Magnetic sensitivity mediated by the Arabidopsis blue-light receptor cryptochrome occurs during flavin reoxidation in the dark

Abstract

Arabidopsis cryptochrome mediates responses to magnetic fields that have been applied in the absence of light, consistent with flavin reoxidation as the primary detection mechanism. Cryptochromes are highly conserved blue-light-absorbing flavoproteins which have been linked to the perception of electromagnetic stimuli in numerous organisms. These include sensing the direction of the earth's magnetic field in migratory birds and the intensity of magnetic fields in insects and plants. When exposed to light, cryptochromes undergo flavin reduction/reoxidation redox cycles leading to biological activation which generate radical pairs thought to be the basis for magnetic sensitivity. However, the nature of the magnetically sensitive radical pairs and the steps at which they act during the cryptochrome redox cycle are currently a matter of debate. Here, we investigate the response of Arabidopsis cryptochrome-1 in vivo to a static magnetic field of 500 μT (10 × earth's field) using both plant growth and light-dependent phosphorylation as an assay. Cryptochrome responses to light were enhanced by the magnetic field, as indicated by increased inhibition of hypocotyl elongation and increased cryptochrome phosphorylation. However, when light and dark intervals were given intermittently, a plant response to the magnetic field was observed even when the magnetic field was given exclusively during the dark intervals between light exposures. This indicates that the magnetically sensitive reaction step in the cryptochrome photocycle must occur during flavin reoxidation, and likely involves the formation of reactive oxygen species.

On the optimal relative orientation of radicals in the cryptochrome magnetic compass

“…[28,29,92] could be at play in the presumably highly-optimized and exquisitely sensitive avian compass. This supposition is further substantiated by the recent claims of magnetoreception in the dark, which seems to conflict with the radical pair paradigm, as it implicates swiftly relaxing species such as superoxide [7,23]. Alternatively, [F •− Y • ]-based systems appear better versed than their tryptophancontaining counterparts.…”

“…A magnetic compass in migratory songbirds is hypothesized to rely on photo-induced radical pairs generated within the flavoprotein cryptochrome, located within the animal's retinae [4,6]. A similar mechanism is thought to apply to certain magnetosensitive phenotypes in plants [7][8][9][10], fruit flies [11], cockroaches [12] and newts [13]. Convincing support for this hypothesis includes the experimental demonstration that the photo-reduction of isolated cryptochromes from A. thaliana and D. melanogaster can be influenced by static magnetic fields, albeit at field strengths exceeding the geomagnetic field (~ 50 T) [14][15][16][17].…”

“…The controversy is fueled by the realization that magnetosensitivity could actually arise in a dark-state reaction. Therefore, an alternative hypothesis focusing on the re-oxidation of the fully reduced flavin cofactor by molecular oxygen in a magnetosensitive pathway has also been considered [7,[23][24][25][26]. This would implicate a radical pair involving the swiftly relaxing superoxide anion, i.e.…”

Viability of superoxide-containing radical pairs as magnetoreceptors

“…38 Although the biological parallels with migratory birds are unclear, similar studies on plants have also reported "dark" cryptochrome-related magnetic field effects. 39 All of these observations have been attributed to an M2 mechanism involving [FADH …”

Transcriptomic profiles of non-embryogenic and embryogenic callus cells in a highly regenerative Upland Cotton line (Gossypium hirsutum L.)

“…7 and Additional le 2: Table S12) that ve of the predicted genes were up-regulated in EC and are as follows: GhUGt73C5, UDP-glycosyltransferase 73C5-like gene (Gohir.A01G078300.1) [50]; GhPin2, auxin transporters, encodes an auxin e ux carrier (Gohir.A05G001400.1) [51]; GhNFYB6, nuclear factor Y subunit B-6, acts as a key component regulating embryogenesis and seed maturation in Arabidopsis thaliana (Gohir.A05G176400.1) [52]; GhORG2, transcription factor ORG2-like gene with basic helix-loop-helix (Gohir.A09G106500.1) [53]; GhBBM, AP2like ethylene-responsive baby boom transcription factor (Gohir.D08G247400.1) [54]. The ve deduced genes that were down-regulated in EC, i.e., GhARF4, auxin response factor 4 like, encodes a member of the ARF family of transcription factors (Gohir.A05G074600.1) [55]; GhACRY1/BLU1, cryptochrome-1-like, a avin-type blue-light photoreceptor with ATP binding and autophosphorylation activity (Gohir.A05G226100.1) [56] (Pooam et al, 2018); GhOMT1, encoding a reticuline 7-O-methyltransferaselike gene (Gohir.D02G181400.1); GhCOMT1, raimondii caffeic acid 3-O-methyltransferase-like (Gohir.D12G246900.1) gene [57]; GhCKX3, cytokinin dehydrogenase 3 (Gohir.D07G011600.1) [58]. The results showed that the expression level evaluated by RT-qPCR exhibited similar patterns to the RNA-seq results of the ten genes, con rmed the results of RNA-sEq.…”