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Article title: Examining the ecological paradox of the ‘mycorrhizal-metal-hyperaccumulators’

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Examining the ecological paradox of the

‘mycorrhizal-metal-hyperaccumulators’

Patrick Audet*

Centre for Mined Land Rehabilitation, University of Queensland, Brisbane, Australia

(Received 8 December 2011; final version received 13 January 2012)

This analysis identifies and attempts to resolve the paradox of combining planthyperaccumulators and arbuscular mycorrhizal fungi (AMF) for the purpose ofpost-industrial bioremediation due to the divergence of their respective ecologicaland evolutionary stress-tolerance behaviors. The identification of a ‘dilemmaof resource allocation’ associated with plant resources consumed in intrinsic(e.g. metabolic) vs. extrinsic (e.g. symbiotic) stress-tolerance mechanisms couldprovide a suitable evolutionary reasoning for the apparent dichotomy existingbetween the hyperaccumulators and AMF–plant life-history strategies. Ulti-mately, it is considered that any efforts toward integrating such biotechnologyinnovations into bioremediation strategies (e.g. ‘mycorrhizal–metal-hyperaccu-mulators’) should first explicitly consider their inherent environmental and (or)evolutionary contexts to avoid misleading and possibly even unproductiveoutcomes prior to incorporating these attributes as potential technologicalsolutions.

Keywords: stress resistance; stress avoidance; investment trade-offs

Introduction

In his latest review of plant metal stress-tolerance mechanisms, Miransari (2011)suggested that metal hyperaccumulators and arbuscular mycorrhizal fungi (AMF),together, should hold promise as ‘a key solution to the issue of heavy metalpollution’ based on their ‘unique abilities’. More specifically, it was proposed thatphysiological adaptations attributed to hyperaccumulators could complement thoseof the AMF (and the function of the mycorrhizosphere) toward synergisticallyenhancing current bioremediation practices. However, representing a major over-sight of the review, little consideration was given as to whether these factors shouldnecessarily be ecologically compatible. For example, the best known and mostintensively studied family of hyperaccumulators (the Brassicaceae) is famously non-mycotrophic (Schreiner and Koide 1993a, 1993b). Meanwhile, the AMF, althoughabundant in a broad range of terrestrial ecosystems, are mostly rare (with someexceptions) among metalliferous environments (Del Val et al. 1999; Meharg andCairney 1999; Leyval et al. 2002). Hence, it could be argued that the environmentalcontext for ‘mycorrhizal–metal-hyperaccumulators’ is paradoxical due to the

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*Email: p.audet@uq.edu.au

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fundamental division of their respective natural ecological niches. In response, thiscritical analysis seeks to identify the environmental boundaries underlying thisparadox using an alternative descriptive framework of plant stress tolerance (Audet2012). Here, the identification of a ‘dilemma of resource allocation’ associated withplant resources consumed (or ‘invested’) in intrinsic (e.g. metabolic) vs. extrinsic (e.g.symbiotic) stress-tolerance mechanisms could provide a suitable evolutionaryreasoning for the apparent dichotomy existing between the hyperaccumulators andAMF–plant life-history strategies (Audet and Charest 2007a, 2007b, 2008), whilebridging certain notions of ecological complexity within the context of bioremedia-tion that may have been previously overlooked.

The paradox of ‘mycorrhizal–metal-hyperaccumulators’

Despite a few lingering semantic issues (Baker and Whiting 2002; Rascio andNavari-Izzo 2011), hyperaccumulation is generally deemed to be a constitutive traitbased on the capability of plants to take up and endure exceedingly high metalconcentrations (e.g.410,000 ppm; Baker and Walker 1990; Boyd 2004) beingattributed to their highly evolved intracellular detoxification and sequestrationmetabolisms (Cobbett 2000; Meagher 2000; Cobbett and Goldsbrough 2002). Thesephysiological qualities are generally representative of ‘true’ stress resistancestemming from an adaptive evolution in relation to extreme metalliferous conditions(e.g. serpentine soils), which, coincidentally, may account for their general ecologicalrarity. Conversely, the role of AMF in plant stress tolerance tends to be more wide-ranging and indicative of a stress-avoidance regime stemming from plant–fungalcoevolution occurring across a broad range of ecological conditioning (Hodge 2001),which might also account for their ubiquity.1 The symbiosis is quintessentiallydefined by the transfer of plant carbohydrates (occasionally up to 20% their totalcarbon budget; Douds et al. 2000) for the development of a viable mycorrhizosphereresponsible for providing an enhanced AM–root nutrient and water uptakecapability and ‘buffered’ proximal growth environment (Figure 1 – Audet 2012).Notwithstanding the role of associated mycorrhizal allies (e.g. plant growthpromoting bacteria, biofilms), as described by Miransari (2011), the most relevantAM-induced process within the present context is the modulation of metalbioavailability via mycelial biosorption and sequestration processes (Gadd 1993;Galli et al. 1994). Considered to be a by-product (or indirect benefit) ofmycorrhizospheric proliferation, these ‘metal-binding’ processes constitute a metal-exclusion mechanism which can delay the onset of toxicity (Leyval et al. 1997, 2002;Christie et al. 2004; Audet and Charest 2006, 2007a, 2009, 2010, 2012 among others).Of course, if combined, the individual stress-tolerance mechanisms of thehyperaccumulators and mycorrhizal symbionts (i.e. ‘true’ resistance and avoid-ance/exclusion) would appear to be highly complementary for the purposes ofbioremediation. However, upon closer examination of their respective ecological andevolutionary contexts (Table 1), it may be postulated that the integration of‘mycorrhizal–metal-hyperaccumulators’ is antagonistic due to:

(1) the evolutionary boundaries which govern the allocation of plant resources;and

(2) the putative ecological origins of ‘true’ resistance vs. stress avoidance inrelation the inherent burden of metal stress.

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Table 1. Hypothesized attributes underlying the ecological and evolutionary origins of stresstolerance among the hyperaccumulators and mycorrhizal symbionts.

Hyperaccumulatorsa Mycorrhizal symbiontsb

Evolutionary andbiogeochemicalconditioning

. Adaptive evolution:Highly selective ecologicalniche

. Coevolution:Persistent and wide-spreadAM–plant interaction

& Phosphorus starvation (e.g.induced deficiency)

& Phosphorus starvation(e.g. ‘true’ deficiency)

General ecologicalvs. metalliferousdistributions

. Relatively rare& Pervasive (dominant)

. Ubiquitous& Sparse (limited)

Tolerance strategy . Intrinsic (e.g., metabolic) . Extrinsic (e.g. symbiotic)& ‘True’ resistance (e.g.

hyperaccumulation)

& Avoidance (e.g. exclusion)

Physiologicalresponses

. Metal partitioning plasticity

. Internal detoxification andsequestration

. Resource allocationplasticity

. External soil matrixstabilization and modulationof soil metal bioavailability

Notes: aBaker and Walker (1990); Baker and Whiting (2002); Meharg and Hartley-Whitaker (2002);Audet and Charest (2007a, 2008). bDel Val et al. (1999); Smith et al. (2003); Audet and Charest (2007b,2008); Audet (2012).

Figure 1. Summary of mycorrhizospheric functions and mechanisms involved in plant stresstolerance (from Audet 2012). 1

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For these reasons, the paradox refers to the notion that plants having divergentlife-history strategies and distinct separations of their natural ecological niches maybe inherently incompatible within the shared ecological context of environmentalbioremediation.

The dilemma of resource allocation and stress tolerance

Based on the notion that plant stress tolerance is fluid (i.e. both flexible andfluctuating) in relation to the intensity of the given environmental stressor (Audetand Charest 2007b, 2008), variations in plant resource allocation (i.e. the trade-offsunderlying this fluidity) can be used to define a continuum of plant life-historystrategies (Figure 2). Such a continuum is useful for describing the inherent trade-offs in relation to stress tolerance when distinguishing between the investment andrelative distribution of resources and energy toward either intrinsic (e.g. metabolic)or extrinsic (e.g. symbiotic) systems (Audet 2012). This ‘investment trade-off’ modelconsiders that plants are known to have developed a number of adaptations (bothintrinsic and extrinsic) in relation to an array of environmental stressors.Accordingly, any combination of these ‘invested’ processes should determine theplant’s generic life-history strategy, ranging from intrinsic specialists to generaliststo extrinsic specialists. As such, a continuum of stress-tolerance behaviors can bedepicted under the assumption that plant resource allocation ‘budgets’ aredetermined by their ecological and evolutionary conditioning – in this case, theburden of metal stress (Foy et al. 1978). From this investigative framework,a ‘dilemma of resource allocation’ (analogous to the model proposed by Herms andMattson 1992 in relation to plant–insect interactions) can be identified from theviewpoint that plants more ‘invested’ in intrinsic processes should necessarily be less‘invested’ in extrinsic ones (and vice versa). Hence, when subjected to environmentalstress, the plant’s stress-tolerance strategy should be bound by the balance-of-tradeassociated with the given resource allocation ‘budget’ (Schwartz and Hoeksema1998). Accordingly, it is suggested that the life-history strategies of hyperaccumu-lators (e.g. having relatively greater intrinsic investments toward phytochelatorand metalothionein metabolisms) and plant mycorrhizal symbionts (e.g. havingrelatively greater extrinsic investments toward maintaining a viable mycorrhizo-sphere) should occupy opposing poles of the continuum of stress tolerance due totheir fundamentally contrasting (or specialist) investment strategies. The ‘dilemma’ isexemplified by the AMF being obligate biotrophs and requiring a suitably resistant

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195Figure 2. Proposed continuum of plant stress tolerance in relation to intrinsic vs. extrinsicplant resource investments (based on Audet and Charest 2008).2

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plant host (i.e. having adequate intrinsic tolerance) to provide a sufficient extrinsicinvestment for the development of the mycorrhizosphere (Bronstein 2001). Thus, theimpending challenge of metal toxicity may prevent any sustainable root colonizationdue to the host plant being metabolically ‘overdrawn’ – as predicted by theconsiderations of mycorrhizal ‘cost-efficiency’ by Koide and Elliott (1989) and laterKoide (1991). Likewise, the hyperaccumulators may be ‘over-invested’ in intrinsicprocesses to accommodate any further investment in external systems (Rascio andNavari-Izzo 2011), such as the mycorrhizal symbiosis2 (Audet and Charest 2008).Although such conceptual reasoning should not assume direct causation, thisapparent evolutionary ‘dilemma’ could account (if, in part) for the natural nicheseparation and associated ecological incompatibility existing between the hyper-accumulators and mycorrhizal symbionts due to the evolutionary boundaries set bytheir respective allocation of resources.

The burden of metal stress

Another aspect somewhat overlooked by Miransari (2011) is that the burden ofmetal stress (as defined by Foy et al. 1978) has a wide range of exposure (i.e. fromdeficiency to toxicity conditions) and that symptoms of deficiency can arisesimultaneously even under impending toxicity conditions (e.g. due to metal-specificantagonisms resulting in rhizospheric nutrient imbalances). That being said, in theirmeta-analyses of plant metal stress-tolerance strategies, Audet and Charest (2007a,200b, 2008) have identified that plants (both hyperaccumulators and mycorrhizalsymbionts) express a certain level of symmetry (or plasticity) regarding theexpression of stress-tolerance mechanisms across the entire metal-exposurespectrum. For example, hyperaccumulators showing similar patterns of metalpartitioning (e.g. greater distribution of metals in roots vs. shoots) when subjected toboth deficiency and toxicity compared with non-stressed (i.e. control) conditions.Or, likewise, mycorrhizal symbionts showing similar patterns of resource allocation(e.g. greater distribution of biomass toward roots vs. shoots) in relation to the samemetal exposure conditions. Accordingly, this apparent symmetry is also observedregarding the expression of nutrient transporters, whereby a suite of macro- andmicronutrients (e.g. ZIP and PT transporter families) (McGrath and Zhao 2003;Miransari 2011; Rascio and Navari-Izzo 2011) are upregulated when subjected toboth deficiency and toxicity conditions; again, likely due to the effects of metal-induced nutrient deficiencies. Given these perspectives, it is suggested here that thelife-history strategies of hyperaccumulators and mycorrhizal symbionts could haveoriginated in response to the entire range of metal stress (or, rather, to the concurrenteffects of toxicity and metal-induced deficiency), as opposed to arising solely inresponse to the extremity of metal toxicity. In this regard, investigations into themechanistic origins of metal stress resistance have identified a single plausibleexplanation accounting for the expression of hyperaccumulation over this entiremetal exposure range referring to the phenomenon of metal-induced phosphorus (P)‘starvation’ (first shown under arsenic toxicity conditions) (Meharg and Macnair1990; Meharg and Hartley-Whitaker 2002; Wang et al. 2002; Zhao et al. 2009).Unlike other available theories such as ‘elemental defense’3 (cited by Miransari2011), the P-starvation hypothesis supposes that hyperaccumulation represents abroader strategy for overcoming metal-induced nutrient antagonisms. Consequently,metal hyperaccumulation is considered to be the phenotypic outcome of plants

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taking up and sequestering excess metals to meet their essential metabolic nutrientrequirements due to the appearance of nutrient imbalances caused by persistentmetal toxicity conditions. The P-starvation hypothesis is compelling because AMFmay also have co-evolved with plants under similar conditions of P deficiency(Hoeksema 2010), whether true deficiency or metal-induced nutrient imbalance. Infact, a classic depiction of AM symbiosis refers to the supplementation of AM–plantnutritional status via the mycorrhizosphere’s increase of soil–surface contact tosubsequently reduce soil–P diffusion distances (Zhu et al. 2001; Smith et al. 2003).Furthermore, symbiotic activity is often indirectly correlated with P-bioavailabilitysuch that symbiotic investments are greater when subjected to more stressful nutrientconditions. Although more in-depth investigations are necessary to verify theseevolutionary facets, the P-starvation scenario described here suggests that thehyperaccumulation and mycorrhizal symbiont life-history strategies representpotentially antithetical strategies derived to overcome the same biogeochemicalchallenges, yet arising under distinct evolutionary circumstances (such as thoseencountered within their respective ecological niches). By extension, these mechan-isms would be inherently antagonistic despite the apparent complementary of someof their ecological applications toward environmental bioremediation.

Reconciling ecological roles for AMF and hyperaccumulators

As discussed above, the environmental context for ‘mycorrhizal–metal-hyperaccu-mulators’ (i.e. the integration of both stress-tolerance behaviors for the purpose ofpost-industrial bioremediation) is considered paradoxical due to the underlyingevolutionary divergence of both life-history strategies leading to a distinct separationbetween their respective natural ecological niches. In fact, the putative origins ofthese stress-tolerance mechanisms were deemed antithetical and potentiallyantagonistic. From this perspective, it would seem improbable that such apparentlyincompatible processes could be easily integrated into current bioremediationstrategies, let alone act synergistically toward their improvement – as originallyproposed by Miransari (2011). At the whole-ecosystem scale, above- and below-ground species interactions often play a quintessential role in determining vegetationpatterns by influencing interspecific competition in relation to the dynamics of plantresource acquisition (Bever 1999, 2003; Klironomos 2002). In this regard, the contextfor environmental bioremediation implies highly challenging growth conditions(Pilon-Smits 2005) due to the scarcity of essential nutrient bioavailability (whetherdue to true deficiency and metal-induced imbalances) and otherwise harsh eco-physiological obstacles (e.g. extreme pH, low water potential, sodicity). As such,these extreme growth conditions often provide a highly selective and inherentlycompetitive ecological arena wherein better-adapted plant life-history strategies (e.g.hyperaccumulation or mycorrhizal symbiosis) could largely determine the speciescomposition of rehabilitated landscapes following a process of competitiveexclusion, for instance, as shown in field studies by Puschel et al. (2007) andRydlova and Vosatka (2001). Over time, the influence of above- and below-groundfeedback relationships (or lack thereof) based on the distribution of mycotrophic vs.non-mycotrophic (or, alternatively, intrinsically vs. extrinsically invested) speciescould alter the intended ecological trajectory and functionality of the rehabilitatedecosystems (Suding et al. 2004; Kardol and Wardle 2010); a perspective sometimesunderlying the behavior of endemic vs. invasive species among natural ecosystems

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(Bever 1999, 2003; Klironomos 2002). As a result, these feedback relationships mayinfluence the course of post-disturbance ecosystem development and cause certainbroad-scale ecological components of the rehabilitated landscapes (e.g. speciescomposition, function) to deviate fundamentally from the desired natural analogues.Evidently, the actual life-history strategies and stress-tolerance behaviors of plantsand AMF are not quite so strictly distinguished by intrinsic vs. extrinsic investmentsand their inherent patterns of ecological distribution are not so uniformly populated.Still, this perspective outlines a primary tenet of landscape rehabilitation: thatenvironmental remediation strategies should aim toward whole-ecosystem rehabi-litation (i.e. regaining appropriate levels of ecological function) (Hobbs and Harris2001; Doley et al. 2012) rather than simply alleviating or circumventing a givenenvironmental stress factor. From an agro-ecological perspective, the mycorrhizo-sphere can afford general stress-tolerance advantages contributing to the long-termstabilization (or buffering) of soil fertility and structure, even under environmentallystressful conditions (Jeffries et al. 2003; Barea et al. 2005). In all likelihood, theseprocesses may have beneficial consequences for environmental remediation practiceswhich coincide, after all, with the ecology of the hyperaccumulators. Yet, thesuccessful integration of such processes into field-level applications hinges on theboundaries set by and the management of both biogeochemical (e.g. the burdenof the given stressor) and eco-physiological factors (e.g. the intrinsic tolerance ofthe plants and AMF to that stressor) being conducive to the development of themycorrhizosphere and the sustainability of the symbiosis; this, rather than relying onserendipity for ‘selecting the right combination of plant and AM species’.

Conclusion

Altogether, the transfer of biotechnology innovations to whole-ecosystem scalesshould require a thoughtful combination of multilateral processes to account forthe inherent complexity of field-level ecosystems and thereby facilitate patterns ofsustainable function (Gunderson 2000). Still, such applications are only feasible solong as appropriate considerations are made regarding their respective ecologicaland evolutionary contexts to avoid misleading and possibly even unproductiveoutcomes.

Notes

1. Having originated *450 million years ago, the AM symbiosis represents a ubiquitousinteraction between species of the Glomeromycota phylum and an estimated 90% of allherbaceous plants which is widely recognized for benefiting both symbionts whensubjected to various environmental stressors (Schußler et al. 2001). The symbiosistypically develops because photosynthetic capacity in shoots exceeds the uptake capacityand (or) soil nutrient supply to support plant growth. In exchange for this surplus CHO 3,AMF can supplement the host plant’s nutritional status by scavenging soil resources andreducing nutrient diffusion distances. Consequently, a key nuance of the notions of‘balance-of-trade’ and ‘cost-efficiency’ (described below) is that the AM symbiosisseemingly loses its physiological efficacy when cultivated without edaphic stresses(i.e. optimal growth conditions), thereby having significant consequences toward generalterrestrial processes (e.g. above/below-ground species interactions), community assem-blages and plant productivity (Koide and Elliott 1989; Koide 1991; Johnson et al. 1997;Schwartz and Hoeksema 1998; Klironomos et al. 2000; Rillig 2004) – a topic certainlydeserving of more in depth discussion.

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2. The present analysis focuses on the generally non-mycotrophic or infrequentlymycotrophic status of hyperaccumulators and their subsequent ecological nicheseparation with AMF. In addition to the ecological and evolutionary factors discussedhere, the non-mycotrophic status of the Brassicaceae is also associated with theirrhizospheric exudation of antifungal metabolites (Schreiner and Koide 1993a, 1993b).

3. ‘Elemental defense’ is suggested as a competing hypothesis underlying hyperaccumulationas a tactic analogous to un-palatability to thwart pests and pathogens (Boyd 2004);however, the hypothesis does not account for the burden of metal stress across its entirerange of exposure, as defined here. To account for this discrepancy, it is considered thathyperaccumulation would first have originated more parsimoniously as a result ofP-starvation (as a result of the longer-termed biogeological interface between plants andsoil, and its inherently wide range of metal exposure conditions), whereas ‘elementaldefense’ would have been manifested as an outcome of the hyperaccumulation phenotypegiven insect predation among metalliferous environments.

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