Integration of root phenes for soil resource acquisition

Frontiers in Plant Science

Volumn 4, Issue SEP, 2013, Pages

  York, Larry M ^a   Nord, Eric A ^a   Lynch, Jonathan P ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Functional traits; Ideotype; Phenomics; Root architecture; Soil resources

Indexed keywords

EID: 84900867976     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00355     Document Type: Article

References (132)

1. Anderson, D. W. (1988). The effect of parent material and soil development on nutrient cycling in temperate ecosystems. Biogeochemistry 5, 71-97. doi: 10.1007/ BF02180318
2. Annicchiarico, P., and Pecetti, L. (1998). Yield vs. morphophysiolog-ical trait-based criteria for selection of durum wheat in a semi-arid Mediterranean region (northern Syria). Field Crops Res. 59, 163-173. doi: 10.1016/S0378-4290(98) 00116-6
3. Arnold, S. J. (1983). Morphology, performance, and fitness. Am. Zool. 23, 347-361. doi: 10.1093/icb/23. 2.347
4. Barber, S. A. (1984). Soil Nutrient Bioavailability. Hoboken: John Wiley and Sons.
5. Bates, T. R., and Lynch, J. P. (2000). Plant growth and phosphorus accumulation of wild type and two root hair mutants of Arabidop-sis thaliana (Brassicaceae). Am. J. Bot. 87, 958-963. doi: 10.2307/ 2656994
6. Bates, T. R., and Lynch, J. P. (2001). Root hairs confer a competitive advantage under low phosphorus availability. Plant Soil 236, 243-250. doi: 10.1023/A:1012791 706800
7. Bayuelo-Jiménez, J. S., Gallardo-Valdéz, M., Pérez-Decelis, V. A., Magdaleno-Armas, L., Ochoa, I., and Lynch, J. P. (2011). Genotypic variation for root traits of maize (Zea mays L.) from the Purhep-echa Plateau under contrasting phosphorus availability. Field Crops Res. 121, 350-362. doi: 10.1016/j.fcr.2011. 01.001
8. Bennett, T., Sieberer, T., Wil-lett, B., Booker, J., Luschnig, C., and Leyser, O. (2006). The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr. Biol. 16, 553-563. doi: 10.1016/j.cub.2006. 01.058
9. Berg, R. (1960). The ecological significance of correlation pleiades. Evolution 14, 171-180. doi: 10.2307/ 2405824
10. Bonser, A. M., Lynch, J. P., and Snapp, S. (1996). Effect of phosphorus deficiency on growth angle of basal roots in Phaseolus vul-garis. New Phytol. 132, 281-288. doi: 10.1111/j.1469-8137.1996. tb01847.x
11. Borch, K., Bouma, T. J., Lynch, J. P., and Brown, K. M. (1999). Ethy-lene: a regulator of root architectural responses to soil phosphorus availability. Plant Cell Environ. 22, 425-431. doi: 10.1046/j.1365-3040.1999. 00405.x
12. Bouma, T. J., Nielsen, K. L., Eissenstat, D. M., and Lynch, J. P. (1997). Soil CO2 concentration does not affect growth or root respiration in bean or citrus. Plant Cell Environ. 20, 1495-1505. doi: 10.1046/j.1365-3040.1997.d01-52.x
13. Bray, R. H. (1954). A nutrient mobility concept of soil-plant relationships. Soil Sci. 78, 9-22. doi: 10.1097/00010694-195407000-00002
14. Brun, F., Richard-Molard, C., Pagès, L., Chelle, M., and Ney, B. (2010). To what extent may changes in the root system architecture of Arabidop-sis thaliana grown under contrasted homogenous nitrogen regimes be explained by changes in carbon supply? A modelling approach. J. Exp. Bot. 61, 2157-2169. doi: 10.1093/jxb/erq090
15. Burton, A. L., Brown, K. M., and Lynch, J. P. (2013a). Phenotypic diversity of root anatomical and architectural traits in Zea species. Crop Sci. 53, 1042-1055. doi: 10.2135/crop-sci2012.07.0440
16. Burton, A. L., Lynch, J. P., and Brown, K. M. (2013b). Spatial distribution and phenotypic variation in root cortical aerenchyma of maize (Zea mays L.). Plant Soil 367, 263-274. doi: 10.1007/s11104-012-1453-7
17. Callaway, R. M., Pennings, S. C., and Richards, C. L. (2003). Phe-notypic plasticity and interactions among plants. Ecology 84, 1115-1128. doi: 10.1890/0012-9658(2003) 084[1115:PPAIAP]2.0.CO;2
18. Chapin, F. S. III, Bloom, A. J., Field, C. B., and Waring, R. H. (1987). Plant responses to multiple environmental factors. Bioscience 37, 49-57. doi: 10.2307/1310177
19. Chen, W., Zeng, H., Eissenstat, D. M., and Guo, D. (2013). Variation of first-order root traits across climatic gradients and evolutionary trends in geological time. Glob. Ecol. Biogeogr. 22, 846-856. doi: 10.1111/geb.12048
20. Comas, L. H., and Eissenstat, D. M. (2009). Patterns in root trait variation among 25 co-existing North American forest species. New Phytol. 182, 919-928. doi: 10.1111/j.1469-8137.2009.02799.x
21. Cordell, D., Drangert, J. O., and White, S. (2009). The story of phosphorus: global food security and food for thought. Glob. Environ. Change 19, 292-305. doi: 10.1016/j.gloenvcha.2008.10.009
22. Craine, J. M., Tilman, D., Wedin, D., Reich, P., Tjoelker, M., and Knops, J. (2002). Functional traits, productivity and effects on nitrogen cycling of 33 grassland species. Funct. Ecol. 16, 563-574. doi: 10.1046/j.1365-2435.2002.00660.x
23. Davies, W., and Zhang, J. (1991). Root signals and the regulation of growth and development of plants in drying soil. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42, 55-76. doi: 10.1146/annurev.pp.42.060191. 000415
24. Diggle, A. J. (1988). ROOTMAP - a model in three-dimensional coordinates of the growth and structure of fibrous root systems. Plant Soil 105, 169-178. doi: 10.1007/BF023 76780
25. Donald, C. M. (1962). In search of yield. Aust. J. Agric. Res. 28, 171-178.
26. Donald, C. M. (1968). The breeding of crop ideotypes. Euphytica 17, 385-403. doi: 10.1007/BF00056241
27. Drew, M. C., and Saker, L. R. (1975). Nutrient supply and the growth of the seminal root system in barley, II. Localized, compensatory increases in lateral root growth and rates of nitrate uptake when nitrate supply is restricted to only part of the root system. J. Exp. Bot. 26, 79-90. doi: 10.1093/jxb/26.1.79
28. Dunbabin, V. (2007). Simulating the role of rooting traits in crop-weed competition. Field Crops Res. 104, 44-51. doi: 10.1016/j.fcr.2007. 03.014
29. Dunbabin, V. M., Postma, J. A., Schnepf, A., Pagès, L., Javaux, M., Wu, L., et al. (2013). Modelling root-soil interactions using three-dimensional models of root growth, architecture and function. Plant Soil doi: 10.1007/s11104-013-1769-y
30. Eissenstat, D. M., Wells, C. E., Yanai, R. D., and Whitbeck, J. L. (2000). Building roots in a changing environment: implications for root longevity. New Phytol. 147, 33-42. doi: 10.1046/j.1469-8137.2000.00686.x
31. Fan, M., Zhu, J., Richards, C., Brown, K. M., and Lynch, J. P. (2003). Physiological roles for aerenchyma in phosphorus-stressed roots. Funct. Plant Biol. 30, 493-506. doi: 10.1071/FP03046
32. FAO. (2008). FAO Statistical Database (FAOSTAT). Rome: FAO.
33. FAO, WFP, and IFAD. (2012). The State of Food Insecurity in the World 2012. Economic Growth is Necessary but not Sufficient to Accelerate Reduction of Hunger and Malnutrition. Rome: FAO.
34. Fargione, J., and Tilman, D. (2005). Niche differences in phenology and rooting depth promote coexistence with a dominant C4 bunchgrass. Oecologia 143, 598-606. doi: 10.1007/s00442-005-0010-y
35. Fiorani, F., and Schurr, U. (2013). Future scenarios for plant pheno-typing. Annu. Rev. Plant Biol. 64, 1-25. doi: 10.1146/annurev-arplant-050312-120137
36. Fitter, A. H., and Stickland, T. R. (1992). Fractal characterization of root system architecture. Funct. Ecol. 6, 632-635. doi: 10.2307/2389956
37. Fitter, A. H., Stickland, T. R., Harvey, M. L., and Wilson, G. W. (1991). Architectural analysis of plant root systems 1. Architectural correlates of exploitation efficiency. New Phytol. 118, 375-382. doi: 10.1111/j.1469-8137.1991.tb00018.x
38. Fitter, A., Williamson, L., Linkohr, B., and Leyser, O. (2002). Root system architecture determines fitness in an Arabidopsis mutant in competition for immobile phosphate ions but not for nitrate ions. Proc. R. Soc. Lond. B Biol. Sci. 269, 2017-2022. doi: 10.1098/rspb.2002.2120
39. Funk, C. C., and Brown, M. E. (2009). Declining global per capita agricultural production and warming oceans threaten food security. Food Sec. 1, 271-289. doi: 10.1007/s12571-009-0026-y
40. Furbank, R. T., and Tester, M. (2011). Phenomics - technologies to relieve the phenotyping bottleneck. Trends Plant Sci. 16, 635-644. doi: 10.1016/j.tplants.2011.09.005
41. Galkovskyi, T., Mileyko, Y., Bucksch, A., Moore, B., Symonova, O., Price, C. A., et al. (2012). GiA roots: software for the high throughput analysis of plant root system architecture. BMC Plant Biol. 12:116-128. doi: 10.1186/1471-2229-12-116
42. Goulding, K. (2000). Nitrate leaching from arable and horticultural land. Soil Use Manag. 16, 145-151. doi: 10.1111/j.1475-2743.2000. tb00218.x
43. Grafius, J. E. (1978). Multiple characters and correlated response. Crop Sci. 18, 931-934. doi: 10.2135/crop-sci1978.0011183X001800060004x
44. Granato, T. C., and Raper, C. D. (1989). Proliferation of maize (Zea mays L.) roots in response to localized supply of nitrate. J. Exp. Bot. 40, 263-275. doi: 10.1093/jxb/40.2.263
45. Grift, T. E., Novais, J., and Bohn, M. (2011). High-throughput phe-notyping technology for maize roots. Biosyst. Eng. 110, 40-48. doi: 10.1016/j.biosystemseng.2011. 06.004
46. Gustafsson, A., Ekman, G., and Dorm-ling, I. (1977). Effects of the Pallas gene in barley: phene analysis, overdominance, variability. Hereditas 86, 251-266. doi: 10.1111/j.1601-5223.1977.tb01235.x
47. Harley, J. L. (1989). The significance of mycorrhiza. Mycol. Res. 92, 129-139. doi: 10.1016/S0953-7562(89) 80001-2
48. Hartwell, L. H., Hopfield, J. J., Leibler, S., and Murray, A. W. (1999). From molecular to modular cell biology. Nature 402(Suppl.), C47-C52. doi: 10.1038/35011540
49. Henry, A., Rosas, J. C., Beaver, J. S., and Lynch, J. P. (2010). Multiple stress response and belowground competition in multilines of common bean (Phaseolus vulgaris L.). Field Crops Res. 117, 209-218. doi: 10.1016/j.fcr.2010.03.004
50. Hirel, B., Le Gouis, J., Ney, B., and Gallais, A. (2007). The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J. Exp. Bot. 58, 2369-2387. doi: 10.1093/jxb/erm097
51. Ho, M. D., and Lynch, J. P. (2004). Optimization modeling of plant root architecture for water and phosphorus acquisition. J. Theor. Biol. 226, 331-340. doi: 10.1016/j.jtbi.2003.09.011
52. Ho, M. D., Rosas, J. C., Brown, K. M., and Lynch, J. P. (2005). Root architectural tradeoffs for water and phosphorus acquisition. Funct. Plant Biol. 32, 737-748. doi: 10.1071/FP05043
53. Houle, D., Govindaraju, D. R., and Omholt, S. (2010). Phenomics: the next challenge. Nat. Rev. Genet. 11, 855-866. doi: 10.1038/ nrg2897
54. Ilic, K., Kellogg, E. A., Jaiswal, P., Zapata, F., Stevens, P. F., Vincent, L. P., et al. (2007). The plant structure ontology, a unified vocabulary of anatomy and morphology of a flowering plant. Plant Physiol. 143, 587-599. doi: 10.1104/pp.106.092825
55. James, C. (2000). Global Review of Commercialized Transgenic Crops: 2000. ISAAA Briefs No. 21: Preview. Ithaca, NY: ISAAA.
56. Jaramillo, R. E., Nord, E. A., Chimungu, J. G., Brown, K. M., and Lynch, J. P. (2013). Root cortical burden influences drought tolerance in maize. Ann. Bot. 112, 429-437. doi: 10.1093/aob/mct069
57. Javaux, M., Schröder, T., Vanderborght, J., and Vereecken, H. (2008). Use of a three-dimensional detailed modeling approach for predicting root water uptake. Vadose Zone J. 7, 1079-1088. doi: 10.2136/vzj2007.0115
58. Jenkinson, D. S. (2001). The impact of humans on the nitrogen cycle, with focus on temperate arable agriculture. Plant Soil 128, 3-15. doi: 10.1023/A:1004870606003
59. Katoch, R., and Thakur, N. (2013). Advances in RNA interference technology and its impact on nutritional improvement, disease and insect control in plants. Appl. Biochem. Biotechnol. 169, 1579-1605. doi: 10.1007/s12010-012-0046-5
60. Kell, D. B. (2011). Breeding crop plants with deep roots: their role in sustainable carbon, nutrient, and water sequestration. Ann. Bot. 108, 407-418. doi: 10.1093/aob/mcr175
61. Kelly, J. D., and Adams, M. W. (1987). Phenotypic recurrent selection in ideotype breeding of pinto beans. Euphytica 36, 69-80. doi: 10.1007/BF00730649
62. Kingsolver, J. G., Gomulkiewicz, R., and Carter, P. A. (2001). Variation, selection, and evolution of function-valued traits. Genetica 112-113, 87-104. doi: 10.1023/A:1013323318612
63. Lambers, H., Shane, M. W., Cramer, M. D., Pearse, S. J., and Veneklaas, E. J. (2006). Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann. Bot. 98, 693-713. doi: 10.1093/aob/ mcl114
64. Lechowicz, M. J., and Pierre, A. B. (1988). Assessing the contributions of multiple interacting traits to plant reproductive success: environmental dependence. J. Evol. Biol. 1, 255-273. doi: 10.1046/j.1420-9101.1998.1030255.x
65. Lewontin, R. C. (1970). The Units of Selection. Annu. Rev. Ecol. Syst. 1, 1-18. doi: 10.1146/annurev.es.01. 110170.000245
66. Liao, H., Yan, X., Rubio, G., Beebe, S. E., Blair, M. W., and Lynch, J. P. (2004). Genetic mapping of basal root gravitropism and phosphorus acquisition efficiency in common bean. Funct. Plant Biol. 31, 959-970. doi: 10.1071/FP03255
67. Lynch, J. P. (1995). Root architecture and plant productivity. Plant Physiol. 109, 7-13. doi: 10.1104/pp.109.1.7
68. Lynch, J. P. (2007a). Rhizoeconomics: the roots of shoot growth limitations. HortScience 42, 1107-1109.
69. Lynch, J. P. (2007b). Roots of the second green revolution. Aust. J. Bot. 55, 493-512. doi: 10.1071/ BT06118
70. Lynch, J. P. (2011). Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol. 156, 1041-1049. doi: 10.1104/pp.111.175414
71. 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
72. Lynch, J. P., and Beebe, S. E. (1995). Adaptation of beans (Phaseolus vul-garis L.) to low phosphorus availability. HortScience 30, 1165-1171.
73. Lynch, J. P., and Brown, K. M. (2008). "Root strategies for phosphorus acquisition," in The Ecophysiology of Plant-Phosphorus Interactions, eds P. White and J. Hammond (Berlin: Springer), 83-116. doi: 10.1007/978-1-4020-8435-5_5
74. Lynch, J. P., and Brown, K. M. (2012). New roots for agriculture: exploiting the root phenome. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 1598-1604. doi: 10.1098/rstb.2011.0243
75. Lynch, J. P., and Ho, M. D. (2005). Rhizoeconomics: carbon costs of phosphorus acquisition. Plant Soil 269, 45-56. doi: 10.1007/s11104-004-1096-4
76. Lynch, J. P., Nielsen, K. L., Davis, R. D., and Jablokow, A. G. (1997). Sim-Root: modeling and visualization of root systems. Plant Soil 188, 139-151. doi: 10.1023/A:1004276724310
77. Lynch, J. P., and Rodriguez, H. N. S. (1994). Photosynthetic nitrogen-use efficiency in relation to leaf longevity in common bean. Crop Sci. 34, 1284-1290. doi: 10.2135/crop-sci1994.0011183X003400050027x
78. Ma, Z., Bielenberg, D. G., Brown, K. M., and Lynch, J. P. (2001a). Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant Cell Environ. 24, 459-467. doi: 10.1046/j.1365-3040.2001. 00695.x
79. Ma, Z., Walk, T. C., Marcus, A., and Lynch, J. P. (2001b). Morphological synergism in root hair length, density, initiation, and geometry for phosphorus acquisition in Arabidopsis thaliana: a modeling approach. Plant Soil 236, 221-235. doi: 10.1023/A:1012728819326
80. Madin, J. S., Bowers, S., Schildhauer, M. P., and Jones, M. B. (2008). Advancing ecological research with ontologies. Trends Ecol. Evol. 23, 159-168. doi: 10.1016/j.tree.2007.11.007
81. Mahall, B. E., and Callaway, R. M. (1992). Root communication mechanisms and intracommunity distributions of two Mojave Desert shrubs. Ecology 73, 2145-2151. doi: 10.2307/1941462
82. Marra, M. C., Piggott, N. E., and Goodwin, B. K. (2010). The anticipated value of SmartStaxTM for US corn growers. AgBioForum 13, 1-12.
83. McClean, P. E., Burridge, J., Beebe, S., Rao, I. M., and Porch, T. G. (2011). Crop improvement in the era of climate change: an integrated, multi-disciplinary approach for common bean (Phaseolus vulgaris). Funct. Plant Biol. 38, 927-933. doi: 10.1071/FP11102
84. McCormack, M. L., Adams, T. S., Smithwick, E. A. H., and Eissenstat, D. M. (2012). Predicting fine root lifespan from plant functional traits in temperate trees. New Phytol. 195, 823-831. doi: 10.1111/j.1469-8137.2012.04198.x
85. Michener, W. K. (2006). Metainformation concepts for ecological data management. Ecol. Inform. 1, 3-7. doi: 10.1016/j.ecoinf.2005.08.004
86. Miguel, M. (2012). Basal Root Whorl Number Influences Phosphorus Acquisition in Common Bean (Phaseolus vulgaris). Dissertation, The Pennsylvania State University, University Park.
87. Miguel, M. A., Widrig, A., Vieira, R. F., Brown, K.M., and Lynch, J. P. (2013). Basal root whorl number: a modulator of phosphorus acquisition in common bean (Phaseolus vulgaris). Ann. Bot. doi: 10.1093/aob/mct164 [Epub ahead of print].
88. Miller, C. R., Ochoa, I., Nielsen, K. L., Beck, D., and Lynch, J. P. (2003). Genetic variation for adventitious rooting in response to low phosphorus availability: potential utility for phosphorus acquisition from stratified soils. Funct. Plant Biol. 30, 973-985. doi: 10.1071/FP03078
89. Mock, J. J., and Pearce, R. B. (1975). An ideotype of maize. Euphytica 24, 613-623. doi: 10.1007/BF00132898
90. Murren, C. J. (2002). Phenotypic integration in plants. Plant Species Biol. 17, 89-99. doi: 10.1046/j.1442-1984.2002.00079.x
91. Nord, E. A., Zhang, C., and Lynch, J. P. (2011). Root responses to neighbouring plants in common bean are mediated by nutrient concentration rather than self/non-self recognition. Funct. Plant Biol. 38, 941-952. doi: 10.1071/FP11130
92. Ochoa, I. E., Blair, M. W., and Lynch, J. P. (2006). QTL analysis of adventitious root formation in common bean under contrasting phosphorus availability. Crop Sci. 46, 1609-1621. doi: 10.2135/cropsci2005.12-0446
93. Pieruschka, R., and Poorter, H. (2012). Phenotyping plants: genes, phenes, and machines. Funct. Plant Biol. 39, 813-820. doi: 10.1071/FPv39 n11_IN
94. Pigliucci, M. (2003). Phenotypic integration: studying the ecology and evolution of complex phe-notypes. Ecology Lett. 6, 265-272. doi: 10.1046/j.1461-0248.2003. 00428.x
95. Postma, J. A., and Lynch, J. P. (2010). Theoretical evidence for the functional benefit of root cortical aerenchyma in soils with low phosphorus availability. Ann. Bot. 107, 829-841. doi: 10.1093/ aob/mcq199
96. Postma, J. A., and Lynch, J. P. (2011). Root cortical aerenchyma enhances the growth of maize on soils with suboptimal availability of nitrogen, phosphorus, and potassium. Plant Physiol. 156, 1190-1201. doi: 10.1104/pp.111. 175489
97. 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
98. Pregitzer, K. S., DeForest, J. L., Burton, A. J., Allen, M. F., Ruess, R. W., and Hendrick, R. L. (2002). Fine root architecture of nine North American trees. Ecol. Monogr. 72, 293-309. doi: 10.1890/0012-9615 (2002)072[0293:FRAONN]2.0.CO;2
99. Prusinkiewicz, P. (2004). Modeling plant growth and development. Curr. Opin. Plant Biol. 7, 79-83. doi: 10.1016/j.pbi.2003.11.007
100. Que, Q., Chilton, M.-D. M., De Fontes, C. M., He, C., Nuccio, M., Zhu, T., et al. (2010). Trait stacking in transgenic crops: challenges and opportunities. GM Crops 1, 220-229. doi: 10.4161/gmcr.1.4. 13439
101. Rasmusson, D. C. (1987). An evaluation of ideotype breeding. Crop Sci. 27, 1140-1146. doi: 10.2135/crop-sci1987.0011183X002700060011x
102. Reynolds, M. P., Acevedo, E., Sayre, K. D., and Fischer, R. A. (1994). Yield potential in modern wheat varieties: its association with a less competitive ideotype. Field Crops Res. 37, 149-160. doi: 10.1016/0378-4290(94)90094-9
103. Roberts, T. L. (2009). The role of fertilizer in growing the world's food. Better Crops 93, 12-15.
104. Rubio, G., and Lynch, J. P. (2007). Compensation among root classes in Phaseolus vulgaris L. Plant Soil 290, 307-321. doi: 10.1007/s11104-006-9163-7
105. Ruffel, S., Krouk, G., Ristova, D., Shasha, D., Birnbaum, K. D., and Coruzzi, G. M. (2011). Nitrogen economics of root foraging: transitive closure of the nitrate - cytokinin relay and distinct systemic signaling for N supply vs. demand. Proc. Natl. Acad. Sci. U.S.A. 108, 18524-18529. doi: 10.1073/pnas. 1108684108
106. Schenk, H. J. (2006). Root competition: beyond resource depletion. J. Ecol. 94, 725-739. doi: 10.1111/j.1365-2745.2006.01124.x
107. Serebrovsky, A. S. (1925). "Somatic segregation" in domestic fowl. J. Genet. 16, 33-42. doi: 10.1007/ BF02983986
108. Shen, L., Courtois, B., McNally, K. L., Robin, S., and Li, Z. (2001). Evaluation of near-isogenic lines of rice introgressed with QTLs for root depth through marker-aided selection. Theor. Appl. Genet. 103, 75-83. doi: 10.1007/s001220100538
109. Singh, S., Sidhu, J. S., Huang, N., Vikal, Y., Li, Z., Brar, D. S., et al. (2001). Pyramiding three bacterial blight resistance genes (xa5, xa13, and Xa21) using marker-assisted selection into indica rice cultivar PR106. Theor. Appl. Genet. 102, 1011-1015. doi: 10.1007/s001220000495
110. Steele, K. A., Price, A. H., Shashid-har, H. E., and Witcombe, J. R. (2006). Marker-assisted selection to introgress rice QTLs controlling root traits into an Indian upland rice variety. Theor. Appl. Genet. 112, 208-221. doi: 10.1007/s00122-005-0110-4
111. Then, C. (2011). Potential Synergies That Can Enhance Bt Toxicity in SmartStax. München: Testbiotech e. V - Institute for Independent Impact Assessment in Biotechnology, 1-11.
112. Thornley, J. H. M. (1972). A balanced quantitative model for root:shoot ratios in vegetative plants. Ann. Bot. 36, 431-441.
113. Trachsel, S., Kaeppler, S. M., Brown, K. M., and Lynch, J. P. (2011). Shov-elomics: high throughput phenotyp-ing of maize (Zea mays L.) root architecture in the field. Plant Soil 341, 75-87. doi: 10.1007/s11104-010-0623-8
114. Trachsel, S., Kaeppler, S. M., Brown, K. M., and Lynch, J. P. (2013). Maize root growth angles become steeper under low N conditions. Field Crops Res. 140, 18-31. doi: 10.1016/j.fcr.2012.09.010
115. Violle, C., Navas, M. L., Vile, D., Kazakou, E., Fortunel, C., Hummel, I., et al. (2007). Let the concept of trait be functional Oikos 116, 882-892. doi: 10.1111/j.0030-1299.2007.15559.x
116. Walk, T. C., Jaramillo, R., and Lynch, J. P. (2006). Architectural tradeoffs between adventitious and basal roots for phosphorus acquisition. Plant Soil 279, 347-366. doi: 10.1007/s11104-005-0389-6
117. Walk, T. C., Van Erp, E., and Lynch, J. P. (2004). Modelling applicability of fractal analysis to efficiency of soil exploration by roots. Ann. Bot. 94, 119-128. doi: 10.1093/aob/ mch116
118. Wang, L., Liao, H., Yan, X., Zhuang, B., and Dong, Y. (2004). Genetic variability for root hair traits as related to phosphorus status in soybean. Plant Soil 261, 77-84. doi: 10.1023/B:PLSO.0000035552. 94249.6a
119. West-Eberhard, M. J. (1989). Pheno-typic plasticity and the origins of diversity. Annu. Rev. Ecol. Syst. 20, 249-278. doi: 10.1146/annurev.es.20. 110189.001341
120. Wilberts, S., Suter, M., Walser, N., Edwards, P. J., Olde Venterink, H., and Ramseier, D. (2013). Testing experimentally the effect of soil resource mobility on plant competition. J. Plant Ecol. 1-11. doi: 10.1093/jpe/rtt029
121. Wilson, J. B. (1988). Shoot competition and root competition. J. Appl. Ecol. 25, 279-296. doi: 10.2307/ 2403626
122. Wright, I. J., Reich, P. B., West-oby, M., Ackerly, D. D., Baruch, Z., Bongers, F., et al. (2004). The worldwide leaf economics spectrum. Nature 428, 821-827. doi: 10.1038/ nature02403
123. Wullschleger, S. D., Lynch, J. P., and Berntson, G. M. (1994). Modeling the belowground response of plants and soil biota to edaphic and climatic change - What can we expect to gain? Plant Soil 165, 149-160. doi: 10.1007/BF00009971
124. Yan, X., Liao, H., Beebe, S. E., Blair, M. W., and Lynch, J. P. (2004). QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant Soil 265, 17-29. doi: 10.1007/s11104-005-0693-1
125. Zhu, J., Brown, K. M., and Lynch, J. P. (2010a). Root cortical aerenchyma improves the drought tolerance of maize (Zea mays L.). Plant Cell Environ. 33, 740-749. doi: 10.1111/j.1365-3040.2009.02099.x
126. Zhu, J., Zhang, C., and Lynch, J. P. (2010b). The utility of pheno-typic plasticity of root hair length for phosphorus acquisition. Funct. Plant Biol. 37, 313-322. doi: 10.1071/ FP09197
127. Zhu, J., Ingram, P. A., Benfey, P. N., and Elich, T. (2011). From lab to field, new approaches to phenotyp-ing root system architecture. Curr. Opin. Plant Biol. 14, 310-317. doi: 10.1016/j.pbi.2011.03.020
128. Zhu, J., Kaeppler, S. M., and Lynch, J. P. (2005a). Mapping of QTL controlling root hair length in maize (Zea mays L.) under phosphorus deficiency. Plant Soil 270, 299-310. doi: 10.1007/s11104-004-1697-y
129. Zhu, J., Kaeppler, S. M., and Lynch, J. P. (2005b). Mapping of QTLs for lateral root branching and length in maize (Zea mays L.) under differential phosphorus supply. Theor. Appl. Genet. 111, 688-695. doi: 10.1007/s00122-005-2051-3
130. Zhu, J., and Lynch, J. P. (2004). The contribution of lateral rooting to phosphorus acquisition efficiency in maize (Zea mays) seedlings. Funct. Plant Biol. 31, 949-958. doi: 10.1071/FP04046
131. Zhu, J., Mickelson, S. M., Kaep-pler, S. M., and Lynch, J. P. (2006). Detection of quantitative trait loci for seminal root traits in maize (Zea mays L.) seedlings grown under differential phosphorus levels. Theor. Appl. Genet. 113, 1-10. doi: 10.1007/s00122-006-0260-z
132. Zobel, R. W. (2011). A developmental genetic basis for defining root classes. Crop Sci. 51, 1410-1413. doi: 10.2135/cropsci2010.11. 0652