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Cited by 75Nitrogen and Sulfur Effects on BrassicaPlant nutrient uptake and metabolismPlant Molecular Biology Research

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Sulfur Deficiency-Induced Glucosinolate Catabolism Attributed to Two β-Glucosidases, BGLU28 and BGLU30, is Required for Plant Growth Maintenance under Sulfur Deficiency

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Zhang, Liu, Kawaguchi, Ryota, Morikawa-Ichinose, Tomomi, Allahham, Alaa, Kim, Sun-Ju, Maruyama-Nakashita, Akiko·2020·Plant and Cell Physiology
DOI 10.1093/pcp/pcaa006
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Abstract

Sulfur (S) is an essential element for plants, and S deficiency causes severe growth retardation. Although the catabolic process of glucosinolates (GSLs), the major S-containing metabolites specific to Brassicales including Arabidopsis, has been recognized as one of the S deficiency (−S) responses in plants, the physiological function of this metabolic process is not clear. Two β-glucosidases (BGLUs), BGLU28 and BGLU30, are assumed to be responsible for this catabolic process as their transcript levels were highly upregulated by −S. To clarify the physiological function of BGLU28 and BGLU30 and their roles in GSL catabolism, we analyzed the accumulation of GSLs and other S-containing compounds in the single and double mutant lines of BGLU28 and BGLU30 and in wild-type plants under different S conditions. GSL levels were highly increased, while the levels of sulfate, cysteine, glutathione and protein were decreased in the double mutant line of BGLU28 and BGLU30 (bglu28/30) under −S. Furthermore, transcript level of Sulfate Transporter1;2, the main contributor of sulfate uptake from the environment, was increased in bglu28/30 mutants under −S. With these metabolic and transcriptional changes, bglu28/30 mutants displayed obvious growth retardation under −S. Overall, our results indicate that BGLU28 and BGLU30 are required for −S-induced GSL catabolism and contribute to sustained plant growth under −S by recycling sulfate to primary S metabolism.

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Research works printed but not linked: 62

  1. Aarabi, 2016, Sulfur deficiency-induced repressor proteins optimize glucosinolate biosynthesis in plants, Sci. Adv., 2, e1601087, 10.1126/sciadv.1601087 · DOI
  2. Alonso, 2003, Genome-wide insertional mutagenesis of Arabidopsis thaliana, Science, 301, 653, 10.1126/science.1086391 · DOI
  3. Andersen, 2013, Integration of biosynthesis and long-distance transport establish organ-specific glucosinolate profiles in Vegetative Arabidopsis, Plant Cell, 25, 3133, 10.1105/tpc.113.110890 · DOI
  4. Bednarek, 2009, A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense, Science, 323, 101, 10.1126/science.1163732 · DOI
  5. Bell, 2018, Taste and flavor perceptions of glucosinolates, isothiocyanates, and related compounds, Mol. Nutr. Food Res., 62, 1700990, 10.1002/mnfr.201700990 · DOI
  6. Bradford, 1976, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem, 72, 248, 10.1016/0003-2697(76)90527-3 · DOI · Paper page
  7. Brown, 2003, Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana, Phytochemistry, 62, 471, 10.1016/S0031-9422(02)00549-6 · DOI
  8. Burow, 2009, Regulation and function of specifier proteins in plants, Phytochem. Rev., 8, 87, 10.1007/s11101-008-9113-5 · DOI
  9. Chhajed, 2019, Chemodiversity of the glucosinolate-myrosinase system at the single cell type resolution, Front. Plant Sci, 10, 618, 10.3389/fpls.2019.00618 · DOI
  10. Christianson, 1965, Steep liquor constituents. Identification and determination of nonprotein nitrogenous substances in corn steep liquor, J. Agric. Food Chem., 13, 277, 10.1021/jf60139a023 · DOI
  11. Christianson, 1965, Nutrient distribution in grain. Location of nonprotein nitrogenous substances in corn grain, J. Agric. Food Chem., 13, 272, 10.1021/jf60139a022 · DOI
  12. Clarke, 2010, Glucosinolates, structures and analysis in food, Anal. Methods, 2, 310, 10.1039/b9ay00280d · DOI
  13. Clay, 2009, Glucosinolate metabolites required for an Arabidopsis innate immune response, Science, 323, 95, 10.1126/science.1164627 · DOI · Paper page
  14. Falk, 2007, The effect of sulfur nutrition on plant glucosinolate content: physiology and molecular mechanisms, Plant Biol, 9, 573, 10.1055/s-2007-965431 · DOI
  15. Felle, 2001, pH: signal and messenger in plant cells, Plant Biol, 3, 577, 10.1055/s-2001-19372 · DOI
  16. Fujiwara, 1992, Effects of sulfur nutrition on expression of the soybean seed storage protein genes in transgenic petunia, Plant Physiol, 99, 263, 10.1104/pp.99.1.263 · DOI
  17. Gigolashvili, 2007, The R2R3-MYB transcription factor HAG1/MYB28 is a regulator of methionine-derived glucosinolate biosynthesis in Arabidopsis thaliana, Plant J, 51, 247, 10.1111/j.1365-313X.2007.03133.x · DOI
  18. Grob, 1979, Vacuolar location of glucosinolates in horseradish root cells, Plant Sci. Lett, 14, 327, 10.1016/S0304-4211(79)90281-5 · DOI
  19. Grubb, 2006, Glucosinolate metabolism and its control, Trends Plant Sci, 11, 89, 10.1016/j.tplants.2005.12.006 · DOI
  20. Halkier, 2006, Biology and biochemistry of glucosinolates, Annu. Rev. Plant Biol., 57, 303, 10.1146/annurev.arplant.57.032905.105228 · DOI
  21. Hanschen, 2018, Brassica vegetables as sources of epithionitriles: Novel secondary products formed during cooking, Food Chem, 245, 546, 10.1016/j.foodchem.2017.10.124 · DOI
  22. Hirai, 1995, Effects of sulfate concentrations on the expression of a soybean seed storage protein gene and its reversibility in transgenic Arabidopsis thaliana, Plant Cell Physiol, 36, 1331
  23. Hirai, 2007, Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis, Proc. Natl. Acad. Sci. USA, 104, 6478, 10.1073/pnas.0611629104 · DOI
  24. Hirai, 2004, Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana, Proc. Natl. Acad. Sci. USA, 101, 10205, 10.1073/pnas.0403218101 · DOI
  25. Hooper, 2017, Multiple marker abundance profiling: combining selected reaction monitoring and data-dependent acquisition for rapid estimation of organelle abundance in subcellular samples, Plant J., 92, 1202, 10.1111/tpj.13743 · DOI
  26. Hooper, 2014, SUBAcon: A consensus algorithm for unifying the subcellular localization data of the Arabidopsis proteome, Bioinformatics, 30, 3356, 10.1093/bioinformatics/btu550 · DOI
  27. Ishida, 2014, Glucosinolate metabolism, functionality and breeding for the improvement of Brassicaceae vegetables, Breed. Sci., 64, 48, 10.1270/jsbbs.64.48 · DOI
  28. Janowitz, 2009, Evolution of nitrilases in glucosinolate-containing plants, Phytochemistry, 70, 1680, 10.1016/j.phytochem.2009.07.028 · DOI
  29. Kataoka, 2004, Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis, Plant Cell, 16, 2693, 10.1105/tpc.104.023960 · DOI
  30. Katz, 2015, The glucosinolate breakdown product indole-3-carbinol acts as an auxin antagonist in roots of Arabidopsis thaliana, Plant J., 82, 547, 10.1111/tpj.12824 · DOI · Paper page
  31. Kimura, 2019, Contribution of root hair development to sulfate uptake in Arabidopsis, Plants (Basel), 8, 106, 10.3390/plants8040106 · DOI
  32. Koroleva, 2011, Single-cell proteomic analysis of glucosinolate-rich S-cells in Arabidopsis thaliana, Methods, 54, 413, 10.1016/j.ymeth.2011.06.005 · DOI
  33. Kutz, 2002, A role for nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana, Plant J., 30, 95, 10.1046/j.1365-313X.2002.01271.x · DOI
  34. Long, 2015, Biochemistry & Molecular Biology of Plants, 746
  35. Malinovsky, 2017, An evolutionarily young defense metabolite influences the root growth of plants via the ancient TOR signaling pathway, eLife, 6, e29353, 10.7554/eLife.29353 · DOI
  36. Maruyama-Nakashita, 2017, Metabolic changes sustain the plant life in low-sulfur environments, Curr. Opin. Plant Biol, 39, 144, 10.1016/j.pbi.2017.06.015 · DOI
  37. Maruyama-Nakashita, 2003, Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways, Plant Physiol., 132, 597, 10.1104/pp.102.019802 · DOI
  38. Maruyama-Nakashita, 2006, Arabidopsis SLIM1 is a central transcriptional regulator of plant sulfur response and metabolism, Plant Cell, 18, 3235, 10.1105/tpc.106.046458 · DOI
  39. Maruyama-Nakashita, 2005, Identification of a novel cis-acting element conferring sulfur deficiency response in Arabidopsis roots, Plant J, 42, 305, 10.1111/j.1365-313X.2005.02363.x · DOI
  40. Matile, 1980, The mustard oil bomb compartmentation of the myrosinase system, Biochem. Physiol. Pflanz, 175, 722, 10.1016/S0015-3796(80)80059-X · DOI
  41. Matsuda, 2009, MS/MS spectral tag-based annotation of non-targeted profile of plant secondary metabolites, Plant J, 57, 555, 10.1111/j.1365-313X.2008.03705.x · DOI
  42. Morikawa-Ichinose, 2019, Glucosinolate distribution in the aerial parts of sel1-10, a disruption mutant of the sulfate transporter SULTR1;2, in mature Arabidopsis thaliana plants, Plants, 8, 95, 10.3390/plants8040095 · DOI
  43. Nakano, 2017, PYK10 myrosinase reveals a functional coordination between endoplasmic reticulum bodies and glucosinolates in Arabidopsis thaliana, Plant J., 89, 204, 10.1111/tpj.13377 · DOI
  44. Nikiforova, 2003, Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity, Plant J, 33, 633, 10.1046/j.1365-313X.2003.01657.x · DOI
  45. Nour-Eldin, 2012, NRT/PTR transporters are essential for translocation of glucosinolate defence compounds to seeds, Nature, 488, 531, 10.1038/nature11285 · DOI
  46. Paulose, 2013, A γ-glutamyl cyclotransferase protects Arabidopsis plants from heavy metal toxicity by recycling glutamate to maintain glutathione homeostasis, Plant Cell, 25, 4580, 10.1105/tpc.113.111815 · DOI
  47. Petersen, 2002, Composition and content of glucosinolates in developing Arabidopsis thaliana, Planta, 214, 562, 10.1007/s004250100659 · DOI
  48. Salehin, 2019, Auxin-sensitive Aux/IAA proteins mediate drought tolerance in Arabidopsis by regulating glucosinolate levels, Nat. Commun., 10, 4021, 10.1038/s41467-019-12002-1 · DOI · Paper page
  49. Sessions, 2002, A high-throughput Arabidopsis reverse genetics system, Plant Cell, 14, 2985, 10.1105/tpc.004630 · DOI
  50. Shimada, 2018, Plant vacuoles, Annu. Rev. Plant Biol., 69, 123, 10.1146/annurev-arplant-042817-040508 · DOI
  51. Sønderby, 2010, Biosynthesis of glucosinolates—gene discovery and beyond, Trends Plant Sci, 15, 283, 10.1016/j.tplants.2010.02.005 · DOI
  52. Takahashi, 2011, Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes, Annu. Rev. Plant Biol., 62, 157, 10.1146/annurev-arplant-042110-103921 · DOI
  53. Talalay, 2001, Phytochemicals from cruciferous plants protect against cancer by modulating carcinogen metabolism, J. Nutr, 131, 3027S, 10.1093/jn/131.11.3027S · DOI
  54. Tanz, 2013, SUBA3: a database for integrating experimentation and prediction to define the SUBcellular location of proteins in Arabidopsis, Nucleic Acids Res, 41, D1185, 10.1093/nar/gks1151 · DOI
  55. Traka, 2016, Health Benefits of Glucosinolates, Adv. Bot. Res, 80, 247, 10.1016/bs.abr.2016.06.004 · DOI
  56. Traka, 2009, Glucosinolates, isothocyanates and human health, Phytochem. Rev, 8, 268, 10.1007/s11101-008-9103-7 · DOI
  57. Wittstock, 2010, Glucosinolate breakdown in Arabidopsis: mechanism, regulation and biological significance, Arabidopsis Book, 8, e0134, 10.1199/tab.0134 · DOI
  58. Wittstock, 2016, NSP-dependent simple nitrile formation dominates upon breakdown of major aliphatic glucosinolates in roots, seeds, and seedlings of Arabidopsis thaliana Columbia-0, Front. Plant Sci, 7, 1821, 10.3389/fpls.2016.01821 · DOI
  59. Xu, 2004, Functional genomic analysis of Arabidopsis thaliana glycoside hydrolase family 1, Plant Mol. Biol., 55, 343, 10.1007/s11103-004-0790-1 · DOI
  60. Yamaguchi, 2016, Effects of cadmium treatment on the uptake and translocation of sulfate in Arabidopsis thaliana, Plant Cell Physiol., 57, 2353, 10.1093/pcp/pcw156 · DOI
  61. Zhang, 2006, The gene controlling the quantitative trait locus EPITHIOSPECIFIER MODIFIER1 alters glucosinolate hydrolysis and insect resistance in Arabidopsis, Plant Cell, 18, 1524, 10.1105/tpc.105.039602 · DOI
  62. Zhou, 2012, Properties of β-thioglucoside hydrolases (TGG1 and TGG2) from leaves of Arabidopsis thaliana, Plant Sci, 191–192, 82, 10.1016/j.plantsci.2012.02.004 · DOI

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Metadata

Authors
Zhang, L., Kawaguchi, R., Morikawa-Ichinose, T., Allahham, A., Kim, S.-J., & Maruyama-Nakashita, A.
Affiliations
  • Kyushu University (JP)
  • Department of Bioscience and Biotechnology, Faculty of Agriculture, Kyushu University, 744 Motooka, Nishi-ku, Fukuoka, 819-0395 Japan
  • Chungnam National University (KR)
ORCID
Venue
Plant and Cell Physiology
Publisher
Oxford University Press (OUP)
Published
2020-02-12
Volume
61
Issue
4
Pages
803-813
ISSN
  • 0032-0781 (ISSN-L)
  • 1471-9053
DOI
10.1093/pcp/pcaa006
OpenAlex
W3006441458
Cited by
75
References
0
Citations by year
2026: 6 · 2025: 8 · 2024: 11 · 2023: 9 · 2022: 24 · 2021: 9 · 2020: 8
FWCI
4.79
Type
journal article
Language
en
Open access
Licence
academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
Locations
  • Plant and Cell Physiology (publishedVersion)
  • PubMed (publishedVersion)
  • Kyushu University Institutional Repository (QIR) (Kyushu University) (submittedVersion)
  • Institutional Repositories DataBase (IRDB) (submittedVersion)
Funders
  • Japan Society for the Promotion of Science
  • JSPS (JP20770044, JP17H03785, JP16J40073)
  • Japan Foundation for Applied Enzymology
Topics
  • Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Nitrogen and Sulfur Effects on Brassica
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant nutrient uptake and metabolism
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
Keywords
sulfur deficiency, β-glucosidase, sulfate transport, growth retardation, cysteine, glutathione, Arabidopsis thaliana, Brassicales
MeSH terms
Cysteine, DNA-Binding Proteins, Glucosinolates, Glutathione, Sulfates, Sulfur, Transcription Factors, Arabidopsis, Gene Expression Regulation, Plant, Arabidopsis Proteins, Cellulases, Plant Development

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