The geomagnetic field (GMF) is a natural component of our environment. Plants, which are known to sense different wavelengths of light, respond to gravity, react to touch and electrical signaling, cannot escape the effect of GMF. While phototropism, gravitropism, and tigmotropism have been thoroughly studied, the impact of GMF on plant growth and development is not well-understood. This review describes the effects of altering magnetic field (MF) conditions on plants by considering plant responses to MF values either lower or higher than those of the GMF. The possible role of GMF on plant evolution and the nature of the magnetoreceptor is also discussed.

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Magnetic field effects on plant growth, development, and evolution.

Night-migratory songbirds are remarkably proficient navigators1. Flying alone and often over great distances, they use various directional cues including, crucially, a light-dependent magnetic compass2,3. The mechanism of this compass has been suggested to rely on the quantum spin dynamics of photoinduced radical pairs in cryptochrome flavoproteins located in the retinas of the birds4–7. Here we show that the photochemistry of cryptochrome 4 (CRY4) from the night-migratory European robin (Erithacus rubecula) is magnetically sensitive in vitro, and more so than CRY4 from two non-migratory bird species, chicken (Gallus gallus) and pigeon (Columba livia). Site-specific mutations of ErCRY4 reveal the roles of four successive flavin–tryptophan radical pairs in generating magnetic field effects and in stabilizing potential signalling states in a way that could enable sensing and signalling functions to be independently optimized in night-migratory birds. Cryptochrome 4 from the night-migratory European robin displays magnetically sensitive photochemistry in vitro, in which four successive flavin–tryptophan radical pairs generate magnetic-field effects and stabilize potential signalling states.

Magnetic sensitivity of cryptochrome 4 from a migratory songbird

This review provides detailed insight on the effects of magnetic fields on germination, growth, development, and yield of plants focusing on ex vitro growth and development and discussing the possible physiological and biochemical responses. The MFs considered in this review range from the nanoTesla (nT) to geomagnetic levels, up to very strong MFs greater than 15 Tesla (T) and also super-weak MFs (near 0 T). The theoretical bases of the action of MFs on plant growth, which are complex, are not discussed here and thus far, there is limited mathematical background about the action of MFs on plant growth. MFs can positively influence the morphogenesis of several plants which allows them to be used in practical situations. MFs have thus far been shown to modify seed germination and affect seedling growth and development in a wide range of plants, including field, fodder, and industrial crops; cereals and pseudo-cereals; grasses; herbs and medicinal plants; horticultural crops (vegetables, fruits, ornamentals); trees; and model crops. This is important since MFs may constitute a non-residual and non-toxic stimulus. In addition to presenting and summarizing the effects of MFs on plant growth and development, we also provide possible physiological and biochemical explanations for these responses including stress-related responses of plants, explanations based on dia-, para-, and ferromagnetism, oriented movements of substances, and cellular and molecular changes.

Magnetic fields: how is plant growth and development impacted?

During interplanetary flights in the near future, a human organism will be exposed to prolonged periods of a hypomagnetic field that is 10,000 times weaker than that of Earth's. Attenuation of the geomagnetic field occurs in buildings with steel walls and in buildings with steel reinforcement. It cannot be ruled out also that a zero magnetic field might be interesting in biomedical studies and therapy. Further research in the area of hypomagnetic field effects, as shown in this article, is capable of shedding light on a fundamental problem in biophysics-the problem of primary magnetoreception. This review contains, currently, the most extensive bibliography on the biological effects of hypomagnetic field. This includes both a review of known experimental results and the putative mechanisms of magnetoreception and their explanatory power with respect to the hypomagnetic field effects. We show that the measured correlations of the HMF effect with HMF magnitude and inhomogeneity and type and duration of exposure are statistically absent. This suggests that there is no general biophysical MF target similar for different organisms. This also suggests that magnetoreception is not necessarily associated with evolutionary developed specific magnetoreceptors in migrating animals and magnetotactic bacteria. Independently, there is nonspecific magnetoreception that is common for all organisms, manifests itself in very different biological observables as mostly random reactions, and is a result of MF interaction with magnetic moments at a physical level-moments that are present everywhere in macromolecules and proteins and can sometimes transfer the magnetic signal at the level of downstream biochemical events. The corresponding universal mechanism of magnetoreception that has been given further theoretical analysis allows one to determine the parameters of magnetic moments involved in magnetoreception-their gyromagnetic ratio and thermal relaxation time-and so to better understand the nature of MF targets in organisms.

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Biological effects of the hypomagnetic field: An analytical review of experiments and theories.

The magnetic compass sense of migratory birds is thought to rely on magnetically sensitive radical pairs formed photochemically in cryptochrome proteins in the retina. An important requirement of this hypothesis is that electron spin relaxation is slow enough for the Earth's magnetic field to have a significant effect on the coherent spin dynamics of the radicals. It is generally assumed that evolutionary pressure has led to protection of the electron spins from irreversible loss of coherence in order that the underlying quantum dynamics can survive in a noisy biological environment. Here, we address this question for a structurally characterized model cryptochrome expected to share many properties with the putative avian receptor protein. To this end we combine all-atom molecular dynamics simulations, Bloch–Redfield relaxation theory and spin dynamics calculations to assess the effects of spin relaxation on the performance of the protein as a compass sensor. Both flavin–tryptophan and flavin–Z˙ radical pairs are studied (Z˙ is a radical with no hyperfine interactions). Relaxation is considered to arise from modulation of hyperfine interactions by librational motions of the radicals and fluctuations in certain dihedral angles. For Arabidopsis thaliana cryptochrome 1 (AtCry1) we find that spin relaxation implies optimal radical pair lifetimes of the order of microseconds, and that flavin–Z˙ pairs are less affected by relaxation than flavin–tryptophan pairs. Our results also demonstrate that spin relaxation in isolated AtCry1 is incompatible with the long coherence times that have been postulated to explain the disruption of the avian magnetic compass sense by weak radiofrequency magnetic fields. We conclude that a cryptochrome sensor in vivo would have to differ dynamically, if not structurally, from isolated AtCry1. Our results clearly mark the limits of the current hypothesis and lead to a better understanding of the operation of radical pair magnetic sensors in noisy biological environments.

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Electron spin relaxation in cryptochrome-based magnetoreception

A near-null magnetic field affects cryptochrome-related hypocotyl growth and flowering in Arabidopsis

Blue light-dependent phosphorylations of cryptochromes are affected by magnetic fields in Arabidopsis

We previously found that flowering of Arabidopsis was suppressed by near-null magnetic field, which was related to the modification of cryptochrome. To disclose the physiological mechanism of this effect, we detected gibberellin (GA) levels and expressions of GA biosynthetic and signaling genes in wild type Arabidopsis plants and cryptochrome double mutant, cry1/cry2, grown in near-null magnetic field. We found that levels of GA4 , GA9 , GA34 , and GA51 in wild type plants in near-null magnetic field were significantly decreased compared with local geomagnetic field controls. However, GA levels in cry1/cry2 mutants in near-null magnetic field were similar to controls. Expressions of three GA20-oxidase (GA20ox) genes (GA20ox1, GA20ox2, and GA20ox3) and four GA3-oxidase (GA3ox) genes (GA3ox1, GA3ox2, GA3ox3, and GA3ox4) in wild type plants in near-null magnetic field were significantly reduced compared with controls, while expressions of GA20ox4, GA20ox5, GA2-oxidase (GA2ox) genes, and GA signaling-related genes in wild type plants in near-null magnetic field were not significantly different from controls. In contrast, expressions of all the detected GA biosynthetic and signaling genes in cry1/cry2 mutants were not affected by near-null magnetic field. Moreover, transcriptions of flowering-related genes, LFY and SOC1, in wild type plants were downregulated by near-null magnetic field, while they were not affected by near-null magnetic field in cry1/cry2 mutants. Our results suggest that the effect of near-null magnetic field on Arabidopsis flowering is GA-related, which is caused by cryptochrome-involved suppression of GA biosynthesis. Bioelectromagnetics. 38:1-10, 2017. © 2016 Wiley Periodicals, Inc.

Gibberellins are involved in effect of near-null magnetic field on Arabidopsis flowering.

The influence of the geomagnetic field-removed environment on Arabidopsis growth was investigated by cultivation of the plants in a near-null magnetic field and local geomagnetic field (45 µT) for the whole growth period under laboratory conditions. The biomass accumulation of plants in the near-null magnetic field was significantly suppressed at the time when plants were switching from vegetative growth to reproductive growth compared with that of plants grown in the local geomagnetic field, which was caused by a delay in the flowering of plants in the near-null magnetic field. At the early or later growth stage, no significant difference was shown in the biomass accumulation between the plants in the near-null magnetic field and local geomagnetic field. The average number of siliques and the production of seeds per plant in the near-null magnetic field was significantly lower by about 22% and 19%, respectively, than those of control plants. These resulted in a significant reduction of about 20% in the harvest index of plants in the near-null magnetic field compared with that of the controls. These results suggest that the removal of the local geomagnetic field negatively affects the reproductive growth of Arabidopsis, which thus affects the yield and harvest index.

Removal of the local geomagnetic field affects reproductive growth in Arabidopsis

We previously reported that a near-null magnetic field suppressed Arabidopsis flowering in white light, which might be related to the function modification of cryptochrome (CRY). To further demonstrate that the effect of near-null magnetic field on Arabidopsis flowering is associated with CRY, Arabidopsis wild type and CRY mutant plants were grown in the near-null magnetic field under blue or red light with different light cycle and photosynthetic photon flux density. We found that Arabidopsis flowering was significantly suppressed by near-null magnetic field in blue light with lower intensity (10 µmol/m2/s) and shorter cycle (12 h period: 6 h light/6 h dark). However, flowering time of CRY1/CRY2 mutants did not show any difference between plants grown in near-null magnetic field and in local geomagnetic field under detected light conditions. In red light, no significant difference was shown in Arabidopsis flowering between plants in near-null magnetic field and local geomagnetic field under detected light cycles and intensities. These results suggest that changes of blue light cycle and intensity alter the effect of near-null magnetic field on Arabidopsis flowering, which is mediated by CRY. Bioelectromagnetics. 36:476–479, 2015. © 2015 Wiley Periodicals, Inc.

Yuxia Zhang

Papers

A near-null magnetic field affects cryptochrome-related hypocotyl growth and flowering in Arabidopsis

Blue light-dependent phosphorylations of cryptochromes are affected by magnetic fields in Arabidopsis

Gibberellins are involved in effect of near-null magnetic field on Arabidopsis flowering.

Removal of the local geomagnetic field affects reproductive growth in Arabidopsis

Suppression of Arabidopsis flowering by near‐null magnetic field is affected by light