Iron–sulfur (Fe–S) clusters play an essential role in plants as protein cofactors mediating diverse electron transfer reactions. Because they can react with oxygen to form reactive oxygen species (ROS) and inflict cellular damage, the biogenesis of Fe–S clusters is highly regulated. A recently discovered group of 2Fe–2S proteins, termed NEET proteins, was proposed to coordinate Fe–S, Fe and ROS homeostasis in mammalian cells. Here we report that disrupting the function of AtNEET, the sole member of the NEET protein family in Arabidopsis thaliana, triggers leaf-associated Fe–S- and Fe-deficiency responses, elevated Fe content in chloroplasts (1.2–1.5-fold), chlorosis, structural damage to chloroplasts and a high seedling mortality rate. Our findings suggest that disrupting AtNEET function disrupts the transfer of 2Fe–2S clusters from the chloroplastic 2Fe–2S biogenesis pathway to different cytosolic and chloroplastic Fe–S proteins, as well as to the cytosolic Fe–S biogenesis system, and that uncoupling this process triggers leaf-associated Fe–S- and Fe-deficiency responses that result in Fe over-accumulation in chloroplasts and enhanced ROS accumulation. We further show that AtNEET transfers its 2Fe–2S clusters to DRE2, a key protein of the cytosolic Fe–S biogenesis system, and propose that the availability of 2Fe–2S clusters in the chloroplast and cytosol is linked to Fe homeostasis in plants.
Bibliographical noteFunding Information:
This work was supported by funding from the National Science Foundation (NSF-BSF MCB-1936590, IOS-1932639 and IOS-1353886 to R.M.; BSF 2015831 to R.N.; and MCB-1818312 to D.G.M.C.), the Bond Life Sciences Early Concept Grant (D.G.M.C. and R.M.), and the University of Missouri. We apologize to all authors of papers not mentioned in this article because of limited space. SIZ, LS, SM, DGG, HBM and NACG performed experiments and analyzed the data. SIZ, SS, DB and RKA conducted bioinformatics and statistical analyses. SIZ, RN, DGMC and RKA designed experiments and analyzed the data. RM, SIZ, DGMC, RN and RKA wrote the article. The authors declare no conflicts of interest.
This work was supported by funding from the National Science Foundation (NSF‐BSF MCB‐1936590, IOS‐1932639 and IOS‐1353886 to R.M.; BSF 2015831 to R.N.; and MCB‐1818312 to D.G.M.C.), the Bond Life Sciences Early Concept Grant (D.G.M.C. and R.M.), and the University of Missouri. We apologize to all authors of papers not mentioned in this article because of limited space.
© 2019 The Authors The Plant Journal © 2019 John Wiley & Sons Ltd
- Arabidopsis thaliana
- iron–sulfur cluster
- reactive oxygen species