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Cited by 46Plant-Microbe Interactions and ImmunityPlant Micronutrient Interactions and EffectsPlant Molecular Biology Research

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The receptor kinase SRF3 coordinates iron-level and flagellin dependent defense and growth responses in plants

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Platre, Matthieu Pierre, Satbhai, Santosh B., Brent, Lukas, Gleason, Matias F., Cao, Min, Grison, Magali, Glavier, Marie, Zhang, Ling, Gaillochet, Christophe, Goeschl, Christian, Giovannetti, Marco, Enugutti, Balaji, Neveu, Julie, von Reth, Marcel, Alcázar, Ruben, Parker, Jane E., Vert, Grégory, Bayer, Emmanuelle, Busch, Wolfgang·2022·Nature Communications
DOI 10.1038/s41467-022-32167-6PMC PMC9343624

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Abstract

Iron is critical for host–pathogen interactions. While pathogens seek to scavenge iron to spread, the host aims at decreasing iron availability to reduce pathogen virulence. Thus, iron sensing and homeostasis are of particular importance to prevent host infection and part of nutritional immunity. While the link between iron homeostasis and immunity pathways is well established in plants, how iron levels are sensed and integrated with immune response pathways remains unknown. Here we report a receptor kinase SRF3, with a role in coordinating root growth, iron homeostasis and immunity pathways via regulation of callose synthases. These processes are modulated by iron levels and rely on SRF3 extracellular and kinase domains which tune its accumulation and partitioning at the cell surface. Mimicking bacterial elicitation with the flagellin peptide flg22 phenocopies SRF3 regulation upon low iron levels and subsequent SRF3-dependent responses. We propose that SRF3 is part of nutritional immunity responses involved in sensing external iron levels.

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Research works printed but not linked: 64

  1. Kobayashi, T. & Nishizawa, N. K. Iron uptake, translocation, and regulation in higher plants. Annu. Rev. Plant Biol. 63, 131–152 (2012). · DOI
  2. Bai, L. et al. Phylogenomic analysis of transferrin family from animals and plants. Comp. Biochem. Physiol. Part D. Genomics Proteom. 17, 1–8 (2016). · DOI
  3. Verbon, E. H., Trapet, P. L., Stringlis, I. A. & Kruijs, S. Iron and Immunity. Annu. Rev. Phytopathol. 55, 1–15 (2017). · DOI · Paper page
  4. Deák, M. et al. Plants ectopically expressing the iron-binding protein, ferritin, are tolerant to oxidative damage and pathogens. Nat. Biotechnol. 17, 192–196 (1999). · DOI
  5. Segond, D. et al. NRAMP genes function in Arabidopsis thaliana resistance to Erwinia chrysanthemi infection. Plant J. 58, 195–207 (2009). · DOI
  6. Aznar, A. et al. Scavenging iron: a novel mechanism of plant immunity activation by microbial siderophores1[C][W]. Plant Physiol. 164, 2167–2183 (2014). · DOI
  7. Zamioudis, C. et al. 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
  8. Xing, Y. et al. Bacterial effector targeting of a plant iron sensor facilitates iron acquisition and pathogen. Plant Cell 33, 2015–2031 (2021). · DOI
  9. Mendoza-Cózatl, D. G. et al. OPT3 is a component of the iron-signaling network between leaves and roots and misregulation of OPT3 leads to an over-accumulation of cadmium in seeds. Mol. Plant 7, 1455–1469 (2014). · DOI
  10. Selote, D., Samira, R., Matthiadis, A., Gillikin, J. W. & Long, T. A. Iron-binding E3 ligase mediates iron response in plants by targeting basic helix-loop-helix transcription factors. Plant Physiol. 167, 273–286 (2015). · DOI
  11. Kim, S. A. et al. Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 314, 1295–1298 (2006). · DOI
  12. Denyer, T. et al. Spatiotemporal developmental trajectories in the arabidopsis root revealed using high-throughput single-cell RNA sequencing. Dev. Cell 49, 19 (2019).
  13. Hohmann, U., Lau, K. & Hothorn, M. The structural basis of ligand perception and signal activation by receptor kinases. https://www.annualreviews.org/doi/abs/10.1146/annurev-arplant-042916-040957https://doi.org/10.1146/annurev-arplant-042916-040957 (2017). · DOI
  14. Grison, M. S. et al. Plasma membrane-associated receptor-like kinases relocalize to plasmodesmata in response to osmotic stress. Plant Physiol. 181, 142–160 (2019). · DOI
  15. Grison, M. S. et al. Specific membrane lipid composition is important for plasmodesmata function in Arabidopsis. Plant Cell 27, 1228–1250 (2015). · DOI
  16. Sager, R. E. & Lee, J.-Y. Plasmodesmata at a glance. J. Cell Sci. 131, jcs209346 (2018). · DOI
  17. Durrett, T. P., Gassmann, W. & Rogers, E. E. The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol. 144, 197–205 (2007). · DOI
  18. Grillet, L., Lan, P., Li, W., Mokkapati, G. & Schmidt, W. IRON MAN is a ubiquitous family of peptides that control iron transport in plants. Nat. Plants 4, 953–963 (2018). · DOI
  19. Kumar, R. K. et al. Iron-nicotianamine transporters are required for proper long distance iron signaling. Plant Physiol. 175, 15 (2017). · DOI
  20. Vatén, A. et al. Callose biosynthesis regulates symplastic trafficking during root development. Dev. Cell 21, 1144–1155 (2011). · DOI
  21. Han, X. et al. Auxin-callose-mediated plasmodesmal gating is essential for tropic auxin gradient formation and signaling. Dev. Cell 28, 132–146 (2014). · DOI
  22. Benitez-Alfonso, Y. et al. Symplastic intercellular connectivity regulates lateral root patterning. Dev.Cell 26, 136–147 (2013). · DOI
  23. Gerlitz, N., Gerum, R., Sauer, N. & Stadler, R. Photoinducible DRONPA-s: a new tool for investigating cell-cell connectivity. Plant J. 94, 751–766 (2018). · DOI
  24. Sager, R. et al. Auxin-dependent control of a plasmodesmal regulator creates a negative feedback loop modulating lateral root emergence. Nat. Commun. 11, 1–10 (2020). · DOI
  25. Cui, W. & Lee, J.-Y. Arabidopsis callose synthases CalS1/8 regulate plasmodesmal permeability during stress. Nat. Plants 2, 16034 (2016). · DOI
  26. Alcázar, R. et al. Natural variation at Strubbelig Receptor Kinase 3 drives immune-triggered incompatibilities between Arabidopsis thaliana accessions. Nat. Genet. 42, 1135–1139 (2010). · DOI
  27. Stringlis, I. A. et al. Root transcriptional dynamics induced by beneficial rhizobacteria and microbial immune elicitors reveal signatures of adaptation to mutualists. Plant J. 93, 166–180 (2018). · DOI
  28. Kreps, J. A. et al. Transcriptome changes for arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol. 130, 2129–2141 (2002). · DOI
  29. Tawab, F. et al. Identification and characterization of a novel multi-stress responsive gene in Arabidopsis. PLoS ONE 15, e0244030 (2020). · DOI
  30. Emonet, A. et al. Spatially restricted immune responses are required for maintaining root meristematic activity upon detection of bacteria. Curr. Biol. https://doi.org/10.1016/j.cub.2020.12.048 (2021). · DOI
  31. Hindt, M. N. et al. BRUTUS and its paralogs, BTS LIKE1 and BTS LIKE2, encode important negative regulators of the iron deficiency response in Arabidopsis thaliana. Metallomics 9, 876–890 (2017). · DOI
  32. Satbhai, S. B. et al. Natural allelic variation of FRO2 modulates Arabidopsis root growth under iron deficiency. Nat. Commun. 8, 15603 (2017). · DOI
  33. Benschop, J. J., Mohammed, S. & Slijper, M. Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol. Cell Proteomics. 6, 1198–1214 (2007). · DOI
  34. Rutschow, H. L., Baskin, T. I. & Kramer, E. M. Regulation of solute flux through plasmodesmata in the root meristem. Plant Physiol. 155, 1817–1826 (2011). · DOI
  35. Fichman, Y., Myers, R. J., Grant, D. G. & Mittler, R. Plasmodesmata-localized proteins and ROS orchestrate light-induced rapid systemic signaling in Arabidopsis. Sci. Signal. 14, eabf0322 (2021). · DOI
  36. Aznar, A. & Dellagi, A. New insights into the role of siderophores as triggers of plant immunity: what can we learn from animals? J. Exp. Bot. 66, 3001–3010 (2015). · DOI
  37. González-Bosch, C. Priming plant resistance by activation of redox-sensitive genes. Free Radic. Biol. Med. 122, 171–180 (2018). · DOI
  38. Haydon, M. J. et al. Vacuolar nicotianamine has critical and distinct roles under iron deficiency and for zinc sequestration in Arabidopsis. Plant Cell 24, 724–737 (2012). · DOI
  39. Klatte, M. et al. The analysis of Arabidopsis nicotianamine synthase mutants reveals functions for nicotianamine in seed iron loading and iron deficiency responses. Plant Physiol. 150, 257 (2009). · DOI
  40. Gruber, B. D., Giehl, R. F. H., Friedel, S. & von Wirén, N. Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol. 163, 161–179 (2013). · DOI
  41. Groen, S. C. et al. Pathogen-triggered ethylene signaling mediates systemic-induced susceptibility to herbivory in Arabidopsis[W]. Plant Cell 25, 4755–4766 (2013). · DOI
  42. Higashi, K. et al. Modulation of defense signal transduction by flagellin-induced WRKY41 transcription factor in Arabidopsis thaliana. Mol. Genet Genomics 279, 303–312 (2008). · DOI
  43. Lee, J.-Y. et al. A plasmodesmata-localized protein mediates crosstalk between cell-to-cell communication and innate immunity in Arabidopsis. Plant Cell 23, 22 (2011). · DOI
  44. Thomas, C. L., Bayer, E. M., Ritzenthaler, C., Fernandez-Calvino, L. & Maule, A. J. Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS Biol. 6, e7 (2008). · DOI
  45. Cutler, S. R., Ehrhardt, D. W., Griffitts, J. S. & Somerville, C. R. Random GFP∷cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc. Natl Acad. Sci. USA 97, 3718–3723 (2000). · DOI
  46. Millet, Y. A., Danna, C. H., Clay, N. K., Songnuan, W. & Simon, M. D. Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns W OA. Plant Cell 22, 18 (2010). · DOI
  47. Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998). · DOI
  48. Meijón, M., Satbhai, S. B., Tsuchimatsu, T. & Busch, W. Genome-wide association study using cellular traits identifies a new regulator of root development in Arabidopsis. Nat. Genet. 46, 77–81 (2013). · DOI
  49. Kisko, M. et al. LPCAT1 controls phosphate homeostasis in a zinc-dependent manner. eLife 7, e32077 (2018). · DOI
  50. Bouain, N. et al. Natural allelic variation of the AZI1 gene controls root growth under zinc-limiting condition. PLoS Genet. 14, e1007304 (2018). · DOI
  51. Ogura, T. et al. Root system depth in arabidopsis is shaped by EXOCYST70A3 via the dynamic modulation of auxin transport. Cell 178, 400–412.e16 (2019). · DOI
  52. Li, B. et al. GSNOR provides plant tolerance to iron toxicity via preventing iron-dependent nitrosative and oxidative cytotoxicity. Nat. Commun. 10, 13 (2019).
  53. Slovak, R. et al. A scalable open-source pipeline for large-scale root phenotyping of Arabidopsis. Plant Cell 26, 2390–2403 (2014). · DOI
  54. Seren, Ü. et al. GWAPP: a web application for genome-wide association mapping in Arabidopsis. Plant Cell 24, 4793–4805 (2012). · DOI
  55. Benjamini, Y. & Yekutieli, D. The control of the false discovery rate in multiple testing under dependency. Ann. Stat. 29, 1165–1188 (2001). · DOI · Paper page
  56. Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013). · DOI · Paper page
  57. Anders, S., Pyl, P. T. & Huber, W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166–169 (2014). · DOI · Paper page
  58. Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2009). · DOI · Paper page
  59. Tian, T. et al. agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res. 45, W122–W129 (2017). · DOI
  60. Boutté, Y. & Grebe, M. Immunocytochemical fluorescent in situ visualization of proteins in arabidopsis. Methods Mol. Biol. 1062, 453–472 (2014). · DOI
  61. Cao, M. et al. TMK1-mediated auxin signalling regulates differential growth of the apical hook. Nature 568, 240–243 (2019). · DOI
  62. Roschzttardtz, H., Conéjéro, G., Curie, C. & Mari, S. Straightforward histochemical staining of Fe by the adaptation of an old-school technique. Plant Signal Behav. 5, 56–57 (2010). · DOI
  63. Stacey, M. G. et al. The Arabidopsis AtOPT3 protein functions in metal homeostasis and movement of iron to developing seeds. Plant Physiol. 146, 589–601 (2008). · DOI
  64. Meguro, R. et al. Nonheme-iron histochemistry for light and electron microscopy: a historical, theoretical and technical review. Arch. Histol. Cytol. 70, 1–19 (2007). · DOI

Metadata

Authors
Platre, M. P., Satbhai, S. B., Brent, L., Gleason, M. F., Cao, M., Grison, M., Glavier, M., Zhang, L., Gaillochet, C., Goeschl, C., Giovannetti, M., Enugutti, B., Neveu, J., von Reth, M., Alcázar, R., Parker, J. E., Vert, G., Bayer, E., & Busch, W.
Affiliations
  • Salk Institute for Biological Studies (US)
  • Centre National de la Recherche Scientifique (FR)
  • Gregor Mendel Institute of Molecular Plant Biology (AT)
  • Max Planck Institute for Plant Breeding Research (DE)
  • Cluster of Excellence on Plant Sciences (DE)
Corresponding author
Busch, Wolfgang
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2022-08-01
Volume
13
Issue
1
Pages
4445-4445
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/s41467-022-32167-6
PMC
PMC9343624
OpenAlex
W4289313504
Cited by
46
References
5
Citations by year
2026: 10 · 2025: 13 · 2024: 13 · 2023: 7 · 2022: 3
FWCI
4.96
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Communications (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • Research Square (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Institutional Research Information System University of Turin (University of Turin) (submittedVersion, other-oa)
  • HAL (submittedVersion, cc-by)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Oskar-Bordeaux (Universite de Bordeaux) (submittedVersion, cc-by)
  • Padua Research Archive (University of Padova) (submittedVersion, cc-by)
Funders
  • European Commission (772103, HORIZON2020)
  • Österreichischen Akademie der Wissenschaften
  • Austrian Science Fund (I 2377)
  • International Max Planck Research School for Advanced Methods in Process and Systems Engineering
  • National Institutes of Health (390686111)
  • National Institute of General Medical Sciences (R01GM127759)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Micronutrient Interactions and Effects
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
Keywords
iron homeostasis, nutritional immunity, flagellin, flg22, callose synthase, plant immunity, root growth, iron sensing, kinase domain, extracellular domain, host-pathogen interaction
MeSH terms
Flagellin, Iron, Protein Kinases, Arabidopsis, Arabidopsis Proteins

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