Root-type-specific plasticity in response to localized high nitrate supply in maize (Zea mays)

Annals of Botany

Volumn 116, Issue 5, 2015, Pages 751-762

  Yu, Peng ^a,b   Hochholdinger, Frank ^b   Li, Chunjian ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

Embryonic root; lateral root; localized high nitrate supply; maize; morphological plasticity; shoot borne root; split root system; Zea mays

Indexed keywords

ANATOMY; GENETIC VARIATION; GROWTH RATE; MAIZE; MORPHOLOGY; NITRATE; NUTRIENT AVAILABILITY; NUTRIENT UPTAKE; NUTRIENT USE EFFICIENCY; PHENOTYPIC PLASTICITY; ROOT; SEEDLING; SHOOT; XYLEM;

ZEA MAYS;

NITRIC ACID DERIVATIVE;

GENETICS; GROWTH, DEVELOPMENT AND AGING; MAIZE; METABOLISM; PHENOTYPE; PLANT ROOT; SEEDLING;

NITRATES; PHENOTYPE; PLANT ROOTS; SEEDLINGS; ZEA MAYS;

EID: 84943545826     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcv127     Document Type: Article

References (75)

1. Comas L, Bouma T, Eissenstat D. 2002. Linking root traits to potential growth rate in six temperate tree species. Oecologia 132: 34-43
2. Comas LH, Eissenstat DM. 2004. Linking fine root traits to maximum potential growth rate among 11 mature temperate tree species. Functional Ecology 18: 388-397
3. Crawford NM. 1995. Nitrate: nutrient and signal for plant growth. The Plant Cell 7: 859-868
4. Dolan L, Janmaat K, Willemsen V, et al. 1993. Cellular organization of the Arabidopsis thaliana root. Development 119: 71-84
5. Drew MC. 1975. Comparison of the effects of a localised supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytologist 75: 479-490
6. Drew MC, Saker LR. 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. Journal of Experimental Botany 26: 79-90
7. Drew MC, Saker LR, Ashley TW. 1973. Nutrient supply and the growth of the seminal root system in barley. I. The effect of nitrate concentration on the growth of axes and laterals. Journal of Experimental Botany 83: 1189-1202
8. Dubrovsky JG, Rost TL, Colon-Carmona A, Doerner P. 2001. Early primordium morphogenesis during lateral root initiation in Arabidopsis thaliana. Planta 214: 30-36
9. Dunbabin V, Diggle A, Rengel Z. 2003. Is there an optimal root architecture for nitrate capture in leaching environments?. Plant, Cell and Environment 26: 835-844
10. Eissenstat DM. 1991. On the relationship between specific root length and the rate of root proliferation: a field study using citrus rootstocks. New Phytologist 118: 63-68
11. Eissenstat DM, Achor DS. 1999. Anatomical characteristics of roots of citrus rootstocks that vary in specific root length. New Phytologist 141: 309-321
12. Eissenstat DM, Caldwell MM. 1988. Seasonal timing of root growth in favorable microsites. Ecology 69: 870-873
13. Eissenstat DM, Yanai RD. 1997. The ecology of root lifespan. Advanced Ecological Research 27: 1-60
14. Eissenstat DM, Wells CE, Yanai RD, Whitbeck JL. 2000. Building roots in a changing environment: implications for root longevity. New Phytologist 147: 33-42
15. Fahn A. 1990. Plant anatomy, 4th edn. New York: Pergamon Press
16. Farley RA, Fitter AH. 1999. The response of seven co-occurring woodland herbaceous perennials to localized nutrient-rich patches. Journal of Ecology 87: 849-859
17. Feldman L. 1994. The maize root. In: M Freeling, V Walbot, eds. The maize handbook. New York: Springer-Verlag, 29-37
18. Fitter AH. 1994. Architecture and biomass allocation as components of the plastic response of root systems to soil heterogeneity. In: MM Caldwell, RW Pearcy, eds. Exploitation of environmental heterogeneity of plants. New York: Academic Press, 305-323
19. Fitter A, Williamson L, Linkohr B, Leyser O. 2002. Root system architecture determines fitness in an Arabidopsis mutant in competition for immobile phosphate ions but not for nitrate ions. Proceedings of the Royal Society B: Biological Sciences 269: 2017-2022
20. Fransen B, Blijjenberg J, de Kroon H. 1999. Root morphological and physiological plasticity of perennial grass species and the exploitation of spatial and temporal heterogeneous nutrient patches. Plant and Soil 211: 179-189
21. Gallais A, CoqueM, Quilléré I, Prioul J, Hirel B. 2006. Modelling postsilking nitrogen fluxes in maize (Zea mays) using 15N-labelling field experiments. New Phytologist 172: 696-707
22. Gao K, Chen F, Yuan L, Zhang F, Mi G. 2014. A comprehensive analysis of root morphological changes and nitrogen allocation in maize in response to low nitrogen stress. Plant, Cell and Environment 38: 740-750
23. Gaudin A, McClymont SA, Holmes BM, Lyons E, RaizadaMN. 2011. 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 and Environment 34: 2122-2137
24. Gifford ML, Dean A, Gutierrez RA, Coruzzi GM, Birnbaum KD. 2008. Cell-specific nitrogen responses mediate developmental plasticity. Proceedings of the National Academy of Sciences, USA 105: 803-808
25. Gilroy S, Trewavas A. 2001. Signal processing and transduction in plant cells: the end of the beginning?. Nature Reviews Molecular Cell Biology 2: 307-314
26. Granato TC, Raper CD. 1989. Proliferation of maize (Zea mays L.) roots in response to localized supply of nitrate. Journal of Experimental Botany 40: 263-275
27. Hammer GL, Dong Z, McLean G, Doherty A, Messina C. 2009. Can changes in canopy and/or root system architecture explain historical maize yield trends in the U.S. corn belt?. Crop Science 49: 299-312
28. Hochholdinger F. 2009. The maize root system: morphology, anatomy and genetics. In: J Bennetzen, S Hake, eds. Handbook of maize: its biology. New York: Springer, 145-160
29. Hochholdinger F, Tuberosa R. 2009. Genetic and genomic dissection of maize root development and architecture. Current Opinion in Plant Biology 12: 172-177
30. Hochholdinger F, Zimmermann R. 2008. Conserved and diverse mechanisms in root development. Current Opinion in Plant Biology 11: 70-74
31. Hochholdinger F, Park WJ, Sauer M, Woll K. 2004. From weeds to crop: genetic analysis of root development in cereals. Trends in Plant Science 9: 42-48
32. Hodge A. 2004. The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytologist 162: 9-24
33. Hodge A. 2006. Plastic plants and patchy soils. Journal of Experimental Botany 57: 401-411
34. Hodge A, Robinson D, Griffiths BS, Fitter AH. 1999. Nitrogen capture by plants grown in N-rich organic patches of contrasting size and strength. Journal of Experimental Botany 50: 1243-1252
35. Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH. 2000. Spatial and physical heterogeneity of N supply from soil does not influence N capture by two grass species. Functional Ecology 14: 645-653
36. Hoecker N, Keller B, Piepho HP, Hochholdinger F. 2006. Manifestation of heterosis during early maize (Zea mays L.) root development. Theoretical and Applied Genetics 112: 421-429
37. Hoppe DC, McCully ME, Wenzel CL. 1986. The nodal roots of Zea: their development in relation to structural features of the stem. Canadian Journal of Botany 64: 2524-2537
38. Jackson RB, Caldwell MM. 1989. The timing and degree of root proliferation in fertile-soil microsites for three cold-desert perennials. Oecologia 81: 149-153
39. Krouk G, Lacombe B, Bielach A, et al. 2010. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Developmental Cell 18: 927-937
40. Kumpf RP, Shi CL, Larrieu A, et al. 2013. Floral organ abscission peptide IDA and its HAE/HSL2 receptors control cell separation during lateral root emergence. Proceedings of the National Academy of Sciences, USA 110: 5235-5240
41. Lynch JP. 2007. Roots of the second green revolution. Australian Journal of Botany 55: 493-512
42. Lynch JP. 2011. Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiology 156: 1041-1049
43. Lynch JP. 2013. Steep, cheap and deep: an ideotype to optimize water and N acquisition bymaize root systems. Annals of Botany 112: 347-357
44. 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
45. Malamy JE. 2005. Intrinsic and environmental response pathways that regulate root system architecture. Plant, Cell and Environment 28: 67-77
46. Marschner P. 2012. Mineral nutrition of higher plants, 3rd edn. London: Academic Press
47. McCullyME. 1995. How do real roots work?. Plant Physiology 109: 1-6
48. McCully ME, Canny MJ. 1988. Pathways and processes of water and nutrient movements in roots. Plant and Soil 111: 159-170
49. Mounier E, Pervent M, Ljung K, Gojon A, Nacry P. 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 and Environment 37: 162-174
50. Nelson DW, Somers LE. 1973. Determination of total nitrogen in plant material. Agronomy Journal 65: 109-112
51. Nibau C, Gibbs DJ, Coates JC. 2008. Branching out in new directions: the control of root architecture by lateral root formation. New Phytologist 179: 595-614
52. Niu JF, Peng YF, Li CJ, Zhang FS. 2010. Changes in root length at the reproductive stage of maize plants grown in the field and quartz sand. Journal of Plant Nutrition and Soil Science 173: 306-314
53. Orman-Ligeza B, Parizot B, Gantet PP, Beeckman T, BennettMJ, Draye X. 2013. Post-embryonic root organogenesis in cereals: branching out from model plants. Trends in Plant Science 18: 459-467
54. Paschold A, Marcon C, Hoecker N, Hochholdinger F. 2010. Molecular dissection of heterosis manifestation during early maize root development. Theoretical and Applied Genetics 120: 383-388
55. Peng Y, Niu J, Peng Z, Zhang F, Li C. 2010. Shoot growth potential drives N uptake in maize plants and correlates with root growth in the soil. Field Crops Research 115: 85-93
56. Peng Y, Li X, Li C. 2012. Temporal and spatial profiling of root growth revealed novel response of maize roots under various nitrogen supplies in the field. PLoS One 7: e37726
57. Peterson CA, Enstone DE. 1996. Functions of passage cells in the endodermis and exodermis of roots. Physiologia Plantarum 97: 592-598
58. Postma J A, Dathe A, Lynch J. 2014. The optimal lateral root branching density for maize depends on nitrogen and phosphorus availability. Plant Physiology 166: 590-602
59. Robinson D, Hodge A, Griffiths BS, Fitter AH. 1999. Plant root proliferation in nitrogen-rich patches confers competitive advantage. Proceedings of the Royal Society B: Biological Sciences 266: 431-435
60. Rose TJ, Impa SM, Rose MT, et al. 2012. Enhancing phosphorus and zinc acquisition efficiency in rice: a critical review of root traits and their potential utility in rice breeding. Annals of Botany 112: 331-345
61. Ruffel S, Krouk G, Ristova D, Shasha D, Birnbaum KD, Coruzzi GM. 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, USA 108: 18524-18529
62. Saengwilai P, Tian X, Lynch J. 2014a. Low crown root number enhances nitrogen acquisition from low nitrogen soils in maize (Zea mays L.). Plant Physiology 166: 581-589
63. Saengwilai P, Nord E, Chimungu J, Brown K, Lynch J. 2014b. Root cortical aerenchyma enhances nitrogen acquisition from low nitrogen soils in maize (Zea mays L.). Plant Physiology 166: 726-735
64. Schortmeyer M, Feil B, Stamp P. 1993. Root morphology and nitrogen uptake of maize simultaneously supplied with ammonium and nitrate in a split-root system. Annals of Botany 72: 107-115
65. ShaneMW, McCullyME. 1999. Root xylem embolisms: implications for water flow to the shoot in single-rooted maize plants. Australian Journal of Plant Physiology 26: 107-114
66. Singh V, van Oost EJ, Jordan DR, Messina CD, Cooper M, Hammer GL. 2010. Morphological and architectural development of root systems in sorghum and maize. Plant and Soil 333: 287-299
67. Smith S, De Smet I. 2012. Root system architecture: insights from Arabidopsis and cereal crops. Philosophical Transactions of the Royal Society B: Biological Sciences 367: 1441-1452
68. Vidal E A, Araus V, Lu C, et al. 2010. Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 107: 4477-4482
69. Vidal EA, Moyano TC, Riveras E, Contreras-López O, Gutiérrez RA. 2013.Systems approaches map regulatory networks downstream of the auxin receptor AFB3 in the nitrate response of Arabidopsis thaliana roots. Proceedings of the National Academy of Sciences, USA 110: 12840-12845
70. Walch-Liu P, Ivanov II, Filleur S, Gan Y, Remans T, Forde BG. 2006. Nitrogen regulation of root branching. Annals of Botany 97: 875-881
71. Wang XL, McCully ME, Canny MJ. 1994. The branch roots of Zea. IV. The maturation and openness of xylem conduits in first-order branches of soil-grown roots. New Phytologist 126: 21-29
72. Yu P, Li X, Yuan L, Li C. 2014a. A novel morphological response of maize (Zea mays) adult roots to heterogeneous nitrate supply revealed by a splitroot experiment. Physiologia Plantarum 150: 133-144
73. Yu P, White PJ, Hochholdinger F, Li C. 2014b. Phenotypic plasticity of the maize root system in response to heterogeneous nitrogen availability. Planta 240: 667-678
74. Zhang H, Forde BG. 1998. An ArabidopsisMADS box gene that controls nutrient-induced changes in root architecture. Science 279: 407-409
75. Zhu J, Ingram PA, Benfey PN, Elich T. 2011. From lab to field, new approaches to phenotyping root system architecture. Current Opinion in Plant Biology 14: 310-317