This is a post-print version of an article published in: Audet, P., & Charest, C. (2007). Dynamics of arbuscular 1 mycorrhizal symbiosis in heavy metal phytoremediation: Meta-analytical and conceptual perspectives. Environmental Pollution, 147(3), 609-614. doi: 10.1016/j.envpol.2006.10.006.123
Dynamics of arbuscular mycorrhizal symbiosis in
heavy metal phytoremediation:
meta-analytical and conceptual perspectives.
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Patrick Audet & Christiane Charest
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Ottawa-Carleton Institute of BiologyDepartment of BiologyUniversity of Ottawa30 Marie-Curie St.
Ottawa, ON, K1N 6N5 CanadaE-mail:
ccharest@science.uottawa.ca J (corresponding author)paude086@uottawa.ca(613) 562-5800 Ext. 6359(613) 562-5486
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Tel: Fax:
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ABSTRACT
To estimate dynamics of arbuscular mycorrhizal (AM) symbiosis in heavy metal (HM)phytoremediation, we conducted a literature survey and correlated HM uptake and relative plantgrowth parameters from published data. After estimating AM feedback responses for theseparameters at low and high soil-HM concentration intervals, we determined that the roles of AMsymbiosis are characterized by (1) an increased HM phytoextraction via mycorrhizospheric‘Enhanced Uptake’ at low soil-HM concentrations, and (2) a reduced HM bioavailability via AMfungal ‘Metal-Binding’ processes at high soil-HM levels, hence resulting in increased plantbiomass and enhanced plant tolerance through HM stress-avoidance. We present two conceptualmodels which illustrate the important compromise between plant growth, plant HM uptake andHM tolerance, and further emphasize the importance of AM symbiosis in buffering the soilenvironment for plants under such stress conditions.
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“Capsule”: This meta-analysis has revealed a transition role of the AM symbiosis inphytoremediation shifting from ‘Enhanced Uptake’ to ‘Metal-Binding’ beyond critical soil-HM
levels.
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Key words: AM feedback; HM bioavailability; HM phytotoxicity; stress-avoidance.Abbreviations: arbuscular mycorrhizal (AM); heavy metal (HM)
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1.INTRODUCTION
The arbuscular mycorrhizal (AM) symbiosis, an ancient interaction between plant roots
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and zygomycetous fungi (Morton & Benny, 1990), is recognized to benefit plants underenvironmental stress conditions such as nutrient deficiency, drought, and heavy metal (HM)pollution (Audet & Charest, 2006a; Charest et al., 1997; Subramanian & Charest, 1998). Twoantithetical hypotheses have been proposed as for the role of AM symbiosis in HM
phytoremediation: (1) Increased HM phytoextraction via an enhanced mycorrhizosphere (Davieset al., 2001, 2002; Díaz et al., 1996; Hovsepyan & Greipsson, 2004); and (2) Increased plant HMtolerance by a reduced HM bioavailability via fungal metal-binding processes (Audet andCharest, 2006a; Chen et al., 2004; Joner et al., 2000; Weissenhorn et al., 1995). The derivedpredictions for the first hypothesis, which we have designated as ‘Enhanced Uptake’, are thatplant HM uptake is increased whereas HM phytotoxicity is reached at lower soil-HM
concentrations in AM than non-AM plants. By contrast, the predictions for the ‘Metal-Binding’hypothesis are that plant HM uptake is decreased whereas HM phytotoxicity is reached at highersoil-HM concentrations in AM than non-AM plants. We have determined in a previous meta-analysis (Audet & Charest, 2006b) that there is an important compromise between plant growthand HM uptake specifically relating to HM tolerance versus production of biomass under soil-HM conditions. To extend these observations, we have evaluated the impact of AM symbiosis inphytoremediation by testing for the first time the ‘Enhanced Uptake’ and ‘Metal-Binding’hypotheses using meta-analytical approaches. Furthermore, we present conceptual models ofHM uptake and plant growth that illustrate the dynamic roles of AM symbiosis inphytoremediation.
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2.2.1.
METHODSMeta-analysis
In this meta-analytical study, based on the methods of Hedges & Olkin (1985) and Lipsey
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& Wilson (2001), we have tested the correlations between the AM feedback on plant HMuptake, the AM feedback on plant biomass, and the AM root colonization in relation to soil-HMconcentrations by using combined results from multiple studies. After a thorough scientificliterature review, we selected 20 articles for having dealt with herbaceous plants and AM fungi,and for having provided measures of plant biomass and HM uptake. For inclusion in ouranalyses, the selected studies consisted of greenhouse experiments having AM and non-AMinoculated treatments with the soil mineral composition described, and the data presented intables. Key variables included soil HM concentration (mg kg-1 dry soil), plant HM concentration(mg kg-1 dry mass) and/or content (mg plant-1) for shoots and/or roots, and plant dry mass (g) forshoots and/or roots. The data of AM root colonization were taken from studies having estimatedthe percent (%) colonized root length according to the method of Giovannetti & Mosse (1980). All the HM (e.g. As, Cd, Co, Cr, Cu, Fe, Mn, Pb, U, and Zn) with their soil concentration rangesalong with plant and AM fungal species analyzed in our study are appended (SupplementaryData). 2.2.
Metrics
The plant HM concentration ([HMplant]) or content (HMplant) for shoots and/or roots wasused to measure the plant HM uptake, whereas the biomass for shoots and/or roots was used tomeasure plant growth. From these measures, we calculated the AM feedback percentage (%) asan estimate of the relative contribution of AM symbiosis to these plant parameters (modifiedfrom Plenchette et al., 1983). The equations of AM feedback on plant HM concentration (1),
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plant HM content (2), and plant biomass (3), estimating the differences in AM relative to non-AM colonized plants, are defined as:
(1)
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([HM]AM−[HM]nonAM)[HM]nonAM×100%79
(2)
(HMAM−HMnonAM)×100%HMnonAM80
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(biomassAM−biomassnonAM)biomassnonAM×100%8182
2.3.Statistical analyses
The Pearson product-moment correlation test (Zar, 1999) was used to calculate the
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strength and significance of the following correlations: between the AM feedback on plant HMuptake, the AM feedback on plant biomass, or the AM root colonization in relation with the soil-HM concentration. We applied logarithmic transformations to each of these variables to enhancethe relationship linearity, and meet normal distribution and homoscedasticity assumptions for allthe analyses. We calculated coefficients for all the parameters at the low (10-3 to 1 mg kg-1 drysoil) and high (1 to 104 mg kg-1 dry soil) soil-HM concentration ranges separately, since the linearrelationships differed between these two intervals. We have detected broadscale trends for thesetwo intervals despite the lower statistical power at the low than the high soil-HM interval giventhat there were fewer available data for the former than the latter. The low soil-HM intervalrefers to the ‘control’ type soils, whereas the high soil-HM interval refers to the ‘treatment’ soilsfrom the studies included in our analyses. All of the p-values were determined using S-Plus® 7.0
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(Insightful, 2005).3.
RESULTS
The AM feedback percentages (%) on plant HM concentration (Fig.1a) and plant HMcontent (Fig.1b) are plotted versus the soil-HM concentration. Their correlation coefficients (Table 1) at the low soil-HM interval were significantly positive (0.83 for both), ranging from100% lower to 200% higher HM uptake in AM than non-AM plants as soil-HM concentrationincreased. Conversely, at the high soil-HM interval, the correlation coefficients were
significantly negative (-0.38 and -0.25) at the high soil-HM interval, ranging from 150% higher to100% lower HM uptake in AM than non-AM plants as soil-HM concentration increased.
The AM feedback % on biomass (Fig.2) is plotted versus the soil-HM concentration. There was no correlation at the low soil-HM interval, but a significant positive correlation (0.24)at the high soil-HM interval (Table 1). The AM feedback % ranged between 25% lower and25% higher biomass at the low soil-HM interval, except a few outliers, whereas it ranged from50% lower to 200% higher biomass at the high soil-HM interval.
The AM root colonization % is plotted versus the soil-HM concentration (Fig.3). Therewas a significantly positive correlation (0.43) at the low soil-HM interval, but no correlation atthe high soil-HM interval (Table 1). The root colonization ranged between 20% and 80%colonized root length at the low soil-HM interval, whereas it ranged between 15% and 90% atthe high soil-HM interval.
Our conceptual model of plant HM uptake in relation to soil-HM level (Fig.4) shows apositive and linear curve that tends to reach a plateau at the high soil-HM level. We havedesignated zones of ‘Enhanced Uptake’ and ‘Metal-Binding’ which show greater HM uptake inAM than non-AM plants at the low soil-HM level, and the reverse at the high soil-HM level. Wealso refer to the transition zone shifting from ‘Enhanced Uptake’ to ‘Metal-Binding’ as the area
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of kinetic equilibrium without any detectable difference between the AM and non-AM plants.
Our conceptual model of relative plant biomass (% of maximum) in relation to soil-HMlevel (Fig.5) shows a parabolic curve of relative plant growth characterized by zones of
deficiency (a), optimum (b), and toxicity (c). Plant growth is greater for AM than non-AM plantswithin the ‘Metal-Binding’ zone at the high soil-HM level, whereas there is no different responsebetween the AM and non-AM plants within the ‘Enhanced Uptake’ and transition zone at thelow to intermediate soil-HM level.
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4.DISCUSSION
Our meta-analytical findings have revealed that AM symbiosis plays dynamic roles for
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plants as soil-HM levels increase. In fact, the AM feedback on plant HM uptake was shown toincrease up to three-fold at the low soil-HM interval, while decreasing by the same factor at thehigh soil-HM interval. As predicted by the ‘Enhanced Uptake’ hypothesis, the greater volume ofthe mycorrhizosphere, compared to the rhizosphere alone, provides an increased access to soilresources, including macro-, micro-, and even non-essential elements. In our study, themycorrhizospheric impact, accounting for nearly 200% greater HM uptake in AM than non-AMplants at the low soil-HM interval, is likely the result of active soil-HM transport to the roots viathe extraradical hyphal network (Burleigh et al., 2003; González-Guerrero et al., 2005;Rosewarne et al., 1999). Our results also showed that the AM feedback decreases andeventually reaches negative values at the high soil-HM interval, accounting for nearly 100%lower HM uptake in AM than non-AM plants. As predicted by the ‘Metal-Binding’ hypothesis,the AM fungi are expected to reduce the soil-HM bioavailability since metals are sequestered inextraradical hyphae (Joner et al., 2000; Rufyikiri et al., 2003), therefore resulting in lower HMuptake in AM than non-AM plants. This sequestration process likely occurs in two phases in
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which metals bind first to the hyphal wall, then diffusing into hyphal cells (Gadd, 1993;Gonzalez-Chavez et al., 2002). Considering all our metal-analytical results, both the ‘EnhancedUptake’ and ‘Metal-Binding’ hypotheses are supported in that plant HM uptake is enhanced atlow soil-HM concentrations, yet reduced at high soil-HM concentrations. Fittingly, ourconceptual model of plant HM uptake incorporates both the ‘Enhanced Uptake’ and ‘Metal-Binding’ in the context of nutrient acquisition kinetics (Kirk, 2002; Marschner, 1995), in whichplant HM uptake should be limited by the bioavailability of soil-HM and the maximum rootuptake capacity. By integrating the AM symbiosis into our model, we revealed that themycorrhizosphere provides ‘Enhanced Uptake’ via increased extraradical uptake sites, thusincreasing the maximum root uptake capacity and resulting in higher HM uptake in AM thannon-AM plants at low soil-HM level. In addition, the mycorrhizosphere also comprises more‘Metal-Binding’ sites involved in the immobilization of soil-HM, hence resulting in decreasedsoil-HM bioavailability and lower HM uptake in AM than non-AM plants at high soil-HM levels. Therefore, we propose that the transition from ‘Enhanced Uptake’ to ‘Metal-Binding’ reflects akinetic equilibrium between these two phenomena whereby their effects offset one another,resulting in no detectable difference in HM uptake between AM and non-AM plants at theintermediate soil-HM level.
Moreover, we measured an increasingly positive AM feedback on plant biomass at thehigh soil-HM interval, whereas no correlation was detected at the low soil-HM interval. Thisimplies that the biomass in AM plants increases up to two-fold higher than non-AM plants, aresponse corresponding to a two-fold lower plant HM level then characterizing some plant stress-avoidance via hyphal ‘Metal-Binding’. Consistent with this hypothesis, the AM fungi have beenshown to buffer the soil environment by immobilizing soil-HM and reducing their bioavailability(Audet and Charest, 2006a; Chen et al., 2004; Joner et al., 2000; Weissenhorn et al., 1995).
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Considering the compromise between plant growth and HM tolerance (Audet & Charest, 2006b),the AM plants most likely invest more in a stress-avoidance strategy via ‘Metal-Binding’ ratherthan in metabolically more costly stress-resistance alternatives, such as HM phytochelation andphytosequestration (Cobbett, 2000; Maier et al., 2003). In view of all our observations, wepropose a conceptual model as to the role of AM symbiosis on relative plant biomass asinfluenced by the soil-HM bioavailability and plant HM uptake. In our model, AM symbiosisenhances plant biomass at high soil-HM levels via ‘Metal-Binding’ by decreasing HM
bioavailability and subsequently reducing potential phytotoxic effects. Although it is well knownthat the ‘Enhanced Uptake’ of any limiting elements usually enhances plant growth (Kothari etal., 1990; Marschner, 1995), our meta-analytical findings rather favour the stress-avoidancescenario via hyphal ‘Metal-Binding’.
Finally, the fact that the percent colonized root length is significantly increased at lowsoil-HM concentrations suggests that plants invest increasingly more in AM symbiosis at low soil-HM levels. Although no significant trend was detected at the high soil-HM levels, the studiesincluded in our analysis reported AM colonization values as high as 90% total root length despitesoil-HM concentrations reaching up to 103 mg kg-1 dry soil. This is remarkable considering thathighly toxic soil-HM conditions have been shown in some cases to adversely affect AM rootcolonization, such as by reducing spore germination or hyphal development (Del Val et al., 1999;Leyval et al., 1997; Pawlowska & Charvat, 2004; Weissenhorn et al., 1995). However, otherstudies also showed that plants invest more in AM symbiosis under increasing soil-HMconditions, as indicated by increasing AM root colonization (Audet & Charest, 2006a). Thesecontrasting results may be attributed to differences in plant or mycorrhizal HM tolerance as wellas specific edaphic conditions, such as soil-HM concentration, HM speciation, and soil-pH (Gilleret al., 1998; Hayman & Tavares, 1985; Leyval et al., 1997). Nevertheless, according to our two
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proposed models of plant HM uptake and relative plant biomass, the AM feedback must beaffected by the mycorrhizospheric volume. Besides the ‘Enhanced Uptake’ and ‘Metal-Binding’phenomena, the mycorrhizosphere was also shown to change soil structure by stabilizingaggregates (Augé et al., 2001; Bearden & Peterson, 2000; Miller & Jastrow, 1990), therebyenhancing soil-HM retention capacity. Furthermore, since metal speciation is greatly influencedby pH (Apak, 2002), soil-HM bioavailability could be affected by mycorrhiza-induced substrate-pH modifications (Rufyikiri et al., 2003). Taking all of these factors into consideration, the AMsymbiosis, by enhancing soil-HM retention either directly via fungal ‘Metal-Binding’ or indirectlyvia soil-aggregate HM sorption, could buffer the soil environment by reducing HMbioavailability.
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5.CONCLUSION
In this meta-analytical survey, we have focused on the dynamic roles of the AM symbiosis inHM phytoremediation as characterized by the ‘Enhanced Uptake’ and ‘Metal-Binding’hypotheses, the latter being associated with an enhanced HM tolerance in AM plants via stress-avoidance at high soil-HM levels. We also recognized the compromise between plant growth andHM tolerance, which points to the importance of ‘Metal-Binding’ processes in buffering the soilenvironment. Hence, a comprehensive survey of the mycorrhizosphere would be valuable tofurther understand plant tolerance mechanisms under various environmental stress conditions,especially with respect to bioremediation.
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ACKNOWLEDGMENTS
The authors wish to thank the Editor-in-Chief and the three anonymous reviewers for this
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publication. This research was funded by a grant from the Natural Sciences and EngineeringResearch Council of Canada (NSERC) to CC.
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Figure 1. AM feedback percentage (%) on plant HM concentration (a) and plant HM content (b)
in relation to soil-HM concentration. The vertical reference line separates the low (10-3 to1 mg kg-1 dry soil) and high (1 to 104 mg kg-1 dry soil) soil-HM intervals.
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Figure 2. AM feedback percentage (%) on plant biomass in relation to soil-HM concentration.
The vertical reference line separates the low (10-3 to 1 mg kg-1 dry soil) and high (1 to 104mg kg-1 dry soil) soil-HM intervals.
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Figure 3. AM root colonization (% colonized root length) in relation to soil-HM concentration.
The vertical reference line separates low (10-3 to 1 mg kg-1 dry soil) and high (1 to 104 mgkg-1 dry soil) soil-HM intervals.
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Figure 4. Conceptual model of plant HM uptake in relation to soil-HM concentration.
Designated are zones of ‘Enhanced Uptake’ and ‘Metal-Binding’ showing greater HMuptake for AM than non-AM plants at low soil-HM levels (1), and lower AM plant HMuptake at high soil-HM level (2). The transition zone switching from ‘Enhanced Uptake’to ‘Metal-Binding’ as the area of kinetic equilibrium showing no detectable differencebetween the AM and non-AM plants.
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Figure 5. Conceptual model of relative plant growth (% of maximum) in relation to soil-HM
concentration. Indicated are zones of deficiency (a) at low soil-HM, optimum (b) atintermediate soil-HM, and toxicity (c) at high soil-HM levels. Designated are zones of‘Enhanced Uptake’ and ‘Metal-Binding’ showing greater biomass for AM than non-AMplants at high soil-HM levels (1), and no growth response associated with the ‘Enhanced
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Uptake’ and transition zones at low to intermediate soil-HM levels.
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Table 1. Correlation coefficients (r) for AM feedback percentages (%) on plant HM content,plant HM concentration, biomass, and colonized root length in relation to the soil HMconcentration. The r values, degrees of freedom (df), and p-values are shown.Parameter
soil-HM concentration
low soil-HM interval(10-3 - 1 mg kg-1 dry soil)r
df22143021
p<10-7<10-40.19<0.05
r-0.38-0.250.24-0.1
high soil-HM interval(1 - 104 mg kg-1 dry soil)
df177131130172
p<10-4<10-3<0.010.21
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332333334335
plant HM concentrationplant HM contentplant biomass
AM colonized root length
0.830.830.240.43
Figure 1Click here to download high resolution imageFigure 2Click here to download high resolution imageFigure 3Click here to download high resolution imageFigure 4Click here to download high resolution imageFigure 5Click here to download high resolution imageSupplementary Data 1
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Appendix 1. Arbuscular mycorrhizal (AM) and plant species included in the meta-analysis.AM speciesGlomus caledonium(Nicol. & Gerd.)
Gerdemann & TrappeGlomus intraradicesSchenck & Smith
Plant speciesZea mays L.Pteris vittata L.Nicotiana rustica L.Nicotiana tabacum L.Pisum sativum L.Pteris vittata L.
Soil HMZnAs, UZnCdCdAs, U
References
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Audet and Charest 2006Janouskova et al. 2005Rivera-Becerril et al. 2002Chen et al. 2006
91011
Glomus mosseae(Nicol. & Gerd.)
Gerdemann & Trappe
Allium cepa L.Cannabis sativa L.Pteris vittata L.Trifolium pratense L.
Zn, CoCd , Cr, NiAs, UCd, Pb, ZnCd, ZnCd
Cd, Cu, Mn, Pb, Zn
Gildon and Tinker 1983Citterio et al. 2005Chen et al. 2006
Bi et al. 2003; Chen et al. 2003; Li andChristie 2001; Vivas et al. 2003aVivas et al. 2003b; Zhu et al. 2001Joner and Leyval 1997
Chen et al. 2004a; Weissenhorn et al.1995
12
Trifolium repens L.Trifolium subterraneum L.Zea mays L.
13
Glomus sp.a
Cynodon dactylon (L.)Pers.
Glycine max L.
Lolium perenne
multiflorum (Lam.)Parnell.
As
Cd, Cu, Fe, Mn, ZnCd
Leung et al. 2006
Heggo et al. 1990Yu et al. 2005
14
Pteris vittata L.
a
Consortium of Glomus sp.
As, U
Leung et al. 2006
Supplementary Data 2
15
Appendix 2. Heavy metals (HM) and soil concentration ranges included in the meta-analysisHMAsCdCoCrCuFeMnNiPbUZn
Soil HM range(mg kg-1 dry soil)1 - 1060.001 - 8 3715 - 7550 - 3000.91 - 457.9 - 77.42.2 - 3105 - 10030 - 8951060.19 - 1 220
References
Chen et al. 2006; Leung et al. 2006
Chen et al. 2004a; Citterio et al. 2005; Heggo et al. 1990; Janouskova et al. 2005; Joner and Leyval1997; Rivera-Becerril et al. 2002; Vivas et al. 2003b; Weissenhorn et al. 1995; Yu et al. 2005Gildon and Tinker 1983Citterio et al. 2005
Heggo et al. 1990; Weissenhorn et al. 1995Heggo et al. 1990
Heggo et al. 1990; Weissenhorn et al. 1995Citterio et al. 2005
Vivas et al. 2003a; Weissenhorn et al. 1995Chen et al. 2006
Audet and Charest 2006; Bi et al. 2003; Chen et al. 2003, 2004b; Gildon and Tinker 1983; Heggoet al. 1990; Li and Christie 2001; Weissenhorn et al. 1995; Zhu et al. 2001
16
1718
19202122232425262728
Supplementary Data 3
293031323334353637383940414243444546474849505152535455
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