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      Photosynthesis in the fleeting shadows: an overlooked opportunity for increasing crop productivity?

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          Summary

          Photosynthesis measurements are traditionally taken under steady‐state conditions; however, leaves in crop fields experience frequent fluctuations in light and take time to respond. This slow response reduces the efficiency of carbon assimilation. Transitions from low to high light require photosynthetic induction, including the activation of Rubisco and the opening of stomata, whereas transitions from high to low light require the relaxation of dissipative energy processes, collectively known as non‐photochemical quenching (NPQ). Previous attempts to assess the impact of these delays on net carbon assimilation have used simplified models of crop canopies, limiting the accuracy of predictions. Here, we use ray tracing to predict the spatial and temporal dynamics of lighting for a rendered mature Glycine max (soybean) canopy to review the relative importance of these delays on net cumulative assimilation over the course of both a sunny and a cloudy summer day. Combined limitations result in a 13% reduction in crop carbon assimilation on both sunny and cloudy days, with induction being more important on cloudy than on sunny days. Genetic variation in NPQ relaxation rates and photosynthetic induction in parental lines of a soybean nested association mapping (NAM) population was assessed. Short‐term NPQ relaxation (<30 min) showed little variation across the NAM lines, but substantial variation was found in the speeds of photosynthetic induction, attributable to Rubisco activation. Over the course of a sunny and an intermittently cloudy day these would translate to substantial differences in total crop carbon assimilation. These findings suggest an unexplored potential for breeding improved photosynthetic potential in our major crops.

          Significance Statement

          Improved photosynthetic efficiency is a means to achieve the sustainable crop yield increases that are a projected need for ensuring global food security over the next 30 years. Improving photosynthetic efficiency during fluctuating light in the field is shown from theory and from measured variability within crop germplasm a potential route to breeding higher efficiency.

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          Most cited references39

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          Rising atmospheric carbon dioxide: plants FACE the future.

          Atmospheric CO(2) concentration ([CO(2)]) is now higher than it was at any time in the past 26 million years and is expected to nearly double during this century. Terrestrial plants with the C(3) photosynthetic pathway respond in the short term to increased [CO(2)] via increased net photosynthesis and decreased transpiration. In the longer term this increase is often offset by downregulation of photosynthetic capacity. But much of what is currently known about plant responses to elevated [CO(2)] comes from enclosure studies, where the responses of plants may be modified by size constraints and the limited life-cycle stages that are examined. Free-Air CO(2) Enrichment (FACE) was developed as a means to grow plants in the field at controlled elevation of CO(2) under fully open-air field conditions. The findings of FACE experiments are quantitatively summarized via meta-analytic statistics and compared to findings from chamber studies. Although trends agree with parallel summaries of enclosure studies, important quantitative differences emerge that have important implications both for predicting the future terrestrial biosphere and understanding how crops may need to be adapted to the changed and changing atmosphere.
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            Food for thought: lower-than-expected crop yield stimulation with rising CO2 concentrations.

            Model projections suggest that although increased temperature and decreased soil moisture will act to reduce global crop yields by 2050, the direct fertilization effect of rising carbon dioxide concentration ([CO2]) will offset these losses. The CO2 fertilization factors used in models to project future yields were derived from enclosure studies conducted approximately 20 years ago. Free-air concentration enrichment (FACE) technology has now facilitated large-scale trials of the major grain crops at elevated [CO2] under fully open-air field conditions. In those trials, elevated [CO2] enhanced yield by approximately 50% less than in enclosure studies. This casts serious doubt on projections that rising [CO2] will fully offset losses due to climate change.
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              Meeting the global food demand of the future by engineering crop photosynthesis and yield potential.

              Increase in demand for our primary foodstuffs is outstripping increase in yields, an expanding gap that indicates large potential food shortages by mid-century. This comes at a time when yield improvements are slowing or stagnating as the approaches of the Green Revolution reach their biological limits. Photosynthesis, which has been improved little in crops and falls far short of its biological limit, emerges as the key remaining route to increase the genetic yield potential of our major crops. Thus, there is a timely need to accelerate our understanding of the photosynthetic process in crops to allow informed and guided improvements via in-silico-assisted genetic engineering. Potential and emerging approaches to improving crop photosynthetic efficiency are discussed, and the new tools needed to realize these changes are presented.
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                Author and article information

                Contributors
                slong@illinois.edu
                Journal
                Plant J
                Plant J
                10.1111/(ISSN)1365-313X
                TPJ
                The Plant Journal
                John Wiley and Sons Inc. (Hoboken )
                0960-7412
                1365-313X
                24 February 2020
                February 2020
                : 101
                : 4 , Advances in Photosynthesis ( doiID: 10.1111/tpj.v101.4 )
                : 874-884
                Affiliations
                [ 1 ] Carl R Woese Institute for Genomic Biology University of Illinois at Urbana‐Champaign Urbana IL 61801 USA
                [ 2 ] Department of Plant Biology University of Illinois at Urbana‐Champaign Urbana IL 61801 USA
                [ 3 ] Department of Crop Sciences University of Illinois at Urbana‐Champaign Urbana IL 61801 USA
                [ 4 ] Lancaster Environment Centre Lancaster University Lancaster LA1 4YQ UK
                Author notes
                [*] [* ] For correspondence (e‐mail slong@ 123456illinois.edu ).

                Author information
                https://orcid.org/0000-0002-6951-2835
                https://orcid.org/0000-0003-2353-7794
                https://orcid.org/0000-0002-7928-2586
                https://orcid.org/0000-0002-8501-7164
                Article
                TPJ14663
                10.1111/tpj.14663
                7064922
                31908116
                c4ee5bba-ce6b-4995-9192-3743143f1ebf
                © 2020 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/3.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 07 October 2019
                : 16 December 2019
                : 19 December 2019
                Page count
                Figures: 6, Tables: 3, Pages: 11, Words: 8974
                Funding
                Funded by: University of Illinois , open-funder-registry 10.13039/100010443;
                Funded by: Foundation for Food and Agriculture Research , open-funder-registry 10.13039/100011929;
                Funded by: Bill and Melinda Gates Foundation , open-funder-registry 10.13039/100000865;
                Funded by: UK Department for International Development (UKAid)
                Award ID: OPP1172157
                Funded by: Carl R. Woese Institute of Genomic Biology Fellowship
                Funded by: Illinois Distinguished Fellowship
                Categories
                SI Advances in Photosynthesis
                Si Advances in Photosynthesis
                Custom metadata
                2.0
                February 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.7 mode:remove_FC converted:11.03.2020

                Plant science & Botany
                photosynthetic induction,non‐photochemical quenching,npq,food security,soybean,wheat,photosystem ii,photoinhibition,stomata,crop breeding,leaf canopy,rubisco activase

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