Comparative transcriptome analysis of iron-overaccumulating Arabidopsis genotypes uncover novel putative regulators of systemic and retrograde signaling

Abstract

Abstract Background Maintaining iron homeostasis requires a precise orchestration of cellular uptake, trafficking through mesophyll cells, translocation via xylem and phloem, and uptake of iron by roots adjusted to the demand of sink organs by systemic signals. Plants defective in the iron transporter OPT3 in the leaves behave as if they were constitutively iron deficient and accumulate toxic iron levels in their leaves. IRONMAN (IMA) genes encode peptides that trigger iron remobilization and uptake by inhibiting the ubiquitin ligase BRUTUS. Ectopic expression of IMA genes also causes iron accumulation. This study aims at bridging the knowledge gap of the mechanisms operating between OPT3-transported iron and the activation of IMA genes, and between phloem-localized IMAs and the activation of iron uptake genes in the epidermis.Results Among the 1999 DEGs identified in all the genotypes, tissues and treatments, a small subset of genes was found to be shared among the three iron-accumulating genotypes and iron-deficient control plants. Root expression profiles were more strongly correlated that those of shoots, confirming a predominant function in the regulation of root processes by IMAs and OPT3. The largest overlap was observed between opt3-2 and wild-type plants. IMA1 Ox and IMA3 Ox lined showed a surprisingly small overlap except for the iron-related genes, suggesting distinct physiological functions. The set genes with discordant expression pattern between IMA1 Ox and IMA3 Ox lines comprised approximately 40 root genes and 40 shoot genes. A small subset of genes was consistently differentially expressed in all the genotypes, including genes involved in root iron uptake and ROS detoxification, a gene encoding an F-Box protein, and two groups of non-protein coding genes.Conclusions The small suite of DEGs common to all genotypes under investigation constitute potential novel regulators of cellular iron homeostasis. A group of plastid genes seem to produce tRNA-alanine, fragments of which possibly target IMA3 transcripts, constituting a retrograde control on iron homeostasis.