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.
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Abbreviations
- AMT:
-
Ammonium transporter
- N:
-
Nitrogen
- NRT:
-
Nitrate transporter
References
Bates TR, Lynch JP (2001) Root hairs confer a competitive advantage under low phosphorus availability. Plant Soil 236:243–250
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 61:2293–2302
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 346:1–14
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 134:67–80
Foehse D, Jungk A (1983) Influence of phosphate and nitrate supply on root hair formation of rape, spinach and tomato plants. Plant Soil 74:359–368
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 26:1759–1766
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 124:425–430
Ho CH, Lin SH, Hu HC, Tsay YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194
Jones VA, Dolan L (2012) The evolution of root hairs and rhizoids. Ann Bot 110:205–212
Jungk A (2001) Root hairs and the acquisition of plant nutrients from soil. J Plant Nutr Soil Sci 164:121–129
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 62:2915–2924
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 142:1075–1086
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 18:927–937
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 21:3610–3622
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 22:3621–3633
Ma Z, Bielenberg DG, Brown KM, Lynch JP (2001) Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant Cell Environ 24:459–467
Masucci JD, Schiefelbein JW (1994) The rhd6 mutation of Arabidopsis thaliana alters root-hair initiation through an auxin- and ethylene-associated process. Plant Physiol 106:1335–1346
Muday GK, Rahman A, Binder BM (2012) Auxin and ethylene: collaborators or competitors? Trends Plant Sci 17:181–195
Müller M, Schmidt W (2004) Environmentally induced plasticity of root hair development in Arabidopsis. Plant Physiol 134:409–419
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 16:2433–2447
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 47:912–918
Piepho HP, Büchse A, Emrich K (2003) A Hitchhiker’s guide to mixed models for randomized experiments. J Agron Crop Sci 189:310–322
Pitts RJ, Cernac A, Estelle M (1998) Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J 16:553–560
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 130:1908–1917
Robinson D, Rorison IH (1987) Root hairs and plant growth at low nitrogen availabilities. New Phytol 107:681–693
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 110:15133–15138
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:e75452
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:e0120604
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 59:3453–3464
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 42:239–251
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 19:2636–2652
Zhang YJ, Lynch JP, Brown KM (2003) Ethylene and phosphorus availability have interacting yet distinct effects on root hair development. J Exp Bot 54:2351–2361
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.
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Vatter, T., Neuhäuser, B., Stetter, M. et al. Regulation of length and density of Arabidopsis root hairs by ammonium and nitrate. J Plant Res 128, 839–848 (2015). https://doi.org/10.1007/s10265-015-0733-8
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DOI: https://doi.org/10.1007/s10265-015-0733-8