Photosynthetic Gains in Super-Nodulating Mutants of Medicago truncatula under Elevated Atmospheric CO2 Conditions

Legumes are generally considered to be more responsive to elevated CO2 (eCO2) conditions due to the benefits provided by symbiotic nitrogen fixation. In response to high carbohydrate demand from nodules, legumes display autoregulation of nodulation (AON) to restrict nodules to the minimum number necessary to sustain nitrogen supply under current photosynthetic levels. AON mutants super-nodulate and typically grow smaller than wild-type plants under ambient CO2. Here, we show that AON super-nodulating mutants have substantially higher biomass under eCO2 conditions, which is sustained through increased photosynthetic investment. We examined photosynthetic and physiological traits across super-nodulating rdn1-1 (Root Determined Nodulation) and sunn4 (Super Numeric Nodules) and non-nodulating nfp1 (Nod Factor Perception) Medicago truncatula mutants. Under eCO2 conditions, super-nodulating plants exhibited increased rates of carboxylation (Vcmax) and electron transport (J) relative to wild-type and non-nodulating counterparts. The substantially higher rate of CO2 assimilation in eCO2-grown sunn4 super-nodulating plants was sustained through increased production of key photosynthetic enzymes, including Rieske FeS. We hypothesize that AON mutants are carbon-limited and can perform better at eCO2 through improved photosynthesis. Nodulating legumes, especially those with higher nitrogen fixation capability, are likely to out-perform non-nodulating plants under future CO2 conditions and will be important tools for understanding carbon and nitrogen partitioning under eCO2 conditions and future crop improvements.

[1]  Caixian Tang,et al.  Differential responses of the sunn4 and rdn1-1 super-nodulation mutants of Medicago truncatula to elevated atmospheric CO2. , 2021, Annals of botany.

[2]  S. Singer,et al.  Potential effects of a high CO2 future on leguminous species , 2020, Plant-environment interactions.

[3]  M. Udvardi,et al.  Celebrating 20 Years of Genetic Discoveries in Legume Nodulation and Symbiotic Nitrogen Fixation[OPEN] , 2019, Plant Cell.

[4]  Ming Xu,et al.  Elevated CO2 concentration induces photosynthetic down-regulation with changes in leaf structure, non-structural carbohydrates and nitrogen content of soybean , 2019, BMC Plant Biology.

[5]  G. Pan,et al.  Changes in plant C, N and P ratios under elevated [CO2] and canopy warming in a rice-winter wheat rotation system , 2019, Scientific Reports.

[6]  J. Frugoli,et al.  The Medicago truncatula CLAVATA3-LIKE CLE12/13 signaling peptides regulate nodule number depending on the CORYNE but not the COMPACT ROOT ARCHITECTURE2 receptor , 2019, Plant signaling & behavior.

[7]  Susanne von Caemmerer,et al.  Overexpression of the Rieske FeS protein of the Cytochrome b6f complex increases C4 photosynthesis in Setaria viridis , 2019, Communications Biology.

[8]  A. Nicotra,et al.  Genes controlling legume nodule numbers affect phenotypic plasticity responses to nitrogen in the presence and absence of rhizobia. , 2018, Plant, cell & environment.

[9]  J. R. Evans,et al.  The nitrogen cost of photosynthesis. , 2018, Journal of experimental botany.

[10]  Guanghua Wang,et al.  Impact of Elevated CO2 on Seed Quality of Soybean at the Fresh Edible and Mature Stages , 2018, Front. Plant Sci..

[11]  P. Gresshoff,et al.  Legume nodulation: The host controls the party. , 2018, Plant, cell & environment.

[12]  Tracy Lawson,et al.  Overexpression of the RieskeFeS Protein Increases Electron Transport Rates and Biomass Yield1[CC-BY] , 2017, Plant Physiology.

[13]  J. Frugoli,et al.  ROOT DETERMINED NODULATION1 Is Required for M. truncatula CLE12, But Not CLE13, Peptide Signaling through the SUNN Receptor Kinase1[OPEN] , 2017, Plant Physiology.

[14]  R. Sicher,et al.  Varying Response of the Concentration and Yield of Soybean Seed Mineral Elements, Carbohydrates, Organic Acids, Amino Acids, Protein, and Oil to Phosphorus Starvation and CO2 Enrichment , 2016, Frontiers in plant science.

[15]  Y. Matsubayashi,et al.  Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase , 2013, Nature Communications.

[16]  M. Udvardi,et al.  Transport and metabolism in legume-rhizobia symbioses. , 2013, Annual review of plant biology.

[17]  G. Fitzgerald,et al.  Understanding crop physiology to select breeding targets and improve crop management under increasing atmospheric CO2 concentrations , 2013 .

[18]  German Spangenberg,et al.  Improving yield potential in crops under elevated CO2: Integrating the photosynthetic and nitrogen utilization efficiencies , 2012, Front. Plant Sci..

[19]  Kevin W Eliceiri,et al.  NIH Image to ImageJ: 25 years of image analysis , 2012, Nature Methods.

[20]  M. Watt,et al.  The Autoregulation Gene SUNN Mediates Changes in Root Organ Formation in Response to Nitrogen through Alteration of Shoot-to-Root Auxin Transport1[W][OA] , 2012, Plant Physiology.

[21]  J. F. Marsh,et al.  The ROOT DETERMINED NODULATION1 Gene Regulates Nodule Number in Roots of Medicago truncatula and Defines a Highly Conserved, Uncharacterized Plant Gene Family1[C][W][OA] , 2011, Plant Physiology.

[22]  K. Novák.  On the efficiency of legume supernodulating mutants , 2010 .

[23]  S. Rombauts,et al.  CLE Peptides Control Medicago truncatula Nodulation Locally and Systemically1[C][W][OA] , 2010, Plant Physiology.

[24]  J. Schulze,et al.  Elevated CO2 concentration around alfalfa nodules increases N2 fixation , 2009, Journal of experimental botany.

[25]  A. Rogers,et al.  Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. , 2009, Journal of experimental botany.

[26]  Simon Buckle,et al.  Mitigation of climate change , 2009, The Daunting Climate Change.

[27]  T. Sharkey,et al.  Fitting photosynthetic carbon dioxide response curves for C(3) leaves. , 2007, Plant, cell & environment.

[28]  Julia Frugoli,et al.  The Medicago truncatula SUNN Gene Encodes a CLV1-like Leucine-rich Repeat Receptor Kinase that Regulates Nodule Number and Root Length , 2005, Plant Molecular Biology.

[29]  S. Long,et al.  What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. , 2004, The New phytologist.

[30]  P. Reich,et al.  Contrasting growth response of an N2-fixing and non-fixing forb to elevated CO2: dependence on soil N supply , 2003, Plant and Soil.

[31]  P. J. Andralojc,et al.  Manipulation of Rubisco: the amount, activity, function and regulation. , 2003, Journal of experimental botany.

[32]  S. Shaw,et al.  The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation. , 2003, The Plant journal : for cell and molecular biology.

[33]  P. Curtis,et al.  A meta‐analysis of elevated [CO2] effects on soybean (Glycine max) physiology, growth and yield , 2002 .

[34]  E. González,et al.  Continuous CO2 enrichment leads to increased nodule biomass, carbon availability to nodules and activity of carbon‐metabolising enzymes but does not enhance specific nitrogen fixation in pea , 2001 .

[35]  P. Reich,et al.  Do species and functional groups differ in acquisition and use of C, N and water under varying atmospheric CO2 and N availability regimes? : a field test with 16 grassland species , 2001 .

[36]  E. Adgo,et al.  Efficiency of N2 fixation in Vicia faba L. in combination with different Rhizobium leguminosarum strains. , 2000 .

[37]  A. Lüscher,et al.  Direct evidence that symbiotic N2 fixation in fertile grassland is an important trait for a strong response of plants to elevated atmospheric CO2 , 2000 .

[38]  T. Nakamura,et al.  The Effect of CO2 Enrichment on the Growth of Nodulated and Non-Nodulated Isogenic Types of Soybean Raised Under Two Nitrogen Concentrations , 1999, Photosynthetica.

[39]  J. E. Harper,et al.  Response of a hypernodulating soybean mutant to increased photosynthate supply , 1997 .

[40]  J. Pate,et al.  Interactions between irradiance levels, nodulation and nitrogenase activity of soybean cv. Bragg and a supernodulating mutant , 1990 .

[41]  L. Tran,et al.  Legume Nitrogen Fixation in a Changing Environment , 2015, Springer International Publishing.

[42]  L. Tran,et al.  Does Elevated CO2 Provide Real Benefits for N2-Fixing Leguminous Symbioses? , 2015 .

[43]  O. Edenhofer,et al.  Climate change 2014 : mitigation of climate change , 2014 .

[44]  G. Oldroyd,et al.  The ROOT DETERMINED NODULATION 1 Gene Regulates Nodule Number in Roots of Medicago truncatula and Defines a Highly Conserved , Uncharacterized Plant Gene Family 1 [ C ] [ W ] [ OA ] , 2011 .

[45]  J. Schulze,et al.  Elevated CO 2 concentration around alfalfa nodules increases N 2 fixation , 2009 .

[46]  K. Giller,et al.  Measuring plant-associated nitrogen fixation in agricultural systems , 2008 .

[47]  S. Long,et al.  Review Tansley Review , 2022 .

[48]  Murray R. Badger,et al.  The interplay between limiting processes in C3 photosynthesis studied by rapid-response gas exchange using transgenic tobacco impaired in photosynthesis , 1998 .

[49]  G. H. Heichel,et al.  CARBON IN N2 FIXATION: Limitation or Exquisite Adaptation , 1991 .

[50]  H. Lichtenthaler.  CHLOROPHYLL AND CAROTENOIDS: PIGMENTS OF PHOTOSYNTHETIC BIOMEMBRANES , 1987 .

[51]  F. Bergersen.  The Growth Of Rhizobium in Synthetic Media , 1961 .