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

The DOI matches its Crossref record.

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

Open access
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
Open this paper in CoChat — free accountOpen PDF

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.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1093/pcp/pcaa006

Cites

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

No references could be resolved yet.

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

Cited by

Sorted by citations

See all 75

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

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

How to cite

Cite CoChat for the checks on this page, and the paper for its own findings.

This page
CoChat. (2026). Citation check: Sulfur Deficiency-Induced Glucosinolate Catabolism Attributed to Two β-Glucosidases, BGLU28 and BGLU30, is Required for Plant Growth Maintenance under Sulfur Deficiency. https://app.cochat.ai/papers/10.1093/pcp/pcaa006
The paper
Zhang, L., Kawaguchi, R., Morikawa-Ichinose, T., Allahham, A., Kim, S.-J., & Maruyama-Nakashita, A. (2020). Sulfur Deficiency-Induced Glucosinolate Catabolism Attributed to Two β-Glucosidases, BGLU28 and BGLU30, is Required for Plant Growth Maintenance under Sulfur Deficiency. Plant and Cell Physiology. https://doi.org/10.1093/pcp/pcaa006