Ferritin gene organization: Differences between plants and animals suggest possible kingdom-specific selective constraints

Abstract

Ferritin, a protein widespread in nature, concentrates iron approximately 10(11)-10(12)-fold above the solubility within a spherical shell of 24 subunits; it derives in plants and animals from a common ancestor (based on sequence) but displays a cytoplasmic location in animals compared to the plastid in contemporary plants. Ferritin gene regulation in plants and animals is altered by development, hormones, and excess iron; iron signals target DNA in plants but mRNA in animals. Evolution has thus conserved the two end points of ferritin gene expression, the physiological signals and the protein structure, while allowing some divergence of the genetic mechanisms. Comparison of ferritin gene organization in plants and animals, made possible by the cloning of a dicot (soybean) ferritin gene presented here and the recent cloning of two monocot (maize) ferritin genes, shows evolutionary divergence in ferritin gene organization between plants and animals but conservation among plants or among animals; divergence in the genetic mechanism for iron regulation is reflected by the absence in all three plant genes of the IRE, a highly conserved, noncoding sequence in vertebrate animal ferritin mRNA. In plant ferritin genes, the number of introns (n = 7) is higher than in animals (n = 3). Second, no intron positions are conserved when ferritin genes of plants and animals are compared, although all ferritin gene introns are in the coding region; within kingdoms, the intron positions in ferritin genes are conserved. Finally, secondary protein structure has no apparent relationship to intron/exon boundaries in plant ferritin genes, whereas in animal ferritin genes the correspondence is high. The structural differences in introns/exons among phylogenetically related ferritin coding sequences and the high conservation of the gene structure within plant or animal kingdoms of the gene structure within plant or animal kingdoms suggest that kingdom-specific functional constraints may exist to maintain a particular intron/exon pattern within ferritin genes. In the case of plants, where ferritin gene intron placement is unrelated to triplet codons or protein structure, and where ferritin is targeted to the plastid, the selection pressure on gene organization may relate to RNA function and plastid/nuclear signaling.

The family of iron responsive RNA structures regulated by changes in cellular iron and oxygen

“…In the case of aconitase B, switching between the catalytic and mRNA-binding modes of protein activity was mediated by iron availability [69] . Such RNAprotein interactions in bacteria and animals could indicate an ancient origin for regulation of proteins important in iron and oxygen metabolism that was lost in plants after plastid infection [15], or may reflect the independent evolution of mRNA regulation for analogous proteins in animals and contemporary bacteria.…”

Regulation of plant ferritin synthesis: how and why

“…Comparison of ferritin gene organisation between plants and animals has been made possible by cloning and sequencing two maize ferritin genes [6], one soybean ferritin gene [7] and one Arabidopsis thaliana ferritin gene [Van Wuytswinkel and Briat, unpublished observations]. From an evolutionary point of view, plant and animal ferritins arose from a common ancestor and are highly conserved proteins [3].…”

“…Indeed, no IRE sequences are present in the 5% untranslated region of any known plant ferritin mRNA sequences deduced from cloned cDNA [14,44,53,54] or genes [6,7]. Furthermore, no IRP activity is detectable in plant cell extracts by RNA gel-shift experiments using animal IRE as a probe [55], or in a translational assay using animal ferritin mRNA and wheat germ extract [56].…”

Cellular regulation and molecular interactions of the ferritins

“…Ferritin synthesis rates respond to changes in cellular iron and oxygen, or oxidants in plants, animals and bacteria [18,[39][40][41][42][43] (fig. 1).…”