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Planta

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CO2 and nitrogen interaction alters root anatomy, morphology, nitrogen partitioning and photosynthetic acclimation of tomato plants

  • Itay CohenEmail author
  • Moshe Halpern
  • Uri Yermiyahu
  • Asher Bar-Tal
  • Tanya Gendler
  • Shimon Rachmilevitch
Original Article
  • 42 Downloads

Abstract

Main conclusion

Nitrogen and CO2 supply interactively regulate whole plant nitrogen partitioning and root anatomical and morphological development in tomato plants.

Abstract

Nitrogen (N) and carbon (C) are the key elements in plant growth and constitute the majority of plant dry matter. Growing at CO2 enrichment has the potential to stimulate the growth of C3 plants, however, growth is often limited by N availability. Thus, the interactive effects of CO2 under different N fertilization rates can affect growth, acclimation to elevated CO2, and yield. However, the majority of research in this field has focused on shoot traits, while neglecting plants’ hidden half—the roots. We hypothesize that elevated CO2 and low N effects on transpiration will interactively affect root vascular development and plant N partitioning. Here we studied the effects of elevated CO2 and N concentrations on greenhouse-grown tomato plants, a C3 crop. Our main objective was to determine in what manner the N fertilization rate and elevated CO2 affected root development and nitrogen partitioning among plant organs. Our results indicate that N interacting with the CO2 level affects the development of the root system in terms of the length, anatomy, and partitioning of the N concentration between the roots and shoot. Both CO2 and N concentrations were found to affect xylem size in an opposite manner, elevated CO2 found to repressed, whereas ample N stimulated xylem development. We found that under limiting N and eCO2, the N% increase in the root, while it decreased in the shoot. Under eCO2, the root system size increased with a coordinated decrease in root xylem area. We suggest that tomato root response to elevated CO2 depends on N fertilization rates, and that a decrease in xylem size is a possible underlying response that limits nitrogen allocation from the root into the shoot. Additionally, the greater abundance of root amino acids suggests increased root nitrogen metabolism at eCO2 conditions with ample N.

Keywords

Climate change CO2 Gas exchange Metabolites Nitrogen Root Tomato Xylem 

Abbreviations

aCO2

Ambient CO2

eCO2

Elevated CO2

Rubisco

Ribulose-1,5-bisphosphate carboxylase/oxygenase

Notes

Acknowledgements

We would like to thank Liron Summerfield for her technical support and encouragement. We would also like to thank David Granot’s ARO lab for their assistance with the Rubisco analysis.

Funding

This study was partially supported by the Frances and Elias Margolin Trust and by the Israel Ministry of Agriculture and Rural Development (Eugene Kandel Knowledge Centers) as part of the Root of the Matter—The Root Zone Knowledge Center for Leveraging Modern Agriculture.

Supplementary material

425_2019_3232_MOESM1_ESM.docx (12 kb)
Supplementary material 1 (DOCX 11 kb)

References

  1. Anten NPR, Hirose T, Onoda Y, Kinugasa T et al (2004) Elevated CO2 and nitrogen availability have interactive effects on canopy carbon gain in rice. New Phytol 161:459–471CrossRefGoogle Scholar
  2. Asensio JSR, Rachmilevitch S, Bloom AJ (2015) Responses of Arabidopsis and wheat to rising CO2 depend on nitrogen source and nighttime CO2 levels. Plant Physiol 168:156–163CrossRefGoogle Scholar
  3. Bahrami H, De Kok LJ, Armstrong R et al (2017) The proportion of nitrate in leaf nitrogen, but not changes in root growth, are associated with decreased grain protein in wheat under elevated [CO2]. J Plant Physiol 216:44–51CrossRefGoogle Scholar
  4. Bloom AJ, Asensio JSR, Randall L et al (2012) CO2 enrichment inhibits shoot nitrate assimilation in C3 but not C4 plants and slows growth under nitrate in C3 plants. Ecology 93:355–367CrossRefGoogle Scholar
  5. Bloom A, Burger M, Kimball B Jr (2014) Nitrate assimilation is inhibited by elevated CO2 in field-grown wheat. Nat Clim Change 4:477–580CrossRefGoogle Scholar
  6. Cai Q, Ji C, Yan Z et al (2017) Anatomical responses of leaf and stem of Arabidopsis thaliana to nitrogen and phosphorus addition. J Plant Res 130:1035–1045CrossRefGoogle Scholar
  7. Carlisle E, Myers S, Raboy V, Bloom A (2012) The effects of inorganic nitrogen form and CO2 concentration on wheat yield and nutrient accumulation and distribution. Front Plant Sci 3:195–205CrossRefGoogle Scholar
  8. Cohen I, Rapaport T, Berger RT, Rachmilevitch S (2018a) The effects of elevated CO2 and nitrogen nutrition on root dynamics. Plant Sci 272:294–300CrossRefGoogle Scholar
  9. Cohen I, Rapaport T, Chalifa-Caspi V, Rachmilevitch S (2018b) Synergistic effects of abiotic stresses in plants: a case study of nitrogen limitation and saturating light intensity in Arabidopsis thaliana. Physiol Plant 165:755–767CrossRefGoogle Scholar
  10. Cotrufo MF, Gorissen A (1997) Elevated CO2 enhances below-ground C allocation in three perennial grass species at different levels of N availability. New Phytol 137:421–431CrossRefGoogle Scholar
  11. Easlon HM, Carlisle E, McKay JK, Bloom AJ (2015) Does low stomatal conductance or photosynthetic capacity enhance growth at elevated CO2 in Arabidopsis? Plant Physiol 167:793–799CrossRefGoogle Scholar
  12. Erice G, Sanz-Sáez Alvaro, Urdiain A et al (2014) Harvest index combined with impaired N availability constrains the responsiveness of durum wheat to elevated CO2 concentration and terminal water stress. Funct Plant Biol 41:1138–1147CrossRefGoogle Scholar
  13. Giehl RFH, Gruber BD, von Wirén N (2014) It’s time to make changes: modulation of root system architecture by nutrient signals. J Exp Bot 65:769–778CrossRefGoogle Scholar
  14. Girondé A, Etienne P, Trouverie J et al (2015) The contrasting N management of two oilseed rape genotypes reveals the mechanisms of proteolysis associated with leaf N remobilization and the respective contributions of leaves and stems to N storage and remobilization during seed filling. BMC Plant Biol 15:59CrossRefGoogle Scholar
  15. Gruber BD, Giehl RFH, Friedel S, von Wirén N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol 163:161–179CrossRefGoogle Scholar
  16. Hachiya T, Sugiura D, Kojima M et al (2014) High CO2 triggers preferential root growth of Arabidopsis thaliana via two distinct systems under low pH and low N stresses. Plant Cell Physiol 55:269–280CrossRefGoogle Scholar
  17. Halpern M, Bar-Tal A, Lugassi N et al (2019) The role of nitrogen in photosynthetic acclimation to elevated [CO2] in tomatoes. Plant Soil 434:397–411CrossRefGoogle Scholar
  18. Hao G-Y, Holbrook NM, Zwieniecki MA et al (2018) Coordinated responses of plant hydraulic architecture with the reduction of stomatal conductance under elevated CO2 concentration. Tree Physiol 2:1041–1052CrossRefGoogle Scholar
  19. Hochberg U, Degu A, Gendler T et al (2015) The variability in the xylem architecture of grapevine petiole and its contribution to hydraulic differences. Funct Plant Biol 42:357CrossRefGoogle Scholar
  20. Jauregui I, Aparicio-Tejo PM, Avila C et al (2015) Root and shoot performance of Arabidopsis thaliana exposed to elevated CO2: a physiologic, metabolic and transcriptomic response. J Plant Physiol 189:65–76CrossRefGoogle Scholar
  21. Jauregui I, Aparicio-Tejo PM, Avila C et al (2016) Root-shoot interactions explain the reduction of leaf mineral content in Arabidopsis plants grown under elevated [CO2] conditions. Physiol Plant 158:65–79CrossRefGoogle Scholar
  22. Kruse J, Hetzger I, Hänsch R et al (2002) Elevated pCO(2)favours nitrate reduction in the roots of wild-type tobacco (Nicotiana tabacum cv. Gat.) and significantly alters N-metabolism in transformants lacking functional nitrate reductase in the roots. J Exp Bot 53:2351–2367CrossRefGoogle Scholar
  23. Kruse J, Hetzger I, Mai C et al (2003) Elevated pCO2 affects N-metabolism of young poplar plants (Populus tremula × P. alba) differently at deficient and sufficient N-supply. New Phytol 157:65–81CrossRefGoogle Scholar
  24. Leakey ADB, Ainsworth EA, Bernacchi CJ et al (2009) Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J Exp Bot 60:2859–2876CrossRefGoogle Scholar
  25. Li P, Bohnert HJ, Grene R (2007) All about FACE–plants in a high [CO2] world. Trends Plant Sci 12:87–89CrossRefGoogle Scholar
  26. Lisec J, Schauer N, Kopka J et al (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat Protoc 1:387–396CrossRefGoogle Scholar
  27. Lugassi N, Kelly G, Fidel L et al (2015) Expression of Arabidopsis hexokinase in citrus guard cells controls stomatal aperture and reduces transpiration. Front Plant Sci 6:1–11CrossRefGoogle Scholar
  28. Lynch JP (2013) Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Ann Bot 112:347–357CrossRefGoogle Scholar
  29. Lynch JP, Chimungu JG, Brown KM (2014) Root anatomical phenes associated with water acquisition from drying soil: targets for crop improvement. J Exp Bot 21:6155–6166CrossRefGoogle Scholar
  30. Meister R, Rajani MS, Ruzicka D, Schachtman DP (2014) Challenges of modifying root traits in crops for agriculture. Trends Plant Sci 19:779–788CrossRefGoogle Scholar
  31. Moore BD, Cheng SH, Sims D, Seemann JR (1999) The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2. Plant Cell Environ 22:567–582CrossRefGoogle Scholar
  32. Pacholski A, Manderscheid R, Weigel HJ (2015) Effects of free air CO2 enrichment on root growth of barley, sugar beet and wheat grown in a rotation under different nitrogen supply. Eur J Agron 63:36–46CrossRefGoogle Scholar
  33. Paudel I, Halpern M, Wagner Y et al (2018) Elevated CO2 compensates for drought effects in lemon saplings via stomatal downregulation, increased soil moisture, and increased wood carbon storage. Environ Exp Bot 148:117–127CrossRefGoogle Scholar
  34. Rachmilevitch S, Cousins AB, Bloom AJ (2004) Nitrate assimilation in plant shoots depends on photorespiration. Proc Natl Acad Sci USA 101:11506–11510CrossRefGoogle Scholar
  35. Reich PB, Hobbie SE, Lee T et al (2006) Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature 440:922–925CrossRefGoogle Scholar
  36. Rubio-Wilhelmi MM, Sanchez-Rodriguez E, Rosales MA et al (2011) Effect of cytokinins on oxidative stress in tobacco plants under nitrogen deficiency. Environ Exp Bot 72:167–173CrossRefGoogle Scholar
  37. Sage RF, Pearcy RW (1987) The nitrogen use efficiency of C3 and C4 plants. II. Leaf nitrogen effects on the gas exchange characteristics of Chenopodium album (L) and Amaranthus retroflexus (L). Plant Physiol 84:959–963CrossRefGoogle Scholar
  38. Shimono H, Bunce JA (2009) Acclimation of nitrogen uptake capacity of rice to elevated atmospheric CO2 concentration. Ann Bot 103:87–94CrossRefGoogle Scholar
  39. Stitt M, Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell Environ 22:553–621CrossRefGoogle Scholar
  40. Stulen I, Hertog J (1993) Root growth and functioning under atmospheric CO2 enrichment. Vegetatio 104–105:99–115CrossRefGoogle Scholar
  41. Takatani N, Ito T, Kiba T et al (2014) Effects of high CO2 on growth and metabolism of Arabidopsis seedlings during growth with a constantly limited supply of nitrogen. Plant Cell Physiol 55:281–292CrossRefGoogle Scholar
  42. Taub DR, Wang X (2008) Why are nitrogen concentrations in plant tissues lower under elevated CO2? A critical examination of the hypotheses. J Integr Plant Biol 50:1365–1374CrossRefGoogle Scholar
  43. Van Oosten JJ, Besford RT (1996) Acclimation of photosynthesis to elevated CO2 through feedback regulation of gene expression: climate of opinion. Photosynth Res 48:353–365CrossRefGoogle Scholar
  44. Vicente R, Pérez P, Martínez-Carrasco R et al (2015) Nitrate supply and plant development influence nitrogen uptake and allocation under elevated CO2 in durum wheat grown hydroponically. Acta Physiol Plant 37:114CrossRefGoogle Scholar
  45. Vicente R, Prez P, Martnez-Carrasco R et al (2016) Metabolic and transcriptional analysis of durum wheat responses to elevated CO2 at low and high nitrate supply. Plant Cell Physiol 57:2133–2146CrossRefGoogle Scholar
  46. Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 63:153–182CrossRefGoogle Scholar
  47. Zhang SR, Dang QL, Yü XG (2006) Nutrient and [CO2] elevation had synergistic effects on biomass production but not on biomass allocation of white birch seedlings. For Ecol Manag 234:238–244CrossRefGoogle Scholar
  48. Zinta G, Abdelgawad H, Domagalska MA (2014) Physiological, biochemical, and genome-wide transcriptional analysis reveals that elevated CO2 mitigates the impact of combined heat wave and drought stress in Arabidopsis thaliana at multiple organizational levels. Glob Chang Biol 20:3670–3685CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Itay Cohen
    • 1
    Email author
  • Moshe Halpern
    • 2
    • 3
  • Uri Yermiyahu
    • 2
  • Asher Bar-Tal
    • 4
  • Tanya Gendler
    • 1
  • Shimon Rachmilevitch
    • 1
  1. 1.The French Associates Institute for Agriculture and Biotechnology of Drylands, The Blaustein Institutes for Desert ResearchBen-Gurion University of the NegevBeershebaIsrael
  2. 2.Agricultural Research Organization, Gilat Research CenterRishon LezionIsrael
  3. 3.The Hebrew University of JerusalemRehovotIsrael
  4. 4.Department of Soil Chemistry, Plant Nutrition and Microbiology, Institute of Soil, Water, and Environmental Sciences, Volcani CenterAgricultural Research Organization (ARO)Rishon LezionIsrael

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