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      Shifts in symbiotic associations in plants capable of forming multiple root symbioses across a long‐term soil chronosequence

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          Abstract

          Changes in soil nutrient availability during long‐term ecosystem development influence the relative abundances of plant species with different nutrient‐acquisition strategies. These changes in strategies are observed at the community level, but whether they also occur within individual species remains unknown. Plant species forming multiple root symbioses with arbuscular mycorrhizal ( AM) fungi, ectomycorrhizal ( ECM) fungi, and nitrogen‐(N) fixing microorganisms provide valuable model systems to examine edaphic controls on symbioses related to nutrient acquisition, while simultaneously controlling for plant host identity. We grew two co‐occurring species, Acacia rostellifera (N 2‐fixing and dual AM and ECM symbioses) and Melaleuca systena ( AM and ECM dual symbioses), in three soils of contrasting ages ( c. 0.1, 1, and 120 ka) collected along a long‐term dune chronosequence in southwestern Australia. The soils differ in the type and strength of nutrient limitation, with primary productivity being limited by N (0.1 ka), co‐limited by N and phosphorus (P) (1 ka), and by P (120 ka). We hypothesized that (i) within‐species root colonization shifts from AM to ECM with increasing soil age, and that (ii) nodulation declines with increasing soil age, reflecting the shift from N to P limitation along the chronosequence. In both species, we observed a shift from AM to ECM root colonization with increasing soil age. In addition, nodulation in A. rostellifera declined with increasing soil age, consistent with a shift from N to P limitation. Shifts from AM to ECM root colonization reflect strengthening P limitation and an increasing proportion of total soil P in organic forms in older soils. This might occur because ECM fungi can access organic P via extracellular phosphatases, while AM fungi do not use organic P. Our results show that plants can shift their resource allocation to different root symbionts depending on nutrient availability during ecosystem development.

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          Most cited references15

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          Phylogenetic distribution and evolution of mycorrhizas in land plants.

          A survey of 659 papers mostly published since 1987 was conducted to compile a checklist of mycorrhizal occurrence among 3,617 species (263 families) of land plants. A plant phylogeny was then used to map the mycorrhizal information to examine evolutionary patterns. Several findings from this survey enhance our understanding of the roles of mycorrhizas in the origin and subsequent diversification of land plants. First, 80 and 92% of surveyed land plant species and families are mycorrhizal. Second, arbuscular mycorrhiza (AM) is the predominant and ancestral type of mycorrhiza in land plants. Its occurrence in a vast majority of land plants and early-diverging lineages of liverworts suggests that the origin of AM probably coincided with the origin of land plants. Third, ectomycorrhiza (ECM) and its derived types independently evolved from AM many times through parallel evolution. Coevolution between plant and fungal partners in ECM and its derived types has probably contributed to diversification of both plant hosts and fungal symbionts. Fourth, mycoheterotrophy and loss of the mycorrhizal condition also evolved many times independently in land plants through parallel evolution.
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            Plant nutrient-acquisition strategies change with soil age.

            Nitrogen (N) tends to limit plant productivity on young soils; phosphorus (P) becomes increasingly limiting in ancient soils because it gradually disappears through leaching and erosion. Plant traits that are regarded as adaptations to N- and P-limited conditions include mycorrhizas and cluster roots. Mycorrhizas 'scavenge' P from solution or 'mine' insoluble organic N. Cluster roots function in severely P-impoverished landscapes, 'mining' P fixed as insoluble inorganic phosphates. The 'scavenging' and 'mining' strategies of mycorrhizal species without and non-mycorrhizal species with cluster roots, respectively, allow functioning on soils that differ markedly in P availability. Based on recent advances in our understanding of these contrasting strategies of nutrient acquisition, we provide an explanation for the distribution of mycorrhizal species on less P-impoverished soils, and for why, globally, cluster-bearing species dominate on severely P-impoverished, ancient soils, where P sensitivity is relatively common.
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              Ecosystem properties and forest decline in contrasting long-term chronosequences.

              During succession, ecosystem development occurs; but in the long-term absence of catastrophic disturbance, a decline phase eventually follows. We studied six long-term chronosequences, in Australia, Sweden, Alaska, Hawaii, and New Zealand; for each, the decline phase was associated with a reduction in tree basal area and an increase in the substrate nitrogen-to-phosphorus ratio, indicating increasing phosphorus limitation over time. These changes were often associated with reductions in litter decomposition rates, phosphorus release from litter, and biomass and activity of decomposer microbes. Our findings suggest that the maximal biomass phase reached during succession cannot be maintained in the long-term absence of major disturbance, and that similar patterns of decline occur in forested ecosystems spanning the tropical, temperate, and boreal zones.
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                Author and article information

                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                08 March 2016
                April 2016
                : 6
                : 8 ( doiID: 10.1002/ece3.2016.6.issue-8 )
                : 2368-2377
                Affiliations
                [ 1 ] School of Plant BiologyThe University of Western Australia 35 Stirling Highway Crawley (Perth) WA 6009Australia
                [ 2 ]Smithsonian Tropical Research Institute Apartado 0843‐03092, Balboa AnconRepublic of Panama
                [ 3 ] Grupo de Estudios AmbientalesIMASL‐CONICET & Universidad Nacional de San Luis Av. Ejercito de los Andes 950 (5700) San LuisArgentina
                [ 4 ] Département de Sciences biologiquesInstitut de Recherche en Biologie Végétale Université de Montréal 4101 Sherbrooke Est Montréal QC H1X 2B2Canada
                Author notes
                [*] [* ] Correspondence

                Felipe E. Albornoz, School of Plant Biology, The University of Western Australia, 35 Stirling Highway, Crawley (Perth), WA 6009, Australia.

                Tel: +61 8 6488 5912;

                Fax: +61 8 6488 1108;

                E‐mail: felipe.albornozramirez@ 123456research.uwa.edu.au

                Article
                ECE32000
                10.1002/ece3.2000
                4782245
                27066229
                248a46f9-0998-4c6f-b2ad-1e89243180ba
                © 2016 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 06 January 2016
                : 19 January 2016
                : 20 January 2016
                Page count
                Pages: 10
                Funding
                Funded by: Australian Research Council (ARC)
                Funded by: DECRA
                Award ID: DE120100352
                Funded by: Discovery Project
                Award ID: DP0985685
                Funded by: UWA Research and Development Award
                Funded by: “Becas Chile” scholarship from the Chilean Government
                Funded by: ANZ Holsworth Wildlife Research Endowment
                Funded by: University of Western Australia
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                ece32000
                April 2016
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.8.6 mode:remove_FC converted:17.04.2016

                Evolutionary Biology
                arbuscular mycorrhizal fungi,chronosequence,ectomycorrhizal fungi,nitrogen fixation,pedogenesis,phosphorus,rhizobia

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