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      N 2-fixing tropical legume evolution: a contributor to enhanced weathering through the Cenozoic?

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          Abstract

          Fossil and phylogenetic evidence indicates legume-rich modern tropical forests replaced Late Cretaceous palm-dominated tropical forests across four continents during the early Cenozoic (58–42 Ma). Tropical legume trees can transform ecosystems via their ability to fix dinitrogen (N 2) and higher leaf N compared with non-legumes (35–65%), but it is unclear how their evolutionary rise contributed to silicate weathering, the long-term sink for atmospheric carbon dioxide (CO 2). Here we hypothesize that the increasing abundance of N 2-fixing legumes in tropical forests amplified silicate weathering rates by increased input of fixed nitrogen (N) to terrestrial ecosystems via interrelated mechanisms including increasing microbial respiration and soil acidification, and stimulating forest net primary productivity. We suggest the high CO 2 early Cenozoic atmosphere further amplified legume weathering. Evolution of legumes with high weathering rates was probably driven by their high demand for phosphorus and micronutrients required for N 2-fixation and nodule formation.

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          Photosynthesis and nitrogen relationships in leaves of C3 plants

          The photosynthetic capacity of leaves is related to the nitrogen content primarily bacause the proteins of the Calvin cycle and thylakoids represent the majority of leaf nitrogen. To a first approximation, thylakoid nitrogen is proportional to the chlorophyll content (50 mol thylakoid N mol-1 Chl). Within species there are strong linear relationships between nitrogen and both RuBP carboxylase and chlorophyll. With increasing nitrogen per unit leaf area, the proportion of total leaf nitrogen in the thylakoids remains the same while the proportion in soluble protein increases. In many species, growth under lower irradiance greatly increases the partitioning of nitrogen into chlorophyll and the thylakoids, while the electron transport capacity per unit of chlorophyll declines. If growth irradiance influences the relationship between photosynthetic capacity and nitrogen content, predicting nitrogen distribution between leaves in a canopy becomes more complicated. When both photosynthetic capacity and leaf nitrogen content are expressed on the basis of leaf area, considerable variation in the photosynthetic capacity for a given leaf nitrogen content is found between species. The variation reflects different strategies of nitrogen partitioning, the electron transport capacity per unit of chlorophyll and the specific activity of RuBP carboxylase. Survival in certain environments clearly does not require maximising photosynthetic capacity for a given leaf nitrogen content. Species that flourish in the shade partition relatively more nitrogen into the thylakoids, although this is associated with lower photosynthetic capacity per unit of nitrogen.
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            Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants.

            Plants associate with a wide range of microorganisms, with both detrimental and beneficial outcomes. Central to plant survival is the ability to recognize invading microorganisms and either limit their intrusion, in the case of pathogens, or promote the association, in the case of symbionts. To aid in this recognition process, elaborate communication and counter-communication systems have been established that determine the degree of ingress of the microorganism into the host plant. In this Review, I describe the common signalling processes used by plants during mutualistic interactions with microorganisms as diverse as arbuscular mycorrhizal fungi and rhizobial bacteria.
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              CO2 enhancement of forest productivity constrained by limited nitrogen availability.

              Stimulation of terrestrial plant production by rising CO(2) concentration is projected to reduce the airborne fraction of anthropogenic CO(2) emissions. Coupled climate-carbon cycle models are sensitive to this negative feedback on atmospheric CO(2), but model projections are uncertain because of the expectation that feedbacks through the nitrogen (N) cycle will reduce this so-called CO(2) fertilization effect. We assessed whether N limitation caused a reduced stimulation of net primary productivity (NPP) by elevated atmospheric CO(2) concentration over 11 y in a free-air CO(2) enrichment (FACE) experiment in a deciduous Liquidambar styraciflua (sweetgum) forest stand in Tennessee. During the first 6 y of the experiment, NPP was significantly enhanced in forest plots exposed to 550 ppm CO(2) compared with NPP in plots in current ambient CO(2), and this was a consistent and sustained response. However, the enhancement of NPP under elevated CO(2) declined from 24% in 2001-2003 to 9% in 2008. Global analyses that assume a sustained CO(2) fertilization effect are no longer supported by this FACE experiment. N budget analysis supports the premise that N availability was limiting to tree growth and declining over time--an expected consequence of stand development, which was exacerbated by elevated CO(2). Leaf- and stand-level observations provide mechanistic evidence that declining N availability constrained the tree response to elevated CO(2); these observations are consistent with stand-level model projections. This FACE experiment provides strong rationale and process understanding for incorporating N limitation and N feedback effects in ecosystem and global models used in climate change assessments.
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                Author and article information

                Journal
                Proc Biol Sci
                Proc. Biol. Sci
                RSPB
                royprsb
                Proceedings of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8452
                1471-2954
                16 August 2017
                16 August 2017
                16 August 2017
                : 284
                : 1860
                : 20170370
                Affiliations
                [1 ]Department of Animal and Plant Sciences, University of Sheffield , Sheffield S10 2TN, UK
                [2 ]School of Geography and Priestley International Centre for Climate, University of Leeds , Leeds LS2 9JT, UK
                [3 ]Smithsonian Tropical Research Institute , Balboa, Ancon, Panama
                [4 ]Department of Ecology and Evolutionary Biology, Princeton University , Princeton, NJ 08544, USA
                Author notes

                Electronic supplementary material is available online at https://dx.doi.org/10.6084/m9.figshare.c.3832519.

                Author information
                http://orcid.org/0000-0001-5711-5480
                http://orcid.org/0000-0002-7703-9873
                http://orcid.org/0000-0003-2364-8187
                http://orcid.org/0000-0003-1869-4314
                Article
                rspb20170370
                10.1098/rspb.2017.0370
                5563791
                28814651
                36339134-99f2-42ae-9a24-f93ac84fd34d
                © 2017 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : 22 February 2017
                : 12 July 2017
                Funding
                Funded by: H2020 European Research Council, http://dx.doi.org/10.13039/100010663;
                Award ID: CDREG, 322998
                Categories
                1001
                60
                204
                144
                Palaeobiology
                Review Article
                Custom metadata
                August 16, 2017

                Life sciences
                tropical forests,n2-fixation,legume trees,rock weathering,co2 sequestration,cenozoic
                Life sciences
                tropical forests, n2-fixation, legume trees, rock weathering, co2 sequestration, cenozoic

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