson, R. & Jellis, G. J.) Vol. 1, 71–83 (Springer, 1992).

  • Chen, S., Petersen, B. L., Olsen, C. E., Schulz, A. & Halkier, B. A. Long-distance phloem transport of glucosinolates in Arabidopsis. Plant Physiol. 127, 194–201 (2001).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ellerbrock, B. L., Kim, J. H. & Jander, G. Contribution of glucosinolate transport to Arabidopsis defence responses. Plant Signal. Behav. 2, 282–283 (2007).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Khan, D. et al. Transcriptome atlas of the Arabidopsis funiculus—a study of maternal seed subregions. Plant J. 82, 41–53 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Mugford, S. G. et al. Disruption of adenosine-5′-phosphosulfate kinase in Arabidopsis reduces levels of sulfated secondary metabolites. Plant Cell 21, 910–927 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ladwig, F. et al. Siliques Are Red1 from Arabidopsis acts as a bidirectional amino acid transporter that is crucial for the amino acid homeostasis of siliques. Plant Physiol. 158, 1643–1655 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Müller, B. et al. Amino acid export in developing Arabidopsis seeds depends on umamit facilitators. Curr. Biol. 25, 3126–3131 (2015).

    Article 
    PubMed 

    Google Scholar
     

  • Besnard, J. et al. Arabidopsis UMAMIT24 and 25 are amino acid exporters involved in seed loading. J. Exp. Bot. 69, 5221–5232 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhao, C. et al. Detailed characterization of the UMAMIT proteins provides insight into their evolution, amino acid transport properties, and role in the plant. J. Exp. Bot. 72, 6400–6417 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Fang, Z. T., Kapoor, R., Datta, A. & Okumoto, S. Tissue specific expression of UMAMIT amino acid transporters in wheat. Sci. Rep. 12, 348 (2022).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dindas, J. et al. AUX1-mediated root hair auxin influx governs SCFTIR1/AFB-type Ca2+ signaling. Nat. Commun. 9, 1174 (2018).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chen, L.-Q. et al. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468, 527–532 (2010).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chen, L.-Q. et al. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335, 207–211 (2012).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Payne, R. M. E. et al. An NPF transporter exports a central monoterpene indole alkaloid intermediate from the vacuole. Nat. Plants 3, 16208 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Larsen, B. et al. Identification of iridoid glucoside transporters in Catharanthus roseus. Plant Cell Physiol. 58, 1507–1518 (2017).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Belew, Z. M. et al. Identification and characterization of phlorizin transporter from Arabidopsis thaliana and its application for phlorizin production in Saccharomyces cerevisiae. Preprint at BioRxiv https://doi.org/10.1101/2020.08.14.248047 (2020).

  • Grunewald, S. et al. The tapetal major facilitator NPF2.8 is required for accumulation of flavonol glycosides on the pollen surface in Arabidopsis thaliana. Plant Cell 32, 1727–1748 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kazachkova, Y. et al. The GORKY glycoalkaloid transporter is indispensable for preventing tomato bitterness. Nat. Plants 7, 468–480 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kanstrup, C. & Nour-Eldin, H. H. The emerging role of the nitrate and peptide transporter family: NPF in plant specialized metabolism. Curr. Opin. Plant Biol. 68, 102243 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Halkier, B. A. & Xu, D. The ins and outs of transporters at plasma membrane and tonoplast in plant specialized metabolism. Nat. Prod. Rep. 39, 1483–1491 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Slaten, M. L. et al. mGWAS uncovers Gln-glucosinolate seed-specific interaction and its role in metabolic homeostasis. Plant Physiol. 183, 483–500 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schulz, A. et al. Proton-driven sucrose symport and antiport are provided by the vacuolar transporters SUC4 and TMT1/2. Plant J. 68, 129–136 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bezrutczyk, M. et al. Impaired phloem loading in zmsweet13a,b,c sucrose transporter triple knock-out mutants in Zea mays. New Phytol. 218, 594–603 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Karmann, J., Müller, B. & Hammes, U. Z. The long and winding road: transport pathways for amino acids in Arabidopsis seeds. Plant Reprod. 31, 253–261 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kim, J.-Y. et al. Cellular export of sugars and amino acids: role in feeding other cells and organisms. Plant Physiol. 187, 1893–1914 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • He, Y. et al. Enhancing canola breeding by editing a glucosinolate transporter gene lacking natural variation. Plant Physiol. 188, 1848–1851 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nintemann, S. J. et al. Localization of the glucosinolate biosynthetic enzymes reveals distinct spatial patterns for the biosynthesis of indole and aliphatic glucosinolates. Physiol. Plant. 163, 138–154 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Liu, H. et al. CRISPR-P 2.0: an improved CRISPR–Cas9 tool for genome editing in plants. Mol. Plant 10, 530–532 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wang, Z.-P. et al. Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biol. 16, 144 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tsutsui, H. & Higashiyama, T. pKAMA-ITACHI vectors for highly efficient CRISPR/Cas9-mediated gene knockout in Arabidopsis thaliana. Plant Cell Physiol. 58, 46–56 (2017).

    CAS 
    PubMed 

    Google Scholar
     

  • Nisar, N., Verma, S., Pogson, B. J. & Cazzonelli, C. I. Inflorescence stem grafting made easy in Arabidopsis. Plant Methods 8, 50 (2012).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Goedhart, J. et al. Structure-guided evolution of cyan fluorescent proteins towards a quantum yield of 93%. Nat. Commun. 3, 751 (2012).

    Article 
    ADS 
    PubMed 

    Google Scholar
     

  • Kurihara, D., Mizuta, Y., Sato, Y. & Higashiyama, T. ClearSee: a rapid optical clearing reagent for whole-plant fluorescence imaging. Development 142, 4168–4179 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jørgensen, M. E., Crocoll, C., Halkier, B. A. & Nour-Eldin, H. H. Uptake assays in Xenopus laevis oocytes using liquid chromatography-mass spectrometry to detect transport activity. Bio Protoc. 7, e2581 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jensen, L. M., Jepsen, H. S. K., Halkier, B. A., Kliebenstein, D. J. & Burow, M. Natural variation in cross-talk between glucosinolates and onset of flowering in Arabidopsis. Front. Plant Sci. 6, 697 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Crocoll, C., Halkier, B. A. & Burow, M. Analysis and quantification of glucosinolates. Curr. Protoc. Plant Biol. 1, 385–409 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Mirza, N., Crocoll, C., Erik Olsen, C. & Ann Halkier, B. Engineering of methionine chain elongation part of glucoraphanin pathway in E. coli. Metab. Eng. 35, 31–37 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Petersen, A., Crocoll, C. & Halkier, B. A. De novo production of benzyl glucosinolate in Escherichia coli. Metab. Eng. 54, 24–34 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Criscuolo, A. & Gribaldo, S. BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol. Biol. 10, 210 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lemoine, F. et al. NGPhylogeny.fr: new generation phylogenetic services for non-specialists. Nucleic Acids Res. 47, W260–W265 (2019).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Trifinopoulos, J., Nguyen, L.-T., von Haeseler, A. & Minh, B. Q. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 44, W232–W235 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 49, W293–W296 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Source link