Environmental selection pressures related to iron utilization are involved in the loss of the flavodoxin gene from the plant genome

PIERELLA KARLUSICH, JUAN J.; CECCOLI, ROMINA D.; GRAÑA, MARTÍN; ROMERO, HÉCTOR; CARRILLO, NÉSTOR

Genome Biology and Evolution

Oxford University Press

Lugar: Oxford; Año: 2015 vol. 7 p. 750 - 767

Oxidative stress and iron limitation represent the grim side of life in an oxygen-rich atmosphere. The versatile electron transfer shuttleferredoxin, an iron-sulfur protein, isparticularly sensitive to these hardships, anditsdownregulationunder adverse conditions severelycompromises survival of phototrophs. Replacement of ferredoxin by a stress-resistant isofunctional carrier, flavin-containing flavodoxin,is a widespread strategy employed by photosyntheticmicroorganisms to overcome environmental adversities. The flavodoxingene was lost in the course of plant evolution, but its reintroduction in transgenic plants confers increased tolerance to environmentalstressand ironstarvation, raisingthequestionas towhyageneticasset with obvious adaptive valuewas not kept by natural selection.Phylogenetic analyses reveal that the evolutionary history of flavodoxin is intricate, with several horizontal gene transfer eventsbetween distant organisms, including Eukarya, Bacteria, and Archaea. The flavodoxin gene is unevenly distributed in most algallineages, with flavodoxin-containing species being overrepresented in iron-limited regions and scarce or absent in iron-rich environments.Evaluation of cyanobacterial genomic and metagenomic data yielded essentially the same results, indicating that there waslittle selection pressure to retain flavodoxin in iron-rich coastal/freshwater phototrophs. Our results showa highly dynamic evolutionpattern of flavodoxin tightly connected to the bioavailability of iron. Evidence presented here also indicates that the high concentrationof iron in coastal and freshwater habitats may have facilitated the loss of flavodoxin in the freshwater ancestor of modernplants during the transition of photosynthetic organisms from the open oceans to the firm land.