Impacts of Nitrogen and Phosphorus: From Genomes to Natural Ecosystems and Agriculture

Nitrogen (N) and/or phosphorus (P) availability can limit growth of primary producers across most of the world’s aquatic and terrestrial ecosystems. These constraints are commonly overcome in agriculture by applying fertilizers to improve yields. However, excessive anthropogenic N and P inputs impact natural environments and have far-reaching ecological and evolutionary consequences, from individual species up to entire ecosystems. The extent to which global N and P cycles have been perturbed over the past century can be seen as a global fertilization experiment with significant redistribution of nutrients across different ecosystems. Here we explore the effects of N and P availability on stoichiometry and genomic traits of organisms, which, in turn, can influence: i) plant and animal abundances; ii) trophic interactions and population dynamics; and iii) ecosystem dynamics and productivity of agricultural crops. We articulate research priorities for a deeper understanding of how bioavailable N and P move through the environment and exert their ultimate impacts on biodiversity and ecosystem services.

[1]  R. Nichols,et al.  Genome size and ploidy influence angiosperm species' biomass under nitrogen and phosphorus limitation , 2016, The New phytologist.

[2]  Helmut Hillebrand,et al.  A cross-system synthesis of consumer and nutrient resource control on producer biomass. , 2008, Ecology letters.

[3]  Timothy M. Lenton,et al.  The impact of temperature on marine phytoplankton resource allocation and metabolism , 2013 .

[4]  Y. Peer,et al.  The evolutionary significance of polyploidy , 2017, Nature Reviews Genetics.

[5]  V. Smil PHOSPHORUS IN THE ENVIRONMENT: Natural Flows and Human Interferences , 2000 .

[6]  Corinne Le Quéré,et al.  Carbon and Other Biogeochemical Cycles , 2014 .

[7]  J. Elser Phosphorus: a limiting nutrient for humanity? , 2012, Current opinion in biotechnology.

[8]  Phillip A. Richmond,et al.  Polyploidy can drive rapid adaptation in yeast , 2015, Nature.

[9]  William F. Fagan,et al.  Phylogenetic and Growth Form Variation in the Scaling of Nitrogen and Phosphorus in the Seed Plants , 2006, The American Naturalist.

[10]  S. Levin,et al.  Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton , 2004, Nature.

[11]  W. M. Lewis Nutrient Scarcity as an Evolutionary Cause of Haploidy , 1985, The American Naturalist.

[12]  Jasper A. Vrugt,et al.  Strong latitudinal patterns in the elemental ratios of marine plankton and organic matter , 2013 .

[13]  Jonathan F Wendel,et al.  Doubling down on genomes: polyploidy and crop plants. , 2014, American journal of botany.

[14]  H. Lambers,et al.  Strategies and agronomic interventions to improve the phosphorus-use efficiency of farming systems , 2011, Plant and Soil.

[15]  D. Cordell,et al.  The story of phosphorus: Global food security and food for thought , 2009 .

[16]  J. Schellberg,et al.  Effect of phosphorus availability on the selection of species with different ploidy levels and genome sizes in a long-term grassland fertilization experiment. , 2013, The New phytologist.

[17]  A. Leitch,et al.  Genome size diversity in angiosperms and its influence on gene space. , 2015, Current opinion in genetics & development.

[18]  C. Eizaguirre,et al.  Experimental evidence that parasites drive eco-evolutionary feedbacks , 2017, Proceedings of the National Academy of Sciences.

[19]  J. Elser,et al.  This journal is © 2009 The Royal SocietyDownloaded from , 2009 .

[20]  N. Yamaji,et al.  Reducing phosphorus accumulation in rice grains with an impaired transporter in the node , 2016, Nature.

[21]  Katherine N. Suding,et al.  Plant–soil feedbacks: the past, the present and future challenges , 2013 .

[22]  Jacob D. Washburn,et al.  Watching the grin fade: tracing the effects of polyploidy on different evolutionary time scales. , 2013, Seminars in cell & developmental biology.

[23]  G. Woodward,et al.  Resource quality and stoichiometric constraints on stream ecosystem functioning , 2009 .

[24]  J. Elser,et al.  Atmospheric nitrogen deposition is associated with elevated phosphorus limitation of lake zooplankton. , 2010, Ecology letters.

[25]  Y. Kuang,et al.  Biological Stoichiometry: An Ecological Perspective on Tumor Dynamics , 2003 .

[26]  Stephen Porder,et al.  Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. , 2010, Ecological applications : a publication of the Ecological Society of America.

[27]  J. Peñuelas,et al.  The elemental stoichiometry of aquatic and terrestrial ecosystems and its relationships with organismic lifestyle and ecosystem structure and function: a review and perspectives , 2011, Biogeochemistry.

[28]  Miska Luoto,et al.  Toward More Integrated Ecosystem Research in Aquatic and Terrestrial Environments , 2015 .

[29]  A. Gerstein Mutational effects depend on ploidy level: all else is not equal , 2013, Biology Letters.

[30]  F. Chapin,et al.  Consequences of changing biodiversity , 2000, Nature.

[31]  F. Chapin,et al.  Planetary boundaries: Exploring the safe operating space for humanity , 2009 .

[32]  Bin Li,et al.  Mapping QTLs for yield and nitrogen-related traits in wheat: influence of nitrogen and phosphorus fertilization on QTL expression , 2013, Theoretical and Applied Genetics.

[33]  Hans Lambers,et al.  Plant and microbial strategies to improve the phosphorus efficiency of agriculture , 2011, Plant and Soil.

[34]  J. Postlethwait,et al.  Polyploidy in Fish and the Teleost Genome Duplication , 2012 .

[35]  S. Kelly,et al.  Dietary nitrogen alters codon bias and genome composition in parasitic microorganisms , 2016, Genome Biology.

[36]  S. Díaz,et al.  Biodiversity Loss Threatens Human Well-Being , 2006, PLoS biology.

[37]  J. Elser,et al.  Biological Stoichiometry in Human Cancer , 2007, PloS one.

[38]  R. Nichols,et al.  Genomic Prediction of Testcross Performance in Canola (Brassica napus) , 2016, PloS one.

[39]  M. Chase,et al.  Is post-polyploidization diploidization the key to the evolutionary success of angiosperms? , 2016 .

[40]  K. A. Segraves The effects of genome duplications in a community context. , 2017, The New phytologist.

[41]  A. Meyer,et al.  The evolutionary significance of ancient genome duplications , 2009, Nature Reviews Genetics.

[42]  Jason G. Bragg,et al.  Opportunities for improving phosphorus-use efficiency in crop plants. , 2012, The New phytologist.

[43]  J. Elser,et al.  Stoichiogenomics: the evolutionary ecology of macromolecular elemental composition. , 2011, Trends in ecology & evolution.

[44]  J. Elser,et al.  Stoichiometry and population dynamics , 2004 .

[45]  H. Hillebrand,et al.  Goldman revisited: Faster‐growing phytoplankton has lower N : P and lower stoichiometric flexibility , 2013 .

[46]  W. Winiwarter,et al.  How a century of ammonia synthesis changed the world , 2008 .

[47]  Plant functional constraints guide macroevolutionary trade‐offs in competitive and conservative growth responses to nitrogen , 2016 .

[48]  M. Loreau,et al.  When microbes and consumers determine the limiting nutrient of autotrophs: a theoretical analysis , 2009, Proceedings of the Royal Society B: Biological Sciences.

[49]  M. Neiman,et al.  Effects of polyploidy and reproductive mode on life history trait expression , 2016, Ecology and evolution.

[50]  Weicong Qi,et al.  Genome-wide identification and functional prediction of nitrogen-responsive intergenic and intronic long non-coding RNAs in maize (Zea mays L.) , 2016, BMC Genomics.

[51]  J. Elser,et al.  Temperature and the chemical composition of poikilothermic organisms , 2003 .

[52]  D. O. Hessen,et al.  Genome streamlining and the elemental costs of growth. , 2010, Trends in ecology & evolution.

[53]  J. Galloway,et al.  A chronology of human understanding of the nitrogen cycle† , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[54]  C. Cleveland,et al.  C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? , 2007 .

[55]  J. Greilhuber,et al.  Genome Size and the Phenotype , 2013 .

[56]  David C. Tank,et al.  Nested radiations and the pulse of angiosperm diversification: increased diversification rates often follow whole genome duplications. , 2015, The New phytologist.

[57]  D. Sankoff,et al.  Polyploidy and angiosperm diversification. , 2009, American journal of botany.

[58]  H. Lambers,et al.  Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies , 2010, Plant and Soil.

[59]  M. Neiman,et al.  SENSITIVITY TO PHOSPHORUS LIMITATION INCREASES WITH PLOIDY LEVEL IN A NEW ZEALAND SNAIL , 2012, Evolution; international journal of organic evolution.

[60]  D. O. Hessen,et al.  Plasticity in algal stoichiometry: Experimental evidence of a temperature‐induced shift in optimal supply N:P ratio , 2017 .

[61]  C. Eizaguirre,et al.  The association of feeding behaviour with the resistance and tolerance to parasites in recently diverged sticklebacks , 2016, Journal of evolutionary biology.

[62]  S. Carpenter,et al.  Reconsideration of the planetary boundary for phosphorus , 2011 .

[63]  Hur-Song Chang,et al.  Transcriptome Changes for Arabidopsis in Response to Salt, Osmotic, and Cold Stress1,212 , 2002, Plant Physiology.

[64]  Lex E. Flagel,et al.  Homoeolog expression bias and expression level dominance in allopolyploids. , 2012, The New phytologist.

[65]  H. Lambers,et al.  Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies , 2011, Plant and Soil.

[66]  M. Neiman,et al.  Can resource costs of polyploidy provide an advantage to sex? , 2012, Heredity.

[67]  Ning Li,et al.  Low Contents of Carbon and Nitrogen in Highly Abundant Proteins: Evidence of Selection for the Economy of Atomic Composition , 2009, Journal of Molecular Evolution.

[68]  Y. Kuzyakov,et al.  Phosphorus mineralization can be driven by microbial need for carbon , 2013 .

[69]  Allison M. Leach,et al.  The global nitrogen cycle in the twenty-first century , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[70]  Helmut Hillebrand,et al.  Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. , 2007, Ecology letters.

[71]  Jonathan F. Wendel,et al.  Polyploidy and Crop Improvement , 2006 .

[72]  D. Rand,et al.  Direct measurement of transcription rates reveals multiple mechanisms for configuration of the Arabidopsis ambient temperature response , 2014, Genome Biology.

[73]  W. McDowell,et al.  Merging aquatic and terrestrial perspectives of nutrient biogeochemistry , 2003, Oecologia.

[74]  Rudolf P. Rohr,et al.  Persist or Produce: A Community Trade-Off Tuned by Species Evenness , 2016, The American Naturalist.

[75]  M. Neiman,et al.  Can phosphorus limitation contribute to the maintenance of sex? A test of a key assumption , 2009, Journal of evolutionary biology.

[76]  F. Chapin,et al.  A safe operating space for humanity , 2009, Nature.

[77]  V. Smith,et al.  Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. , 1999, Environmental pollution.

[78]  B. Guenet,et al.  Priming effect: bridging the gap between terrestrial and aquatic ecology. , 2010, Ecology.

[79]  J. Catalán,et al.  Atmospheric phosphorus deposition may cause lakes to revert from phosphorus limitation back to nitrogen limitation , 2012, Nature Communications.

[80]  D. O. Hessen,et al.  Phosphorus use and excretion varies with ploidy level in Daphnia , 2015 .

[81]  Alexander E Vinogradov,et al.  Selfish DNA is maladaptive: evidence from the plant Red List. , 2003, Trends in genetics : TIG.

[82]  D. O. Hessen,et al.  Endopolyploidy as a potential driver of animal ecology and evolution , 2017, Biological reviews of the Cambridge Philosophical Society.

[83]  G. Woodward,et al.  Impact of genomic diversity in river ecosystems. , 2014, Trends in plant science.

[84]  V. Raboy Seeds for a better future: 'low phytate' grains help to overcome malnutrition and reduce pollution. , 2001, Trends in plant science.

[85]  J. Elser,et al.  Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere , 2002 .

[86]  F. Chapin,et al.  Principles of Terrestrial Ecosystem Ecology , 2002, Springer New York.

[87]  T. Daufresne,et al.  SCALING OF C:N:P STOICHIOMETRY IN FORESTS WORLDWIDE: IMPLICATIONS OF TERRESTRIAL REDFIELD‐TYPE RATIOS , 2004 .

[88]  Paul J. A. Withers,et al.  Greening the global phosphorus cycle: how green chemistry can help achieve planetary P sustainability , 2015 .

[89]  J. Ramsey,et al.  Ecological studies of polyploidy in the 100 years following its discovery , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[90]  D. Petrov,et al.  The large genome constraint hypothesis: evolution, ecology and phenotype. , 2005, Annals of botany.

[91]  Brendan G. McKie,et al.  Continental-Scale Effects of Nutrient Pollution on Stream Ecosystem Functioning , 2012, Science.

[92]  R. Sterner The Ratio of Nitrogen to Phosphorus Resupplied by Herbivores: Zooplankton and the Algal Competitive Arena , 1990, The American Naturalist.

[93]  A. Hendry,et al.  Eco-evolutionary dynamics , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[94]  J. Lynch,et al.  Rhizoeconomics: Carbon costs of phosphorus acquisition , 2005, Plant and Soil.

[95]  N. Mahowald,et al.  Is atmospheric phosphorus pollution altering global alpine Lake stoichiometry? , 2015 .

[96]  S. Rothstein,et al.  Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency. , 2011, Journal of experimental botany.

[97]  Amborella Genome The Amborella Genome and the Evolution of Flowering Plants , 2013, Science.

[98]  A. P. Williams,et al.  Use of commercial bio-inoculants to increase agricultural production through improved phosphrous acquisition , 2015 .

[99]  D. O. Hessen,et al.  Genome size as a determinant of growth and life-history traits in crustaceans , 2009 .

[100]  J. Elser,et al.  Ecological nitrogen limitation shapes the DNA composition of plant genomes. , 2009, Molecular biology and evolution.

[101]  A. Leitch,et al.  Genomic Plasticity and the Diversity of Polyploid Plants , 2008, Science.

[102]  P. Harrison,et al.  Linkages between biodiversity attributes and ecosystem services: A systematic review , 2014 .

[103]  Pamela S Soltis,et al.  Ancient WGD events as drivers of key innovations in angiosperms. , 2016, Current opinion in plant biology.

[104]  Millenium Ecosystem Assessment Ecosystems and human well-being: synthesis , 2005 .

[105]  Peter Kareiva,et al.  Domesticated Nature: Shaping Landscapes and Ecosystems for Human Welfare , 2007, Science.

[106]  I. Leitch,et al.  Genome downsizing in polyploid plants , 2004 .

[107]  C. Violle,et al.  Let the concept of trait be functional , 2007 .

[108]  Stefan Reis,et al.  Towards a climate-dependent paradigm of ammonia emission and deposition , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[109]  James P Grover,et al.  The Impact of Variable Stoichiometry on Predator‐Prey Interactions: A Multinutrient Approach , 2003, The American Naturalist.

[110]  P. Reich,et al.  Global patterns of plant leaf N and P in relation to temperature and latitude. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[111]  M. Brehm,et al.  Maximizing growth rate at low temperatures: RNA:DNA allocation strategies and life history traits of Arctic and temperate Daphnia , 2010, Polar Biology.

[112]  J. Elser,et al.  Shifts in Lake N:P Stoichiometry and Nutrient Limitation Driven by Atmospheric Nitrogen Deposition , 2009, Science.

[113]  Ilia J. Leitch,et al.  The largest eukaryotic genome of them all , 2010 .

[114]  S. Güsewell N : P ratios in terrestrial plants: variation and functional significance. , 2004, The New phytologist.

[115]  O. Gutiérrez The Story of Phosphorus , 2017 .

[116]  R. Bommarco,et al.  Ecological intensification: harnessing ecosystem services for food security. , 2013, Trends in ecology & evolution.

[117]  David Tilman,et al.  Human-caused environmental change: Impacts on plant diversity and evolution , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[118]  Q. Read,et al.  Plant–soil feedbacks: connecting ecosystem ecology and evolution , 2016 .

[119]  R. Varshney,et al.  Genomic Selection for Crop Improvement , 2017, Springer International Publishing.

[120]  Claude W. dePamphilis,et al.  Ancestral polyploidy in seed plants and angiosperms , 2011, Nature.