Advertisement

Plant and Soil

, Volume 350, Issue 1–2, pp 117–130 | Cite as

Elevated CO2 affects plant responses to variation in boron availability

  • Sasmita Mishra
  • Scott A. Heckathorn
  • Jonathan M. Frantz
Regular Article

Abstract

Aim

Effects of elevated CO2 on N relations are well studied, but effects on other nutrients, especially micronutrients, are not. We investigated effects of elevated CO2 on response to variation in boron (B) availability in three unrelated species: seed geranium (Pelargonium x hortorum), barley (Hordeum vulgare), and water fern (Azolla caroliniana).

Methods

Plants were grown at two levels of CO2 (370, 700 ppm) and low, medium, and high B. Treatment effects were measured on biomass, net photosynthesis (Pn) and related variables, tissue nutrient concentrations, and B transporter protein BOR1.

Results

In geranium, there were interactive effects (P < 0.05) of B and CO2 on leaf, stem, and total plant mass, root:shoot ratio, leaf [B], B uptake rate, root [Zn], and Pn. Elevated CO2 stimulated growth at 45 μM B, but decreased it at 450 μM B and did not affect it at 4.5 μM B. Pn was stimulated by elevated CO2 only at 45 μM B and chlorophyll was enhanced only at 450 μM B. Soluble sugars increased with high CO2 only at 4.5 and 45 μM B. High CO2 decreased leaf [B] and B uptake rate, especially at 450 μM B. Though CO2 and B individually affected the concentration of several other nutrients, B x CO2 interactions were evident only for Zn in roots, wherein [Zn] decreased under elevated CO2. Interactive effects of B and CO2 on growth were confirmed in (1) barley grown at 0, 30, or 1,000 μM B, wherein growth at high CO2 was stimulated more at 30 μM B, and (2) Azolla grown at 0, 10, and 1,000 μM B, wherein growth at high CO2 was stimulated at 0 and 10 μM B.

Conclusion

Thus, low and high B both may limit growth stimulation under elevated vs. current [CO2], and B deficiency and toxicity, already common, may increase in the future.

Keywords

Azolla Barley Boron stress Boron transporter protein (BOR1) Geranium Nutrients Photosynthesis 

Notes

Acknowledgment

This research was supported by the U.S. Department of Agriculture, Agricultural Research Service (SCA 58-3607-4-119 to J. Gray and S.A. Heckathorn). The authors thank Douglas Sturtz and Alycia Pittenger for nutrient analysis.

References

  1. Barnes JD, Balaguer L, Manrique E, Elvira S, Davison AW (1992) A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants. Environ Expt Bot 32:85–100CrossRefGoogle Scholar
  2. Blank RR, Derner JD (2004) Effects of CO2 enrichment on plant-soil relationships of Lepidium latifolium. Plant Soil 262:159–167CrossRefGoogle Scholar
  3. Blevins DG, Lukaszewski KM (1998) Boron in plant structure and function. Annu Rev Plant Physiol Plant Mol Biol 49:481–500PubMedCrossRefGoogle Scholar
  4. Bolaños L, Lukaszewski K, Bonilla I, Blevins D (2004) Why boron? Plant Physiol Biochem 42:907–912PubMedCrossRefGoogle Scholar
  5. Boote KJ (1976) Root-shoot relationships. Soil Crop Sci Soc Florida 36:15–23Google Scholar
  6. Brown PH, Bellaloui N, Wimmer MA, Bassil ES, Ruiz J, Hu H, Pfeffer H, Dannel F, Römheld V (2002) Boron in plant biology. Plant Biol 4:205–223CrossRefGoogle Scholar
  7. Cakmak I, Hengeler C, Marschner H (1994) Partitioning of shoot and root dry matter and carbohydrates in bean plants suffering from phosphorus, potassium and magnesium deficiency. J Exp Bot 45:1245–1250CrossRefGoogle Scholar
  8. Campbell CD, Sage RF (2002) Interactions between atmospheric CO2 concentration and phosphorus nutrition on the formation of proteoid roots in white lupin. Plant Cell Environ 25:1051–1059CrossRefGoogle Scholar
  9. Coleman JS, McConnaughay KDM, Bazzaz FA (1993) Elevated CO2 and plant nitrogen-use: is reduced tissue nitrogen concentration size-dependent? Oecologia 93:195–200CrossRefGoogle Scholar
  10. Conroy JP (1992) Influence of elevated atmospheric CO2 concentrations on plant nutrition. Aust J Bot 40:445–456Google Scholar
  11. Cure JD, Acock B (1986) Crop responses to carbon dioxide doubling: a literature survey. Agric For Meteorol 38:127–145CrossRefGoogle Scholar
  12. Cure JD, Rufty TW, Israel DW (1988) Phosphorus stress effects on growth and seed yield of nonnodulated soybean exposed to elevated carbon dioxide. Agron J 80:897–902CrossRefGoogle Scholar
  13. Deng Y (2009) Biomarkers for the monitoring of boron deficiency in Arabidopsis and Pelargonium. Thesis, University of ToledoGoogle Scholar
  14. Dordas C, Brown PH (2000) Permeability of boric acid across lipid bilayers and factors affecting it. J Membr Biol 175:95–105PubMedCrossRefGoogle Scholar
  15. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356CrossRefGoogle Scholar
  16. Ehleringer JR, Cerling TE, Dearing MD (2002) Atmospheric CO2 as a global change driver influencing plant-animal interactions. Integr Compart Biol 42:424–430CrossRefGoogle Scholar
  17. Ellsworth D, Reich PB, Naumburg ES, Koch GW, Kubiske ME, Smith SD (2004) Photosynthesis, carboxylation, and leaf nitrogen responses of 16 species to elevated CO2 across four free-air CO2 enrichment experiments in forest, grassland and desert. Glob Chang Biol 10:2121–2138CrossRefGoogle Scholar
  18. El-Shintinawy F (1999) Structural and functional damage caused by boron deficiency in sunflower leaves. Photosynth 36:565–573CrossRefGoogle Scholar
  19. Fangmeier A, Grüters U, Hertstein U, Sandhage-Hofmann A, Vermehren B, Jäger H-J (1996) Effects of elevated CO2, nitrogen supply and tropospheric ozone on spring wheat. I Growthand yield Environ Pollut 91:381–390Google Scholar
  20. Fangmeier A, Gruters U, Hogy P, Vermehren B, Jäger H-J (1997) Effects of elevated CO2, nitrogen supply, and tropospheric ozone on spring wheat-II. Nutrients (N, P, K, S, Ca, Mg, Fe, Mn, Zn). Environ Pollut 96:43–59PubMedCrossRefGoogle Scholar
  21. Gebauer RLE, Reynolds JF, Strain BR (1996) Allometric relations and growth in Pinus taeda: the effect of elevated CO2 and changing N availability. New Phytol 134:85–93CrossRefGoogle Scholar
  22. Geiger M, Haake V, Ludewig F, Sonnewald U, Stitt M (1999) The nitrate and ammonium nitrate supply have a major influence on the response of photosynthesis, carbon metabolism and nitrogen metabolism and growth to elevated carbon dioxide in tobacco. Plant Cell Environ 22:1177–1199CrossRefGoogle Scholar
  23. Ghosh S, Gepstein S, Heikkila JJ, Dumbroff EB (1988) Use of a scanning densitometer or an ELISA reader for measurement of nanogram amount of protein in crude extracts from biological tissue. Anal Biochem 169:227–233PubMedCrossRefGoogle Scholar
  24. Goldbach HE (1997) A critical review on current hypothesis concerning the role of boron in higher plants: suggestions for further research and methodological requirements. J Trace Microprobe Tech 15:51–91Google Scholar
  25. Gutschick VP (1993) Nutrients-limited growth rates: Roles of nutrient-use efficiency and of adaptation to increase nutrient uptake. J Exp Bot 44:41–51CrossRefGoogle Scholar
  26. Hagedorn F, Landolt W, Tarjan D, Egli P, Bucher JB (2002) Elevated CO2 influences nutrient availability in young beech-spruce communities on two soil types. Oecologia 132:109–117CrossRefGoogle Scholar
  27. Jin CW, Du ST, Chen WW, Li GX, Zhang YS, Zheng SJ (2009) Elevated carbon dioxide improves plant iron nutrition through enhancing the iron-deficiency-induced response under iron limited conditions in tomato. Plant Physiol 150:272–280PubMedCrossRefGoogle Scholar
  28. Kobayashi M, Matoh T, Azuma J (1996) Two chains of rhamnogalacturonan-II are cross-linked by borate-diol ester bonds in higher plant cell walls. Plant Physiol 110:1017–1020PubMedGoogle Scholar
  29. Kouchi H (1977) Rapid cessation of mitosis and elongation of root tip cells of Vicia faba by boron deficiency. Soil Sci Plant Nutr 23:113–118Google Scholar
  30. Kramer PJ, Boyer JS (1995) Water relations of plants and soils. Academic, San DiegoGoogle Scholar
  31. Liu L, King JS, Giarddina CP (2007) Effects of elevated atmospheric CO2 and tropospheric O3 on nutrient dynamics: decomposition of leaf litter in trembling aspen and paper brich communities. Plant Soil 299:65–82CrossRefGoogle Scholar
  32. Lloyd J, Farquhar GD (1996) The CO2 dependence of photosynthesis, plant growth responses to elevated atmospheric CO2 concentrations and their interaction with soil nutrient status. I. General principles and forest ecosystems. Funct Ecol 10:4–32CrossRefGoogle Scholar
  33. Luomala E-M, Laitinen K, Sutinen S, Kellomäki S, Vapaavuori E (2005) Stomatal density, anatomy and nutrient concentrations of Scots pine needles are affected by elevated CO2 and temperature. Plant Cell Environ 28:733–749CrossRefGoogle Scholar
  34. Manderscheid R, Bender J, Jäger H-J, Weigel HJ (1995) Effects of season long CO2 enrichment on cereals: II. Nutrient concentrations and grain quality. Agric Ecosyst Environ 54:175–185CrossRefGoogle Scholar
  35. Marschner H (1995) Mineral nutrition of higher plants. Academic, LondonGoogle Scholar
  36. Matoh T (1997) Boron in plant cell walls. Plant Soil 193:59–70CrossRefGoogle Scholar
  37. McKee IF, Woodward FI (1994) CO2 enrichment responses of wheat: interactions with temperature, nitrate and phosphate. New Phytol 127:447–453CrossRefGoogle Scholar
  38. Mishra S, Hecakathorn S, Barua D, Wang D, Joshi P, Hamilton EW, Frantz J (2008) Interactive effects of elevated CO2 and ozone on leaf thermotolerance in field-grown Glycine max. J Integ Plant Biol 50:1396–1405CrossRefGoogle Scholar
  39. Mishra S, Hecakathorn S, Frantz J, Futong Y, Gray J (2009) Effects of boron deficiency on geranium grown under different nonphotoinhibitory light levels. J Am Soc Hortic Sci 134:183–193Google Scholar
  40. Miwa K, Kamiya T, Fujiwara T (2009) Homeostasis of the structurally important micronutrients, B and Si. Curr Opin Plant Biol 12:307–311PubMedCrossRefGoogle Scholar
  41. Nelson MR (1988) Index to EPA methods. EPA Circ. 901/3-88-01. U.S. Environmental Protection Agency, Washington, DCGoogle Scholar
  42. Norby RJ, O’Neill EG, Luxmoore RJ (1986) Effects of atmospheric CO2enrichment on the growth and mineral nutrition of Quercus alba seedlings in nutrient-poor soil. Plant Physiol 82:83–89PubMedCrossRefGoogle Scholar
  43. O’Neill EG, Luxmoore RJ, Norby RJ (1987) Elevated atmospheric CO2effects on seedling growth nutrient uptake and rhizosphere bacterial populations of Liriodendron tulipifera L. Plant Soil 104:3–11CrossRefGoogle Scholar
  44. Pal M, Karthikeyapandian V, Jain V, Srivastava AC, Raj A, Sengupta UK (2004) Biomass production and nutritional levels of berseem (Trifolium alexandrium) grown under elevated CO2. Agric Ecosyst Environ 101:31–38CrossRefGoogle Scholar
  45. Peñuelas J, Idso SB, Ribas A, Kimball BA (1997) Effects of long-term atmospheric CO2 enrichment on the mineral concentration of Citrus aurantium leaves. New Phytol 135:439–444CrossRefGoogle Scholar
  46. Peñuelas J, Filella I, Tognetti R (2001) Leaf mineral concentrations of Erica arborea, Juniperus communis and Myrtus communis growing in the proximity of natural CO2 spring. Glob Chang Biol 7:291–301CrossRefGoogle Scholar
  47. Pettersson R, McDonald AJS, Stadenberg I (1993) Response of small birch plants (Betula pendula Roth.) to elevated CO2 and nitrogen supply. Plant Cell Environ 16:1115–1121CrossRefGoogle Scholar
  48. Power PP, Woods WG (1997) The chemistry of boron and its speciation in plants. Plant Soil 193:1–13CrossRefGoogle Scholar
  49. Prior SA, Rogers HH, Runion GB, Mauney JR (1994) Effects of free-air CO2 enrichment on cotton root growth. Agric For Meteorol 70:69–86CrossRefGoogle Scholar
  50. Prior SA, Torbert HA, Runion GB, Mullins GL, Rogers HH, Mauney JR (1998) Effects of CO2 enrichment on cotton nutrient dynamics. J Plant Nutr 21:1407–1426CrossRefGoogle Scholar
  51. Reid RJ, Hayes JE, Post A, Stangoulis JCR, Graham RD (2004) A critical analysis of the causes of boron toxicity in plants. Plant Cell Environ 25:1405–1414CrossRefGoogle Scholar
  52. Roberntz P, Stockfors J (1998) Effects of elevated CO2 concentration and nutrition on net photosynthesis, stomatal conductance and needle respiration of field-grown Norway spruce trees. Tree Physiol 18:233–241PubMedGoogle Scholar
  53. Rogers HH, Peterson CM, McCrimmon JN, Cure JD (1992) Response of plant roots to elevated atmospheric carbon dioxide. Plant Cell Environ 15:749–752CrossRefGoogle Scholar
  54. Rogers GS, Payne L, Milham P, Conroy J (1993) Nitrogen and phosphorus requirements of cotton and wheat under changing atmospheric CO2 concentrations. Plant Soil 155(156):231–234CrossRefGoogle Scholar
  55. Rogers GS, Milham PJ, Gillings M, Conroy JP (1996) Sink strength may be the key to growth and nitrogen responses in N-deficient wheat at elevated CO2. Aust J Plant Physiol 23:253–264CrossRefGoogle Scholar
  56. Shorrocks VM (1997) The occurrence and correction of boron deficiency. Plant Soil 193:121–148CrossRefGoogle Scholar
  57. Sicher RC Jr (2005) Interactive effects of inorganic phosphate nutrition and carbon dioxide enrichment on assimilate partitioning in barley roots. Physiol Plant 123:219–226CrossRefGoogle Scholar
  58. Sicher RC, Bunce JA (1999) Photosynthetic enhancement and conductance to water vapor of field-grown Solanum tuberosum (L.) in response to CO2 enrichment. Photosyn Res 62:155–163CrossRefGoogle Scholar
  59. Silvola J, Ahlholm U (1995) Combined effects of CO2concentration and nutrient status on the biomass production and nutrient uptake of birch seedlings (Betula pendula). Plant Soil 169:547–553CrossRefGoogle Scholar
  60. Stitt M, Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell Environ 22:583–621CrossRefGoogle Scholar
  61. Takano J, Noguchi K, Yasumori M, Kobayashi M, Gajdos Z, Miwa K, Hayashi H, Yoneyama T, Fujiwara T (2002) Arabidopsis boron transporter for xylem loading. Nature 420:337–340PubMedCrossRefGoogle Scholar
  62. Takano J, Miwa K, Yuan L, von Wirén N, Fujiwara T (2005) Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc Natl Acad Sci 102:12276–12281PubMedCrossRefGoogle Scholar
  63. Takano J, Wada M, Ludewig U, Schaaf G, von Wirén N, Fujiwara T (2006) The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell 18:1498–1509PubMedCrossRefGoogle Scholar
  64. Tang J, Chen J, Chen X (2006) Response of 12 weedy species to elevated CO2 in low-phosphorus-availability soil. Ecol Res 21:664–670CrossRefGoogle Scholar
  65. Taub DR, Wang X (2008) Why are nitrogen concentrations in plant tissues lower under elevated CO2? A critical examination of the hypotheses. J Integ Plant Biol 50:1365–1374CrossRefGoogle Scholar
  66. Vandermeiren K, Black C, Lawson T, Casanova MA, Ojanperä K (2002) Photosynthetic and stomatal responses of potatoes grown under elevated CO2 and/or O3– results from the European CHIP-programme. Europ J Agron 17:337–352CrossRefGoogle Scholar
  67. Wilson JB (1988) A review of evidence on the control of shoot:root ratio, in relation to models. Ann Bot 61:433–449Google Scholar
  68. Wimmer MA, Baassil ES, Brown PH, Läuchli A (2005) Boron response in wheat is genotype-dependent and related to boron uptake, translocation, allocation, plant phenological development and growth rate. Funct Plant Biol 32:507–515CrossRefGoogle Scholar
  69. Ziska LH (2003) The impact of nitrogen supply on the potential response of a noxious, invasive weed, Canada thistle (Cirsium arvense) to recent increases in atmospheric carbon dioxide. Physiol Plant 119:105–112CrossRefGoogle Scholar
  70. Ziska LH, Weerakoon W, Namuco OS, Pamplona R (1996) The influence of nitrogen on the elevated CO2 response in field grown rice. Aust J Plant Physiol 23:45–52CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Sasmita Mishra
    • 1
  • Scott A. Heckathorn
    • 1
  • Jonathan M. Frantz
    • 2
  1. 1.Department of Environmental SciencesUniversity of ToledoToledoUSA
  2. 2.USDA-ARSUniversity of ToledoToledoUSA

Personalised recommendations