Digital imaging approaches for phenotyping whole plant nitrogen and phosphorus response in Brachypodium distachyon

Journal of Integrative Plant Biology

Volumn 56, Issue 8, 2014, Pages 781-796

  Poiré, Richard ^a   Chochois, Vincent ^a   Sirault, Xavier R R ^a   Vogel, John P ^b   Watt, Michelle ^a   Furbank, Robert T ^a  

^a CSIRO   (Australia)

^b WESTERN REGIONAL RESEARCH CENTER   (United States)

Author keywords

Nutrients uptake; Phenomics; Photosynthesis; Root; Shoot

Indexed keywords

DIGITAL IMAGE; GENOME; GRASS; GROWTH RATE; GROWTH RESPONSE; NUTRIENT AVAILABILITY; NUTRIENT UPTAKE; PHENOTYPE; PHOSPHORUS; PHOTOSYNTHESIS; ROOT; SHOOT;

BRACHYPODIUM; BRACHYPODIUM DISTACHYON;

NITROGEN; PHOSPHORUS;

BIOLOGICAL MODEL; BIOMASS; BRACHYPODIUM; EVALUATION STUDY; GROWTH, DEVELOPMENT AND AGING; IMAGE PROCESSING; METABOLISM; PHENOTYPE; PHOTOSYNTHESIS; PLANT; PLANT ROOT;

BIOMASS; BRACHYPODIUM; IMAGE PROCESSING, COMPUTER-ASSISTED; MODELS, BIOLOGICAL; NITROGEN; PHENOTYPE; PHOSPHORUS; PHOTOSYNTHESIS; PLANT ROOTS; PLANT SHOOTS;

EID: 84905013487     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/jipb.12198     Document Type: Article

References (76)

1. An DG, Su JY, Liu QY, Zhu YG, Tong YP, Li JM, Jing RL, Li B, Li ZS (2006) Mapping QTLs for nitrogen uptake in relation to the early growth of wheat (Triticum aestivum L.). Plant Soil 284: 73-84
2. Baker NR (2008) Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annu Rev Plant Biol 59: 89-113
3. 2. Oecologia 79: 223-235
4. Berendse F, Aerts R (1987) Nitrogen-use-efficiency: A biologically meaningful definition? Funct Ecol 1: 293-296
5. Bertin P, Gallais A (2001) Genetic variation for nitrogen use efficiency in a set of recombinant inbred lines II-QTL detection and coincidences. Maydica 46: 53-68
6. Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol 24: 225-252
7. Black AL (1970) Adventitious roots, tillers, and grain yields of spring wheat as influenced by N-P fertilization. Agron J 62: 32-36
8. Borell A, Garside AL, Fukai S, Reid DJ (1998) Season nitrogen rate and plant type affect nitrogen uptake and nitrogen use efficiency in rice. Aust J Agric Res 49: 829
9. Chochois V, Vogel JP, Watt M (2012) Application of Brachypodium to the genetic improvement of wheat roots. J Exp Bot 63: 3467-3474
10. Coste S, Baraloto C, Leroy C, Marcon E, Renaud A, Richardson AD, Roggy JC, Schimann H, Uddling J, Herault B (2010) Assessing foliar chlorophyll contents with the SPAD-502 chlorophyll meter: A calibration test with thirteen tree species of tropical rainforest in French Guiana. Ann For Sci 67: 607
11. Dalal RC, Wang WJ, Robertson GP, Parton WJ (2003) Nitrous oxide emission from Australian agricultural lands and mitigation options: A review. Aust J Soil Res 41: 165-195
12. Fageria NK, Wright RJ, Baligar VC (1988) Rice cultivar evaluation for phosphorus use efficiency. Plant Soil 111: 105-109
13. FAO report 2011 (n°4 December 2011) Crop prospects and food. Available on-line: situationhttp://www.fao.org/docrep/014/al983e/al983e00.pdf
14. Furbank RT, Chitty JA, von Caemmerer S, Jenkins CLD (1996) Antisense RNA inhibition of RbcS gene expression reduces Rubisco level and photosynthesis in the C4 plant Flaveria bidentis. Plant Physiol 111: 725-734
15. Furbank RT, Tester M (2011) Phenomics-Technologies to relieve the phenotyping bottleneck. Trends Plant Sci 16: 635-644
16. Gamuyao R, Chin JH, Pariasca-Tanaka J, Pesaresi P, Catausan S, Dalid C, Slamet-Loedin I, Tecson-Mendoza EM, Wissuwa M, Heuer S (2012) The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature 488: 535-539
17. Gedroc JJ, McConnaughay KDM, Coleman JS (1996) Plasticity in root/shoot partitioning: Optimal, ontogenetic, or both? Funct Ecol 10: 44-50
18. Good AG, Johnson SJ, De Pauw M, Carroll RT, Savidov N, Vidmar J, Lu Z, Taylor G, Stroeher V (2007) Engineering nitrogen use efficiency with alanine aminotransferase. Can J Bot 85: 252-262
19. Hammond JP, Broadley MR, White PJ, King GJ, Bowen HC, Hayden R, Meacham MC, Mead A, Overs T, Spracklen WP, Greenwood DJ (2009) Shoot yield drives phosphorus use efficiency in Brassica oleracea and correlates with root architecture traits. J Exp Bot 60: 1953-1968
20. Hill J, Nelson E, Tilman D, Polasky S, Tiffany D (2006) Environmental, economic, and energetic costs and benefits of biodiesel and ethanol biofuels. PNAS 103: 11206-11210
21. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. California Agricultural Experiment Station, Circular - 347. Published 1950 by College of Agriculture, University of California in Berkeley, California
22. Hoffmann WA, Poorter H (2002) Avoiding bias in calculations of relative growth rate. Ann Bot 90: 37-42
23. Ingestad T (1979) Nitrogen stress in birch seedlings. 2. N, K, P, Ca, and Mg nutrition. Physiol Plant 45: 149-157
24. Ingram PA, Zhu JM, Shariff A, Davis IW, Benfey PN, Elich T (2012) High-throughput imaging and analysis of root system architecture in Brachypodium distachyon under differential nutrient availability. Philos Trans R Soc Lond B Biol Sci 367: 1559-1569
25. Ishimaru K, Kobayashi N, Ono K, Yano M, Ohsugi R (2001) Are contents of Rubisco, soluble protein and nitrogen in flag leaves of rice controlled by the same genetics? J Exp Bot 52: 1827-1833
26. Jensen E, Robson P, Norris J, Cookson A, Farrar K, Donnison I, Clifton-Brown J (2013) Flowering induction in the bioenergy grass Miscanthus sacchariflorus is a quantitative short-day response, whilst delayed flowering under long days increases biomass accumulation. J Exp Bot 64: 541-552
27. Koide Y, Tanaka JP, Rose T, Fukuo A, Konisho K, Yanagihara S, Fukuta Y, Wissuwa M (2013) QTLs for phosphorus deficiency tolerance detected in upland NERICA varieties. Plant Breed 132: 259-265
28. Krassovsky I (1926) Physiological activity of the seminal and nodal roots of crop plants. Soil Sci 21: 307-325
29. Laird NM, Ware JH (1982) Random-effects models for longitudinal data. Biometrics 38: 963-974
30. le Gouis J, Beghin D, Heumez E, Pluchard P (2000) Genetic differences for nitrogen uptake and nitrogen utilization efficiencies in winter wheat. Eur J Agron 2: 163-173
31. Leegood RC, Furbank RT (1986) Stimulation of photosynthesis by 2-percent oxygen at low-temperatures is restored by phosphate. Planta 168: 84-93
32. Lewandowski I, Schmidt U (2006) Nitrogen, energy and land use efficiencies of miscanthus, reed canary grass and triticale as determined by the boundary line approach. Agric Ecosyst Environ 112: 335-346
33. Lynch JP (2007) TURNER REVIEW No. 14. Roots of the Second Green Revolution. Aust J Bot 55: 493
34. Lynch JP, Brown KM (2001) Topsoil foraging-An architectural adaptation of plants to low phosphorus availability. Plant Soil 237: 225-237
35. 2-transfer resistance. Plant Physiol 100: 1737-1743
36. Markwell J, Osterman JC, Mitchell JL (1995) Calibration of the Minolta SPAD-502 leaf chlorophyll meter. Photosynth Res 46: 467-472
37. McAllister CH, Beatty PH, Good AG (2012) Engineering nitrogen use efficient crop plants: The current status. Plant Biotech J 10: 1011-1025
38. Moll RH, Kamprath EJ, Jackson WA (1982) Analysis and interpretation of factors which contribute to efficiency of nitrogen-utilization. Agron J 74: 562-564
39. Neset TSS, Cordell D (2012) Global phosphorus scarcity: Identifying synergies for a sustainable future. J Sci Food Agr 92: 2-6
40. Nielsen KL, Eshel A, Lynch JP (2001) The effect of phosphorus availability on the carbon economy of contrasting common bean (Phaseolus vulgaris L.) genotypes. J Exp Bot 52: 329-339
41. Obara M, Kashiba K, Nagano A, Tateshita N, Ebitani T, Yano M, Sato T, Yamaya T (2004) Linkage analysis for QTL associated with panicle number on chromosome 2 in rice (Oryza sativa L.); Toward identification of the regulatory gene. Plant Cell Physiol 45: S126-S126
42. Osmond CB, Grace SC (1995) Perspectives on photoinhibition and photorespiration in the field-quintessential inefficiencies of the light and dark reactions of photosynthesis. J Exp Bot 46: 1351-1362
43. Ozturk L, Eker S, Torun B, Cakmak I (2005) Variation in phosphorus efficiency among 73 bread and durum wheat genotypes grown in a phosphorus-deficient calcareous soil. Plant Soil 269: 69-80
44. Paine CET, Mathews TR, Vogt DR, Purves D, Rees M, Hector A, Turnbull LA (2012) How to fit nonlinear plant growth models and calculate growth rates: An update for ecologists. Meth Ecol Evol 3: 245-256
45. Parry MAJ, Hawkesford MJ (2012) An integrated approach to crop genetic improvement. J Integr Plant Biol 54: 250-259
46. Parry MAJ, Reynolds M, Salvucci ME, Raines C, Andralojc PJ, Zhu XG, Price GD, Condon AG, Furbank RT (2011) Raising yield potential of wheat. II. Increasing photosynthetic capacity and efficiency. J Exp Bot 62: 453-467
47. Passioura JB (2006) The perils of pot experiments. Funct Plant Biol 33: 1075-1079
48. Patterson HD, Thompson R (1971) Recovery of inter-block information when block sizes are unequal. Biometrika 58: 545-554
49. Pellerin S, Mollier A, Plenet D (2000) Phosphorus deficiency affects the rate of emergence and number of maize adventitious nodal roots. Agron J 92: 690-697
50. Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: Meta-analyses of interspecific variation and environmental control. New Phytol 193: 30-50
51. Poorter H, van Rijn CPE, Vanhala TK, Verhoeven KJF, de Jong YEM, Stam P, Lambers H (2005) A genetic analysis of relative growth rate and underlying components in Hordeum spontaneum. Oecologia 142: 360-377
52. Quraishi UM, Abrouk M, Murat F, Pont C, Foucrier S, Desmaizieres G, Confolent C, Riviere N, Charmet G, Paux E, Murigneux A, Guerreiro L, Lafarge S, Le Gouis J, Feuillet C, Salse J (2011) Cross-genome map based dissection of a nitrogen use efficiency ortho-metaQTL in bread wheat unravels concerted cereal genome evolution. Plant J 65: 745-756
53. Reich PB, Oleksyn J, Wright IJ (2009) Leaf phosphorus influences the photosynthesis-nitrogen relation: A cross-biome analysis of 314 species. Oecologia 160: 207-212
54. Reynolds M, Foulkes J, Furbank R, Griffiths S, King J, Murchie E, Parry M, Slafer G (2012) Achieving yield gains in wheat. Plant Cell Environ 35: 1799-1823
55. Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Ryan MH, Veneklaas EJ, Lambers H, Oberson A, Culvenor RA, Simpson RJ (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349: 121-156
56. Robinson N, Fletcher A, Whan A, Critchley C, von Wiren N, Lakshmanan P, Schmidt S (2007) Sugarcane genotypes differ in internal nitrogen use efficiency. Funct Plant Biol 34: 1122-1129
57. Sebilo M, Mayer B, Nicolardot B, Pinay G, Mariotti A (2013) Long-term fate of nitrate fertilizer in agricultural soils. Proc Nat Acad Sci USA 110: 18185-18189
58. Shen JB, Li CJ, Mi GH, Li L, Yuan LX, Jiang RF, Zhang FS (2013) Maximizing root/rhizosphere efficiency to improve crop productivity and nutrient use efficiency in intensive agriculture of China. J Exp Bot 64: 1181-1192
59. Shi L, Shi TX, Broadley MR, White PJ, Long Y, Meng JL, Xu FS, Hammond JP (2013) High-throughput root phenotyping screens identify genetic loci associated with root architectural traits in Brassica napus under contrasting phosphate availabilities. Ann Bot 112: 381-389
60. Shingleton A (2010) Allometry: The study of biological scaling. Nat Educ Knowledge 3: 2
61. Sivak M, Walker DA (1986) Photosynthesis in vivo can be limited by phosphate supply. New Phytol 102: 499-512
62. Solari F, Shanahan JF, Ferguson RB, Adamchuk VI (2010) An active sensor algorithm for corn nitrogen recommendations based on a chlorophyll meter algorithm. Agron J 102: 1090-1098
63. Su JY, Zheng Q, Li HW, Li B, Jing RL, Tong YP, Li ZS (2009) Detection of QTLs for phosphorus use efficiency in relation to agronomic performance of wheat grown under phosphorus sufficient and limited conditions. Plant Sci 176: 824-836
64. Tennant D (1976) Root growth of wheat. 1. Early patterns of multiplication and extension of wheat roots including effects of levels of nitrogen, phosphorus and potassium. Aust J Agric Res 27: 183-196
65. Tessmer OL, Jiao YH, Cruz JA, Kramer DM, Chen J (2013) Functional approach to high-throughput plant growth analysis. BMC Syst Biol 7 (Suppl 6): S17
66. Topp CN, Iyer-Pascuzzi AS, Anderson JT, Lee CR, Zurek PR, Symonova O, Zheng Y, Bucksch A, Mileyko Y, Galkovskyi T, Moore BT, Harer J, Edelsbrunner H, Mitchell-Olds T, Weitz JS, Benfey PN (2013) 3D phenotyping and quantitative trait locus mapping identify core regions of the rice genome controlling root architecture. Proc Natl Acad Sci USA 110: E1695-E1704
67. Uddling J, Gelang-Alfredsson J, Piikki K, Pleijel H (2007) Evaluating the relationship between leaf chlorophyll concentration and SPAD-502 chlorophyll meter readings. Photosynth Res 91: 37-46
68. Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible WR, Shane MW, White PJ, Raven JA (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol 195: 306-320
69. Vesterager JM, Nielsen NE, Hogh-Jensen H (2006) Variation in phosphorus uptake and use efficiencies between pigeonpea genotypes and cowpea. J Plant Nutr 29: 1869-1888
70. Vogel JP, Gu YQ, Twigg P, Lazo GR, Laudencia-Chingcuanco D, Hayden DM, Donze TJ, Vivian LA, Stamova B, Coleman-Derr D (2006) EST sequencing and phylogenetic analysis of the model grass Brachypodium distachyon. Theor Appl Genet 113: 186-195
71. Vogel JP, Tuna M, Budak H, Huo NX, Gu YQ, Steinwand MA (2009) Development of SSR markers and analysis of diversity in Turkish populations of Brachypodium distachyon. BMC Plant Biol 9: 88
72. Walter A, Schurr U (2005) Dynamics of leaf and root growth: Endogenous control versus environmental impact. Ann Bot 95: 891-900
73. Walter A, Silk WK, Schurr U (2009) Environmental effects on spatial and temporal patterns of leaf and root growth. Annu Rev Plant Biol 60: 279-304
74. Watt M, Schneebeli K, Dong P, Wilson IW (2009) The shoot and root growth of Brachypodium and its potential as a model for wheat and other cereal crops. Funct Plant Biol 36: 960-969
75. Wissuwa M, Wegner J, Ae N, Yano M (2002) Substitution mapping of Pup1: A major QTL increasing phosphorus uptake of rice from a phosphorus-deficient soil. Theor Appl Genet 105: 890-897
76. Yaseen M, Malhi SS (2011) Exploitation of genetic variability among wheat genotypes for tolerance to phosphorus deficiency stress. J Plant Nut 34: 665-699