TY - JOUR
T1 - Spatial IMA1 regulation restricts root iron acquisition on MAMP perception
AU - Cao, Min
AU - Platre, Matthieu Pierre
AU - Tsai, Huei Hsuan
AU - Zhang, Ling
AU - Nobori, Tatsuya
AU - Armengot, Laia
AU - Chen, Yintong
AU - He, Wenrong
AU - Brent, Lukas
AU - Coll, Nuria S.
AU - Ecker, Joseph R.
AU - Geldner, Niko
AU - Busch, Wolfgang
N1 - Data availability statement: Raw RNA-seq data have been uploaded to the NCBI Gene Expression Omnibus (GSE213557). Uncropped gel and blot source data are provided in Supplementary Fig. 1. Gene sequences for RNA-seq read mapping were obtained from the TAIR10 reference genome. Source data are provided with this paper.
Code availability statement: Scripts for imaging quantification in Fiji and code for RNA-seq analysis in R are available at GitHub (https://github.com/cm010713/immunity-iron-project). All bioinformatic tools used in this study are cited in the Methods.
Funding information: This study was funded by the National Institute of General Medical Sciences of the National Institutes of Health (grant number R01GM127759 to W.B.), start-up funds from the Salk Institute for Biological Studies (to W.B.), funds from the Hess Chair in Plant Science (to W.B.), a long-term postdoctoral fellowship (LT000340/2019 L) by the Human Frontier Science Program Organization to M.P.P., funds from the Taiwan’s Ministry of Science and Technology (grant number 111-2917-I-564-021 to H.-H.T.), funds from the Human Frontiers Science Program (HFSP) Long-term Fellowship (grant number LT000661/2020-L to T.N.). This study was supported by the NGS Core Facility of the Salk Institute with funding from NIH-NCI CCSG: P30 014195, the Chapman Foundation and the Helmsley Charitable Trust. J.R.E. is an investigator of the Howard Hughes Medical Institute. L.A. is supported by a Maria Zambrano postdoctoral fellowship by de Ministerio de Universidades and the European Union—NextGenerationEU. Research at CRAG was supported by grant MCIN/AEI/PID2019-108595RB-I00 funded by MCIN/AEI/10.13039/501100011033, grant TED2021-131457B-I00 funded by MCIN/AEI/10.13039/501100011033 and by the ‘European Union NextGenerationEU/PRTR’, through the ‘Severo Ochoa Programme for Centres of Excellence in R&D’ (CEX2019-000917 funded by MCIN/AEI/10.13039/501100011033), and by the CERCA Pro-gram/Generalitat de Catalunya (N.S.C.).
PY - 2024/1/25
Y1 - 2024/1/25
N2 - Iron is critical during host–microorganism interactions 1–4. Restriction of available iron by the host during infection is an important defence strategy, described as nutritional immunity 5. However, this poses a conundrum for externally facing, absorptive tissues such as the gut epithelium or the plant root epidermis that generate environments that favour iron bioavailability. For example, plant roots acquire iron mostly from the soil and, when iron deficient, increase iron availability through mechanisms that include rhizosphere acidification and secretion of iron chelators 6–9. Yet, the elevated iron bioavailability would also be beneficial for the growth of bacteria that threaten plant health. Here we report that microorganism-associated molecular patterns such as flagellin lead to suppression of root iron acquisition through a localized degradation of the systemic iron-deficiency signalling peptide Iron Man 1 (IMA1) in Arabidopsis thaliana. This response is also elicited when bacteria enter root tissues, but not when they dwell on the outer root surface. IMA1 itself has a role in modulating immunity in root and shoot, affecting the levels of root colonization and the resistance to a bacterial foliar pathogen. Our findings reveal an adaptive molecular mechanism of nutritional immunity that affects iron bioavailability and uptake, as well as immune responses.
AB - Iron is critical during host–microorganism interactions 1–4. Restriction of available iron by the host during infection is an important defence strategy, described as nutritional immunity 5. However, this poses a conundrum for externally facing, absorptive tissues such as the gut epithelium or the plant root epidermis that generate environments that favour iron bioavailability. For example, plant roots acquire iron mostly from the soil and, when iron deficient, increase iron availability through mechanisms that include rhizosphere acidification and secretion of iron chelators 6–9. Yet, the elevated iron bioavailability would also be beneficial for the growth of bacteria that threaten plant health. Here we report that microorganism-associated molecular patterns such as flagellin lead to suppression of root iron acquisition through a localized degradation of the systemic iron-deficiency signalling peptide Iron Man 1 (IMA1) in Arabidopsis thaliana. This response is also elicited when bacteria enter root tissues, but not when they dwell on the outer root surface. IMA1 itself has a role in modulating immunity in root and shoot, affecting the levels of root colonization and the resistance to a bacterial foliar pathogen. Our findings reveal an adaptive molecular mechanism of nutritional immunity that affects iron bioavailability and uptake, as well as immune responses.
UR - http://www.scopus.com/inward/record.url?scp=85182169536&partnerID=8YFLogxK
U2 - 10.1038/s41586-023-06891-y
DO - 10.1038/s41586-023-06891-y
M3 - Article
C2 - 38200311
AN - SCOPUS:85182169536
SN - 0028-0836
VL - 625
SP - 750
EP - 759
JO - Nature
JF - Nature
IS - 7996
ER -