Skip to main content
Log in

The effect of boron availability, CO2, and irradiance on relative accumulation of the major boron transport proteins, BOR1 and NIP5;1

  • Original papers
  • Published:
Biologia Plantarum

Abstract

Boron (B) is an essential plant micronutrient. Two major B-transport proteins have been recently identified and partially characterized: BOR1, a high-affinity B efflux transporter involved in xylem loading, and NIP5;1, a plasma-membrane boric-acid channel involved in B uptake. To date, studies of these B transporters have investigated their expression individually (mainly as mRNA), and only in response to variation in B availability (mostly B deficiency); the influence of other factors, such as plant resource status, has not been studied. To address this, we grew geranium (Pelargonium × hortorum cv. Maverick White) plants under ambient or elevated CO2 concentration, different sub-saturating irradiances, and different B availability. For comparison we also grew three other species (Arabidopsis thaliana, Azolla caroliniana, and Hordeum vulgare) under broad range of B supply. Relative accumulation of BOR1 and NIP5;1 proteins were measured using protein-specific antibodies and Western blotting or ELISA. Elevated CO2 significantly increased content of NIP5;1, while increases in irradiance increased BOR1 content, but decreased NIP5;1 content. Across species, content of both transporters often decreased with increasing B availability, but sometimes remained unchanged or even increased, depending on CO2, irradiance, species, or transporter. Content of BOR1 and NIP5;1 was correlated with root proteins, B content, and sugar content (for high CO2 only), as well as B uptake, but CO2 and irradiance often affected these relationships. Thus, relative accumulation of BOR1 and NIP5;1 is influenced not only by B content, as expected, but by other environmental factors as well.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

BOR1:

boron transporter protein 1

CE:

carboxylation efficiency of photosynthesis

EDTA:

ethylenediaminetetraacetic acid

NIP:

NOD26-like intrinsic proteins

PAR:

photosynthetically active radiation

pNPP:

para-nitrophenylphosphate

References

  • An, J., Liu, Y., Yang, C., Zhou, G., Wei, Q., Peng, S.: Isolation and expression analysis of CiNIP5, a citrus boron transport gene involved in tolerance to boron deficiency. — Sci. Hort. 142: 149–154, 2012.

    Article  CAS  Google Scholar 

  • Bassiri Rad, H.: Kinetics of nutrient uptake by roots: responses to global change. — New Phytol. 147: 155–169, 2000.

    Article  CAS  Google Scholar 

  • Blevins, D.G., Lukaszewski, K.M.: Boron in plant structure and function. — Annu. Rev. Plant Physiol. Plant mol. Biol. 49: 481–500, 1998.

    Article  CAS  PubMed  Google Scholar 

  • Bolaños, L., Lukaszewski, K., Bonilla, I., Blevins, D.: Why boron? — Plant Physiol. Biochem. 42: 907–912, 2004.

    Article  PubMed  Google Scholar 

  • Brown, H.P., Bellaloui, N., Wimmer, A.M., Bassil, S.E., Ruiz, J., Hu, H., Pfeffer, H., Dannel, F.: Boron in plant biology. — Plant Biol. 4: 205–223, 2002.

    Article  CAS  Google Scholar 

  • Chen, M., Mishra, S., Heckathorn, S.A, Frantz, J.M., Krause, C.: Proteomic analysis of Arabidopsis thaliana leaves in response to acute boron deficiency and toxicity reveals effects on photosynthesis, carbohydrate metabolism, and protein synthesis. — J. Plant Physiol. 171: 235–242, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Cheng, L., Tang, X., Vance, C.P., White, P.J., Zhang, F., Shen, J.: Interactions between light intensity and phosphorus nutrition affect the phosphate-mining capacity of white lupin (Lupinus albus L.). — J. exp. Bot. 65: 2995–3003, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dannel, F., Pfeffer, H., Römheld, V.: Update on boron in higher plants - uptake, primary translocation and compartmentation. — Plant Biol. 4: 193–204, 2002.

    Article  CAS  Google Scholar 

  • Dordas, C., Brown, P.H.: Evidence for channel mediated transport of boric acid in squash (Cucurbita pepo). — Plant Soil 235: 95–103, 2001.

    Article  CAS  Google Scholar 

  • Dordas, C., Chrispeels, M.J., Brown, P.H.: Permeability and channel-mediated transport of boric acid across membrane vesicles isolated from squash roots. — Plant Physiol. 124: 1349–1362, 2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A., Smith, F.: Colorimetric method for determination of sugars and related substances. — Anal. Chem. 28: 350–356, 1956.

    Article  CAS  Google Scholar 

  • Feng, H., Yan, M., Fan, X., Li, B., Shen, Q., Miller, A.J., Xu, G.: Spatial expression and regulation of rice high-affinity nitrate transporters by nitrogen and carbon status. — J. exp. Bot. 62: 2319–2332, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Ghosh, S., Gepstein, S., Heikkila, J.J., Dumbroff, E.B.: 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: 227–233, 1988.

    Article  CAS  PubMed  Google Scholar 

  • Goldbach, H.E.: 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: 51–91, 1997.

    CAS  Google Scholar 

  • Hayes, J.E., Reid, R.J.: Boron tolerance in barley is mediated by efflux of boron from the roots. — Plant Physiol. 136: 3376–3382, 2004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hurkman, W.J., Tanaka, C.K.: Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. — Plant Physiol. 81: 802–806, 1986.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin, C.W., Du, S.T., Chen, W.W., Li, G.X., Zhang, Y.S., Zheng, S.J.: Elevated carbon dioxide improves plant iron nutrition through enhancing the iron-deficiency-induced response under iron limited conditions in tomato. — Plant Physiol. 150: 272–280, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lambers, H., Chapin, F.S., Pons, T. Plant Physiological Ecology. - Springer, New York 2008.

    Book  Google Scholar 

  • Lekshmy, S., Jain, V., Khetarpal, S., Pandey, R., Singh, R.: Effect of elevated carbon dioxide on kinetics of nitrate uptake in wheat roots. — Indian J. Plant Physiol. 14: 16–22, 2009.

    CAS  Google Scholar 

  • Marschner, H.: Mineral Nutrition of Higher Plants. - Academy Press, London 1995.

    Google Scholar 

  • Matoh, T.: Boron in plant cell walls. — Plant Soil 193: 59–70, 1997.

    Article  CAS  Google Scholar 

  • Mishra, S., Heckathorn, S., Frantz, J., Yu, F., Gray, J.: Effects of boron deficiency on geranium grown under different nonphotoinhibitory light levels. — J. amer. Soc. hort. Sci. 134: 183–193, 2009.

    Google Scholar 

  • Mishra, S., Heckathorn, S.A., Frantz, J.M.: Elevated CO2 affects plant responses to variation in boron availability. — Plant Soil 350: 117–130, 2012.

    Article  CAS  Google Scholar 

  • Mishra, S., Heckathorn, S.A., Frantz, J., Krause, C.: Effects of growth light level on tolerance of geranium (Pelargonium ×hortorum) to sub-and supra-optimal boron supply. — Biol. Plant. 58: 582–588, 2014.

    Article  CAS  Google Scholar 

  • Miwa, K., Takano, J., Omori, H., Seki, M., Shinozaki, K., Fujiwara, T.: Plants tolerant of high boron levels. — Science 318: 1417, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Miwa, K., Tanaka, M., Kamiya, T., Fujiwara, T.: Molecular mechanism of boron transport in plants: involvement of Arabidopsis NIP5;1 and NIP6;1. - In: Jahn, T.P., Bienert, G.P. (ed.): MPIs and their Role in Exchange of Metalloids. Pp. 83–96. Landes Biosciences and Springer, New York 2010.

    Chapter  Google Scholar 

  • Nable, O.R., Bañuelos, S.G., Paull, J.G.: Boron toxicity. — Plant Soil 193: 181–198, 1997.

    Article  CAS  Google Scholar 

  • Nakagawa, Y., Hanaoka, H., Kobayashi, M., Miyoshi, K., Miwa, K., Fujiwara, T.: Cell-type specificity of the expression of OsBOR1, a rice efflux boron transporter gene, is regulated in-response to boron availability for efficient boron uptake and xylem loading. — Plant Cell 19: 2624–2635, 2007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Neill, M.A., Ishii, T., Albersheim, P., Darvill, A.G.: Rhamnogalacturonan. II. Structure and function of a borate cross-linked cell wall pectic polysaccharide. — Annu. Rev. Plant Biol. 55: 109–139, 2004.

    Article  PubMed  Google Scholar 

  • Pallotta, M., Schnurbusch, T., Hayes, J., Hay, A., Baumann, U., Paull, J., Langridge, P., Sutton, T.: Molecular basis of adaptation to high soil boron in wheat landraces and elite cultivars. — Nature 514: 88–91, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Reid, R.: Identification of boron transporter genes likely to be responsible for tolerance to boron toxicity in wheat and barley. — Plant Cell Physiol. 48: 1673–1678, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Reid, R.: Understanding the boron transport network in plants. — Plant Soil 385: 1–13, 2014.

    Article  CAS  Google Scholar 

  • Schnurbusch, T., Hayes, J., Hrmova, M., Baumann, U., Ramesh, S.A., Tyerman, S.D., Langridge, P., Sutton, T.: Boron toxicity tolerance in barley through reduced expression of the multifunctional aquaporin HvNip2,1. — Plant Physiol. 153: 1760–1715, 2010.

    Article  Google Scholar 

  • Shorrocks, V.M.: The occurrence and correction of boron deficiency. — Plant Soil 193: 121–148, 1997.

    Article  CAS  Google Scholar 

  • Sutton, T., Baumann, U., Hayes, J., Collins, N.C., Shi, B.J., Schnurbusch, T., Hay, A., Mayo, G., Pallotta, M., Tester, M., Langridge. P.: Boron-toxicity tolerance in barley arising from efflux transporter amplification. — Science 318: 1446–1449, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Takada, S., Miwa, K., Omori, H., Fujiwara, T., Naito, S., Takanao, J.: Improved tolerance to boron deficiency by enhanced expression of the boron transporter BOR2. — Soil Sci. Plant Nutr. 60: 341–348, 2014.

    Article  CAS  Google Scholar 

  • Takano, J., Miwa, K., Yuan, L., Von Wirén, N., Fujiwara, T.: Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. — Proc. nat. Acad. Sci. USA 102: 12276–122181, 2005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takano, J., Miwa, K., Fujiwara, T.: Boron transport mechanisms: collaboration of channels and transporters. — Trends Plant Sci. 13: 451–457, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Takano, J., Noguchi, K., Yasumori, M., Kobayashi, M., Gajdos, Z., Miwa, K., Hayashi, H., Yoneyama, T., Fujiwara, T.: Arabidopsis boron transporter for xylem loading. — Nature 420: 337–340, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Takano, J., Tanaka, M., Toyoda, A., Miwa, K., Kasai, K., Fuji, K., Onouchi, H., Naito, S., Fujiwara, T.: Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. — Proc. nat. Acad. Sci. USA 107: 5220–5225, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takano, J., Wada, M., Ludewig, U., Schaaf, G., Von Wirén, N., Fujiwara, T.: The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. — Plant Cell 18: 1498–1509, 2006.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tanaka, M., Wallace, I.S., Takano, J., Roberts, D.M., Fujiwara, T.: NIP6,1 is a boric acid channel for preferential transport of boron to growing shoot tissues in Arabidopsis. — Plant Cell 20: 2860–2875, 2008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka, M., Takano, J., Chiba, Y., Lombardo, F., Ogasawara, Y., Onouchi, H., Naito, S., Fujiwara, T.: Boron-dependent degradation of NIP5;1 mRNA for acclimation to excess boron conditions in Arabidopsis. — Plant Cell 23: 3547–3559, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taub, D.R., Wang, X.: Why are nitrogen concentrations in plant tissues lower under elevated CO2? A critical examination of the hypotheses. — J. Integr. Plant Biol. 50: 1365–1374, 2008.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. Mishra.

Additional information

Acknowledgements: This research was supported by the U.S. Department of Agriculture, Agricultural Research Service (SCA 58-3607-9-741 to Scott Heckathorn). The authors thank Douglas Sturtz, Alycia Pittenger, and Russ Friedrich for assistance. Mention of proprietary products or company is included for the reader’s convenience and does not imply any endorsement or preferential treatment by USDA/ARS.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mishra, S., Heckathorn, S.A., Frantz, J.M. et al. The effect of boron availability, CO2, and irradiance on relative accumulation of the major boron transport proteins, BOR1 and NIP5;1. Biol Plant 62, 121–128 (2018). https://doi.org/10.1007/s10535-017-0744-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-017-0744-5

Additional key words

Navigation