Environmental Selection Pressures Related to Iron Utilization Are Involved in the Loss of the Flavodoxin Gene from the Plant Genome

Abstract

Oxidative stress and iron limitation represent the grim side of life in an oxygen-rich atmosphere. The versatile electron transfer shuttle ferredoxin, an iron-sulfur protein, is particularly sensitive to these hardships, and its downregulation under adverse conditions severely compromises survival of phototrophs. Replacement of ferredoxin by a stress-resistant isofunctional carrier, flavin-containing flavodoxin, is a widespread strategy employed by photosynthetic microorganisms to overcome environmental adversities. The flavodoxin gene was lost in the course of plant evolution, but its reintroduction in transgenic plants confers increased tolerance to environmental stress and iron starvation, raising the question as to why a genetic asset with obvious adaptive value was not kept by natural selection. Phylogenetic analyses reveal that the evolutionary history of flavodoxin is intricate, with several horizontal gene transfer events between distant organisms, including Eukarya, Bacteria, and Archaea. The flavodoxin gene is unevenly distributed in most algal lineages, 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 was little selection pressure to retain flavodoxin in iron-rich coastal/freshwater phototrophs. Our results show a highly dynamic evolution pattern of flavodoxin tightly connected to the bioavailability of iron. Evidence presented here also indicates that the high concentration of iron in coastal and freshwater habitats may have facilitated the loss of flavodoxin in the freshwater ancestor of modern plants during the transition of photosynthetic organisms from the open oceans to the firm land.

Community‐Level Responses to Iron Availability in Open Ocean Plankton Ecosystems

“…Global Biogeochemical Cycles qualitative shifts in genotypes highlighted above with changes in transcriptional outputs in cyanobacteria (Figures 9a and 9b), eukaryotic phytoplankton (Figures 9c, 9d, and S5), metazoans ( Figure S6 and supporting information S4), and more specifically in diatoms (Figures 9c, 9d, and S7). Importantly, ISIP levels were decreased in the leeward stations (Figures 5a, 9c, and 9d), and study of gene switches proposed to be responsive to ambient iron concentrations such as ferredoxin/flavodoxin, plastocyanin/cytochrome c 6 , and FBAI/FBAII (Allen et al, 2012;Mackey et al, 2015;Marchetti et al, 2012;Peers & Price, 2006;Pierella Karlusich et al, 2015;Thompson et al, 2011) revealed patterns generally consistent with increased bioavailability at Stations TARA_123-125 with respect to HNLC Station TARA_122 both in Synechococcus (Figures 9a and 9b) and in the major groups of eukaryotic phytoplankton (Figures 9c, 9d, S5, and S7). The abundance of proteorhodopsin and ferritin genes and mRNA in diatoms were generally also consistent with this hypothesis, with decreases in proteorhodopsin transcripts and increases in ferritin in Station TARA_123 with respect to Station TARA_122 (Figures 9c, 9d, and S7d).…”

Stalled flavodoxin binds its cofactor while fully exposed outside the ribosome

“…The flavodoxin-like fold is among the most ancestral folds [27] and is considered to be an archetype for the entire class of αβα sandwiches. Though flavodoxin is absent from plants and animals [28], it is found in most algal lineages [29] and the flavodoxinlike fold is part of many multi-domain eukaryotic proteins such as cytochrome P450 reductase [30] and nitric oxide synthase [31].…”

Reactive oxygen species generated in chloroplasts contribute to tobacco leaf infection by the necrotrophic fungus Botrytis cinerea

“…Fld is a flavin mononucleotide‐containing electron shuttle that can mediate essentially the same reactions as the iron‐sulfur protein ferredoxin (Fd), and is induced in cyanobacteria and some algae under conditions of environmental stress that cause a decline of Fd levels (Lodeyro et al ., ; Pierella Karlusich et al ., ). This flavoprotein is not found in plants (Pierella Karlusich et al ., ), but when a cyanobacterial Fld was expressed in tobacco and targeted to chloroplasts, it was able to functionally interact with plastidic enzymes, driving reducing equivalents away from oxygen and into productive oxido‐reductive pathways of the chloroplast (Tognetti et al ., ; Zurbriggen et al ., ). As a consequence, Fld prevented ROS build‐up in plastids without affecting their production in other cellular compartments (Zurbriggen et al ., ).…”