Student or educator? Sign up with your school email and get 6 months of Pro free.
CoChat
Sign Up
Cited by 1,001

The DOI matches its Crossref record; 4 of the 4 references it cites were found in a registry or an index.

MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health

Open access
Stringlis, Ioannis A., Yu, Ke, Feussner, Kirstin, de Jonge, Ronnie, Van Bentum, Sietske, Van Verk, Marcel C., Berendsen, Roeland L., Bakker, Peter A. H. M., Feussner, Ivo, Pieterse, Corné M. J.·2018·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.1722335115
Open this paper in CoChat — free account

Abstract

Significance: Plant roots nurture a large diversity of soil microbes via exudation of chemical compounds into the rhizosphere. In turn, beneficial root microbiota promote plant growth and immunity. The root-specific transcription factor MYB72 has emerged as a central regulator in this process. Here, we show that MYB72 regulates the excretion of the coumarin scopoletin, an iron-mobilizing phenolic compound with selective antimicrobial activity that shapes the root-associated microbial community. Selected soil-borne fungal pathogens appeared to be highly sensitive to the antimicrobial activity of scopoletin, while two MYB72- inducing beneficial rhizobacteria were tolerant. Our results suggest that probiotic root-associated microbes that activate the iron-deficiency response during colonization stimulate MYB72-dependent excretion of scopoletin, thereby potentially improving their niche establishment and enhancing plant growth and protection.

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 · 10.1073/pnas.1722335115

Cites

4 of 4 references verified0 citation errors · 0 not checkable

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

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

Show all 4 references

Research works printed but not linked: 80

  1. HP Bais, TL Weir, LG Perry, S Gilroy, JM Vivanco, The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57, 233–266 (2006). · DOI · Paper page
  2. R Mendes, , Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332, 1097–1100 (2011). · DOI · Paper page
  3. S Hacquard, S Spaepen, R Garrido-Oter, P Schulze-Lefert, Interplay between innate immunity and the plant microbiota. Annu Rev Phytopathol 55, 565–589 (2017). · DOI · Paper page
  4. RL Berendsen, , Unearthing the genomes of plant-beneficial Pseudomonas model strains WCS358, WCS374 and WCS417. BMC Genomics 16, 539 (2015). · DOI · Paper page
  5. CMJ Pieterse, , A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10, 1571–1580 (1998). · DOI · Paper page
  6. BW Verhagen, , The transcriptome of rhizobacteria-induced systemic resistance in arabidopsis. Mol Plant Microbe Interact 17, 895–908 (2004). · DOI · Paper page
  7. A Martinez-Medina, , Recognizing plant defense priming. Trends Plant Sci 21, 818–822 (2016). · DOI · Paper page
  8. MJ Pozo, S Van Der Ent, LC Van Loon, CMJ Pieterse, Transcription factor MYC2 is involved in priming for enhanced defense during rhizobacteria-induced systemic resistance in Arabidopsis thaliana. New Phytol 180, 511–523 (2008). · DOI · Paper page
  9. C Zamioudis, J Hanson, CMJ Pieterse, β-Glucosidase BGLU42 is a MYB72-dependent key regulator of rhizobacteria-induced systemic resistance and modulates iron deficiency responses in Arabidopsis roots. New Phytol 204, 368–379 (2014). · DOI · Paper page
  10. IA Stringlis, , Root transcriptional dynamics induced by beneficial rhizobacteria and microbial immune elicitors reveal signatures of adaptation to mutualists. Plant J 93, 166–180 (2018). · DOI · Paper page
  11. S Van der Ent, , MYB72 is required in early signaling steps of rhizobacteria-induced systemic resistance in Arabidopsis. Plant Physiol 146, 1293–1304 (2008). · DOI · Paper page
  12. A Martínez-Medina, SCM Van Wees, CMJ Pieterse, Airborne signals from Trichoderma fungi stimulate iron uptake responses in roots resulting in priming of jasmonic acid-dependent defences in shoots of Arabidopsis thaliana and Solanum lycopersicum. Plant Cell Environ 40, 2691–2705 (2017). · DOI · Paper page
  13. G Segarra, S Van der Ent, I Trillas, CMJ Pieterse, MYB72, a node of convergence in induced systemic resistance triggered by a fungal and a bacterial beneficial microbe. Plant Biol (Stuttg) 11, 90–96 (2009). · DOI · Paper page
  14. CM Palmer, MN Hindt, H Schmidt, S Clemens, ML Guerinot, MYB10 and MYB72 are required for growth under iron-limiting conditions. PLoS Genet 9, e1003953 (2013). · DOI · Paper page
  15. T Kobayashi, NK Nishizawa, Iron uptake, translocation, and regulation in higher plants. Annu Rev Plant Biol 63, 131–152 (2012). · DOI · Paper page
  16. EP Colangelo, ML Guerinot, The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16, 3400–3412 (2004). · DOI · Paper page
  17. S Santi, W Schmidt, Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. New Phytol 183, 1072–1084 (2009). · DOI · Paper page
  18. D Eide, M Broderius, J Fett, ML Guerinot, A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci USA 93, 5624–5628 (1996). · DOI · Paper page
  19. NJ Robinson, CM Procter, EL Connolly, ML Guerinot, A ferric-chelate reductase for iron uptake from soils. Nature 397, 694–697 (1999). · DOI · Paper page
  20. C Zamioudis, , Rhizobacterial volatiles and photosynthesis-related signals coordinate MYB72 expression in Arabidopsis roots during onset of induced systemic resistance and iron-deficiency responses. Plant J 84, 309–322 (2015). · DOI · Paper page
  21. P Fourcroy, , Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency. New Phytol 201, 155–167 (2014). · DOI · Paper page
  22. J Rodríguez-Celma, , Mutually exclusive alterations in secondary metabolism are critical for the uptake of insoluble iron compounds by Arabidopsis and Medicago truncatula. Plant Physiol 162, 1473–1485 (2013). · DOI · Paper page
  23. NB Schmid, , Feruloyl-CoA 6′-Hydroxylase1-dependent coumarins mediate iron acquisition from alkaline substrates in Arabidopsis. Plant Physiol 164, 160–172 (2014). · DOI · Paper page
  24. P Fourcroy, N Tissot, F Gaymard, JF Briat, C Dubos, Facilitated Fe nutrition by phenolic compounds excreted by the Arabidopsis ABCG37/PDR9 transporter requires the IRT1/FRO2 high-affinity root Fe(2+) transport system. Mol Plant 9, 485–488 (2016). · DOI
  25. EH Verbon, , Iron and immunity. Annu Rev Phytopathol 55, 355–375 (2017). · DOI · Paper page
  26. G Castrillo, , Root microbiota drive direct integration of phosphate stress and immunity. Nature 543, 513–518 (2017). · DOI · Paper page
  27. HH Tsai, W Schmidt, One way. Or another? Iron uptake in plants. New Phytol 214, 500–505 (2017). · DOI
  28. J Ziegler, , Non-targeted profiling of semi-polar metabolites in Arabidopsis root exudates uncovers a role for coumarin secretion and lignification during the local response to phosphate limitation. J Exp Bot 67, 1421–1432 (2016). · DOI
  29. LC Carvalhais, , Activation of the jasmonic acid plant defence pathway alters the composition of rhizosphere bacterial communities. PLoS One 8, e56457 (2013). · DOI · Paper page
  30. FD Dakora, DA Phillips, Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245, 35–47 (2002). · DOI · Paper page
  31. LC Carvalhais, , Linking jasmonic acid signaling, root exudates, and rhizosphere microbiomes. Mol Plant Microbe Interact 28, 1049–1058 (2015). · DOI · Paper page
  32. SL Lebeis, , PLANT MICROBIOME. Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349, 860–864 (2015). · DOI · Paper page
  33. PAHM Bakker, CMJ Pieterse, R de Jonge, RL Berendsen, The soil-borne legacy. Cell 172, 1178–1180 (2018). · DOI · Paper page
  34. GJB Gnonlonfin, A Sanni, L Brimer, Review scopoletin–A coumarin phytoalexin with medicinal properties. Crit Rev Plant Sci 31, 47–56 (2012). · DOI · Paper page
  35. M El Oirdi, A Trapani, K Bouarab, The nature of tobacco resistance against Botrytis cinerea depends on the infection structures of the pathogen. Environ Microbiol 12, 239–253 (2010). · DOI
  36. YH Kim, , Scopoletin production related to induced resistance of tobacco plants against Tobacco mosaic virus. Plant Pathol J 16, 264–268 (2000).
  37. H Sun, , Scopoletin is a phytoalexin against Alternaria alternata in wild tobacco dependent on jasmonate signalling. J Exp Bot 65, 4305–4315 (2014). · DOI
  38. A Kaever, , MarVis-pathway: Integrative and exploratory pathway analysis of non-targeted metabolomics data. Metabolomics 11, 764–777 (2015). · DOI
  39. YO Ahn, , Scopolin-hydrolyzing beta-glucosidases in roots of Arabidopsis. Plant Cell Physiol 51, 132–143 (2010). · DOI
  40. J Le Roy, B Huss, A Creach, S Hawkins, G Neutelings, Glycosylation is a major regulator of phenylpropanoid availability and biological activity in plants. Front Plant Sci 7, 735 (2016). · doi:10.3389/fpls.2016.00735
  41. K Kai, , Scopoletin is biosynthesized via ortho-hydroxylation of feruloyl CoA by a 2-oxoglutarate-dependent dioxygenase in Arabidopsis thaliana. Plant J 55, 989–999 (2008). · DOI · Paper page
  42. RL Berendsen, , Disease-induced assemblage of a plant-beneficial bacterial consortium. ISME J, 2018). · DOI · Paper page
  43. T Mimmo, , Rhizospheric organic compounds in the soil-microorganism-plant system: Their role in iron availability. Eur J Soil Sci 65, 629–642 (2014). · DOI · Paper page
  44. P Menzel, KL Ng, A Krogh, Fast and sensitive taxonomic classification for metagenomics with Kaiju. Nat Commun 7, 11257 (2016). · DOI · Paper page
  45. EF Fradin, , Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiol 150, 320–332 (2009). · DOI · Paper page
  46. CMJ Pieterse, SCM van Wees, E Hoffland, JA van Pelt, LC van Loon, Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell 8, 1225–1237 (1996).
  47. AG Medentsev, AIu Arinbasarova, VK Akimenko, Biosynthesis of naphthoquinone pigments by fungi of the genus Fusarium. Prikl Biokhim Mikrobiol 41, 573–577 (2005).
  48. SW Son, , Bikaverin and fusaric acid from Fusarium oxysporum show antioomycete activity against Phytophthora infestans. J Appl Microbiol 104, 692–698 (2008). · doi:10.1111/j.1365-2672.2007.03581.x
  49. D Turrà, M El Ghalid, F Rossi, A Di Pietro, Fungal pathogen uses sex pheromone receptor for chemotropic sensing of host plant signals. Nature 527, 521–524 (2015). · DOI · Paper page
  50. J Liu, A Osbourn, P Ma, MYB transcription factors as regulators of phenylpropanoid metabolism in plants. Mol Plant 8, 689–708 (2015). · DOI · Paper page
  51. AV Morant, , beta-Glucosidases as detonators of plant chemical defense. Phytochemistry 69, 1795–1813 (2008). · DOI · Paper page
  52. P Jones, T Vogt, Glycosyltransferases in secondary plant metabolism: Tranquilizers and stimulant controllers. Planta 213, 164–174 (2001). · doi:10.1007/s004250000492
  53. PAHM Bakker, RL Berendsen, RF Doornbos, PC Wintermans, CMJ Pieterse, The rhizosphere revisited: Root microbiomics. Front Plant Sci 4, 165 (2013).
  54. TR Turner, , Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. ISME J 7, 2248–2258 (2013). · DOI · Paper page
  55. D Bulgarelli, , Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17, 392–403 (2015). · DOI · Paper page
  56. J Edwards, , Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci USA 112, E911–E920 (2015). · DOI · Paper page
  57. DS Lundberg, , Defining the core Arabidopsis thaliana root microbiome. Nature 488, 86–90 (2012). · DOI · Paper page
  58. R Zgadzaj, , Root nodule symbiosis in Lotus japonicus drives the establishment of distinctive rhizosphere, root, and nodule bacterial communities. Proc Natl Acad Sci USA 113, E7996–E8005 (2016). · DOI · Paper page
  59. Y Zhang, , Huanglongbing impairs the rhizosphere-to-rhizoplane enrichment process of the citrus root-associated microbiome. Microbiome 5, 97 (2017). · DOI · Paper page
  60. G Aliotta, V De Feo, G Pinto, A Pollio, In vitro inhibition of algal growth by Ruta graveolens L. extracts: Biological and chemical aspects. Plant Biosyst 133, 185–191 (1999). · doi:10.1080/11263509909381547
  61. KK Kim, MK Kim, JH Lim, HY Park, ST Lee, Transfer of Chryseobacterium meningosepticum and Chryseobacterium miricola to Elizabethkingia gen. nov. as Elizabethkingia meningoseptica comb. nov. and Elizabethkingia miricola comb. nov. Int J Syst Evol Microbiol 55, 1287–1293 (2005). · DOI
  62. S Krishnamurthi, A Ruckmani, R Pukall, T Chakrabarti, Psychrobacillus gen. nov. and proposal for reclassification of Bacillus insolitus Larkin & Stokes, 1967, B. psychrotolerans Abd-El Rahman et al., 2002 and B. psychrodurans Abd-El Rahman et al., 2002 as Psychrobacillus insolitus comb. nov., Psychrobacillus psychrotolerans comb. nov. and Psychrobacillus psychrodurans comb. nov. Syst Appl Microbiol 33, 367–373 (2010). · DOI
  63. TN Nazina, , Taxonomic study of aerobic thermophilic bacilli: Descriptions of Geobacillus subterraneus gen. nov., sp. nov. and Geobacillus uzenensis sp. nov. from petroleum reservoirs and transfer of Bacillus stearothermophilus, Bacillus thermocatenulatus, Bacillus thermoleovorans, Bacillus kaustophilus, Bacillus thermodenitrificans to Geobacillus as the new combinations G. stearothermophilus, G. th. Int J Syst Evol Microbiol 51, 433–446 (2001). · DOI · Paper page
  64. S Guan, , Aflatoxin B(1) degradation by Stenotrophomonas maltophilia and other microbes selected using coumarin medium. Int J Mol Sci 9, 1489–1503 (2008). · DOI · Paper page
  65. R de Nys, PD Steinberg, Linking marine biology and biotechnology. Curr Opin Biotechnol 13, 244–248 (2002). · DOI
  66. JI Han, , Complete genome sequence of the metabolically versatile plant growth-promoting endophyte Variovorax paradoxus S110. J Bacteriol 193, 1183–1190 (2011). · DOI · Paper page
  67. N Pérez Rodríguez, , The role of bacterial consortium and organic amendment in Cu and Fe isotope fractionation in plants on a polluted mine site. Environ Sci Pollut Res Int 21, 6836–6844 (2014). · DOI
  68. LA Sauder, , Cultivation and characterization of Candidatus Nitrosocosmicus exaquare, an ammonia-oxidizing archaeon from a municipal wastewater treatment system. ISME J 11, 1142–1157 (2017). · DOI · Paper page
  69. LLM Fries, RS Pacovsky, GR Safir, JO Siqueira, Plant growth and arbuscular mycorrhizal fungal colonization affected by exogenously applied phenolic compounds. J Chem Ecol 23, 1755–1767 (1997). · doi:10.1023/b:joec.0000006449.09141.cd
  70. L Zhang, X Shen, Y Liu, S Li, Nafulsella turpanensis gen. nov., sp. nov., a member of the phylum Bacteroidetes isolated from soil. Int J Syst Evol Microbiol 63, 1639–1645 (2013). · doi:10.1099/ijs.0.044651-0
  71. SG Dastager, CK Deepa, A Pandey, Plant growth promoting potential of Pontibacter niistensis in cowpea (Vigna unguiculata (L.) Walp.). Appl Soil Ecol 49, 250–255 (2011). · doi:10.1016/j.apsoil.2011.04.016
  72. MJ McBride, W Liu, X Lu, Y Zhu, W Zhang, The family Cytophagaceae. The Prokaryotes (Springer, Berlin), pp. 577–593 (2014). · doi:10.1007/978-3-642-38954-2_382
  73. S Srinivasan, , Complete genome sequence of Rufibacter sp. DG31D, a bacterium resistant to gamma and UV radiation toxicity. Mol Cell Toxicol 11, 415–421 (2015). · doi:10.1007/s13273-015-0044-0
  74. DV Badri, JM Chaparro, R Zhang, Q Shen, JM Vivanco, Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 288, 4502–4512 (2013). · DOI · Paper page
  75. C Simon, , The differential spatial distribution of secondary metabolites in Arabidopsis leaves reacting hypersensitively to Pseudomonas syringae pv. tomato is dependent on the oxidative burst. J Exp Bot 61, 3355–3370 (2010). · doi:10.1093/jxb/erq157
  76. JA Gutiérrez-Barranquero, FJ Reen, RR McCarthy, F O’Gara, Deciphering the role of coumarin as a novel quorum sensing inhibitor suppressing virulence phenotypes in bacterial pathogens. Appl Microbiol Biotechnol 99, 3303–3316 (2015). · DOI
  77. JH Lee, , Coumarins reduce biofilm formation and the virulence of Escherichia coli O157:H7. Phytomedicine 21, 1037–1042 (2014). · DOI · Paper page
  78. MC Limón, R Rodríguez-Ortiz, J Avalos, Bikaverin production and applications. Appl Microbiol Biotechnol 87, 21–29 (2010). · doi:10.1007/s00253-010-2551-1
  79. JE van de Mortel, , Metabolic and transcriptomic changes induced in Arabidopsis by the rhizobacterium Pseudomonas fluorescens SS101. Plant Physiol 160, 2173–2188 (2012). · DOI · Paper page
  80. C Zhou, , Paenibacillus polymyxa BFKC01 enhances plant iron absorption via improved root systems and activated iron acquisition mechanisms. Plant Physiol Biochem 105, 162–173 (2016). · DOI · Paper page

Cited by

See all 1,001

Metadata

Authors
Stringlis, I. A., Yu, K., Feussner, K., de Jonge, R., Van Bentum, S., Van Verk, M. C., Berendsen, R. L., Bakker, P. A. H. M., Feussner, I., & Pieterse, C. M. J.
Venue
Proceedings of the National Academy of Sciences
Publisher
Proceedings of the National Academy of Sciences
Published
2018-04-23
Volume
115
Issue
22
Pages
E5213-E5222
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
DOI
10.1073/pnas.1722335115
OpenAlex
W2799721285
Cited by
1,001
References
4
FWCI
61.29
Type
journal article
Language
en
Open access
hybrid
Licence
creativecommons.org/licenses/by-nc-nd/4.0/ (vor)
Funders
  • EC | FP7 | FP7 Ideas: European Research Council (269072)
  • China Scholarship Council (201306300051)
  • Fonds Wetenschappelijk Onderzoek (12B8116N)
  • Deutsche Forschungsgemeinschaft (ZUK 45/2010)

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: MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health. https://app.cochat.ai/papers/10.1073/pnas.1722335115
The paper
Stringlis, I. A., Yu, K., Feussner, K., de Jonge, R., Van Bentum, S., Van Verk, M. C., Berendsen, R. L., Bakker, P. A. H. M., Feussner, I., & Pieterse, C. M. J. (2018). MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health. Proceedings of the National Academy of Sciences. https://doi.org/10.1073/pnas.1722335115

Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.