Analysis of Sequence, Map Position, and Gene Expression Reveals Conserved Essential Genes for Iron Uptake in Arabidopsis and Tomato

Abstract

Arabidopsis (Arabidopsis thaliana) and tomato (Lycopersicon esculentum) show similar physiological responses to iron deficiency, suggesting that homologous genes are involved. Essential gene functions are generally considered to be carried out by orthologs that have remained conserved in sequence and map position in evolutionarily related species. This assumption has not yet been proven for plant genomes that underwent large genome rearrangements. We addressed this question in an attempt to deduce functional gene pairs for iron reduction, iron transport, and iron regulation between Arabidopsis and tomato. Iron uptake processes are essential for plant growth. We investigated iron uptake gene pairs from tomato and Arabidopsis, namely sequence, conserved gene content of the regions containing iron uptake homologs based on conserved orthologous set marker analysis, gene expression patterns, and, in two cases, genetic data. Compared to tomato, the Arabidopsis genome revealed more and larger gene families coding for the iron uptake functions. The number of possible homologous pairs was reduced if functional expression data were taken into account in addition to sequence and map position. We predict novel homologous as well as partially redundant functions of ferric reductase-like and iron-regulated transporter-like genes in Arabidopsis and tomato. Arabidopsis nicotianamine synthase genes encode a partially redundant family. In this study, Arabidopsis gene redundancy generally reflected the presumed genome duplication structure. In some cases, statistical analysis of conserved gene regions between tomato and Arabidopsis suggested a common evolutionary origin. Although involvement of conserved genes in iron uptake was found, these essential genes seem to be of paralogous rather than orthologous origin in tomato and Arabidopsis.

Ethylene involvement in the regulation of the H+-ATPase CsHA1 gene and of the new isolated ferric reductase CsFRO1 and iron transporter CsIRT1 genes in cucumber plants

“…The Arabidopsis FRU protein (also named FIT1), a homolog of the tomato FER protein, is necessary for the activation of the ferric reductase AtFRO2 [7,18], the H + -ATPase AtAHA7 [7] and the iron transporter AtIRT1 [18] gene expression, although in the regulation of the iron transporter there is discrepancy between the results of Colangelo and Guerinot [7] and those of Jakoby et al [18]. LeFER and AtFRU expression is induced in roots in response to Fe deficiency [1,5,7,18]. Very recently, Lucena et al [23] have shown that ethylene could regulate FRO and IRT gene expression by affecting the FER (or FERlike) gene activity.…”

Nicotianamine Functions in the Phloem-Based Transport of Iron to Sink Organs, in Pollen Development and Pollen Tube Growth in Arabidopsis

“…However, this accumulation of Fe is not likely the trigger for the induction of NAS genes in the root. Several of the root-expressed NAS genes are induced by Fe deficiency signals in roots and are part of the Fe deficiency response that serves to increase Fe acquisition (Bauer et al, 2004). The upregulation of NAS genes by Fe deficiency and in the roots of frd3 mutants indicates that under Fe deficiency and in the absence of a functional Fe-citrate transport, NA is used as an alternative to enhance the transport of Fe, presumably in the phloem.…”

“…Many genes and mutants are being characterized in this species, and they serve as tools in our investigation of NA functions. A. thaliana has four NAS genes, NAS1, NAS2, NAS3, and NAS4 (Bauer et al, 2004), and we have been able to generate two quadruple mutants, nas4x-1 and nas4x-2, by combining different mutant nas T-DNA insertion alleles . Both mutants harbor the full loss-offunction alleles nas1-1, nas3-1, and nas4-1, while they differ at their nas2 allele.…”

Iron deficiency-mediated stress regulation of four subgroup Ib BHLH genes in Arabidopsis thaliana

“…At low iron supply FRO2 and IRT1 genes are induced whereas upon suYcient iron supply the genes are down regulated (Eide et al 1996;Robinson et al 1999;Vert et al 2002). A central transcriptional regulator in this process in tomato is the basic helix-loop-helix (bHLH) factor FER; the A. thaliana ortholog is encoded by the gene FIT (= fer-like iron deWciency-induced transcription factor, previously known as FRU and FIT1, gene number At2 g28160; Bauer et al 2004;Colangelo and Guerinot 2004;Jakoby et al 2004;Yuan et al 2005; FIT was renamed by Bauer, Guerinot and Ling). FER and FIT share higher sequence similarity with each other rather than with any other known bHLH protein from the two species.…”

“…FER and FIT share higher sequence similarity with each other rather than with any other known bHLH protein from the two species. FER is required for induction of iron reductase and iron transporter genes in tomato (Ling et al 2002;Bereczky et al 2003;Bauer et al 2004;Li et al 2004). FIT was found essential for the induction of FRO2 upon iron deWciency in Arabidopsis (Colangelo and Guerinot 2004;Jakoby et al 2004) as well as for induction of IRT1 (Jakoby et al 2004).…”