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• W2945583551 abstract "Most terrestrial plants depend strongly on associations with arbuscular mycorrhizal (AM) fungi (Subphylum: Glomeromycotina) to establish and survive (van der Heijden et al., 1998; Bever, 2002; Klironomos et al., 2011; Veresoglou et al., 2017), and have evolved a nutritional mutualism. In this mutualism, the plant provides carbon to the fungus, usually subject to the availability of light (Hayman, 1974; Heinemeyer et al., 2003; Shi et al., 2014; Konvalinkova & Jansa, 2016), and the fungus provides the plant with mineral nutrients acquired from soil. Because of light constraints, it is expected that latitude exerts a strong influence on reciprocal exchange of resources between mycorrhizal plants and fungi, and this could have consequences on the responsiveness of plants to mycorrhizal fungi. Latitude induces changes in the amount of solar energy and the timing when this is made available to primary producers during the year and in the day. At the same time, there is a strong negative relationship between latitude and temperature that may also impact the functioning of the mycorrhizal symbiosis, and in some cases (e.g. in north temperate systems), a general relationship between latitude and several edaphic factors (Read & Perez-Moreno, 2003). There is compelling evidence that the alpha-diversity of Glomeromycotinian fungi, which form AM symbioses, decreases with latitude (Davison et al., 2015). This finding can be partially explained by the transition from ecosystems dominated by AM host plants in the tropics, to ectomycorrhizal and ericoid mycorrhizal dominated ecosystems at higher latitudes (Smith & Read, 2008). We know less about the extent to which latitude impacts the functioning of AM symbioses, which could occur either through latitudinal differences in solar radiation or resulting changes in temperature (Clarke & Gaston, 2006; Schluter, 2016). Here, we propose the ‘sun-worshipper’ hypothesis that discriminates three different types of underlying responses of latitudinal gradient-induced changes in plant host mycorrhizal responsiveness (Fig. 1). Changes in abiotic conditions may allow plants to derive more benefits from the symbiosis at lower latitudes through phenotypic plasticity (Mechanism 1 – Fig. 1). A likely example of phenotypic plasticity might involve changes in the expression of genes that allow crosstalk with AM fungi when light availability is low as has been shown for drought (Li et al., 2016). Abiotic conditions more favourable for the symbiosis close to the tropics could further exclude, via competition, species less dependent on AM fungi, resulting in distinct plant communities from a perspective of AM fungal-associating behaviour; such a process can be described as environmental filtering (Mechanism 2 – Fig. 1). Finally, we know that AM plants at high latitudes encounter a less diverse pool of potential symbiotic partners (e.g. because of the observed latitudinal gradient in Glomeromycotinian diversity; Davison et al., 2015) and at the same time communities at high latitudes are in general dominated by plants that associate with ectomycorrhizal and ericoid mycorrhizal fungi. Plants distant from the tropics could thus form less profitable AM symbioses (but also support fewer AM partners) because of a more limited pool of suitable AM fungal partners, and this mechanism is analogous to the indirect eco-evolutionary causes (Pärtel, 2002) (Mechanism 3 – Fig. 1). Here, we use the term eco-evolutionary processes to describe combined effects of latitude on phenotypic plasticity, environmental filtering and eco-evolutionary adaptation of the host plant trait mycorrhizal dependency (Thuiller et al., 2013). Even though these different mechanisms are not mutually exclusive, it is important to disentangle how each of them influences the way in which host plants respond to mycorrhizal symbioses along gradients of latitude and solar radiation. The benefits that plants receive from the symbiosis in relation to the carbon costs vary considerably depending on abiotic growth conditions (Johnson et al., 1997; Hoeksema et al., 2010; Grman & Robinson, 2013), compatibility of the plant host with the local AM fungal community (Klironomos, 2003) and the degree to which a plant can take advantage of non-nutritional functions of mycorrhiza such as protection from pathogens (Veresoglou & Rillig, 2013). Resource stoichiometry of phosphorus (P), nitrogen (N) and light, in particular, represents a proven tool explaining variance in growth responses of mycorrhizal hosts at various spatial scales (Johnson, 2010). Latitude-related predictions could complement such existing tools in understanding why mycorrhizal growth responses differ at large scales. It may additionally illuminate systematic differences in mycorrhizal responsiveness such as those explained by the life history of the hosts (Boerner, 1992; Roumet et al., 2005). This would be the case if the latitudinal effects are mediated through differences in solar radiation. Annual terrestrial plants may never experience light-duration stress during winter, whereas the opposite is the case for perennials that represent the majority of terrestrial plants (e.g. over 70% of species in the LEDA database are perennials – Kleyer et al., 2008). There is good evidence that perennial AM fungi can survive over winter in the roots of their hosts (Buwalda et al., 1985; Dodd & Jeffries, 1986; but see Hetrick et al., 1984; Mohammad et al., 1998), which could affect the carbon economy of their plant hosts. During winter, plant requirements for nutrients are limited and photo-assimilates are in short supply; therefore, plants that can confine the activity of their mycorrhizal partners may benefit through improved survival rates. As a result, we expect that there is evolutionary pressure for perennials to further confine mycorrhizal responsiveness when growing outside the tropics, compared to annuals. We undertook three synthesis activities to establish whether the expectations outlined earlier are plausible for mycorrhizal systems (Supporting Information Notes S1). We first compiled a database on crop plant responses to mycorrhiza to identify phenotypic responses to latitude (Notes S2; Table S1; Fig. S1). To assess environmental filtering due to AM fungi with regards to latitude, we synthesized data from a common garden experiment on comparative mycorrhizal responsiveness of North American annual and perennial herbaceous plants (Wilson & Hartnett, 1998) with plant distribution data for the specific plants from USDA (2016; Notes S3). We also tested for differences in mycorrhizal responsiveness across genotypes of Zea mays (maize) that are routinely used either in temperate or tropical systems, despite that genetic variability could effectively be attributed to breeding (Notes S4). These syntheses activities were not sufficiently robust to address the mechanistic constituents of the sun worshipper hypothesis but were carried out to support the over-arching concept and encourage larger syntheses or experiments exploring the hypothesis in the future. Variance in the database on crop plant responses could be best explained, in our models consisting of a single predictor, by photosynthetic radiation (Fig. 2a). The optimal model had an intercept of −0.5 (F = 9.7, P < 0.001) and a slope per MJ m−2 d−1 radiation of 0.23 (F = 6.1, P = 0.019). Fitted intercepts for the different plant species shared a standard deviation of 0.048 (Fig. 2a). Analysis of maize lines demonstrated that eco-evolutionary processes also drive latitude-dependencies on mycorrhizal responsiveness. The Mann–Whitney test between temperate- (i.e. middle two quartiles) and tropical-climate adapted lines of maize revealed higher responsiveness for temperate lines (U = 24.5, P = 0.034). When we repeated this analysis for tropical lines through maintaining the two middle quartiles, the differences became even more apparent (U = 4, P < 0.001, Fig. 2b). Mycorrhizal responsiveness of species in Wilson & Hartnett (1998) could be predicted by latitude of their distribution, which suggests that mycorrhizal responsiveness might induce an environmental filtering. We raised latitude to the fourth power to address fitting issues and obtained an intercept of 0.65; latitude slope of −2.44 × 10−8 (Flat = 23.32; P < 0.001; = 0.19; Fig. 2c). We subsequently fitted an additional parameter that differentiated between annual and perennial plants. Inclusion of the categorical variable perennial was significant (F = 23.36, P < 0.001) and there was a significant interaction between this parameter and latitude (F = 9.47, P = 0.003) suggesting that slopes also differed. When we analysed annual and perennial plants separately, we found a significant relationship only for perennials (Kendall tau was −0.32 – P = 0.004, whereas for annuals the Kendall tau was 0.03 – P = 0.87). The sun-worshipper hypothesis predicts that latitude impacts mycorrhizal responsiveness in plants via three complementary mechanisms, namely phenotypic responses, eco-evolutionary processes and environmental filtering (Fig. 1). Even though the analyses we report have limited resolution, they were supportive of the sun worshipper hypothesis. We found evidence that phenotypic plasticity (Fig. 2a), eco-evolutionary processes (Fig. 2b) and environmental filtering (Fig. 2c) might be operational for all three different types of latitude related differences in mycorrhizal responsiveness (Thuiller et al., 2013). Despite the findings from our analyses, it is important to highlight additional factors that may also influence mycorrhizal responsiveness, and which have the potential to confound our findings. For example, our observations may correlate with systematic differences in soil fertility; high weathering rates generally lead to poorer fertility, as occurs in many parts of the tropics (Read & Perez-Moreno, 2003). Therefore, disentangling the specific role of light vs other edaphic and environmental factors in driving mycorrhizal responsiveness likely requires additional experimentation. Testing competing hypotheses could be done with carefully designed common garden experiments or synthesizing evidence from altitudinal experiments. Nevertheless, our analysis and associated hypothesis prompts further mechanistic analyses to test how resource stoichiometry and other critical functions undertaken by mycorrhizal fungi are influenced by latitudinal gradients. SDV is partly supported by the DFG project Metacorrhiza (VE 736/2-1). DJ is partly supported by the N8 AgriFood programme and NERC. TH is partly supported by the BBSRC grant BB/L026007/1. The letter has benefited considerably from comments and suggestions from Ian Dickie and three anonymous reviewers. SDV conceived the project and carried out the analyses; SDV, TH, APM, MCR, AR and DJ discussed and further developed the idea; SDV and DJ wrote the manuscript; all authors (SDV, BC, MMF, TH, APM, MCR, AR, DJ) commented on the manuscript and approved the final version of it. Please note: Wiley Blackwell are not responsible for the content or functionality of any Supporting Information supplied by the authors. Any queries (other than missing material) should be directed to the New Phytologist Central Office. Fig. S1 Locations of the 40 studies included in the meta-analysis. Notes S1 Mycorrhizal dependency as proxy of investment. Notes S2 Meta-analysis on phenotypic plasticity. Notes S3 Environmental filtering on LGMR. Notes S4 Eco-evolutionary processes on LGMR. Table S1 Primary data on the 42 studies which we considered in our meta-analysis. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article." @default.
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• W2945583551 title "Latitudinal constraints in responsiveness of plants to arbuscular mycorrhiza: the ‘sun‐worshipper’ hypothesis" @default.
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