Root anatomical phenes associated with water acquisition from drying soil: Targets for crop improvement

Journal of Experimental Botany

Volumn 65, Issue 21, 2014, Pages 6155-6166

  Lynch, Jonathan P ^a   Chimungu, Joseph G ^a   Brown, Kathleen M ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Aerenchyma; Cereals; Cortex; Drought; Root anatomy; Xylem

Indexed keywords

SOIL; WATER;

ANATOMY AND HISTOLOGY; BREEDING; CROP; PHENOTYPE; PHYSIOLOGY; PLANT ROOT; SOIL;

BREEDING; CROPS, AGRICULTURAL; PHENOTYPE; PLANT ROOTS; SOIL; WATER;

EID: 84907632639     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru162     Document Type: Review

References (132)

1. Abdalla A, Hettiaratchi D, Reece A. 1969. The mechanics of root growth in granular media. Journal of Agricultural Research 14, 236-248.
2. Amthor JS. 2000. The McCree-de Wit-Penning de Vries-Thornley respiration paradigms: 30 years later. Annals of Botany 86, 1-20.
3. Bates TR, Lynch JP. 2001. Root hairs confer a competitive advantage under low phosphorus availability. Plant and Soil 236, 243-250.
4. Bengough AG, Bransby MF, Hans J, McKenna SJ, Roberts TJ, Valentine TA. 2006. Root responses to soil physical conditions; growth dynamics from field to cell. Journal of Experimental Botany 57, 437-447.
5. Bingham IJ. 2007. Quantifying the presence and absence of turgor for the spatial characterization of cortical senescence in roots of Triticum aestivum (Poaceae). American Journal of Botany 94, 2054-2058.
6. Bloom A, Chapin FI, Mooney H. 1985. Resource limitation in plants-an economic analogy. Annual Review of Ecology and Systematics 16, 363-392.
7. Blum A. 2009. Effective use of water (EUW) and not water-use efficiency is the target of crop yield improvement under drought stress. Field Crops Research 112, 119-123.
8. Bouranis DL, Chorianopoulou SN, Siyiannis VF, Protonotarios VE, Hawkesford MJ. 2003. Aerenchyma formation in roots of maize during sulphate starvation. Planta 217, 382-391.
9. Brown LK, George TS, Dupuy LX, White PJ. 2012a. A conceptual model of root hair ideotypes for future agricultural environments: what combination of traits should be targeted to cope with limited P availability? Annals of Botany 112, 317-330.
10. Brown LK, George TS, Thompson JA, Wright G, Lyon J, Dupuy L, Hubbard SF, White PJ. 2012b. What are the implications of variation in root hair length on tolerance to phosphorus deficiency in combination with water stress in barley (Hordeum vulgare)? Annals of Botany 110, 319-328.
11. Bruce WB, Edmeades GO, Barker TC. 2002. Molecular and physiological approaches to maize improvement for drought tolerance. Journal of Experimental Botany 53, 13-25.
12. Burton AL. 2010. Phenotypic evaluation and genetic basis of anatomical and architectural root traits in the genus Zea. PhD thesis, The Pennsylvania State University, University Park, PA, USA.
13. Burton AL, Brown KM, Lynch JP. 2013. Phenotypic diversity of root anatomical and architectural traits in Zea species. Crop Science 53, 1042-1055.
14. Burton AL, Lynch JP, Brown KM. 2012a. Spatial distribution and phenotypic variation in root cortical aerenchyma of maize (Zea mays L.). Plant and Soil 367, 263-274.
15. Burton AL, Williams MS, Lynch JP, Brown KM. 2012b. RootScan: software for high-throughput analysis of root anatomical traits. Plant and Soil 357, 189-203.
16. Clark L, Cope R, Whalley W, Barraclough PB, Wade LJ. 2002. Root penetration of strong soil in rainfed lowland rice: comparison of laboratory screens with field performance. Field Crops Research 76, 189-198.
17. Clark LJ, Price AH, Steele KA, Whalley WR. 2008. Evidence from near-isogenic lines that root penetration increases with root diameter and bending stiffness in rice. Functional Plant Biology 35, 1163-1171.
18. Clark LJ, Whalley WR, Barraclough PB. 2003. How do roots penetrate strong soil? Plant and Soil 255, 93-104.
19. Colmer TD. 2003. Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant, Cell and Environment 26, 17-36.
20. Deacon JW, Drew MC, Darling A. 1986. Progressive cortical senescence and formation of lysigenous gas space (aerenchyma) distinguished by nuclear staining in adventitious roots of Zea mays. Annals of Botany 58, 719-727.
21. Deacon JW, Lewis SJ. 1982. Natural senescence of the root cortex of spring wheat in relation to susceptibility to common root rot (Cochliobolus sativus) and growth of a free-living nitrogen-fixing bacterium. Plant and Soil 66, 13-20.
22. Delhaize E, James RA, Ryan PR. 2012. Aluminium tolerance of root hairs underlies genotypic differences in rhizosheath size of wheat (Triticum aestivum) grown on acid soil. New Phytologist 195, 609-619.
23. Dexter A, Hewitt J. 1978. The deflection of plant roots. Journal of Agricultural Engineering Research 23, 17-22.
24. Drew MC, Jackson MB, Giffard SC, Campbell R. 1981. Inhibition by silver ions of gas space (aerenchyma) formation in adventitious roots of Zea mays L. subjected to exogenous ethylene or to oxygen deficiency. Planta 153, 217-224.
25. Drew MC, Jiu He C, Morgan PW. 1989. Decreased ethylene biosynthesis, and induction of aerenchyma, by nitrogen- or phosphatestarvation in adventitious roots of Zea mays L. Plant Physiology 91, 266-271.
26. Drew MC, Jiu He C, Morgan PW. 2000. Programmed cell death and aerenchyma formation in roots. Trends in Plant Science 5, 123-127.
27. Eghball B, Maranville JW. 1993. Root development and nitrogen influx of corn genotypes grown under combined drought and nitrogen stresses. Agronomy Journal 85, 147-152.
28. Enstone DE, Peterson CA, Ma F. 2003. Root endodermis and exodermis: structure, function, and responses to the environment. Journal of Plant Growth Regulation 21, 335-351.
29. Evans DE. 2003. Aerenchyma formation. New Phytologist 161, 35-49.
30. Fan MS, Bai RQ, Zhao XF, Zhang JH. 2007. Aerenchyma formed under phosphorus deficiency contributes to the reduced root hydraulic conductivity in maize roots. Journal of Integrative Plant Biology 49, 598-604.
31. Fan MS, Zhu JM, Richards C, Brown KM, Lynch JP. 2003. Physiological roles for aerenchyma in phosphorus-stressed roots. Functional Plant Biology 30, 493-506.
32. Fisher MCT, Eissenstat DM, Lynch JP. 2002. Lack of evidence for programmed root senescence in common bean (Phaseolus vulgaris) grown at different levels of phosphorus supply. New Phytologist 153, 63-71.
33. Gahoonia TS, Nielsen NE. 1997. Variation in root hairs of barley cultivars doubled soil phosphorus uptake. Euphytica 98, 177-182.
34. Gahoonia TS, Nielsen NE. 1998. Direct evidence on participation of root hairs in phosphorus (P-32) uptake from soil. Plant and Soil 198, 147-152.
35. Gahoonia TS, Nielsen NE. 2004. Barley genotypes with long root hairs sustain high grain yields in low-P field. Plant and Soil 262, 55-62.
36. 2 loss in adventitious roots of Hordeum marinum. New Phytologist 179, 405-416.
37. Gillespie IMM, Deacon JW. 1988. Effects of mineral nutrients on senescence of the cortex of wheat roots and root pieces. Soil Biology and Biochemistry 20, 525-531.
38. Gowda VRP, Henry A, Yamauchi A, Shashidhar HE, Serraj R. 2011. Root biology and genetic improvement for drought avoidance in rice. Field Crops Research 122, 1-13.
39. Guinel FC, McCully ME. 1986. Some water-related physical properties of maize root-cap mucilage. Plant, Cell and Environment 9, 657-666.
40. Gunawardena AHLA N, Pearce DM, Jackson MB, Hawes CR, Evans DE. 2001. Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta 212, 205-214.
41. Haling RE, Brown LK, Bengough AG, Young IM, Hallett PD, White PJ, George TS. 2013. Root hairs improve root penetration, root-soil contact, and phosphorus acquisition in soils of different strength. Journal of Experimental Botany 64, 3711-3721.
42. Haling RE, Richardson AE, Culvenor RA, Lambers H, Simpson RJ. 2010a. Root morphology, root-hair development and rhizosheath formation on perennial grass seedlings is influenced by soil acidity. Plant and Soil 335, 457-468.
43. Haling R, Simpson R, Delhaize E, Hocking P, Richardson A. 2010b. Effect of lime on root growth, morphology and the rhizosheath of cereal seedlings growing in an acid soil. Plant and Soil 327, 199-212.
44. Hansey CN, Johnson JM, Sekhon RS, Kaeppler SM, De Leon N. 2011. Genetic diversity of a maize association population with restricted phenology. Crop Science 51, 704.
45. Haque ME, Chang TT, Tepora N, Loresto GC. 1989. Root characters as selection indices for drought resistance in rice. Philippine Journal of Crop Science 14, 7-9.
46. Hawes MC, Brigham LA, Wen F, Woo HH, Zhu Y. 1998. Function of root border cells in plant heath: pioneers in the rhizosphere. Annual Review of Phytopathology 36, 311.
47. Henry A. 2013. IRRI's drought stress research in rice with emphasis on roots: accomplishments over the last 50 years. Plant Root 7, 92-106.
48. Henry A, Cal AJ, Batoto TC, Torres RO, Serraj R. 2012. Root attributes affecting water uptake of rice (Oryza sativa) under drought. Journal of Experimental Botany 63, 4751-4763.
49. Henry A, Gowda VRP, Torres RO, McNally KL, Serraj R. 2011. Variation in root system architecture and drought response in rice (Oryza sativa): phenotyping of the OryzaSNP panel in rainfed lowland fields. Field Crops Research 120, 205-214.
50. Henry C, Deacon JW. 1981. Natural (non-pathogenic) death of the cortex of wheat and barley seminal roots, as evidenced by nuclear staining with acridine orange. Plant and Soil 60, 255-274.
51. Hettiaratchi D. 1990. Soil compaction and plant root growth. Philosophical Transactions of the Royal Society B: Biological Sciences 329, 343-355.
52. Hose E, Clarkson DT, Steudle E, Schreiber L, Hartung W. 2001. The exodermis: a variable apoplastic barrier. Journal of Experimental Botany 52, 2245-2264.
53. Hu B, Henry A, Brown KM, Lynch JP. 2014. Root cortical aerenchyma inhibits radial nutrient transport in maize (Zea mays L.). Annals of Botany 113, 181-189.
54. Hunt R. 1982. Plant growth curves: the functional approach to plant growth analysis. London: Edward Arnold.
55. Jackson MB, Armstrong W. 1999. Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence. Plant Biology 1, 274-287.
56. Jaramillo RE, Nord EA, Chimungu JG, Brown KM, Lynch JP. 2013. Root cortical burden influences drought tolerance in maize. Annals of Botany 112, 1-9.
57. Jiang Z, Song X, Zhou Z, Wang L, Li J, Deng X, Fan H. 2010. Aerenchyma formation: programmed cell death in adventitious roots of winter wheat (Triticum aestivum) under waterlogging. Functional Plant Biology 37, 748-755.
58. Kirby J, Bengough A. 2002. Influence of soil strength on root growth: experiments and analysis using a critical-state model. European Journal of Soil Science 53, 119-128.
59. Kirk JJ, Deacon JW. 1987. Invasion of naturally senescing root cortices of cereal and grass seedlings by Microdochium bolleyi. Plant and Soil 98, 239-246.
60. Kondo M, Aguilar A, Abe J, Morita S. 2000. Anatomy of nodal roots in tropical upland and lowland rice varieties. Plant Production Science 3, 437-445.
61. Krishnamurthy P, Ranathunge K, Nayak S, Schreiber L, Mathew MK. 2011. Root apoplastic barriers block Na+ transport to shoots in rice (Oryza sativa L.). Journal of Experimental Botany 62, 4215-28.
62. Lambers H, Atkin OK, Millenaar FF. 2002. Respiratory patterns in roots in relation to their functioning. In: Waisel Y, Eshel A, Kafkaki K, eds. Plant roots: the hidden half. New York: Marcel Dekker, Inc., 521-552.
63. Lascaris D, Deacon JW. 1991a. Comparison of methods to assess senescence of the cortex of wheat and tomato roots. Soil Biology and Biochemistry 23, 979-986.
64. Lascaris D, Deacon JW. 1991b. Relationship between root cortical senescence and growth of wheat as influenced by mineral nutrition, Idriella bolleyi (Sprague) von Arx and pruning of leaves. New Phytologist 118, 391-396.
65. Lee R. 2011. The outlook for population growth. Science 333, 569-573.
66. Liedgens M, Richner W. 2001. Minirhizotron observations of the spatial distribution of the maize root system. Agronomy Journal 93, 1097-1104.
67. Liljeroth E. 1995. Comparisons of early root cortical senescence between barley cultivars, Triticum species and other cereals. New Phytologist 130, 495-501.
68. Liljeroth E, Bryngelsson T. 2001. DNA fragmentation in cereal roots indicative of programmed root cortical cell death. Physiologia Plantarum 111, 365-372.
69. Lingua G, Sgorbati S, Citterio A, Fusconi A, Trotta A, Gnavi E, Berta G. 1999. Arbuscular mycorrhizal colonization delays nucleus senescence in leek root cortical cells. New Phytologist 141, 161-169.
70. Lobell DB, Gourdji SM. 2012. The influence of climate change on global crop productivity. Plant Physiology 160, 1686-1697.
71. Lynch JP. 1995. Root architecture and plant productivity. Plant Physiology 109, 7-13.
72. Lynch JP. 2007. Roots of the second green revolution. Australian Journal of Botany 55, 493-512.
73. Lynch JP. 2011. Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiology 156, 1041-1049.
74. Lynch JP. 2013. Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Annals of Botany 112, 347-357.
75. Lynch JP, Brown KM. 2006. Whole plant adaptations to low phosphorus availability. In: Huang B, ed. Plant-environment interactions. Boca Raton, FL: Taylor & Francis, 209-242.
76. Lynch JP, Brown KM. 2008. Root strategies for phosphorus acquisition. In: White PJ, Hammond JP, eds. The ecophysiology of plant-phosphorus interaction. Dordrecht: Springer, 83-116.
77. Lynch JP, Brown KM. 2012. New roots for agriculture: exploiting the root phenome. Philosophical Transactions of the Royal Society B: Biological Sciences 367, 1598-1604.
78. Lynch JP, Ho MD. 2005. Rhizoeconomics: carbon costs of phosphorus acquisition. Plant and Soil 269, 45-56.
79. Lynch JP, Nielsen KL, Davis RD, Jablokow AG. 1997. SimRoot: modelling and visualization of root systems. Plant and Soil 188, 139-151.
80. Ma F, Peterson CA. 2003. Current insights into the development, structure, and chemistry of the endodermis and exodermis of roots. Canadian Journal of Botany 421, 405-421.
81. Mano Y, Omori F. 2008. Verification of QTL controlling root aerenchyma formation in a maizexteosinte 'Zea nicaraguensis' advanced backcross population. Breeding Science 58, 217-223.
82. Mano Y, Omori F. 2009. High-density linkage map around the root aerenchyma locus Qaer1.06 in the backcross populations of maize Mi29xteosinte 'Zea nicaraguensis'. Breeding Science 59, 427-433.
83. Manschadi AM, Christopher J, De Voil P, Hammer GL. 2006. The role of root architectural traits in adaptation of wheat to water-limited environments. Functional Plant Biology 33, 823-837.
84. Mapfumo E, Aspinall D, Hancock T. 1994. Vessel-diameter distribution in roots of grapevines (Vitis vinifera L. cv. Shiraz). Plant and Soil 160, 49-55.
85. Materechera SA, Dexter AR, Alston AM. 1991. Penetration of very strong soils by seedling roots of different plant species. Plant and Soil 135, 31-41.
86. McCully M. 1995. How do real roots work-some new views of root structure. Plant Physiology 109, 1-6.
87. McCully ME. 1999. Roots in soil: unearthing the complexities of roots and their rhizospheres. Annual Review of Plant Physiology and Plant Molecular Biology 50, 695-718.
88. McElrone AJ, Pockman WT, Martinez-Vilalta J, Jackson RB. 1999. Variation in xylem structure and function in stems and roots of trees to 20 m depth. New Phytologist 163, 507-517.
89. McKenzie BM, Bengough A. G, Hallett PD, Thomas WTB, Forster B, McNicol JW. 2009. Deep rooting and drought screening of cereal crops: a novel field-based method and its application. Field Crops Research 112, 165-171.
90. Nambiar EKS. 1976. Uptake of Zn65 from dry soil by plants. Plant and Soil 44, 267-271.
91. Nielsen KL, Bouma TJ, Lynch JP, Eissenstat DM. 1998. Effects of phosphorus availability and vesicular-arbuscular mycorrhizas on the carbon budget of common bean (Phaseolus vulgaris). New Phytologist 139, 647-656.
92. Nielsen KL, Eshel A, Lynch JP. 2001. The effect of phosphorus availability on the carbon economy of contrasting common bean (Phaseolus vulgaris L.) genotypes. Journal of Experimental Botany 52, 329-339.
93. North GB, Nobel PS. 1995. Hydraulic conductivity of concentric root tissues of Agave deserti Engelm. under wet and drying conditions. New Phytologist 130, 47-57.
94. North GB, Nobel PS. 1996. Radial hydraulic conductivity of individual root tissues of Opuntia ficus-indica (L.) Miller as soil moisture varies. Annals of Botany 77, 133-142.
95. North GB, Nobel PS. 1997. Drought-induced changes in soil contact and hydraulic conductivity for roots of Opuntia ficus-indica with and without rhizosheaths. Plant and Soil 191, 249-258.
96. Palta JA, Gregory PJ. 1997. Drought affects the fluxes of carbon to roots and soil in 13C pulse-labelled plants of wheat. Soil Biology and Biochemistry 29, 1395-1403.
97. Passioura JB. 1983. Roots and drought resistance. Agricultural Water Management 7, 265-280.
98. Poorter H, Remkes C. 1990. Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate. Oecologia 83, 553-559.
99. Postma JA, Lynch JP. 2010. Theoretical evidence for the functional benefit of root cortical aerenchyma in soils with low phosphorus availability. Annals of Botany 107, 829-841.
100. Postma JA, Lynch JP. 2011. Root cortical aerenchyma enhances the growth of maize on soils with suboptimal availability of nitrogen, phosphorus, and potassium. Plant Physiology 156, 1190-1201.
101. Przywara G, Stepniewski W. 2000. Influence of flooding and different temperatures of the soil on gas-filled porosity of pea, maize and winter wheat roots. International Agrophysics 14, 401-410.
102. Ranathunge K, Schreiber L. 2011. Water and solute permeabilities of Arabidopsis roots in relation to the amount and composition of aliphatic suberin. Journal of Experimental Botany 62, 1961-74.
103. Ranathunge K, Steudle E, Lafitte R. 2005. Blockage of apoplastic bypass-flow of water in rice roots by insoluble salt precipitates analogous to a Pfeffer cell. Plant, Cell and Environment 28, 121-133.
104. Richards RA, Passioura JB. 1981a. Seminal root morphology and water-use of wheat. 1. Environmental effects. Crop Science 21, 249-252.
105. Richards RA, Passioura JB. 1981b. Seminal root morphology and water use of wheat. II. Genetic variation. Crop Science 21, 253-255.
106. Richards RA, Passioura JB. 1989. A breeding program to reduce the diameter of the major xylem vessel in the seminal roots of wheat and its effect on grain yield in rain-fed environments. Australian Journal of Agricultural Research 40, 943-950.
107. Rincon CA, Raper CD, Patterson RP. 2003. Genotypic differences in root anatomy affecting water movement through roots of soybean. International Journal of Plant Sciences 164, 543-551.
108. Roberts L. 2011. 9 Billion? Science 333, 540-573.
109. Robinson D. 1990. Phosphorus availability and cortical senescence in cereal roots. Journal of Theoretical Biology 145, 257-265.
110. Saengwilai P. 2013. Root traits for efficient nitrogen acquisition and genome-wide association study of root anatomical traits in maize (Zea mays L.). PhD thesis, The Pennsylvania State University, University Park, PA, USA.
111. Sponchiado BN, White JW, Castillo JA, Jones PG. 1989. Root growth of four common bean cultivars in relation to drought tolerance in environments with contrasting soil types. Experimental Agriculture 25, 249-257.
112. Steudle E. 2000. Water uptake by plant roots: an integration of views. Plant and Soil 226, 45-56.
113. Striker GG, Insausti P, Grimoldi AA, Vega AS. 2007. Trade-off between root porosity and mechanical strength in species with different types of aerenchyma. Plant, Cell and Environment 30, 580-589.
114. Sutka M, Li G, Boudet J, Boursiac Y, Doumas P, Maurel C. 2011. Natural variation of root hydraulics in Arabidopsis grown in normal and salt-stressed conditions. Plant Physiology 155, 1264-1276.
115. Trachsel S, Kaeppler S, Brown KM, Lynch JP. 2011. Shovelomics: high throughput phenotyping of maize (Zea mays L.) root architecture in the field. Plant and Soil 341, 75-87.
116. Uga Y, Okuno K, Yano M. 2008. QTLs underlying natural variation in stele and xylem structures of rice root. Breeding Science 58, 7-14.
117. Vasellati V, Oesterheld M, Medan D, Loreti J. 2001. Effects of flooding and drought on the anatomy of Paspalum dilatatum. Annals of Botany 88, 355-360.
118. Vermeer J, McCully ME. 1982. The rhizosphere in Zea: new insight into its structure and development. Planta 156, 45-61.
119. Walker TS, Bais HP, Grotewold E, Vivanco JM. 2003. Root exudation and rhizosphere biology. Plant Physiology 132, 44-51.
120. Watt M, McCully ME, Canny MJ. 1994. Formation and stabilization of rhizosheaths of Zea mays L. (Effect of soil water content). Plant Physiology 106, 179-186.
121. Watt M, Wasson A, Chochois V. 2013. Root-based solutions to increasing crop productivity. In: Eshel A, Beeckman T, eds. Plant roots: the hidden half. Boca Raton, FL: CRC Press, 21-1-21-17.
122. Wenzel CL, McCully ME. 1991. Early senescence of cortical cells in the roots of cereals. How good is the evidence? American Journal of Botany 78, 1528-1541.
123. Whalley WR, Dodd IC, Watts CW, Webster CP, Phillips AL, Andralojc J, White RP, Davies WJ, Parry MAJ. 2012. Genotypic variation in the ability of wheat roots to penetrate wax layers. Plant and Soil 364, 171-179.
124. White JW, Castillo JA. 1989. Relative effect of root and shoot genotypes on yield of common bean under drought stress. Crop Science 29, 360-362.
125. Whiteley G, Hewitt J, Dexter A. 1982. The buckling of plant roots. Physiologia Plantarum 54, 333-342.
126. Wissuwa M. 2003. How do plants achieve tolerance to phosphorus deficiency? Small causes with big effects. Plant Physiology 133, 1947-1958.
127. Yambao EB, Ingram KT, Real JG. 1992. Root xylem influence on the water relations and drought resistance of rice. Journal of Experimental Botany 43, 925-932.
128. Yeates JS, Parker CA. 1986. Rate of natural senescence of seminal root cortical cells of wheat, barley and oats, with reference to invasion by Gaeumannomyces graminis. Transactions of the British Mycological Society 86, 683-685.
129. York LM, Nord EA, Lynch JP. 2013. Integration of root phenes for soli resource acquisition. Frontiers in Plant Science 4, article 355.
130. Young IM. 1995. Variation in moisture contents between bulk soil and the rhizosheath of wheat (Triticum aestivum L. cv. Wembley). New Phytologist 130, 135-139.
131. Zhu JM, Brown KM, Lynch JP. 2010a. Root cortical aerenchyma improves the drought tolerance of maize (Zea mays L.). Plant, Cell and Environment 33, 740-749.
132. Zhu J, Zhang C, Lynch JP. 2010b. The utility of phenotypic plasticity of root hair length for phosphorus acquisition. Functional Plant Biology 37, 313-322.