Journal of Plant Research

, Volume 128, Issue 5, pp 839–848 | Cite as

Regulation of length and density of Arabidopsis root hairs by ammonium and nitrate

  • Thomas Vatter
  • Benjamin Neuhäuser
  • Markus Stetter
  • Uwe Ludewig
Regular Paper

Abstract

Root hairs expand the effective root surface to increase the uptake of nutrients and water from the soil. Here the local effects of the two major nitrogen sources, ammonium and nitrate, on root hairs were investigated using split plates. In three contrasting accessions of A. thaliana, namely Col-0, Tsu-0 and Sha, root hairs were differentially affected by the nitrogen forms and their concentration. Root hairs in Sha were short in the absence of nitrate. In Col-0, hair length was moderately decreased with increasing nitrate or ammonium. In all accessions, the root hair density was insensitive to 1,000-fold changes in the ammonium concentrations, when supplied locally as the exclusive nitrogen form. In contrast, the root hair density generally increased with nitrate as the exclusive local nitrogen source. The nitrate sensitivity was reduced at mM concentrations in a loss-of-function mutant of the nitrate transporter and sensor gene NRT1;1 (NPF6.3). Little differences with respect to ammonium were found in a mutant lacking four high affinity AMT-type ammonium transporters, but interestingly, the response to high nitrate was reduced and may indicate a general defect in nitrogen signaling in that mutant. Genetic diversity and the presence of the nitrogen transceptor NRT1;1 explain heterogeneity in the responses of root hairs to different nitrogen forms in Arabidopsis accessions.

Keywords

Ammonium Arabidopsis Nitrate Nitrogen transporter Nutrient sensing Root hair 

Abbreviations

AMT

Ammonium transporter

N

Nitrogen

NRT

Nitrate transporter

Notes

Acknowledgments

This work was partially financed by a Hohenheim-Rehovot partnership grant to U. L. We thank the Arabidopsis stock center for the nrt1;1 mutant and Dr. N von Wiren for the qko mutant.

References

  1. Bates TR, Lynch JP (2001) Root hairs confer a competitive advantage under low phosphorus availability. Plant Soil 236:243–250CrossRefGoogle Scholar
  2. Chardon F, Barthelemy J, Daniel-Vedele F, Masclaux-Daubresse C (2010) Natural variation of nitrate uptake and nitrogen use efficiency in Arabidopsis thaliana cultivated with limiting and ample nitrogen supply. J Exp Bot 61:2293–2302CrossRefPubMedGoogle Scholar
  3. Datta S, Kim CM, Pernas M, Pires ND, Proust H, Tam T, Vijayakumar P, Dolan L (2011) Root hairs: development, growth and evolution at the plant-soil interface. Plant Soil 346:1–14CrossRefGoogle Scholar
  4. Fizames C, Munos S, Cazettes C, Nacry P, Boucherez J, Gaymard F, Piquemal D, Delorme V, Commes T, Doumas P, Cooke R, Marti J, Sentenac H, Gojon A (2004) The Arabidopsis root transcriptome by serial analysis of gene expression. Gene identification using the genome sequence. Plant Physiol 134:67–80PubMedCentralCrossRefPubMedGoogle Scholar
  5. Foehse D, Jungk A (1983) Influence of phosphate and nitrate supply on root hair formation of rape, spinach and tomato plants. Plant Soil 74:359–368CrossRefGoogle Scholar
  6. Gahoonia TS, Nielsen NE (2003) Phosphorus (P) uptake and growth of a root hairless barley mutant (bald root barley, brb) and wild type in low- and high-P soils. Plant Cell Environ 26:1759–1766CrossRefGoogle Scholar
  7. Hachiya T, Mizokami Y, Miyata K, Tholen D, Watanabe CK, Noguchi K (2011) Evidence for a nitrate-independent function of the nitrate sensor NRT1.1 in Arabidopsis thaliana. J Plant Res 124:425–430CrossRefPubMedGoogle Scholar
  8. Ho CH, Lin SH, Hu HC, Tsay YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194CrossRefPubMedGoogle Scholar
  9. Jones VA, Dolan L (2012) The evolution of root hairs and rhizoids. Ann Bot 110:205–212PubMedCentralCrossRefPubMedGoogle Scholar
  10. Jungk A (2001) Root hairs and the acquisition of plant nutrients from soil. J Plant Nutr Soil Sci 164:121–129CrossRefGoogle Scholar
  11. Kapulnik Y, Resnick N, Mayzlish-Gati E, Kaplan Y, Wininger S, Hershenhorn J, Koltai H (2011) Strigolactones interact with ethylene and auxin in regulating root-hair elongation in Arabidopsis. J Exp Bot 62:2915–2924CrossRefPubMedGoogle Scholar
  12. Krouk G, Tillard P, Gojon A (2006) Regulation of the high-affinity NO3—uptake system by NRT1.1-mediated NO3—demand signaling in Arabidopsis. Plant Physiol 142:1075–1086PubMedCentralCrossRefPubMedGoogle Scholar
  13. Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinska K, Mounier E, Hoyerova K, Tillard P, Leon S, Ljung K, Zazimalova E, Benkova E, Nacry P, Gojon A (2010) Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev Cell 18:927–937CrossRefPubMedGoogle Scholar
  14. Lanquar V, Loque D, Hormann F, Yuan L, Bohner A, Engelsberger WR, Lalonde S, Schulze WX, von Wiren N, Frommer WB (2009) Feedback inhibition of ammonium uptake by a phospho-dependent allosteric mechanism in Arabidopsis. Plant Cell 21:3610–3622PubMedCentralCrossRefPubMedGoogle Scholar
  15. Lima JE, Kojima S, Takahashi H, von Wiren N (2010) Ammonium triggers lateral root branching in Arabidopsis in an AMMONIUM TRANSPORTER1;3-dependent manner. Plant Cell 22:3621–3633PubMedCentralCrossRefPubMedGoogle Scholar
  16. Ma Z, Bielenberg DG, Brown KM, Lynch JP (2001) Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant Cell Environ 24:459–467CrossRefGoogle Scholar
  17. Masucci JD, Schiefelbein JW (1994) The rhd6 mutation of Arabidopsis thaliana alters root-hair initiation through an auxin- and ethylene-associated process. Plant Physiol 106:1335–1346PubMedCentralPubMedGoogle Scholar
  18. Muday GK, Rahman A, Binder BM (2012) Auxin and ethylene: collaborators or competitors? Trends Plant Sci 17:181–195CrossRefPubMedGoogle Scholar
  19. Müller M, Schmidt W (2004) Environmentally induced plasticity of root hair development in Arabidopsis. Plant Physiol 134:409–419PubMedCentralCrossRefPubMedGoogle Scholar
  20. Munos S, Cazettes C, Fizames C, Gaymard F, Tillard P, Lepetit M, Lejay L, Gojon A (2004) Transcript profiling in the chl1-5 mutant of Arabidopsis reveals a role of the nitrate transporter NRT1.1 in the regulation of another nitrate transporter, NRT2.1. Plant Cell 16:2433–2447PubMedCentralCrossRefPubMedGoogle Scholar
  21. North KA, Ehlting B, Koprivova A, Rennenberg H, Kopriva S (2009) Natural variation in Arabidopsis adaptation to growth at low nitrogen conditions. Plant Physiol Biochem 47:912–918CrossRefPubMedGoogle Scholar
  22. Piepho HP, Büchse A, Emrich K (2003) A Hitchhiker’s guide to mixed models for randomized experiments. J Agron Crop Sci 189:310–322CrossRefGoogle Scholar
  23. Pitts RJ, Cernac A, Estelle M (1998) Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J 16:553–560CrossRefPubMedGoogle Scholar
  24. Rahman A, Hosokawa S, Oono Y, Amakawa T, Goto N, Tsurumi S (2002) Auxin and ethylene response interactions during Arabidopsis root hair development dissected by auxin influx modulators. Plant Physiol 130:1908–1917PubMedCentralCrossRefPubMedGoogle Scholar
  25. Robinson D, Rorison IH (1987) Root hairs and plant growth at low nitrogen availabilities. New Phytol 107:681–693CrossRefGoogle Scholar
  26. Rosas U, Cibrian-Jaramillo A, Ristova D, Banta JA, Gifford ML, Fan AH, Zhou RW, Kim GJ, Krouk G, Birnbaum KD, Purugganan MD, Coruzzi GM (2013) Integration of responses within and across Arabidopsis natural accessions uncovers loci controlling root systems architecture. Proc Natl Acad Sci USA 110:15133–15138PubMedCentralCrossRefPubMedGoogle Scholar
  27. Savage N, Yang TJ, Chen CY, Lin KL, Monk NA, Schmidt W (2013) Positional signaling and expression of ENHANCER OF TRY AND CPC1 are tuned to increase root hair density in response to phosphate deficiency in Arabidopsis thaliana. PLoS One 8:e75452PubMedCentralCrossRefPubMedGoogle Scholar
  28. Stetter MG, Schmid K, Ludewig U (2015) Uncovering Genes and ploidy involved in the high diversity in root hair density, length and response to local scarce phosphate in Arabidopsis thaliana. PLoS One 10:e0120604PubMedCentralCrossRefPubMedGoogle Scholar
  29. Yang TJ, Perry PJ, Ciani S, Pandian S, Schmidt W (2008) Manganese deficiency alters the patterning and development of root hairs in Arabidopsis. J Exp Bot 59:3453–3464CrossRefPubMedGoogle Scholar
  30. Yang H, von der Fecht-Bartenbach J, Friml J, Lohmann JU, Neuhäuser B, Ludewig U (2015) Auxin-modulated root growth inhibition in Arabidopsis thaliana seedlings with ammonium as the sole nitrogen source. Funct Plant Biol 42:239–251Google Scholar
  31. Yuan L, Loque D, Kojima S, Rauch S, Ishiyama K, Inoue E, Takahashi H, von Wiren N (2007) The organization of high-affinity ammonium uptake in Arabidopsis roots depends on the spatial arrangement and biochemical properties of AMT1-type transporters. Plant Cell 19:2636–2652PubMedCentralCrossRefPubMedGoogle Scholar
  32. Zhang YJ, Lynch JP, Brown KM (2003) Ethylene and phosphorus availability have interacting yet distinct effects on root hair development. J Exp Bot 54:2351–2361CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2015

Authors and Affiliations

  • Thomas Vatter
    • 1
  • Benjamin Neuhäuser
    • 1
  • Markus Stetter
    • 1
  • Uwe Ludewig
    • 1
  1. 1.Institute of Crop Science, Nutritional Crop PhysiologyUniversity of HohenheimStuttgartGermany

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