Natural variation of Arabidopsis thaliana root architecture in response to nitrate availability

References

• Bouguyon, E., Brun, F. D. Meynard, M. Kubeš, M. Pervent, S. Leran, B. Lacombe, G. Krouk, E. Guiderdoni, E. Zažímalová, K., et al. 2015. Multiple mechanisms of nitrate sensing by Arabidopsis nitrate transceptor NRT1.1. Nature Plants 1 (3):15015. doi: 10.1038/nplants.2015.15.
   PubMed Web of Science ®Google Scholar
• Castaings, L., C. Marchive, C. Meyer, and A. Krapp. 2011. Nitrogen signalling in Arabidopsis: How to obtain insights into a complex signalling network. Journal of Experimental Botany 62 (4):1391–1397. doi: 10.1093/jxb/erq375.
   PubMed Web of Science ®Google Scholar
• Cataldo, D. A., M. Maroon, L. E. Schrader, and V. L. Youngs. 1975. Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Communications in Soil Science and Plant Analysis 6 (1):71–80. doi: 10.1080/00103627509366547.
   Web of Science ®Google Scholar
• Chardon, F., J. Barthélémy, F. Daniel-Vedele, and C. Masclaux-Daubresse. 2010. Natural variation of nitrate uptake and nitrogen use efficiency in Arabidopsis thaliana cultivated with limiting and ample nitrogen supply. Journal of Experimental Botany 61 (9):2293–2302. doi: 10.1093/jxb/erq059.
   PubMed Web of Science ®Google Scholar
• Crawford, N. M. 1995. Nitrate: nutrient and signal for plant growth. The Plant Cell 7 (7):859–868. doi: 10.1105/tpc.7.7.859
   PubMed Web of Science ®Google Scholar
• De Pessemier, J., F. Chardon, M. Juraniec, P. Delaplace, and C. Hermans. 2013. Natural variation of the root morphological response to nitrate supply in Arabidopsis thaliana. Mechanisms of Development 130 (1):45–53. doi: 10.1016/j.mod.2012.05.010.
   PubMed Web of Science ®Google Scholar
• Desnos, T. 2008. Root branching responses to phosphate and nitrate. Current Opinion in Plant Biology 11 (1):82–87. doi: 10.1016/j.pbi.2007.10.003
   PubMed Web of Science ®Google Scholar
• Drechsler, N., Y. Zheng, A. Bohner, B. Nobmann, N. von Wirén, R. Kunze, and C. Rausch. 2015. Nitrate-dependent control of shoot K homeostasis by the nitrate transporter1/peptide transporter family member NPF7.3/NRT1.5 and the stelar K + outward rectifier SKOR in Arabidopsis. Plant Physiology 169 (4):2832–2847. doi: 10.1104/pp.15.01152
   PubMed Web of Science ®Google Scholar
• Forde, B. G. 2014. Nitrogen signalling pathways shaping root system architecture: An update. Current Opinion in Plant Biology 21:30–36. doi: 10.1016/j.pbi.2014.06.004.
   PubMed Web of Science ®Google Scholar
• Forde, B. G., and P. I. A. Walch-Liu. 2009. Nitrate and glutamate as environmental cues for behavioural responses in plant roots. Plant, Cell & Environment 32 (6):682–693. doi: 10.1111/j.1365-3040.2008.01927.x
   PubMed Web of Science ®Google Scholar
• Giehl, R. F., and N. von Wiren. 2014. Root nutrient foraging. Plant Physiology 166 (2):509–517. doi: 10.1104/pp.114.245225.
   PubMed Web of Science ®Google Scholar
• Giehl, R. F. H., J. E. Lima, and N. von Wirén. 2012. Localized iron supply triggers lateral root elongation in Arabidopsis by altering the AUX1-mediated auxin distribution. The Plant Cell 24 (1):33–49. doi: 10.1105/tpc.111.092973.
   PubMed Web of Science ®Google Scholar
• Good, A. G., A. K. Shrawat, and D. G. Muench. 2004. Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends in Plant Science 9 (12):597–605. doi: 10.1016/j.tplants.2004.10.008.
   PubMed Web of Science ®Google Scholar
• Guan, P. Z., R. C. Wang, P. Nacry, G. Breton, S. A. Kay, J. L. Pruneda-Paz, A. Davani, and N. M. Crawford. 2014. Nitrate foraging by Arabidopsis roots is mediated by the transcription factor TCP20 through the systemic signaling pathway. Proceedings of the National Academy of Sciences 111 (42):15267–15272. doi: 10.1073/pnas.1411375111.
   PubMed Web of Science ®Google Scholar
• Hermans, C., J. P. Hammond, P. J. White, and N. Verbruggen. 2006. How do deficiencies of essential mineral elements alter biomass allocation. Trends Plant Science 11 (12):610–617. doi: 10.1016/j.tplants.2006.10.007.
   PubMed Web of Science ®Google Scholar
• Ikram, S., M. Bedu, F. Daniel-Vedele, S. Chaillou, and F. Chardon. 2012. Natural variation of Arabidopsis response to nitrogen availability. Journal of Experimental Botany 63 (1):91–105. doi: 10.1093/jxb/err244.
   PubMed Web of Science ®Google Scholar
• Kellermeier, F., P. Armengaud, T. J. Seditas, J. Danku, D. E. Salt, and A. Amtmann. 2014. Analysis of the root system architecture of Arabidopsis provides a quantitative readout of crosstalk between nutritional signals. The Plant Cell 26 (4):1480–1496. doi: 10.1105/tpc.113.122101.
   PubMed Web of Science ®Google Scholar
• Kiba, T., and A. Krapp. 2016. Plant nitrogen acquisition under low availability: regulation of uptake and root architecture. Plant and Cell Physiology 57 (4):707–714. doi: 10.1093/pcp/pcw052.
   PubMed Web of Science ®Google Scholar
• Kobayashi, Y., T. Ikka, K. Kimura, O. Yasuda, and H. Koyama. 2007. Characterisation of lanthanum toxicity for root growth of Arabidopsis thaliana from the aspect of natural genetic variation. Functional Plant Biology 34 (11):984–994. doi: 10.1071/FP07133.
   Web of Science ®Google Scholar
• Krouk, G., Lacombe, B. A. Bielach, F. Perrine-Walker, K. Malinska, E. Mounier, K. Hoyerova, P. Tillard, S. Leon, K. Ljung, E., et al. 2010. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Developmental Cell 18 (6):927–937. doi: 10.1016/j.devcel.2010.05.008.
   PubMed Web of Science ®Google Scholar
• López-Bucio, J., A. Cruz-Ramı́rez, and, and L. Herrera-Estrella. 2003. The role of nutrient availability in regulating root architecture. Current Opinion in Plant Biology 6 (3):280–287. doi: 10.1016/S1369-5266(03)00035-9.
   PubMed Web of Science ®Google Scholar
• Lemaître, T., L. Gaufichon, S. Boutet-Mercey, A. Christ, and C. Masclaux-Daubresse. 2008. Enzymatic and metabolic diagnostic of nitrogen deficiency in Arabidopsis thaliana wassileskija accession. Plant and Cell Physiology 49 (7):1056–1065. doi: 10.1093/pcp/pcn081.
   PubMed Web of Science ®Google Scholar
• Linkohr, B. I., L. C. Williamson, A. H. Fitter, and H. M. Ottoline Leyser. 2002. Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. The Plant Journal 29 (6):751–760. doi: 10.1046/j.1365-313X.2002.01251.x.
   PubMed Web of Science ®Google Scholar
• Loudet, O., S. Chaillou, P. Merigout, J. Talbotec, and F. Daniel-Vedele. 2003. Quantitative trait loci analysis of nitrogen use efficiency in Arabidopsis. Plant Physiology 131 (1):345–358. doi: 10.1104/pp.102.010785.
   PubMed Web of Science ®Google Scholar
• Lynch, J. P. 2013. Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Annals of Botany 112 (2):347–357. doi: 10.1093/aob/mcs293
   PubMed Web of Science ®Google Scholar
• Masclaux-Daubresse, C., and F. Chardon. 2011. Exploring nitrogen remobilization for seed filling using natural variation in Arabidopsis thaliana. Journal of Experimental Botany 62 (6):2131–2142. doi: 10.1093/jxb/erq405.
   PubMed Web of Science ®Google Scholar
• Masclaux-Daubresse, C., F. Daniel-Vedele, J. Dechorgnat, F. Chardon, L. Gaufichon, and A. Suzuki. 2010. Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Annals of Botany 105 (7):1141–1157. doi: 10.1093/aob/mcq028.
   PubMed Web of Science ®Google Scholar
• Mounier, E., M. Pervent, K. Ljung, A. Gojon, and P. Nacry. 2014. Auxin-mediated nitrate signalling by NRT1.1 participates in the adaptive response of Arabidopsis root architecture to the spatial heterogeneity of nitrate availability. Plant, Cell & Environment 37 (1):162–174. doi: 10.1111/pce.12143.
   PubMed Web of Science ®Google Scholar
• North, K. A., B. Ehlting, A. Koprivova, H. Rennenberg, and S. Kopriva. 2009. Natural variation in Arabidopsis adaptation to growth at low nitrogen conditions. Plant Physiology and Biochemistry 47 (10):912–918. doi: 10.1016/j.plaphy.2009.06.009.
   PubMed Web of Science ®Google Scholar
• Péret, B., B. D. Rybel, I. Casimiro, E. Benková, R. Swarup, L. Laplaze, T. Beeckman, and M. J. Bennett. 2009. Arabidopsis lateral root development: an emerging story. Trends in Plant Science 14 (7):399–408. doi: 10.1016/j.tplants.2009.05.002
   PubMed Web of Science ®Google Scholar
• Poorter, H., K. J. Niklas, P. B. Reich, J. Oleksyn, P. Poot, and L. Mommer. 2012. Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytologist 193 (1):30–50. doi: 10.1111/j.1469-8137.2011.03952.x.
   PubMed Web of Science ®Google Scholar
• Rauh, B. L., C. Basten, and E. S. Buckler. 2002. Quantitative trait loci analysis of growth response to varying nitrogen sources in Arabidopsis thaliana. Theoretical and Applied Genetics 104 (5):743–750. doi: 10.1007/s00122-001-0815-y.
   PubMed Web of Science ®Google Scholar
• Richard-Molard, C., A. Krapp, F. Brun, B. Ney, F. Daniel-Vedele, and S. Chaillou. 2008. Plant response to nitrate starvation is determined by N storage capacity matched by nitrate uptake capacity in two Arabidopsis genotypes. Journal of Experimental Botany 59 (4):779–791. doi: 10.1093/jxb/erm363.
   PubMed Web of Science ®Google Scholar
• Ruffel, S., G. Krouk, D. Ristova, D. Shasha, K. D. Birnbaum, and G. M. Coruzzi. 2011. Nitrogen economics of root foraging: Transitive closure of the nitrate–cytokinin relay and distinct systemic signaling for N supply vs. demand. Proceedings of the National Academy of Sciences of the United States of America 108 (45):18524–18529. doi: 10.1073/pnas.1108684108.
   PubMed Web of Science ®Google Scholar
• Tian, H. Y., I. de Smet, and Z. H. Ding. 2014. Shaping a root system: regulating lateral versus primary root growth. Trends in Plant Science 19 (7):426–431. doi: 10.1016/j.tplants.2014.01.007.
   PubMed Web of Science ®Google Scholar
• Vendrell, P. F., and J. Zupancic. 1990. Determination of soil nitrate by transnitration of salicylic acid. Communications in Soil Science and Plant Analysis 21 (13–16):1705–1713. doi: 10.1080/00103629009368334.
   Web of Science ®Google Scholar
• Vidal, E. A., V. Araus, C. Lu, G. Parry, P. J. Green, G. M. Coruzzi, and R. A. Gutierrez. 2010. Nitrate-responsive miR393/AFB3regulatory module controls root system architecture in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 107 (9):4477–4482. doi: 10.1073/pnas.0909571107.
   PubMed Web of Science ®Google Scholar
• Vidal, E. A., K. P. Tamayo, and R. A. Gutierrez. 2010. Gene networks for nitrogen sensing, signaling, and response in Arabidopsis thaliana. Wiley Interdisciplinary Reviews: Systems Biology and Medicine 2 (6):683–693. doi: 10.1002/wsbm.87.
   PubMed Web of Science ®Google Scholar
• Xiao, Q. Y., H. D. Gernier, L. Kupcsik, J. D. Pessemier, K. Dittert, K. Fladung, N. Verbruggen, and C. Hermans. 2015. Natural genetic variation of Arabidopsis thaliana root morphological response to magnesium supply. Crop and Pasture Science 66 (12):1249–1258. doi: 10.1071/CP15108.
   Web of Science ®Google Scholar
• Xu, G. H., X. R. Fan, and A. J. Miller. 2012. Plant nitrogen assimilation and use efficiency. Annual Review of Plant Biology 63:153–182. doi: 10.1146/annurev-arplant-042811-105532
   PubMed Web of Science ®Google Scholar
• Xu, N., R. C. Wang, L. F. Zhao, C. F. Zhang, Z. H. Li, Z. Lei, F. Liu, P. Z. Guan, Z. H. Chu, N. M. Crawford, and Y. Wang. 2016. The Arabidopsis NRG2 protein mediates nitrate signaling and interacts with and regulates key nitrate regulators. The Plant Cell 28 (2):485–504. doi: 10.1105/tpc.15.00567
   PubMed Web of Science ®Google Scholar
• Zhang, H. M., and B. G. Forde. 2000. Regulation of Arabidopsis root development by nitrate availability. Journal of Experimental Botany 51 (342):51–59. doi: 10.1093/jxb/51.342.51.
   PubMed Web of Science ®Google Scholar
• Zhang, H. M., A. Jennings, P. W. Barlow, and B. G. Forde. 1999. Dual pathways for regulation of root branching by nitrate. Proceedings of the National Academy of Sciences of the United States of America 96 (11):6529–6534. doi: 10.1073/pnas.96.11.6529
   PubMed Web of Science ®Google Scholar
• Zolla, G., Y. M. Heimer, and S. Barak. 2010. Mild salinity stimulates a stress-induced morphogenic response in Arabidopsis thaliana roots. Journal of Experimental Botany 61 (1):211–224. doi: 10.1093/jxb/erp290.
   PubMed Web of Science ®Google Scholar