Whole plant acclimation responses by finger millet to low nitrogen stress

Frontiers in Plant Science

Volumn 6, Issue AUG, 2015, Pages

  Goron, Travis L ^a   Bhosekar, Vijay K ^a   Shearer, Charles R ^a   Watts, Sophia ^a   Raizada, Manish N ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

Crown root; Finger millet; Grain; Lateral root; Nitrogen stress; Root; Root hair; Shoot

Indexed keywords

ELEUSINE CORACANA;

EID: 84940175072     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00652     Document Type: Article

References (68)

1. Alzueta, I., Abeledo, L. G., Mignone, C. M., and Miralles, D. J. (2012). Differences between wheat and barley in leaf and tillering coordination under contrasting nitrogen and sulfur conditions. Eur. J. Agron. 41, 92-102. doi: 10.1016/j.eja.2012.04.002
2. Bhoite, S. V., and Nimbalkar, V. S. (1996). Response of finger millet cultivars to nitrogen and phosphorus under rain-fed conditions. J. Maharashtra Agric. Univ. 20, 189-190.
3. Bloch, D., Monshausen, G., Singer, M., Gilroy, S., and Yalovsky, S. (2011). Nitrogen source interacts with ROP signalling in root hair tip-growth. Plant Cell Environ. 34, 76-88. doi: 10.1111/j.1365-3040.2010.02227.x
4. Bremner, J. M. (1996). "Nitrogen-total," in Methods of Soil Analysis. Part 3. Chemical Methods, ed. J. M. Bartels (Madison, WI: Soil Society of America and American Society of Agronomy), 1085-1091.
5. Cavalcante, V. A., and Dobereiner, J. (1988). A new acid-tolerant nitrogen-fixing bacterium associated with sugarcane. Plant Soil 108, 23-31. doi: 10.1007/BF02370096
6. Chapin, F. S., Bloom, A. J., Field, C. B., and Waring, R. H. (1987). Plant responses to multiple environmental factors. Bioscience37, 49-57. doi: 10.2307/1310177
7. Chen, Y., Xiao, C., Wu, D., Xia, T., Chen, Q., Chen, F., et al. (2015). Effects of nitrogen application rate on grain yield and grain nitrogen concentration in two maize hybrids with contrasting nitrogen remobilization efficiency. Eur. J. Agron. 62, 79-89. doi: 10.1016/j.eja.2014.09.008
8. Chun, L., Mi, G., Li, J., Chen, F., and Zhang, F. (2005). Genetic analysis of maize root characteristics in response to low nitrogen stress. Plant Soil 276, 369-382. doi: 10.1007/s11104-005-5876-2
9. Ciampitti, I. A., Murrell, S. T., Camberato, J. J., Tuinstra, M., Xia, Y., Friedemann, P., et al. (2013). Physiological dynamics of maize nitrogen uptake and partitioning in response to plant density and N stress factors: I. vegetative phase. Crop Sci. 53, 2105-2119. doi: 10.2135/cropsci2013.01.0040
10. Coudert, Y., Périn, C., Courtois, B., Khong, N. G., and Gantet, P. (2010). Genetic control of root development in rice, the model cereal. Trends Plant Sci. 15, 219-226. doi: 10.1016/j.tplants.2010.01.008
11. DeBruin, J., and Butzen, S. (2014). Nitrogen uptake in corn. Pioneer Crop Insights 24.
12. Dida, M. M., Wanyera, N., Harrison, M. L., Bennetzen, J. L., and Devos, K. M. (2008). Population structure and diversity in finger millet (Eleusine coracana) germplasm. Trop. Plant Biol. 1, 131-141. doi: 10.1007/s12042-008-9012-3
13. Doebley, J., Stec, A., and Gustus, C. (1995). Teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 141, 333-346.
14. Dorosh, P. A., Dradri, S., and Haggblade, S. (2009). Regional trade, government policy and food security: recent evidence from Zambia. Food Policy 34, 350-366. doi: 10.1016/j.foodpol.2009.02.001
15. Dubley, O. P., and Shrivas, B. N. (1999). Response of finger millet (Eleusine coracana) genotypes to nitrogen. Indian J. Agron.44, 564-566.
16. Eghball, B., and Maranville, J. W. (1993). Root development and nitrogen influx of corn genotypes grown under combined drought and nitrogen stresses. Agron. J. 85, 147-152. doi: 10.2134/agronj1993.00021962008500010027x
17. Etheridge, R. D., Pesti, G. M., and Foster, E. H. (1998). A comparison of nitrogen values obtained utilizing the Kjeldahl nitrogen and Dumas combustion methodologies (Leco CNS 2000) on samples typical of an animal nutrition analytical laboratory. Anim. Feed Sci. Technol. 73, 21-28. doi: 10.1016/S0377-8401(98)00136-9
18. Fiedler, R., Proksch, G., and Koepf, A. (1973). The determination of total nitrogen in plant materials with an automatic nitrogen analyser. Anal. Chim. Acta 63, 435-443. doi: 10.1016/S0003-2670(01)82368-0
19. Garnier, E. (1992). Growth analysis of congeneric annual and perennial grass species. J. Ecol. 80, 665-675. doi: 10.2307/2260858
20. Garnier, E., and Laurent, G. (1994). Leaf anatomy, specific mass and water content in congeneric annual and perennial grass species. New Phytol. 128, 725-736. doi: 10.1111/j.1469-8137.1994.tb04036.x
21. Gaudin, A. C. M., McClymont, S. A., Holmes, B. M., Lyons, E., and Raizada, M. N. (2011a). Novel temporal, fine-scale and growth variation phenotypes in roots of adult-stage maize (Zea mays L.) in response to low nitrogen stress. Plant Cell Environ.34, 2122-2137. doi: 10.1111/j.1365-3040.2011.02409.x
22. Gaudin, A. C. M., McClymont, S. A., and Raizada, M. N. (2011b). The nitrogen adaptation strategy of the wild teosinte ancestor of modern maize, Zea mays subsp. parviglumis. Crop Sci. 51, 2780-2795. doi: 10.2135/cropsci2010.12.0686
23. Gaudin, A. C. M., McClymont, S. A., Soliman, S. S. M., and Raizada, M. N. (2014). The effect of altered dosage of a mutant allele of Teosinte branched 1 (tb1-ref) on the root system of modern maize. BMC Genet. 15:23. doi: 10.1186/1471-2156-15-23
24. Goron, T. L., and Raizada, M. N. (2015). Genetic diversity and genomic resources available for the small millet crops to accelerate a New Green Revolution. Front. Plant Sci. 6:157. doi: 10.3389/fpls.2015.00157
25. Goron, T. L., Watts, S., Shearer, C., and Raizada, M. N. (2015). Growth in Turface clay permits root hair phenotyping along the entire crown root in cereal crops and demonstrates that root hair growth can extend well beyond the root hair zone. BMC Res. Notes 8:143. doi: 10.1186/s13104-015-1108-x
26. Gruère, G., Nagarajan, L., and King, E. D. I. O. (2009). The role of collective action in the marketing of underutilized plant species: lessons from a case study on minor millets in South India. Food Policy 34, 39-45. doi: 10.1016/j.foodpol.2008.10.006
27. Gupta, A. K., Guar, V. S., Gupta, S., and Kumar, A. (2013). Nitrate signals determine the sensing of nitrogen through differential expression of genes involved in nitrogen uptake and assimilation in finger millet. Funct. Integr. Genomics 13, 179-190. doi: 10.1007/s10142-013-0311-x
28. Gupta, N., Gupta, A. K., Gaur, V. S., and Kumar, A. (2012). Relationship of nitrogen use efficiency with the activities of enzymes involved in nitrogen uptake and assimilation of finger millet genotypes grown under different nitrogen inputs. Sci. World J. 2012, 1-10. doi: 10.1100/2012/625731
29. Gupta, S., Gupta, S. M., Gupta, A. K., Gaur, V. S., and Kumar, A. (2014). Fluctuation of Dof1/Dof2 expression ratio under the influence of varying nitrogen and light conditions: involvement in differential regulation of nitrogen metabolism in two genotypes of finger millet (Eleusine coracana L.). Gene 546, 327-335. doi: 10.1016/j.gene.2014.05.057
30. Gupta, S., Malviya, N., Kushwaha, H., Nasim, J., Bisht, N. C., Singh, V. K., et al. (2015). Insights into structural and functional diversity of Dof (DNA binding with one finger) transcription factor. Planta 241, 549-562. doi: 10.1007/s00425-014-2239-3
31. Havlin, J., Beaton, J., Tisdale, S., and Nelson, W. (1999). "Nitrogen," in Soil Fertility and Fertilizers, 6th Edn, eds M. Carnis and L. Harvey (Upper Saddle River, NJ: Prentice-Hall, Inc).
32. Hay, R., and Porter, J. (2006). "Limiting factors and the achievement of high yield," in The Physiology of Crop Yield (Oxford: Blackwell Publishing Inc.), 180-204.
33. Hubbard, L., McSteen, P., Doebley, J., and Hake, S. (2002). Expression patterns and mutant phenotype of teosinte branched1 correlate with growth suppression in maize and teosinte. Genetics 162, 1927-1935.
34. Ikram, S., Bedu, M., Daniel-Vedele, F., Chaillou, S., and Chardon, F. (2012). Natural variation of Arabidopsis response to nitrogen availability. J. Exp. Bot. 63, 91-105. doi: 10.1093/jxb/err244
35. Inukai, Y., Sakamoto, T., Ueguchi-Tanaka, M., Shibata, Y., Gomi, K., Umemura, I., et al. (2005). Crown rootless1, which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE FACTOR in auxin signaling. Plant Cell 17, 1387-1396. doi: 10.1105/tpc.105.030981
36. James, E., Reis, V., Olivares, F., Baldani, J., and Döbereiner, J. (1994). Infection of sugar cane by the nitrogen-fixing bacteriumAcetobacter diazotrophicus. J. Exp. Bot. 45, 757-766. doi: 10.1093/jxb/45.6.757
37. Jarvis, D. I., Brown, A. H. D., Cuong, P. H., Collado-panduro, L., Latournerie-moreno, L., Gyawali, S., et al. (2008). A global perspective of the richness and evenness of tradtitional crop-variety diversity maintained by farming communities. Proc. Natl. Acad. Sci. U.S.A. 105, 5326-5331. doi: 10.1073/pnas.0800607105
38. Johnston-Monje, D., Mousa, W., Lazarovits, G., and Raizada, M. N. (2014). Impact of swapping soils on the endophytic bacterial communities of pre-domesticated, ancient and modern maize. BMC Plant Biol. 14:233. doi: 10.1186/s12870-014-0233-3
39. Keeney, D. R., and Bremner, J. M. (1966). Comparison and evaluation of labroratory methods of obtaining an index of soil nitrogen availability. Agron. J. 58, 498-503. doi: 10.2134/agronj1966.00021962005800050013x
40. Kitomi, Y., Ito, H., Hobo, T., Aya, K., Kitano, H., and Inukai, Y. (2011). The auxin responsive AP2 / ERF transcription factor CROWN ROOTLESS5 is involved in crown root initiation in rice through the induction of OsRR1, a type-A response regulator of cytokinin signaling. Plant J. 3, 472-484. doi: 10.1111/j.1365-313X.2011.04610.x
41. Kumar, A., Kanwal, P., Gupta, A. K., Singh, B. R., and Gaur, V. S. (2014). A full-length Dof1 transcription factor of finger millet and its response to a circadian cycle. Plant Mol. Biol. Report. 32, 419-427. doi: 10.1007/s11105-013-0653-5
42. Lee, R. B., Purves, J. V., Ratcliffe, R. G., and Saker, L. R. (1992). Nitrogen assimilation and the control of ammonium and nitrate absorption by maize roots. J. Exp. Bot. 43, 1385-1396. doi: 10.1093/jxb/43.11.1385
43. Liu, J., Chen, F., Olokhnuud, C., Glass, A. D. M., Tong, Y., Zhang, F., et al. (2009). Root size and nitrogen-uptake activity in two maize (Zea mays) inbred lines differing in nitrogen-use efficiency. J. Plant Nutr. Soil Sci. 172, 230-236. doi: 10.1002/jpln.200800028
44. Lukens, L., and Doebley, J. (2001). Molecular evolution of the teosinte branched gene among maize and related grasses. Mol. Biol. Evol. 18, 627-638. doi: 10.1093/oxfordjournals.molbev.a003843
45. Mae, T. (1997). Physiological nitrogen efficiency in rice: nitrogen utilization, photosynthesis, and yield potential. Plant Soil196, 201-210. doi: 10.1023/A:1004293706242
46. Møller, A. L. B., Pedas, P., Andersen, B., Svensson, B., Schjoerring, J. K., and Finnie, C. (2011). Responses of barley root and shoot proteomes to long-term nitrogen deficiency, short-term nitrogen starvation and ammonium. Plant Cell Environ. 34, 2024-2037. doi: 10.1111/j.1365-3040.2011.02396.x
47. Moll, R. H., Kamprath, E. J., and Jackson, W. A. (1982). Analysis and interpretation of factors which contribute to efficiency of nitrogen-utilization. Agron. J. 74, 562-564. doi: 10.2134/agronj1982.00021962007400030037x
48. Muñoz-Huerta, R. F., Guevara-Gonzalez, R. G., Contreras-Medina, L. M., Torres-Pacheco, I., Prado-Olivarez, J., and Ocampo-Velazquez, R. V. (2013). A review of methods for sensing the nitrogen status in plants: advantages, disadvantages and recent advances. Sensors 13, 10823-10843. doi: 10.3390/s130810823
49. Nacry, P., Bouguyon, E., and Gojon, A. (2013). Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource. Plant Soil 370, 1-29. doi: 10.1007/s11104-013-1645-9
50. National Research Council. (1996). Lost Crops of Africa. Washington, DC: National Academy Press.
51. Page, E. R., Liu, W., Cerrudo, D., Lee, E. A., and Swanton, C. J. (2011). Shade avoidance influences stress tolerance in maize.Weed Sci. 59, 326-334. doi: 10.1614/WS-D-10-00159.1
52. Pradhan, A., Thakur, A., Patel, S., and Mishra, N. (2011). Effect of different nitrogen levels on kodo and finger millet under rainfed conditions. Res. J. Agric. Sci. 2, 136-138.
53. Puttaswamy, S., and Krishnamurthy, K. (1976). Relative dry-matter efficiency in finger millet genotypes in relation to levels of spacing and nitrogen. Mysore J. Agr. Sci. 10, 345-352.
54. Robinson, D., and Rorison, I. H. (1987). Root hairs and plant growth at low nitrogen availabilities. New Phytol. 107, 681-693. doi: 10.1111/j.1469-8137.1987.tb00906.x
55. Roy, D., Chakraborty, T., Sounda, G., and Maitra, S. (2001). Effect of fertility levels and plant population on yield and uptake of nitrogen, phosphorus and potassium in finger millet (Eleusine coracana) in lateritic soil of West Bengal. Indian J. Agron.464, 707-711.
56. Schluter, U., Mascher, M., Colmsee, C., Scholz, U., Brautigam, A., Fahnenstich, H., et al. (2012). Maize source leaf adaptation to nitrogen deficiency affects not only nitrogen and carbon metabolism but also control of phosphate homeostasis. Plant Physiol. 160, 1384-1406. doi: 10.1104/pp.112.204420
57. Shin, R., Berg, R. H., and Schachtman, D. P. (2005). Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant Cell Physiol. 46, 1350-1357. doi: 10.1093/pcp/pci145
58. Széles, A. V., Megyes, A., and Nagy, J. (2012). Irrigation and nitrogen effects on the leaf chlorophyll content and grain yield of maize in different crop years. Agric. Water Manag. 107, 133-144. doi: 10.1016/j.agwat.2012.02.001
59. Taramino, G., Sauer, M., Stauffer, J. L. S. Jr., Multani, D., Niu, X., and Sakai, H. (2007). The maize (Zea mays L.) RTCS gene encodes a LOB domain protein that is a key regulator of embryonic seminal and post-embryonic shoot-borne root initiation.Plant J. 1, 649-659. doi: 10.1111/j.1365-313X.2007.03075.x
60. Thilakarathna, M. S., and Raizada, M. N. (2015). A review of nutrient management studies involving finger millet in the semi-arid tropics of Asia and Africa. Agronomy 5, 262-290. doi: 10.3390/agronomy5030262
61. Tollenaar, M., and Migus, W. (1984). Dry matter accumulation of maize grown hydroponically under controlled-environment and field conditions. Can. J. Plant Sci. 64, 475-485. doi: 10.4141/cjps84-070
62. Upadhyaya, H. D., Gowda, C. L. L., Pundir, R. P. S., Reddy, V. G., and Singh, S. (2006). Development of core subset of finger millet germplasm using geographical origin and data on 14 quantitative traits. Genet. Resour. Crop Evol. 53, 679-685. doi: 10.1007/s10722-004-3228-3
63. Wang, G., Bronson, K. F., Thorp, K. R., Mon, J., and Badaruddin, M. (2014). Multiple leaf measurements improve effectiveness of chlorophyll meter for durum wheat nitrogen management. Crop Sci. 54, 817-826. doi: 10.2135/cropsci2013.03.0160
64. Wang, Y., Mi, G., Chen, F., and Zhang, J. (2004). Response of root morphology to nitrate supply and its contribution to nitrogen accumulation in maize. J. Plant Nutr. 27, 2189-2202. doi: 10.1081/LPLA-200034683
65. Waramit, N., Moore, K. J., and Heaton, E. (2014). Nitrogen and harvest date affect developmental morphology and biomass yield of warm-season grasses. GCB Bioenergy 6, 534-543. doi: 10.1111/gcbb.12086
66. Wolie, A., and Dessalegn, T. (2011). Correlation and path coefficient analyses of some yield related traits in finger millet (Eleusine coracana (L.) Gaertn.) germplasms in northwest Ethiopia. Afr. J. Agric. Res. 6, 5099-5105. doi: 10.5897/AJAR11.616
67. Yang, W., Yoon, J., Choi, H., Fan, Y., Chen, R., and An, G. (2015). Transcriptome analysis of nitrogen-starvation- responsive genes in rice. BMC Plant Biol. 15:31. doi: 10.1186/s12870-015-0425-5
68. Zhao, Y., Hu, Y., Dai, M., Huang, L., and Zhou, D.-X. (2009). The WUSCHEL-related homeobox gene WOX11 is required to activate shoot-borne crown root development in rice. Plant Cell 21, 736-748. doi: 10.1105/tpc.108.061655