Computed tomography scanning can monitor the effects of soil medium on root system development: An example of salt stress in corn

Frontiers in Plant Science

Volumn 6, Issue APR, 2015, Pages

  Subramanian, Sowmyalakshmi ^a   Han, Liwen ^a   Dutilleul, Pierre ^a   Smith, Donald L ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Computed tomography (CT) scanning; Corn (Zea mays L.); Developing root systems; Fractal dimension (FD); NaCl salt stress; Root lengths and increments; Root volumes and relative growth rates; Structural complexity

Indexed keywords

ZEA MAYS;

EID: 84934876515     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00256     Document Type: Article

References (57)

1. Abbe, E. C., and Stein, O. L. (1954). The origin of the shoot apex in maize: embryogeny. Am. J. Bot. 41, 285-293. doi: 10. 2307/2438600.
2. Almansouri, M., Kinet, J. M., and Lutts, S. (2001). Effect of salt and osmotic stresses on germination in durum wheat (Triticum durum Desf.). Plant Soil 231, 243-254. doi: 10. 1023/A: 1010378409663.
3. Armengaud, P., Zambaux, K., Hills, A., Sulpice, R., Pattison, R. J., Blatt, M. R., et al. (2009). EZ-RHIZO: integrated software for the fast and accurate measurement of root system architecture. Plant J. 57, 945-995. doi: 10. 1111/j. 1365-313X. 2008. 03739. x.
4. Baoa, Y., Aggarwal, P., Robbins, N. E., Sturrocke, C. J., Thompsone, M. C., Tan, H. Q., et al. (2014). Plant roots use a patterning mechanism to position lateral root branches toward available water. Proc. Natl. Acad. Sci. U. S. A. 111, 9319-9324. doi: 10. 1073/pnas. 1400966111.
5. Bengough, A. G., Gordon, D. C., Al-Menaie, H., Ellis, R. P., Allan, D., Keith, R., et al. (2004). Gel observation chamber for rapid screening of root traits in cereal seedlings. Plant Soil 262, 63-70. doi: 10. 1023/B: PLSO. 0000037029. 82618. 27.
6. Carpici, E. B., Celik, N., and Bayram, G. (2009). Effects of salt stress on germination of some maize (Zea mays L.) cultivars. Afr. J. Biotechnol. 8, 4918-4922.
7. 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.
8. Crowder, M. J., and Hand, D. J. (1990). Analysis of Repeated Measures. London: Chapman and Hall.
9. de Dorlodot, S., Forster, B., Pagés, L., Price, A., Tuberosa, R., and Draye, X. (2007). Root system architecture: opportunities and constraints for genetic improvement of crops. Trends Plant Sci. 12, 474-481. doi: 10. 1016/j. tplants. 2007. 08. 012.
10. Dutilleul, P. (2011). Spatio-Temporal Heterogeneity: Concepts and Analyses. Cambridge: Cambridge University Press.
11. Dutilleul, P., Han, L., and Smith, D. L. (2008). Plant light interception can be explained via computed tomography scanning: demonstration with pyramidal cedar (Thuja occidentalis, fastigiata). Ann. Bot. 101, 19-23. doi: 10. 1093/aob/mcm273.
12. Dutilleul, P., Lontoc-Roy, M., and Prasher, S. O. (2005). Branching out with a CT scanner. Trends Plant Sci. 10, 411-412. doi: 10. 1016/j. tplants. 2005. 06. 004.
13. FAO. (2014). FAOSTAT. Food and Agriculture Organization of the United Nations, Rome. Available at: http://faostat. fao. org (accessed June 10, 2014).
14. Flavel, R. J., Guppy, C. N., Tighe, M., Watt, M., McNeill, A., and Young, I. M. (2012). Non-destructive quantification of cereal roots in soil using high-resolution X-ray tomography. J. Exp. Bot. 63, 2503-2511. doi: 10. 1093/jxb/err421.
15. Foolad, M. R., Hyman, J. R., and Lin, G. Y. (1999). Relationships between cold and salt tolerance during seed germination in tomato: analysis of response and correlated response to selection. Plant Breed. 118, 49-52. doi: 10. 1046/j. 1439-0523. 1999. 118001049. x.
16. Foroutan-pour, K., Dutilleul, P., and Smith, D. L. (1999a). Soybean canopy development as affected by population density and intercropping with corn: fractal analysis in comparison with other quantitative approaches. Crop Sci. 39, 1784-1791. doi: 10. 2135/cropsci1999. 3961784x.
17. Foroutan-pour, K., Dutilleul, P., and Smith, D. L. (1999b). Advances in the implementation of the box-counting method of fractal dimension estimation. Appl. Math. Comput. 105, 195-210. doi: 10. 1016/S0096-3003(98)10096-6.
18. Greenway, H., and Munns, R. (1980). Mechanisms of salt tolerance in non-halophytes. Annu. Rev. Plant Physiol. 31, 149-190. doi: 10. 1146/annurev. pp. 31. 060180. 001053.
19. Han, L., Dutilleul, P., Prasher, S. O., Beaulieu, C., and Smith, D. L. (2008). Assessment of common scab-inducing pathogen effects on potato underground organs via computed tomography scanning. Phytopathology 98, 1118-1125. doi: 10. 1094/PHYTO-98-10-1118.
20. Han, L., Dutilleul, P., Prasher, S. O., Beaulieu, C., and Smith, D. L. (2009). Assessment of density effects of the common scab-inducing pathogen on the seed and peripheral organs of potato during growth using computed tomography scanning data. Trans. Am. Soc. Agric. Biol. Eng. 52, 305-311.
21. Heeraman, D. A., Hopmans, J. W., and Clausnitzer, V. (1997). Three dimensional imaging of plant roots in situ with X-ray computed tomography. Plant Soil 189, 167-179. doi: 10. 1023/B: PLSO. 0000009694. 64377. 6f.
22. Hoagland, D. R., and Arnon, D. I. (1950). A comparison of water culture and soil as media for crop production. Science 89, 512-514.
23. Hochholdinger, F., Woll, K., Sauer, M., and Dembinsky, D. (2004). Genetic dissection of root formation in maize (Zea mays) reveals root-type specific developmental programmes. Ann. Bot. 93, 359-368. doi: 10. 1093/aob/mch056.
24. Jia, W., Wang, Y., Zhang, S., and Zhang, J. (2002). Salt-stress-induced ABA accumulation is more sensitively triggered in roots than in shoots. J. Exp. Bot. 53, 2201-2206. doi: 10. 1093/jxb/erf079.
25. Kalender, W. A. (2000). Computed Tomography. Munich: MCD Verlag.
26. Kao, W. Y., Tsai, T. T., and Shih, C. N. (2003). Photosynthetic gas exchange and chlorophyll a fluorescence of three wild soybean species in response to NaCl treatments. Photosynthetica 41, 415-419. doi: 10. 1023/B: PHOT. 0000015466. 22288. 23.
27. Ketcham, R. A., and Carlson, W. D. (2001). Acquisition, optimization and interpretation of X-ray computed tomographic imagery: applications to the geosciences. Comput. Geosci. 27, 381-400. doi: 10. 1016/S0098-3004(00)00116-3.
28. Kirst, G. (1990). Salinity tolerance of eukaryotic marine algae. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41, 21-53. doi: 10. 1146/annurev. pp. 41. 060190. 000321.
29. Levitt, J. (1980). Responses of Plants to Environmental Stresses, 2nd Edn. New York, NY: Academic Press.
30. Lontoc-Roy, M., Dutilleul, P., Prasher, S. O., Han, L., Brouillet, T., and Smith, D. L. (2006). Advances in the acquisition and analysis of CT scan data to isolate a crop root system from the soil medium and quantify root system complexity in 3-D space. Geoderma 137, 231-241. doi: 10. 1016/j. geoderma. 2006. 08. 025.
31. Lontoc-Roy, M., Dutilleul, P., Prasher, S. O., Han, L., and Smith, D. L. (2005). Computed tomography scanning for three-dimensional imaging and complexity analysis of developing root systems. Can. J. Bot. 83, 1434-1442. doi: 10. 1139/b05-118.
32. Lynch, J. P. (2013). Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Ann. Bot. 112, 347-357. doi: 10. 1093/aob/mcs293.
33. Mansour, M. M. F., Salama, K. H. A., Ali, F. Z. M., and Hadid, A. F. A. (2005). Cell and plant responses to NaCl in Zea mays L. cultivars differing in salt tolerance. Gen. Appl. Plant Physiol. 31, 29-41.
34. Munns, R. (2005). Genes and salt tolerance: bringing them together. New Phytol. 167, 645-663. doi: 10. 1111/j. 1469-8137. 2005. 01487. x.
35. Munns, R., James, R. A., and Lauchli, A. (2006). Approaches to increasing the salt tolerance of wheat and other cereals. J. Exp. Bot. 57, 1025-1043. doi: 10. 1093/jxb/erj100.
36. Neumann, G., George, T. S., and Plassard, C. (2009). Strategies and methods for studying the rhizosphere-the plant science toolbox. Plant Soil 321, 431-456. doi: 10. 1007/s11104-009-9953-9.
37. Parida, A. K., Das, A. B., and Mittra, B. (2003). Effects of NaCl stress on the structure, pigment complex composition, and photosynthetic activity of mangrove Bruguiera parviflorachloroplasts. Photosynthetica 41, 191-200. doi: 10. 1023/B: PHOT. 0000011951. 37231. 69.
38. Perret, J. S., Al-Belushib, M. E., and Deadman, M. (2007). Non-destructive visualization and quantification of roots using computed tomography. Soil Biol. Biochem. 39, 391-399. doi: 10. 1016/j. soilbio. 2006. 07. 018.
39. Postma, J. A., and Lynch, J. P. (2012). Complementarity in root architecture for nutrient uptake in ancient maize/bean and maize/bean/squash polycultures. Ann. Bot. 110, 521-534. doi: 10. 1093/aob/mcs082.
40. Rahnama, A., Munns, R., Poustini, K., and Watt, M. (2011). A screening method to identify genetic variation in root growth response to a salinity gradient. J. Exp. Bot. 62, 69-77. doi: 10. 1093/jxb/erq359.
41. Rengasamy, P. (2008). Salinity in the landscape: a growing problem in Australia. Geotimes 53, 34-39.
42. Richards, R. A. (2008). Genetic opportunities to improve cereal root systems for dryland agriculture. Plant Prod. Sci. 11, 12-16. doi: 10. 1626/pps. 11. 12.
43. Rodríguez, H. G., Roberts, J. K. M., Jordan, W. R., and Drew, M. C. (1997). Growth, water relations, and accumulation of organic and inorganic solutes in roots of maize seedlings during salt stress. Plant Physiol. 113, 881-893.
44. Schwinning, S., and Weiner, J. (1998). Mechanisms determining the degree of size asymmetry in competition among plants. Oecologia 113, 447-455. doi: 10. 1007/s004420050397.
45. Shelden, M. C., Roessner, U., Sharp, R. E., Tester, M., and Bacic, A. (2013). Genetic variation in the root growth response of barley genotypes to salinity stress. Funct. Plant Biol. 40, 516-530. doi: 10. 1071/FP12290.
46. Smet, I. D., White, P. J., Bengough, A. G., Dupuy, L., Parizot, B., Casimiro, I., et al. (2012). Analyzing lateral root development: how to move forward. Plant Cell 24, 15-20. doi: 10. 1105/tpc. 111. 094292.
47. Spickett, C. M., Smirnoff, N., and Ratcliffe, R. C. (1993). An in vivo nuclear magnetic resonance investigation of ion transport in maize (Zea mays) and Spartina anglica roots during exposure to high salt concentrations. Plant Physiol. 102, 629-638. doi: 10. 1111/nph. 13173.
48. Sun, F., Zhang, W., Hu, H., Li, B., Wang, Y., Zhao, Y., et al. (2008). Salt modulates gravity signaling pathway to regulate growth direction of primary roots in Arabidopsis. Plant Physiol. 146, 178-188. doi: 10. 1104/pp. 107. 109413.
49. Tillich, H. J. (1977). Vergleichend morphologische Untersuchungen zur Identität der Gramineen-Primärwurzel. Flora 166, 415-421.
50. van Kaick, G., and Delorme, S. (2005). Computed tomography in various fields outside medicine. Eur. Radiol. Suppl. 15, D74-D81. doi: 10. 1007/s10406-005-0138-1.
51. Wiebe, B. H., Eilers, R. G., Eilers, W. D., and Brierley, J. A. (2007). Application of a risk indicator for assessing trends in dryland salinization risk on the Canadian Prairies. Can. J. Soil Sci. 87, 213-224. doi: 10. 4141/S06-068.
52. Wu, J., and Guo, Y. (2014). An integrated method for quantifying root architecture of field-grown maize. Ann. Bot. 114, 841-851. doi: 10. 1093/aob/mcu009.
53. Xu, X.-Y., Fan, R., Zheng, R., Li, C.-M., and Yu, D.-Y. (2011). Proteomic analysis of seed germination under salt stress in soybeans. J. Zhejiang Univ. Sci. B 12, 507-517. doi: 10. 1631/jzus. B1100061.
54. Yan, L. (2008). Effect of salt stress on seed germination and seedling growth of three salinity plants. Pak. J. Biol. Sci. 11, 1268-1272. doi: 10. 3923/pjbs. 2008. 1268. 1272.
55. Zappala, S., Helliwell, J. R., Tracy, S. R., Mairhofer, S., Sturrock, C. J., Pridmore, T., et al. (2013). Effects of X-ray dose on rhizosphere studies using X-ray computed tomography. PLoS ONE8: e67250. doi: 10. 1371/journal. pone. 0067250.
56. Zhu, J., Ingram, P. A., Benfey, P. N., and Elich, T. (2011). From lab to field, new approaches to phenotyping root system architecture. Curr. Opin. Plant Biol. 14, 310-317. doi: 10. 1016/j. pbi. 2011. 03. 020.
57. Zörb, C., Geilfus, C.-M., Muhling, K. H., and Ludwig-Muller, J. (2013). The influence of salt stress on ABA and auxin concentrations in two maize cultivars differing in salt resistance. J. Plant Physiol. 170, 220-224. doi: 10. 1016/j. jplph. 2012. 09. 012.