The long goodbye: the rise and fall of flavodoxin during plant evolution

JUAN J. PIERELLA KARLUSICH; ANABELLA F. LODEYRO; NÉSTOR CARRILLO

JOURNAL OF EXPERIMENTAL BOTANY

OXFORD UNIV PRESS

Lugar: Oxford; Año: 2014 vol. 18 p. 5161 - 5178

0022-0957

Ferredoxins are electron shuttles harboring iron-sulfur clusters which connect multiple oxido-reductive pathways in organisms displaying different lifestyles. Some prokaryotes and algae express an isofunctional electron carrier, flavodoxin, which contains flavin mononucleotide as cofactor. Both proteins evolved in the anaerobic environment preceding the appearance of oxygenic photosynthesis. The advent of an oxygen-rich atmosphere proved detrimental to ferredoxin due to iron limitation and oxidative damage to the iron-sulfur cluster, and many microorganisms induced flavodoxin expression to replace ferredoxin under stress conditions. Paradoxically, ferredoxin was maintained throughout the tree of life, whereas flavodoxin is absent from plants and animals. Noteworthy, flavodoxin expression in transgenic plants results in increased tolerance to multiple stresses and iron deficit, through mechanisms similar to those operating in microorganisms. Then, the question remains open as to why a trait which still confers plants so obvious adaptive benefits was not retained. We compare herein the properties of ferredoxin and flavodoxin, and their contrasting modes of expression in response to different environmental stimuli. Phylogenetic analyses suggest that the flavodoxin gene was already absent in the algal lineages immediately preceding land plants. Geographical distribution of phototrophs shows a bias against flavodoxin-containing organisms in iron rich coastal/freshwater habitats. Based on these observations, we propose that  plants evolved from freshwater macroalgae which already lacked flavodoxin  because they thrived in an iron-rich habitat with no need to back up ferredoxin  functions and therefore, no selective pressure to keep the flavodoxin gene.  Conversely, ferredoxin retention in the plant lineage is likely related to its higher  efficiency as electron carrier compared to flavodoxin. Several lines of evidence  supporting these contentions are presented and discussed.