Export of defensive glucosinolates is key for their accumulation in seeds.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
May 2023
May 2023
Historique:
received:
18
07
2021
accepted:
17
03
2023
medline:
5
5
2023
pubmed:
20
4
2023
entrez:
19
04
2023
Statut:
ppublish
Résumé
Plant membrane transporters controlling metabolite distribution contribute key agronomic traits
Identifiants
pubmed: 37076627
doi: 10.1038/s41586-023-05969-x
pii: 10.1038/s41586-023-05969-x
doi:
Substances chimiques
Arabidopsis Proteins
0
Glucosinolates
0
Membrane Transport Proteins
0
At4g01440 protein, Arabidopsis
0
At4g01450 protein, Arabidopsis
0
At4g01430 protein, Arabidopsis
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
132-138Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Schroeder, J. I. et al. Using membrane transporters to improve crops for sustainable food production. Nature 497, 60–66 (2013).
pubmed: 23636397
pmcid: 3954111
doi: 10.1038/nature11909
Moore, J. W. et al. A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nat. Genet. 47, 1494–1498 (2015).
pubmed: 26551671
doi: 10.1038/ng.3439
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).
pubmed: 26471973
doi: 10.1111/pbi.12491
Oliva, R. et al. Broad-spectrum resistance to bacterial blight in rice using genome editing. Nat. Biotechnol. 37, 1344–1350 (2019).
pubmed: 31659337
pmcid: 6831514
doi: 10.1038/s41587-019-0267-z
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).
pubmed: 28288105
doi: 10.1038/nbt.3823
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).
pubmed: 31036930
doi: 10.1038/s41587-019-0104-4
Nour-Eldin, H. H. et al. NRT/PTR transporters are essential for translocation of glucosinolate defence compounds to seeds. Nature 488, 531–534 (2012).
pubmed: 22864417
doi: 10.1038/nature11285
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).
pubmed: 23995084
pmcid: 3784604
doi: 10.1105/tpc.113.110890
Jørgensen, M. E. et al. Origin and evolution of transporter substrate specificity within the NPF family. eLife 6, e19466 (2017).
pubmed: 28257001
pmcid: 5336358
doi: 10.7554/eLife.19466
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).
pmcid: 5853541
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).
pubmed: 25209984
pmcid: 4226354
doi: 10.1104/pp.114.246249
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).
pubmed: 31260813
doi: 10.1016/j.molp.2019.06.008
Dreyer, I. Nutrient cycling is an important mechanism for homeostasis in plant cells. Plant Physiol. 187, 2246–2261 (2021).
pubmed: 34890457
pmcid: 8644529
doi: 10.1093/plphys/kiab217
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).
pubmed: 31197015
doi: 10.1126/science.aav8197
Itkin, M. et al. Biosynthesis of antinutritional alkaloids in solanaceous crops is mediated by clustered genes. Science 341, 175–179 (2013).
pubmed: 23788733
doi: 10.1126/science.1240230
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).
doi: 10.1016/j.tifs.2019.07.051
Alseekh, S. et al. Domestication of crop metabolomes: desired and unintended consequences. Trends Plant Sci. 26, 650–661 (2021).
pubmed: 33653662
doi: 10.1016/j.tplants.2021.02.005
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).
doi: 10.1016/0261-2194(92)90081-F
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).
pubmed: 11553747
pmcid: 117975
doi: 10.1104/pp.127.1.194
Ellerbrock, B. L., Kim, J. H. & Jander, G. Contribution of glucosinolate transport to Arabidopsis defence responses. Plant Signal. Behav. 2, 282–283 (2007).
pubmed: 19704682
pmcid: 2634151
doi: 10.4161/psb.2.4.4014
Khan, D. et al. Transcriptome atlas of the Arabidopsis funiculus—a study of maternal seed subregions. Plant J. 82, 41–53 (2015).
pubmed: 25684030
doi: 10.1111/tpj.12790
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).
pubmed: 19304933
pmcid: 2671714
doi: 10.1105/tpc.109.065581
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).
pubmed: 22312005
pmcid: 3320175
doi: 10.1104/pp.111.192583
Müller, B. et al. Amino acid export in developing Arabidopsis seeds depends on umamit facilitators. Curr. Biol. 25, 3126–3131 (2015).
pubmed: 26628011
doi: 10.1016/j.cub.2015.10.038
Besnard, J. et al. Arabidopsis UMAMIT24 and 25 are amino acid exporters involved in seed loading. J. Exp. Bot. 69, 5221–5232 (2018).
pubmed: 30312461
pmcid: 6184519
doi: 10.1093/jxb/ery302
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).
pubmed: 34223868
doi: 10.1093/jxb/erab288
Fang, Z. T., Kapoor, R., Datta, A. & Okumoto, S. Tissue specific expression of UMAMIT amino acid transporters in wheat. Sci. Rep. 12, 348 (2022).
pubmed: 35013480
pmcid: 8748447
doi: 10.1038/s41598-021-04284-7
Dindas, J. et al. AUX1-mediated root hair auxin influx governs SCFTIR1/AFB-type Ca
pubmed: 29563504
pmcid: 5862985
doi: 10.1038/s41467-018-03582-5
Chen, L.-Q. et al. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468, 527–532 (2010).
pubmed: 21107422
pmcid: 3000469
doi: 10.1038/nature09606
Chen, L.-Q. et al. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335, 207–211 (2012).
pubmed: 22157085
doi: 10.1126/science.1213351
Payne, R. M. E. et al. An NPF transporter exports a central monoterpene indole alkaloid intermediate from the vacuole. Nat. Plants 3, 16208 (2017).
pubmed: 28085153
pmcid: 5238941
doi: 10.1038/nplants.2016.208
Larsen, B. et al. Identification of iridoid glucoside transporters in Catharanthus roseus. Plant Cell Physiol. 58, 1507–1518 (2017).
pubmed: 28922750
pmcid: 5921532
doi: 10.1093/pcp/pcx097
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).
pubmed: 32156687
pmcid: 7203936
doi: 10.1105/tpc.19.00801
Kazachkova, Y. et al. The GORKY glycoalkaloid transporter is indispensable for preventing tomato bitterness. Nat. Plants 7, 468–480 (2021).
pubmed: 33707737
doi: 10.1038/s41477-021-00865-6
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).
pubmed: 35709542
doi: 10.1016/j.pbi.2022.102243
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).
pubmed: 35481602
doi: 10.1039/D2NP00016D
Slaten, M. L. et al. mGWAS uncovers Gln-glucosinolate seed-specific interaction and its role in metabolic homeostasis. Plant Physiol. 183, 483–500 (2020).
pubmed: 32317360
pmcid: 7271782
doi: 10.1104/pp.20.00039
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).
pubmed: 21668536
doi: 10.1111/j.1365-313X.2011.04672.x
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).
pubmed: 29451311
doi: 10.1111/nph.15021
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).
pubmed: 29549431
doi: 10.1007/s00497-018-0334-5
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).
pubmed: 34015139
pmcid: 8644676
doi: 10.1093/plphys/kiab228
He, Y. et al. Enhancing canola breeding by editing a glucosinolate transporter gene lacking natural variation. Plant Physiol. 188, 1848–1851 (2022).
pubmed: 35078248
pmcid: 8968350
doi: 10.1093/plphys/kiac021
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).
pubmed: 29194649
doi: 10.1111/ppl.12672
Liu, H. et al. CRISPR-P 2.0: an improved CRISPR–Cas9 tool for genome editing in plants. Mol. Plant 10, 530–532 (2017).
pubmed: 28089950
doi: 10.1016/j.molp.2017.01.003
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).
pubmed: 26193878
pmcid: 4507317
doi: 10.1186/s13059-015-0715-0
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).
pubmed: 27856772
Nisar, N., Verma, S., Pogson, B. J. & Cazzonelli, C. I. Inflorescence stem grafting made easy in Arabidopsis. Plant Methods 8, 50 (2012).
pubmed: 23249585
pmcid: 3567951
doi: 10.1186/1746-4811-8-50
Goedhart, J. et al. Structure-guided evolution of cyan fluorescent proteins towards a quantum yield of 93%. Nat. Commun. 3, 751 (2012).
pubmed: 22434194
doi: 10.1038/ncomms1738
Kurihara, D., Mizuta, Y., Sato, Y. & Higashiyama, T. ClearSee: a rapid optical clearing reagent for whole-plant fluorescence imaging. Development 142, 4168–4179 (2015).
pubmed: 26493404
pmcid: 4712841
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).
pubmed: 34595263
pmcid: 8438454
doi: 10.21769/BioProtoc.2581
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).
pubmed: 26442014
pmcid: 4561820
doi: 10.3389/fpls.2015.00697
Crocoll, C., Halkier, B. A. & Burow, M. Analysis and quantification of glucosinolates. Curr. Protoc. Plant Biol. 1, 385–409 (2016).
pubmed: 30775863
doi: 10.1002/cppb.20027
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).
pubmed: 26410451
doi: 10.1016/j.ymben.2015.09.012
Petersen, A., Crocoll, C. & Halkier, B. A. De novo production of benzyl glucosinolate in Escherichia coli. Metab. Eng. 54, 24–34 (2019).
doi: 10.1016/j.ymben.2019.02.004
pubmed: 30831267
Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).
pubmed: 15034147
pmcid: 390337
doi: 10.1093/nar/gkh340
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).
pubmed: 20626897
pmcid: 3017758
doi: 10.1186/1471-2148-10-210
Lemoine, F. et al. NGPhylogeny.fr: new generation phylogenetic services for non-specialists. Nucleic Acids Res. 47, W260–W265 (2019).
pubmed: 31028399
pmcid: 6602494
doi: 10.1093/nar/gkz303
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).
pubmed: 27084950
pmcid: 4987875
doi: 10.1093/nar/gkw256
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).
pubmed: 33885785
pmcid: 8265157
doi: 10.1093/nar/gkab301