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Letters How harmonious are arbuscular mycorrhizal symbioses? Inconsistent concepts reflect different mindsets as well as results Overview Arbuscular mycorrhizal (AM) symbioses involve transfer of soil nutrients to plants and plant-derived organic compounds to AM fungi. Many experiments have shown that individual symbioses are ‘mutualistic’ (Table 1). However, outcomes in relation to the nonmycorrhizal (NM) state are not always positive for plants, although they are for all AM fungi, which are obligate symbionts. Different AM fungi produce different growth-related responses in individual plants and there are large differences in responsiveness among different plant taxa in relation to colonization by the same AM fungal taxon (Klironomos, 2003). Neutral outcomes for the plant may be termed ‘commensal’, and negative ones ‘parasitic’ (Table 1). Outcomes are influenced by many abiotic and biotic factors (Johnson et al., 1997). Here we address the extent to which AM symbiosis can be validly interpreted as a fundamentally ‘harmonious’ relationship, as is suggested by use of terms such as ‘cooperation’ and ‘rewards’ (Table 1). Although harmony may not be a familiar term, it has been used in relation to plant–microbe symbioses (Broughton et al., 2000; Oldroyd et al., 2005; Martin et al., 2007). The issue is also addressed briefly in a report of the 33rd New Phytologist Symposium, Zurich, May 2014 (Bender et al., 2014). We focus on four concepts in the literature that relate to uptake of phosphate (P), a growth-limiting nutrient in many soils. The concepts are relevant to other nutrients that are taken up via AM fungi, such as inorganic nitrogen (N). We comment specifically on whether increasing use of subjective terminology actually facilitates interpretation of results and will help experimental design in future.
Concept 1: the mutualism–parasitism continuum This concept considers AM ‘function’ (Table 1) and its diversity in relation to net costs and benefits to plants with respect to the NM state (Johnson et al., 1997). Outcomes are usually measured in pot experiments in terms of plant biomass (mycorrhizal growth response, MGR), or growth-related parameters such as P content per plant, and we previously suggested that considering a continuum of responsiveness would be preferable (Smith & Smith, Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust
2011a). Potential ‘fitness’, for example as measured by plant fecundity and survival (see Table 1), might be a better indicator of position on the continuum as long as experiments include appropriate measurements, which most do not (Johnson et al., 1997; Jones & Smith, 2004; Lekberg & Koide, 2014). Even in pot experiments it is not easy to quantify net costs and benefits to the partners in physiological terms. For example, MGRs do not always relate to amounts of P taken up by the AM fungal pathway. This has been shown by tracking the AM pathway of P uptake and transfer to the plant with radioactive P. The data in Table 2 demonstrate (1) interplay between uptake between the AM and direct (epidermal) root uptake pathways and (2) differences between individual AM fungi. Such results show that zero or negative MGR usually does not result from AM fungal parasitism where AM P transfer would be zero. We suggested that negative MGR may result directly from decreased direct epidermal P uptake that lowers photosynthesis rather than excess carbon (C)-drain to the fungus (Li et al., 2008; Smith et al., 2009). Physiological diversity is also displayed by experiments employing root-organ culture with AM fungi (e.g. Kiers et al., 2011 and references cited therein), though these systems necessarily lack controls exerted from shoots and hence the existence of a natural feedback loop for resource exchange (Fortin et al., 2002; Smith & Smith, 2011b). Physiological diversity is important in helping interpret ecological outcomes where plants are colonized by many AM fungi, especially when AM plants are connected by common mycelial networks (e.g. Walder et al., 2012; Fellbaum et al., 2014). However, there is a major problem in extrapolating the significance of experiments with individual AM plants and fungi to higher scales such as plant communities and ecosystems (Francis & Read, 1995; Lekberg & Koide, 2014). In focusing on growth-related outcomes, the mutualism– parasitism continuum has no subjective elements. It does not even imply cause–effect issues of partner recognition and subsequent resource transfer, though these can be introduced in interpreting the mechanistic basis (Smith & Smith, 2013). Accordingly, Table 1 gives the components zero subjectivity. This situation contrasts to some extent with frequent descriptions of AM resource transfer as resource trade. ‘Trade’ implies an element of cooperation; both terms have low subjectivity (Table 1). By definition, trade does not cover fungal parasitism, where transfer is one-way (C from the plant); mycoheterotrophy is also a complication.
Concept 2: reciprocal rewards Bidirectional resource transfers are increasingly described as ‘rewards’. The term implies higher harmony than does trade, because traders (at least human ones) do not acquire rewards: they seek the most favourable terms of trade. We consider that the rewards concept has high subjectivity (Table 1). ‘Reciprocal’ New Phytologist (2015) 205: 1381–1384 1381 www.newphytologist.com
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Table 1 Glossary of terms, in order of appearance Term
Definition and comments
Subjectivity
Symbiosis Mutualism
Living in close association; does not imply mutualism. Both partners benefit in terms of a tangible outcome, in relation to a nonsymbiotic state One partner benefits (here an arbuscular mycorrhizal (AM) fungus); no tangible benefit to the other (autotrophic plant) in relation to a nonsymbiotic state One partner benefits (AM fungus); the other (plant) suffers in comparison with a nonsymbiotic state One partner (AM fungus) drains resources from the other (plant) while providing none in return, as in ‘parasitic fungus’ Peaceful outcome (does not imply specific processes) Joint operation to achieve an outcome Gift received for a service (here, resource transfer) Outcome (here, of AM symbiosis, but the term is used more generally, as in ‘functional groups’ of plants: trees, shrubs, legumes, etc.); can be misinterpreted – see next entry Mode of action, mechanism, as in ‘functional diversity’: diversity in resource transfer; can be misinterpreted – see previous entry Success in relation to future generations – see also text. Traits are not always well defined, which can result in subjectivity Exchange of resources; implies an agreement as to ‘balance’ of trade Partner that receives resources while providing few or none in comparison with others (here an AM fungus) Gaining an advantage by selfish means Buying, selling, trade, barter; also used for the location. Paraphrasing Werner et al. (2014), a market framework can theoretically be applied to AM symbioses if resources are exchanged between individual AM fungi and plants, which can choose or switch partners; and there are potentially opportunities for ‘outbidding’ (whatever this means). Most markets are also characterized by temporal variation in supply and demand, which can initiate ‘price’ fluctuations.
Zero Zero
Commensalism
Parasitism (ecological use) Parasitism (physiological use) Harmony Cooperation Reward Function (ecological use)
Function (physiological use)
Fitness Trade Cheater Exploitation Market
Zero
Zero Zero Low Low High Zero
Zero
Zero or Low Zero Zero High Zero or Low, depending on issues such as ‘choice’, ‘bidding’, etc. See also text.
All are conventional dictionary definitions as applied to mycorrhizal symbioses in the literature, and are given as nouns. Heterotrophic plants are not considered. ‘Subjectivity’ refers to the extent that the term reflects a perception of the meaning of findings, reflecting mindset.
rewards are claimed to lead to plant-based pressures disadvantaging AM fungi that obtain C but restrict P supply to the host (‘cheaters’: Table 1). So-called ‘preferential rewards’ to ‘high-quality’ partners are said to stabilize cooperation in AM symbiosis, with evolutionary consequences (Kiers et al., 2011). There appears to be an element of circularity, as the rewards (resource transfers) are the mechanistic basis of the cooperation. The AM fungi that transfer the most P or N inevitably require the most C, because uptake of P and transfer to the plant requires energy, while hyphal transfer of N as arginine requires organic C skeletons. In other words, rewards inevitably carry a cost, the significance of which for an AM plant depends on its ability to lower C costs of growth compared with the NM state (Johnson et al., 1997). There is a parallel even in NM plants which extend parts of their root system into nutrient-rich patches, but the C-nutrient trade would not normally be described as ‘reciprocal rewards’ – ‘supply and demand’ would be conventional terms in this context. Cause–effect issues of which reward (P or C) comes first once colonization is established are unresolved. Kiers et al. (2011) New Phytologist (2015) 205: 1381–1384 www.newphytologist.com
commented that AM fungi may ‘choose’ to transfer P to the host that offers the highest C benefit. By contrast, Fitter (2006) suggested that plants do not provide C to fungi that transfer no P. The result should then be inhibition of ongoing colonization if this cheating can be recognized by the plant. Although the degree of colonization can be very variable in pot experiments with individual AM fungi, there is no physiological evidence to our knowledge that low colonization is necessarily linked to a plant response to prevent or minimize fungal cheating. However, physiological measurements suggest that cheating in the extreme sense of little or no P supply in return for C is much less common than previously inferred from lack of positive MGRs (Smith & Smith, 2011b). This may be a consolation for researchers who think of the symbiosis in terms of rewards. It is sometimes suggested that AM fungi that are not the most beneficial in terms of nutrient transfers may confer non-nutritional benefits that result in increased fitness in the presence of stress such as disease. This possibility is feasible over evolutionary time, but it looks contrary to a simple ‘rewards’ concept if a host preferentially Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust
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Table 2 Examples of plants with different mycorrhizal growth responses (MGRs) along the mutualism–parasitism continuum, summarizing total phosphate (P) uptake of shoots, and amounts obtained from the arbuscular mycorrhizal (AM) fungal P uptake pathway, and from direct uptake by roots (all as mg P per shoot) (plants were grown in low-P soil)
Flax (‘mutualism’) Nonmycorrhizal Rhizophagus irregularis Glomus caledonium Tomato (‘commensalism’) Nonmycorrhizal R. irregularis G. caledonium Barley2 (‘parasitism’) Nonmycorrhizal R. irregularis
Total P uptake
AM uptake
Direct uptake
0.1 2.2 1.5
— 2.0 0.6
0.11 0.21 0.9
3.1 2.8 3.0
— 2.1 0.9
3.1 0.7 2.1
4.8 2.4
— 1.0
4.8 1.4
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AM pathway. The trade is highly context-dependent in relation to the wide range of factors that influence AM physiology and outcomes of individual symbioses along the (nonsubjective) mutualism–parasitism continuum. However, the underlying mindset is less subjective than with ‘mutual rewards’ (Table 1).
Mindsets and terminology
Values for AM uptake are extrapolated from 32P or 33P taken up from small compartments accessible only to hyphae, and calculated from data for flax and tomato in Smith et al. (2004) and for barley in Grace et al. (2009), which give details. 1 Not significantly different. 2 There was no treatment with G. caledonium.
rewards a fungus that is not of ‘high quality’ in the absence of the stress in the anticipation that its value increases in the presence of the stress.
Concept 3: mutual exploitation Resource transfer in AM symbioses can be also regarded as mutual exploitation of the partners’ resources (Egger & Hibbett, 2004), also with high subjectivity (Table 1). Mutual parasitism would be a similar but more extreme term. The exploitation terminology reflects a different mindset than does ‘rewards’ about the physiological aspects of the symbiosis and the outcomes across the mutualism–parasitism continuum of responsiveness, again without necessarily specifying causes and effects. The terminology does not imply AM cooperation or harmony: perhaps that is why it receives little use.
Concept 4: AM symbiosis as a biological market Ecologists have used economic theory to consider mutualisms in general as ‘biological markets’ since the 1990s. The concept is being extended to microbes (Werner et al., 2014), including mycorrhizas (Kiers et al., 2011; Fellbaum et al., 2014). The details are summarized in Table 1 and go a long way beyond traditional cost–benefit analyses that have been extensively used in relation to AM symbioses (e.g. Koide & Elliott, 1989; Johnson et al., 1997 and references cited therein; Jones et al., 1998). A problem in applying this concept to AM symbiosis is that there is no monetary price: a bartering process determines ‘rate of exchange’ of resources. ‘Unfair’ trade (cheating) is a complication (No€e & Hammerstein, 1995), as is interplay between direct epidermal uptake via the roots (‘nonmarketing’) and uptake via the Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust
It is worth pursuing mindsets in more detail beyond issues of harmony. Although the biological market concept by definition focuses on the AM state, much of the terminology used by researchers (including ourselves) uses the NM state as the basis. This applies to MGR: conventionally 100(AM NM)/NM, in terms of weight or other growth-related parameters such as plant P uptake. An alternative term is ‘dependency’ (or ‘dependence’), which appears more AM-focused, but is again conventionally defined with reference to the NM state: 100(AM NM)/AM (Habte & Manjunath, 1991). Where dependency is zero (NM = AM) it has been interpreted as implying that there is no AM P uptake but, as emphasized earlier, this is not necessarily the case. In other words, ‘dependency’ must again be defined, and used as an outcome, not a resource-based mechanism. In nature the NM state of a potentially AM plant is usually artificial, unless the soil lacks AM fungal propagules. Perhaps we should really talk of nonmycorrhizal growth response (NMGR). The same NM mindset is reflected in our own use of ‘suppression’ or ‘inhibition’ of direct P uptake when plants receive P via the AM pathway but have zero or negative MGR (Grace et al., 2008; Smith et al., 2009; Smith & Smith, 2011b). More realistically in the (abnormal) NM state these plants can respond by upregulating direct P uptake beyond that in the AM state. This can be regarded as a response to stress (Smith et al., 2011) and may be highly relevant to the evolutionary success of plants with zero or even negative MGR in low-P soil.
Conclusions The answer to our question in the title is that most AM symbioses can validly be regarded as harmonious in terms of recognition by symbionts and evolutionary success of the symbiosis. Even AM fungal cheating can be regarded as harmonious to the extent that the plant tolerates it (using ‘tolerates’ as yet another subjective term). However, the extent to which there is harmony in competition among AM fungi co-existing in a root, or among plants sharing a mycelial network, is not clear. Accordingly, we are not advocating use of the term. Subjective terminology is inevitable in describing AM symbioses, just as it is with other symbioses. The danger is that it can lead to over-simple generalizations and may then unhelpfully influence subsequent experimental approaches. Our particular concern is uncritical use in interpreting AM physiology in ecological or evolutionary contexts. The market concept is attractive because it deals with partitioning of resources when roots contain several AM fungal taxa and when plants are connected by common mycelial networks. However, it is not clear how much it helps understand AM New Phytologist (2015) 205: 1381–1384 www.newphytologist.com
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functional diversity, especially when this extends to mycoheterotrophy (Selosse & Rousset, 2011). The concept may extend impact of research with AM fungi into a wider research arena but a detailed assessment of its value beyond general principles is certainly needed. Irrespective of terminologies, we believe that physiological bases of resource transfer in AM symbioses need to be much better understood in terms of causes and effects, and the range of mineral nutrients that can be transferred. Inevitably, experiments will be reductionist compared with the real world of plant growth in the field, but as long as limitations are recognized in relation to relevance across scales this should not be a problem in moving forward.
Acknowledgements This letter developed from a poster at the 33rd New Phytologist Symposium (Zurich, May 2014), and we thank the New Phytologist Trust for grants to attend. The title was influenced by the official Symposium cartoon that showed a mycorrhizal fungus and root shaking hands. We showed boxing gloves in the poster, while Bender et al. (2014) illustrated both versions. We are grateful to Nancy Johnson and two anonymous reviewers whose comments were very helpful for revision. F. Andrew Smith* and Sally E. Smith Soil Science, School of Agriculture, Food & Wine, the University of Adelaide, Adelaide, SA 5005, Australia (*Author for correspondence: tel +61 (8) 83136517; email [email protected])
References Bender SF, Valdares RBdaS, Taudiere A. 2014. Mycorrhizas: dynamic and complex networks of power and influence. New Phytologist 204: 15–18. Broughton WJ, Jabbouri S, Perret X. 2000. Keys to symbiotic harmony. Journal of Bacteriology 182: 5641–5652. Egger KN, Hibbett DS. 2004. The evolutionary implications of exploitation in mycorrhizas. Canadian Journal of Botany 82: 1110–1121. Fellbaum CR, Mensah JA, Cloos AJ, Strahan GE, Pfeffer PE, Kiers ET, B€ ucking H. 2014. Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants. New Phytologist 203: 646– 656. Fitter AH. 2006. What is the link between carbon and phosphorus fluxes in arbuscular mycorrhizas? A null hypothesis for symbiotic function. New Phytologist 172: 3–6. Fortin JA, Becard G, Declerck S, Dalpe Y, St Arnaud M, Coughlan AP, Piche Y. 2002. Arbuscular mycorrhiza on root-organ cultures. Canadian Journal of Botany 80: 1–20. Francis R, Read DJ. 1995. Mutualism and antagonism in the mycorrhizal symbiosis, with special reference to impacts on plant community structure. Canadian Journal of Botany 73: S1301–S1309. Grace EJ, Cotsaftis O, Tester M, Smith FA, Smith SE. 2009. Arbuscular mycorrhizal inhibition of growth in barley cannot be attributed to extent of colonization, fungal phosphorus uptake or effects on expression of plant phosphate transporter genes. New Phytologist 181: 938–949. Grace EJ, Smith FA, Smith SE. 2008. Deciphering the arbuscular mycorrhizal pathway of P uptake in non-responsive hosts. In: Azcon-Aguilar C, Barea JM,
New Phytologist (2015) 205: 1381–1384 www.newphytologist.com
Gianinazzi S, Gianinazzi-Pearson V, eds. Mycorrhizas: functional processes and ecological impact. Berlin, Germany: Springer, 89–106. Habte M, Manjunath A. 1991. Categories of vesicular–arbuscular mycorrhizal dependency of host species. Mycorrhiza 1: 3–12. Johnson NC, Graham JH, Smith FA. 1997. Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytologist 135: 575–586. Jones MD, Durall DM, Tinker PB. 1998. A comparison of arbuscular and ectomycorrhizal Eucalyptus coccifera: growth response, phosphorus uptake efficiency and external hyphal production. New Phytologist 140: 125–134. Jones MD, Smith SE. 2004. Exploring functional definitions of mycorrhizas: are mycorrhizas always mutualisms? Canadian Journal of Botany 82: 1089– 1109. Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM et al. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333: 880–882. Klironomos JN. 2003. Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84: 2292–2301. Koide RT, Elliott G. 1989. Cost, benefit and efficiency of vesicular-arbuscular mycorrhizal symbiosis. Functional Ecology 3: 4–7. Lekberg Y, Koide RT. 2014. Integrating physiological, community, and evolutionary perspectives on the arbuscular mycorrhizal symbiosis. Botany 92: 241–251. Li H, Smith FA, Dickson S, Holloway RE, Smith SE. 2008. Plant growth depressions in arbuscular mycorrhizal symbiosis: not just caused by carbon drain? New Phytologist 178: 852–862. Martin F, Kohler A, Duplessis S. 2007. Living in harmony in the wood underground: ectomycorrhizal genomics. Current Opinion in Plant Biology 10: 204–210. No€e R, Hammerstein P. 1995. Biological markets. Trends in Ecology and Evolution 10: 336–339. Oldroyd GED, Harrison MJ, Udvardi M. 2005. Peace talks and trade deals. Keys to long-term harmony in legume-microbe symbioses. Plant Physiology 137: 1205– 1210. Selosse M-A, Rousset F. 2011. The plant–fungal marketplace. Science 333: 828. Smith FA, Grace EJ, Smith SE. 2009. More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytologist 182: 347–358. Smith FA, Smith SE. 2011a. What is the significance of the arbuscular mycorrhizal colonisation of many economically important crop plants? Plant and Soil 348: 63– 79. Smith FA, Smith SE. 2013a. How useful is the mutualism–parasitism continuum of arbuscular mycorrhizal functioning? Plant and Soil 363: 7–18. Smith SE, Jakobsen I, Grønlund M, Smith FA. 2011. Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiology 156: 1050–1057. Smith SE, Smith FA. 2011b. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annual Review of Plant Biology 62: 227–250. Smith SE, Smith FA, Jakobsen I. 2004. Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytologist 162: 511–524. Walder F, Niemann H, Natarajan M, Lehmann MF, Boller T, Wiemken A. 2012. Mycorrhizal networks: common goods of plants shared under unequal terms of trade. Plant Physiology 159: 789–797. Werner GDA, Strassmann JE, Ivens ABF, Engelmoer DJP, Verbruggene E, Queller DC, No€e R, Johnson NC, Hammerstein P, Kiers ET. 2014. Evolution of microbial markets. Proceedings of the National Academy of Sciences, USA 111: 1237–1244. Key words: arbuscular mycorrhizas (AMs), biological market place, functional diversity, mutual exploitation, mutual rewards, mutualism–parasitism continuum.
Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust
Letters How harmonious are arbuscular mycorrhizal symbioses? Inconsistent concepts reflect different mindsets as well as results Overview Arbuscular mycorrhizal (AM) symbioses involve transfer of soil nutrients to plants and plant-derived organic compounds to AM fungi. Many experiments have shown that individual symbioses are ‘mutualistic’ (Table 1). However, outcomes in relation to the nonmycorrhizal (NM) state are not always positive for plants, although they are for all AM fungi, which are obligate symbionts. Different AM fungi produce different growth-related responses in individual plants and there are large differences in responsiveness among different plant taxa in relation to colonization by the same AM fungal taxon (Klironomos, 2003). Neutral outcomes for the plant may be termed ‘commensal’, and negative ones ‘parasitic’ (Table 1). Outcomes are influenced by many abiotic and biotic factors (Johnson et al., 1997). Here we address the extent to which AM symbiosis can be validly interpreted as a fundamentally ‘harmonious’ relationship, as is suggested by use of terms such as ‘cooperation’ and ‘rewards’ (Table 1). Although harmony may not be a familiar term, it has been used in relation to plant–microbe symbioses (Broughton et al., 2000; Oldroyd et al., 2005; Martin et al., 2007). The issue is also addressed briefly in a report of the 33rd New Phytologist Symposium, Zurich, May 2014 (Bender et al., 2014). We focus on four concepts in the literature that relate to uptake of phosphate (P), a growth-limiting nutrient in many soils. The concepts are relevant to other nutrients that are taken up via AM fungi, such as inorganic nitrogen (N). We comment specifically on whether increasing use of subjective terminology actually facilitates interpretation of results and will help experimental design in future.
Concept 1: the mutualism–parasitism continuum This concept considers AM ‘function’ (Table 1) and its diversity in relation to net costs and benefits to plants with respect to the NM state (Johnson et al., 1997). Outcomes are usually measured in pot experiments in terms of plant biomass (mycorrhizal growth response, MGR), or growth-related parameters such as P content per plant, and we previously suggested that considering a continuum of responsiveness would be preferable (Smith & Smith, Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust
2011a). Potential ‘fitness’, for example as measured by plant fecundity and survival (see Table 1), might be a better indicator of position on the continuum as long as experiments include appropriate measurements, which most do not (Johnson et al., 1997; Jones & Smith, 2004; Lekberg & Koide, 2014). Even in pot experiments it is not easy to quantify net costs and benefits to the partners in physiological terms. For example, MGRs do not always relate to amounts of P taken up by the AM fungal pathway. This has been shown by tracking the AM pathway of P uptake and transfer to the plant with radioactive P. The data in Table 2 demonstrate (1) interplay between uptake between the AM and direct (epidermal) root uptake pathways and (2) differences between individual AM fungi. Such results show that zero or negative MGR usually does not result from AM fungal parasitism where AM P transfer would be zero. We suggested that negative MGR may result directly from decreased direct epidermal P uptake that lowers photosynthesis rather than excess carbon (C)-drain to the fungus (Li et al., 2008; Smith et al., 2009). Physiological diversity is also displayed by experiments employing root-organ culture with AM fungi (e.g. Kiers et al., 2011 and references cited therein), though these systems necessarily lack controls exerted from shoots and hence the existence of a natural feedback loop for resource exchange (Fortin et al., 2002; Smith & Smith, 2011b). Physiological diversity is important in helping interpret ecological outcomes where plants are colonized by many AM fungi, especially when AM plants are connected by common mycelial networks (e.g. Walder et al., 2012; Fellbaum et al., 2014). However, there is a major problem in extrapolating the significance of experiments with individual AM plants and fungi to higher scales such as plant communities and ecosystems (Francis & Read, 1995; Lekberg & Koide, 2014). In focusing on growth-related outcomes, the mutualism– parasitism continuum has no subjective elements. It does not even imply cause–effect issues of partner recognition and subsequent resource transfer, though these can be introduced in interpreting the mechanistic basis (Smith & Smith, 2013). Accordingly, Table 1 gives the components zero subjectivity. This situation contrasts to some extent with frequent descriptions of AM resource transfer as resource trade. ‘Trade’ implies an element of cooperation; both terms have low subjectivity (Table 1). By definition, trade does not cover fungal parasitism, where transfer is one-way (C from the plant); mycoheterotrophy is also a complication.
Concept 2: reciprocal rewards Bidirectional resource transfers are increasingly described as ‘rewards’. The term implies higher harmony than does trade, because traders (at least human ones) do not acquire rewards: they seek the most favourable terms of trade. We consider that the rewards concept has high subjectivity (Table 1). ‘Reciprocal’ New Phytologist (2015) 205: 1381–1384 1381 www.newphytologist.com
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Table 1 Glossary of terms, in order of appearance Term
Definition and comments
Subjectivity
Symbiosis Mutualism
Living in close association; does not imply mutualism. Both partners benefit in terms of a tangible outcome, in relation to a nonsymbiotic state One partner benefits (here an arbuscular mycorrhizal (AM) fungus); no tangible benefit to the other (autotrophic plant) in relation to a nonsymbiotic state One partner benefits (AM fungus); the other (plant) suffers in comparison with a nonsymbiotic state One partner (AM fungus) drains resources from the other (plant) while providing none in return, as in ‘parasitic fungus’ Peaceful outcome (does not imply specific processes) Joint operation to achieve an outcome Gift received for a service (here, resource transfer) Outcome (here, of AM symbiosis, but the term is used more generally, as in ‘functional groups’ of plants: trees, shrubs, legumes, etc.); can be misinterpreted – see next entry Mode of action, mechanism, as in ‘functional diversity’: diversity in resource transfer; can be misinterpreted – see previous entry Success in relation to future generations – see also text. Traits are not always well defined, which can result in subjectivity Exchange of resources; implies an agreement as to ‘balance’ of trade Partner that receives resources while providing few or none in comparison with others (here an AM fungus) Gaining an advantage by selfish means Buying, selling, trade, barter; also used for the location. Paraphrasing Werner et al. (2014), a market framework can theoretically be applied to AM symbioses if resources are exchanged between individual AM fungi and plants, which can choose or switch partners; and there are potentially opportunities for ‘outbidding’ (whatever this means). Most markets are also characterized by temporal variation in supply and demand, which can initiate ‘price’ fluctuations.
Zero Zero
Commensalism
Parasitism (ecological use) Parasitism (physiological use) Harmony Cooperation Reward Function (ecological use)
Function (physiological use)
Fitness Trade Cheater Exploitation Market
Zero
Zero Zero Low Low High Zero
Zero
Zero or Low Zero Zero High Zero or Low, depending on issues such as ‘choice’, ‘bidding’, etc. See also text.
All are conventional dictionary definitions as applied to mycorrhizal symbioses in the literature, and are given as nouns. Heterotrophic plants are not considered. ‘Subjectivity’ refers to the extent that the term reflects a perception of the meaning of findings, reflecting mindset.
rewards are claimed to lead to plant-based pressures disadvantaging AM fungi that obtain C but restrict P supply to the host (‘cheaters’: Table 1). So-called ‘preferential rewards’ to ‘high-quality’ partners are said to stabilize cooperation in AM symbiosis, with evolutionary consequences (Kiers et al., 2011). There appears to be an element of circularity, as the rewards (resource transfers) are the mechanistic basis of the cooperation. The AM fungi that transfer the most P or N inevitably require the most C, because uptake of P and transfer to the plant requires energy, while hyphal transfer of N as arginine requires organic C skeletons. In other words, rewards inevitably carry a cost, the significance of which for an AM plant depends on its ability to lower C costs of growth compared with the NM state (Johnson et al., 1997). There is a parallel even in NM plants which extend parts of their root system into nutrient-rich patches, but the C-nutrient trade would not normally be described as ‘reciprocal rewards’ – ‘supply and demand’ would be conventional terms in this context. Cause–effect issues of which reward (P or C) comes first once colonization is established are unresolved. Kiers et al. (2011) New Phytologist (2015) 205: 1381–1384 www.newphytologist.com
commented that AM fungi may ‘choose’ to transfer P to the host that offers the highest C benefit. By contrast, Fitter (2006) suggested that plants do not provide C to fungi that transfer no P. The result should then be inhibition of ongoing colonization if this cheating can be recognized by the plant. Although the degree of colonization can be very variable in pot experiments with individual AM fungi, there is no physiological evidence to our knowledge that low colonization is necessarily linked to a plant response to prevent or minimize fungal cheating. However, physiological measurements suggest that cheating in the extreme sense of little or no P supply in return for C is much less common than previously inferred from lack of positive MGRs (Smith & Smith, 2011b). This may be a consolation for researchers who think of the symbiosis in terms of rewards. It is sometimes suggested that AM fungi that are not the most beneficial in terms of nutrient transfers may confer non-nutritional benefits that result in increased fitness in the presence of stress such as disease. This possibility is feasible over evolutionary time, but it looks contrary to a simple ‘rewards’ concept if a host preferentially Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust
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Table 2 Examples of plants with different mycorrhizal growth responses (MGRs) along the mutualism–parasitism continuum, summarizing total phosphate (P) uptake of shoots, and amounts obtained from the arbuscular mycorrhizal (AM) fungal P uptake pathway, and from direct uptake by roots (all as mg P per shoot) (plants were grown in low-P soil)
Flax (‘mutualism’) Nonmycorrhizal Rhizophagus irregularis Glomus caledonium Tomato (‘commensalism’) Nonmycorrhizal R. irregularis G. caledonium Barley2 (‘parasitism’) Nonmycorrhizal R. irregularis
Total P uptake
AM uptake
Direct uptake
0.1 2.2 1.5
— 2.0 0.6
0.11 0.21 0.9
3.1 2.8 3.0
— 2.1 0.9
3.1 0.7 2.1
4.8 2.4
— 1.0
4.8 1.4
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AM pathway. The trade is highly context-dependent in relation to the wide range of factors that influence AM physiology and outcomes of individual symbioses along the (nonsubjective) mutualism–parasitism continuum. However, the underlying mindset is less subjective than with ‘mutual rewards’ (Table 1).
Mindsets and terminology
Values for AM uptake are extrapolated from 32P or 33P taken up from small compartments accessible only to hyphae, and calculated from data for flax and tomato in Smith et al. (2004) and for barley in Grace et al. (2009), which give details. 1 Not significantly different. 2 There was no treatment with G. caledonium.
rewards a fungus that is not of ‘high quality’ in the absence of the stress in the anticipation that its value increases in the presence of the stress.
Concept 3: mutual exploitation Resource transfer in AM symbioses can be also regarded as mutual exploitation of the partners’ resources (Egger & Hibbett, 2004), also with high subjectivity (Table 1). Mutual parasitism would be a similar but more extreme term. The exploitation terminology reflects a different mindset than does ‘rewards’ about the physiological aspects of the symbiosis and the outcomes across the mutualism–parasitism continuum of responsiveness, again without necessarily specifying causes and effects. The terminology does not imply AM cooperation or harmony: perhaps that is why it receives little use.
Concept 4: AM symbiosis as a biological market Ecologists have used economic theory to consider mutualisms in general as ‘biological markets’ since the 1990s. The concept is being extended to microbes (Werner et al., 2014), including mycorrhizas (Kiers et al., 2011; Fellbaum et al., 2014). The details are summarized in Table 1 and go a long way beyond traditional cost–benefit analyses that have been extensively used in relation to AM symbioses (e.g. Koide & Elliott, 1989; Johnson et al., 1997 and references cited therein; Jones et al., 1998). A problem in applying this concept to AM symbiosis is that there is no monetary price: a bartering process determines ‘rate of exchange’ of resources. ‘Unfair’ trade (cheating) is a complication (No€e & Hammerstein, 1995), as is interplay between direct epidermal uptake via the roots (‘nonmarketing’) and uptake via the Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust
It is worth pursuing mindsets in more detail beyond issues of harmony. Although the biological market concept by definition focuses on the AM state, much of the terminology used by researchers (including ourselves) uses the NM state as the basis. This applies to MGR: conventionally 100(AM NM)/NM, in terms of weight or other growth-related parameters such as plant P uptake. An alternative term is ‘dependency’ (or ‘dependence’), which appears more AM-focused, but is again conventionally defined with reference to the NM state: 100(AM NM)/AM (Habte & Manjunath, 1991). Where dependency is zero (NM = AM) it has been interpreted as implying that there is no AM P uptake but, as emphasized earlier, this is not necessarily the case. In other words, ‘dependency’ must again be defined, and used as an outcome, not a resource-based mechanism. In nature the NM state of a potentially AM plant is usually artificial, unless the soil lacks AM fungal propagules. Perhaps we should really talk of nonmycorrhizal growth response (NMGR). The same NM mindset is reflected in our own use of ‘suppression’ or ‘inhibition’ of direct P uptake when plants receive P via the AM pathway but have zero or negative MGR (Grace et al., 2008; Smith et al., 2009; Smith & Smith, 2011b). More realistically in the (abnormal) NM state these plants can respond by upregulating direct P uptake beyond that in the AM state. This can be regarded as a response to stress (Smith et al., 2011) and may be highly relevant to the evolutionary success of plants with zero or even negative MGR in low-P soil.
Conclusions The answer to our question in the title is that most AM symbioses can validly be regarded as harmonious in terms of recognition by symbionts and evolutionary success of the symbiosis. Even AM fungal cheating can be regarded as harmonious to the extent that the plant tolerates it (using ‘tolerates’ as yet another subjective term). However, the extent to which there is harmony in competition among AM fungi co-existing in a root, or among plants sharing a mycelial network, is not clear. Accordingly, we are not advocating use of the term. Subjective terminology is inevitable in describing AM symbioses, just as it is with other symbioses. The danger is that it can lead to over-simple generalizations and may then unhelpfully influence subsequent experimental approaches. Our particular concern is uncritical use in interpreting AM physiology in ecological or evolutionary contexts. The market concept is attractive because it deals with partitioning of resources when roots contain several AM fungal taxa and when plants are connected by common mycelial networks. However, it is not clear how much it helps understand AM New Phytologist (2015) 205: 1381–1384 www.newphytologist.com
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functional diversity, especially when this extends to mycoheterotrophy (Selosse & Rousset, 2011). The concept may extend impact of research with AM fungi into a wider research arena but a detailed assessment of its value beyond general principles is certainly needed. Irrespective of terminologies, we believe that physiological bases of resource transfer in AM symbioses need to be much better understood in terms of causes and effects, and the range of mineral nutrients that can be transferred. Inevitably, experiments will be reductionist compared with the real world of plant growth in the field, but as long as limitations are recognized in relation to relevance across scales this should not be a problem in moving forward.
Acknowledgements This letter developed from a poster at the 33rd New Phytologist Symposium (Zurich, May 2014), and we thank the New Phytologist Trust for grants to attend. The title was influenced by the official Symposium cartoon that showed a mycorrhizal fungus and root shaking hands. We showed boxing gloves in the poster, while Bender et al. (2014) illustrated both versions. We are grateful to Nancy Johnson and two anonymous reviewers whose comments were very helpful for revision. F. Andrew Smith* and Sally E. Smith Soil Science, School of Agriculture, Food & Wine, the University of Adelaide, Adelaide, SA 5005, Australia (*Author for correspondence: tel +61 (8) 83136517; email [email protected])
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