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Magnetoreception:Anunavoidablestepforplantevolution?

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ImpactFactor:12.93·DOI:10.1016/j.tplants.2013.10.007·Source:PubMed

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AndreaOcchipinti

UniversitàdegliStudidiTorino

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AngeloDeSantis

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MassimoEMaffei

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Magnetoreception: an unavoidable step for plantevolution?

Andrea Occhipinti1, Angelo De Santis2, and Massimo E. Maffei1

1 Department of Life Sciences and Systems Biology, Innovation Centre, Via Quarello 15/A, University of Turin, 10135 Turin, Italy2 Istituto Nazionale di Geofisica e Vulcanologia, Via di Vigna Murata, 605 00143 Rome, Italy

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The geomagnetic field (GMF) is steadily acting on livingsystems, and influences many biological processes. Inanimals, the mechanistic origin of the GMF effect hasbeen clarified and cryptochrome has been suggested asa chemical magnetoreceptor. Here we propose a possi-ble role for the GMF variations in plant evolution.

The GMF and its dynamic changesThroughout evolution the GMF has been a natural compo-nent of the environment for living organisms. The presentmagnetism of the Earth, the GMF, is slowly varying, fairlyhomogeneous, and relatively weak. A magnetic field (MF) isusually measured in terms of its magnetic induction, B,whose units are given in Tesla (T). The strength of the GMFat the surface of the Earth ranges from less than 30 mT in anarea including most of South America and South Africa (theso-called South Atlantic anomaly) to over 60 mT around themagnetic poles in northern Canada, the south of Australia,and in part of Siberia. Most of the MF observed at the surfaceof the Earth surface has an internal origin. It is mainlyproduced by the dynamo action of turbulent flows in the fluidmetallic outer core of the planet, and little is due to externalMFs located in the ionosphere and the magnetosphere [1]:the ionosphere is the ionized atmospheric layer with maxi-mum ionization at an altitude of �200 km; the magneto-sphere is the region several tens of thousands of kilometersfrom the Earth where the GMF extends its effects into space.It is the presence of the GMF that, through the magneto-sphere, protects the Earth, together with its biosphere, fromthe solar wind (a stream of energetic charged particlesemanating from the Sun), deflecting most of its chargedparticles. Only occasionally, during the so-called magneticstorms produced by increased solar activity, some amountsof charged particles of the solar wind and cosmic rayspenetrate the magnetosphere, causing stronger externalMFs of thousands of nT all over the planetary surface. Inthe history of the Earth the GMF has exhibited severalchanges of magnetic polarity, with the so-called geomagnet-ic reversals or excursions, characterized by persistent per-iods with the same polarity. These have occurred somehundred times since the formation of the Earth, and the

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� 2013 Published by Elsevier Ltd. http://dx.doi.org/10.1016/j.tplants.2013.10.007

Corresponding author: Maffei, M.E. (massimo.maffei@unito.it).

mean time between one reversal and the next has beenestimated to be around 300 000 years. Because the presentnormal polarity started around 780 000 years ago, andsignificant field decay has been taking place during the past1000 years, an imminent geomagnetic reversal would not beunexpected. The South Atlantic anomaly, a surface mani-festation of a reversed magnetic flux in the outer core, couldbe the initial symptom of a future change of polarity [2].Moreover, the extrapolation of the present behavior wouldpredict a GMF reversal in less than 1000 years, which is, ingeological and evolutionary terms, a very short time.

It has been suggested that the GMF might have impor-tant consequences over the biosphere [3], especially onhumans and animals [4], but very little is known aboutits effect on plants.

Plant magnetoreceptionIn the past 50 years several studies have been performed toevaluate plant responses to exposure to different MFstrengths, from near-null (0–40 mT) to low (up to 40 mT)and extremely high values (up to 30 T). The reportedresults show a variety of plant responses at the biochemical[the activity of scavenging enzymes for reactive oxygenspecies (ROS)], molecular (gene expression of the crypto-chrome pathway), cellular (ultrastructural studies andamyloplast displacement), and whole-plant (flowering de-lay and phenotypic effects) levels [5]. Most of the reportedresults are in agreement that the impact of a MF on abiological organism varies depending on its style of appli-cation, time, and intensity. High-intensity MFs have de-structive effects on plants; however, at low intensitiesthese phenomena are of special interest because of thecomplexity of plant responses. Compared to studies inanimals, very little is known about magnetoreception inplants, although early studies on plants were initiatedmore than 70 years ago. Nevertheless, fundamental ques-tions such as whether or not plants perceive MF, thephysical nature of the MF receptor(s), and whether ornot (G)MFs have any bearing on the physiology and sur-vival of plants are beginning to be resolved.

Are there magnetoreceptors in plants?Unlike plants, some animals show evident utilization ofGMF for their own purposes. For instance, a model of avianmagnetoreception postulates a magnetic sensory system inthe eye that delivers a magnetic reference direction andemploys the blue-light photoreceptor protein cryptochrometo sense the GMF. The unique biological function of

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cryptochrome supposedly arises from a photoactivationreaction involving transient radical pair formation byphoto-induced electron transfer reactions. The radical-pairmechanism (RPM) is currently the only physically plausi-ble mechanism by which magnetic interactions that areorders of magnitude weaker than the average thermalenergy, kBT, can affect chemical reactions. The kineticsand quantum yields of photo-induced flavin–tryptophanradical pairs in cryptochrome are indeed magneticallysensitive, and cryptochrome is a good candidate for achemical magnetoreceptor. Cryptochromes have alsoattracted attention as potential mediators of biologicaleffects of extremely low frequency (ELF) electromagneticfields, and possess properties required to respond toEarth-strength (approximately 50 mT) fields at physiologicaltemperatures [6].

Recently, a combination of quantum biology and molecu-lar dynamics simulations on plant cryptochrome has dem-onstrated that a radical pair forms after photoexcitation,becomes stabilized through proton transfer, and decays backto the protein resting state on timescales allowing theprotein, in principle, to act as a radical pair-based magneticsensor, as has been suggested for the avian compass ([7] andreferences therein) (Figure 1A). Furthermore, elimina-tion of the local GMF weakens the inhibition of Arabi-dopsis (Arabidopsis thaliana) hypocotyl growth by whitelight, and delays flowering time. The expression changesof three Arabidopsis cryptochrome signaling-relatedgenes (PHYB, CO, and FT) suggest that the effects of anear-null MF are cryptochrome-related, and might in-volve a modification of the active state of cryptochromeand the subsequent signaling cascade [8]. Figure 1Ashows the proposed involvement of cryptochrome in plantmagnetoreception.

Why a plant magnetoreceptor?Magnetoreception in animals is well documented, espe-cially in the context of orientation during migration,whereas the role of this mechanism in plants is lessunderstood. As sedentary organisms, plants should notrequire long-distance orientation. Pollen and seed dis-persal are passive mechanisms of dispersion that do notrequire orientating systems. Thus, there must be someother reason for plant magnetoreception. Physiologicaloscillations occur under constant conditions of light, tem-perature, and humidity. We commonly refer to theseoscillations as endogenous biological rhythms. Thereare several examples of plant responses to oscillationsincluding thigmotropism, phototropism, and gravitrop-ism. Understanding the mechanisms of plant tropic reac-tions is a central problem in plant biology becausetropisms comprise the complete signal–response chainthat plants use to maintain growth and development.Oscillating MFs induce oscillation of Ca2+ ions and changethe rate and/or the direction of Ca2+ ion flux; moreover,they affect the distribution of amyloplasts in the stato-cytes of gravistimulated roots because amyloplasts aremore diamagnetic than the aqueous cytoplasm [9]. Geo-magnetic storms induce aberration at the plant cellularand tissue levels, and alter the patterns of leaf attachmentto the stem [10]. Because plants react to changes in the

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GMF we cannot exclude the potential contribution of GMFto plant adaptation and evolution.

The GMF and plant evolutionTogether with gravity, light, temperature, and water avail-ability, the GMF has been present since the beginning ofplant evolution. Apart from gravity, all other factors, includ-ing the GMF, have changed consistently during plant evo-lution, thereby representing important abiotic stress factorsthat eventually contribute to plant diversification and spe-ciation. Some authors have pointed out that, during geomag-netic reversals, the biological material of the Earth isexposed to more intense cosmic radiation and/or UV light.As a consequence, mutations may occur, and these could leadto higher rates of speciation [11]. Mass extinction eventsprofoundly reshaped the biota of the Earth during the earlyand late Mesozoic, and terrestrial plants were among themost severely affected groups. Several plant families werewiped out, while some new families emerged and eventuallybecame dominant (Figure 1B). The behavior of the GMFduring the Mesozoic and late Paleozoic, or more preciselybetween 86 and 276.5 millions of years (Myr) ago, is ofparticular interest. Its virtual dipole moment (VDM) seemsto have been significantly reduced (�4 � 1022 Am2) com-pared to present day values [12]. Because the strength ofthe GMF is strongly reduced during polarity transitions, ascompared to stable normal or reversed polarities, we proposethat these variations might correlate with plant evolution.We do not have measurable records of GMF polarity reversalbefore the late Jurassic, therefore we compared variations ofGMF polarity with diversion of families and orders of angios-perms in the Tertiary and Cretaceous periods. Angiospermsare regarded as one of the greatest terrestrial radiations ofrecent geological times. The oldest angiosperm fossils datefrom the early Cretaceous, 130–136 Myr ago, followed by arise to ecological dominance in many habitats before the endof the Cretaceous [13]. We found that the periods of normalpolarity transitions overlapped with the diversion of most ofthe familial angiosperm lineages (Figure 1B, inset). Thiscorrelation appears to be particularly relevant for angios-perms compared to other plants. Patterns of diversificationreconstructed onto phylogenetic trees depend on the age oflineages, their intrinsic attributes, and the environmentsexperienced since their origins. Global environments havechanged considerably during the history of angiospermradiation; for example, the rise of grasses to dominanceduring the late Tertiary has been linked to global coolingand drying. We argue that magnetoreception might be arelevant factor in plant evolution.

Further studies and directionsGiven the fragmentation of studies conducted to dateregarding the biophysical and biological effects of theGMF, we have only preliminary insights into its physio-logical effects upon plants. To achieve a noteworthy break-through, and confirm the role of magnetoreception inplants, it is mandatory to identify the biochemical natureof magnetoreceptor(s) and to explore the downstream cel-lular pathways that convert the biophysical event to cellu-lar responses, eventually leading to regulation of plantgrowth and development.

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TRENDS in Plant Science

FADH-

Figure 1. Magnetoreception and plant evolution. (A) Cryptochrome activation and inactivation reactions. Blue light activates cryptochrome via the absorption of a photon

by the flavin cofactor. The electron transfer pathway leading from the protein surface to the FAD cofactor buried within the protein is shown. FAD becomes promoted to an

excited FAD* state and receives an electron from a nearby tryptophan, leading to the formation of the [FADH� + Trp�] radical pair, which exists in singlet (1) and triplet (3)

overall electron spin states by coherent geomagnetic field (GMF)-dependent interconversions. Under aerobic conditions, FADH� slowly reverts back to the initial inactive

FAD state through the also inactive FADH� state of the flavin cofactor. Rate constant (k) abbreviations: et, electron transfer; ox, oxidation; red, reduction; rel, relaxation; rp;

S; T. (B) The evolutionary history of plants. The abundance and diversity of plant fossils increase in the Silurian (Sil.) period where the first macroscopic evidence for land

plants has been found. There is evidence for the evolution of several plant groups of the late Devonian (Dev.) and early Carboniferous (Car.) periods (homosporous ferns

and gymnosperms). From the late Devonian through to the base of the late Cretaceous (Cret.), gymnosperms underwent dramatic evolutionary radiations and became the

dominant group of vascular plants in most habitats. Flowering plants probably also originated during this time, but they did not become a significant part of the fossil flora

until the middle of the Cretaceous. The inset shows a direct comparison between GMF polarity and the diversification of the angiosperms. It is interesting to note that most

of the diversification occurred during periods of normal magnetic polarity. Other abbreviations: Jur., Jurassic, Myr, million years ago; Perm., Permian; Quat., Quaternary;

Tert., Tertiary; Tri., Triassic.

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Despite numerous papers on the effect of GMF onplants, many unanswered questions remain and will needto be addressed in future studies: (i) why should plantsregulate their physiological processes in response to vari-ation of GMF? (ii) How does GMF affect plant development,and do cryptochrome-related biophysical mechanisms playa role in plant magnetoreception? (iii) Do geological varia-tions of GMF have a role in plant evolution?

References1 Merrill, R.T. et al. (1996) The Magnetic Field of the Earth:

Paleomagnetism, the Core and the Deep Mantle, Academic Press2 De Santis, A. et al. (2004) Information content and K-entropy of the

present geomagnetic field. Earth Planet. Sci. Lett. 218, 269–2753 Raup, D.M. (1985) Magnetic reversals and mass extinctions. Nature

314, 341–3434 Benhamou, S. et al. (2011) The role of geomagnetic cues in green turtle

open sea navigation. PLoS ONE 6, e266725 Galland, P. and Pazur, A. (2005) Magnetoreception in plants. J. Plant

Res. 118, 371–389

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6 Maeda, K. et al. (2012) Magnetically sensitive light-induced reactionsin cryptochrome are consistent with its proposed role as amagnetoreceptor. Proc. Natl. Acad. Sci. U.S.A. 109, 4774–4779

7 Solov’yov, I.A. and Schulten, K. (2012) Reaction kinetics andmechanism of magnetic field effects in cryptochrome. J. Phys. Chem.B 116, 1089–1099

8 Xu, C.X. et al. (2012) A near-null magnetic field affects cryptochrome-related hypocotyl growth and flowering in Arabidopsis. Adv. Space Res.49, 834–840

9 Kordyum, E.L. et al. (2005) A weak combined magnetic field changesroot gravitropism. Adv. Space Res. 36, 1229–1236

10 Minorsky, P.V. (2007) Do geomagnetic variations affect plant function?J. Atm. Solar-Terrestr. Phys. 69, 1770–1774

11 Tsakas, S.C. and David, J.R. (1986) Speciation burst hypothesis – anexplanation for the variation in rates of phenotypic evolution. Genet.Sel. Evol. 18, 351–358

12 Shcherbakov, V.P. et al. (2002) Variations in the geomagnetic dipoleduring the past 400 million years (volcanic rocks). Izvestiya-Phys. SolidEarth 38, 113–119

13 Soltis, D.E. et al. (2008) Origin and early evolution of angiosperms.Ann. N. Y. Acad. Sci. 1133, 3–25