Global plant–symbiont organization and emergence of biogeochemical cycles resolved by evolution-based trait modelling

Lu, Mingzhen; Hedin, Lars O.

doi:10.1038/s41559-018-0759-0

Cited by 103 publications

(125 citation statements)

References 72 publications

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“…By contrast, AMF lack or have only limited enzymatic capacities to degrade organic compounds (Hodge, 2001;Read & Perez-Moreno, 2003), and depend primarily on saprotrophic microbiota to mineralize nutrients or liberate simple organic and inorganic compounds before uptake (Smith & Smith, 2011). However, the carbon costs of ectomycorrhizal symbiosis to plants may be higher than those of arbuscular mycorrhizal symbiosis (Leake et al, 2004;Hobbie, 2006;Brzostek et al, 2014;Lu & Hedin, 2019), in part because EMF produce greater amounts of biomass, as thick mantles covering the root tip and prolific extramatrical hyphae and rhizomorphs that allow more extensive soil resource exploitation and long-distance transport to the host plant (Smith & Read, 2008;Phillips et al, 2013). Because of the varying costs and benefits to trees of hosting EMF vs AMF, mycorrhizal mediated plant-soil feedbacks shape forest structure and dynamics (Corrales et al, 2016;Bennett et al, 2017;Corrales et al, 2018;Steidinger et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Lithological constraints on resource economies shape the mycorrhizal composition of a Bornean rain forest

et al. 2020

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Summary Arbuscular mycorrhizal fungi (AMF) and ectomycorrhizal fungi (EMF) produce contrasting plant–soil feedbacks, but how these feedbacks are constrained by lithology is poorly understood. We investigated the hypothesis that lithological drivers of soil fertility filter plant resource economic strategies in ways that influence the relative fitness of trees with AMF or EMF symbioses in a Bornean rain forest containing species with both mycorrhizal strategies. Using forest inventory data on 1245 tree species, we found that although AMF‐hosting trees had greater relative dominance on all soil types, with declining lithological soil fertility EMF‐hosting trees became more dominant. Data on 13 leaf traits and wood density for a total of 150 species showed that variation was almost always associated with soil type, whereas for six leaf traits (structural properties; carbon, nitrogen, phosphorus ratios, nitrogen isotopes), variation was also associated with mycorrhizal strategy. EMF‐hosting species had slower leaf economics than AMF‐hosts, demonstrating the central role of mycorrhizal symbiosis in plant resource economies. At the global scale, climate has been shown to shape forest mycorrhizal composition, but here we show that in communities it depends on soil lithology, suggesting scale‐dependent abiotic factors influence feedbacks underlying the relative fitness of different mycorrhizal strategies.

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Section: Introductionmentioning

confidence: 99%

Lithological constraints on resource economies shape the mycorrhizal composition of a Bornean rain forest

et al. 2020

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“…This characterization can be thought of in terms of functional traits, where the more evolutionarily ancient AM types co-evolved with the development of vascular plant roots (Feijen, Vos, Nuytinck, & Merckx, 2018;Hoysted et al, 2018;Selosse & Tacon, 1998) and confer an advantage for plant development when accessing any nutrients, but especially limited phosphorus. The other two types of important mycorrhizae (EM and ericoid mycorrhizae) arose later through convergent evolution (Tedersoo & Smith, 2013), and recent evidence from evolution-based trait modelling (Lu & Hedin, 2019) highlights saprotrophic ancestors that were able to metabolize less accessible organic nitrogen sources through the production of hydrolytic and oxidative enzymes.…”

Section: Introductionmentioning

confidence: 99%

Species and intra-specific competition affect growth in greenhouse more than mycorrhizal colonization onQuercus rubraandAcer rubrumseedlings

Maier

2020

Preprint

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AimsDistributions of mycorrhizal guilds correlate with differences in soil nutrient availability and tend to predominate ecosystems where plant growth and development are limited by either soil phosphorus (AM, arbuscular mycorrhiza) or nitrogen (EM, ectomycorrhiza) (Read, 1991). In an effort to characterize functional trait differences, we designed a common garden greenhouse experiment to measure growth and colonization responses between two tree seedling species (Acer rubrum and Quercus rubra) that associate with the two major mycorrhizal guilds.MethodsIn a fully factorial, 12-week greenhouse common garden experiment, seedlings were treated to three levels of nitrogen and phosphorus availability, and grown under inter- and intra-species competition. Change in heights and stem diameters were tracked and mycorrhizal colonization was quantified by percent of total and morphology.ResultsRelative growth rates were higher for Acer rubrum seedlings across treatments and intra-species competition had a strong negative effect on height and stem diameter, especially for Quercus rubra. Both species were highly colonized (>50%) by typically endomycorrhizal forms (arbuscules and vesicles) but varied in the distribution of morphological forms present in cells.ConclusionsThis study highlights the plasticity of tree seedling symbiosis during early developmental stages and challenges the strict static categorization of plant species associations with particular mycorrhizal guilds.

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“…In contrast, the relative number of legume species in Southeast Asia was lower than in the Neotropics and tropical Africa (Gentry, ), although he had many fewer plots in Southeast Asia than in the Neotropics. A recent study (Lu & Hedin, ) classified the taxa in Gentry's plots by N‐fixing status, but did not report patterns across continents. A study from the Center for Tropical Forest Science‐Forest Global Earth Observatory (CTFS‐ForestGEO) network—a network of large, mainly mature forest plots—showed that on average, legumes had a higher relative abundance in three plots in tropical Africa than in four plots in tropical America, which in turn had a higher relative abundance of legumes than in nine plots in tropical Asia (Losos & Leigh, ).…”

Section: Introductionmentioning

confidence: 99%

Patterns of nitrogen‐fixing tree abundance in forests across Asia and America

et al. 2019

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1. Symbiotic nitrogen (N)-fixing trees can provide large quantities of new N to ecosystems, but only if they are sufficiently abundant. The overall abundance and latitudinal abundance distributions of N-fixing trees are well characterised in the Americas, but less well outside the Americas.2. Here, we characterised the abundance of N-fixing trees in a network of forest plots spanning five continents, ~5,000 tree species and ~4 million trees. The majority of the plots (86%) were in America or Asia. In addition, we examined whether the observed pattern of abundance of N-fixing trees was correlated with mean annual temperature and precipitation.3. Outside the tropics, N-fixing trees were consistently rare in the forest plots we examined. Within the tropics, N-fixing trees were abundant in American but not Asian forest plots (~7% versus ~1% of basal area and stems). This disparity was not explained by mean annual temperature or precipitation. Our finding of low N-fixing tree abundance in the Asian tropics casts some doubt on recent high estimates of N fixation rates in this region, which do not account for disparities in N-fixing tree abundance between the Asian and American tropics. Synthesis.Inputs of nitrogen to forests depend on symbiotic nitrogen fixation, which is constrained by the abundance of N-fixing trees. By analysing a large dataset of ~4 million trees, we found that N-fixing trees were consistently rare in the Asian tropics as well as across higher latitudes in Asia, America and Europe. The rarity of N-fixing trees in the Asian tropics compared with the American tropics might stem from lower intrinsic N limitation in Asian tropical forests, although direct support for any mechanism is lacking. The paucity of N-fixing trees throughout Asian forests suggests that N inputs to the Asian tropics might be lower than previously thought. K E Y W O R D Sforest, legume, nitrogen fixation, nutrient limitation, Smithsonian ForestGEO, symbiosis Correspondence Tak Fung

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Global plant–symbiont organization and emergence of biogeochemical cycles resolved by evolution-based trait modelling

Cited by 103 publications

References 72 publications

Lithological constraints on resource economies shape the mycorrhizal composition of a Bornean rain forest

Lithological constraints on resource economies shape the mycorrhizal composition of a Bornean rain forest

Species and intra-specific competition affect growth in greenhouse more than mycorrhizal colonization onQuercus rubraandAcer rubrumseedlings

Patterns of nitrogen‐fixing tree abundance in forests across Asia and America

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