Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Counting the costs: nitrogen partitioning in Sorghum mutants

Cecilia K. Blomstedt A , Viviana C. Rosati A , Birger Lindberg Møller B and Ros Gleadow A C
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences, Monash University, Clayton, Vic. 3800, Australia.

B Plant Biochemistry Laboratory and VILLUM Research Centre for Plant Plasticity, Department of Plant and Environmental Sciences, University of Copenhagen, 40 Thorvaldsensvej, DK-1871 Frederiksberg C, Copenhagen, Denmark.

C Corresponding author. Email: ros.gleadow@monash.edu

Functional Plant Biology 45(7) 705-718 https://doi.org/10.1071/FP17227
Submitted: 11 August 2017  Accepted: 14 January 2018   Published: 21 February 2018

Abstract

Long-standing growth/defence theories state that the production of defence compounds come at a direct cost to primary metabolism when resources are limited. However, such trade-offs are inherently difficult to quantify. We compared the growth and nitrogen partitioning in wild type Sorghum bicolor (L.) Moench, which contains the cyanogenic glucoside dhurrin, with unique mutants that vary in dhurrin production. The totally cyanide deficient 1 (tcd1) mutants do not synthesise dhurrin at all whereas mutants from the adult cyanide deficient class 1 (acdc1) have decreasing concentrations as plants age. Sorghum lines were grown at three different concentrations of nitrogen. Growth, chemical analysis, physiological measurements and expression of key genes in biosynthesis and turnover were determined for leaves, stems and roots at four developmental stages. Nitrogen supply, ontogeny, tissue type and genotype were all important determinants of tissue nitrate and dhurrin concentration and turnover. The higher growth of acdc1 plants strongly supports a growth/defence trade-off. By contrast, tcd1 plants had slower growth early in development, suggesting that dhurrin synthesis and turnover may be beneficial for early seedling growth rather than being a cost. The relatively small trade-off between nitrate and dhurrin suggests these may be independently regulated.

Additional keywords: cyanogenesis, CYP79A1, defence, defense, dhurrin, nitrate, NIT4A/B2, resource allocation.


References

Ballhorn DJ, Kautz S, Jensen M, Schmitt I, Heil M, Hegeman AD (2011) Genetic and environmental interactions determine plant defences against herbivores. Journal of Ecology 99, 313–326.
Genetic and environmental interactions determine plant defences against herbivores.Crossref | GoogleScholarGoogle Scholar |

Balotf S, Kavoosi G, Kholdebarin B (2016) Nitrate reductase, nitrite reductase, glutamine synthetase, and glutamate synthase expression and activity in response to different nitrogen sources in nitrogen-starved wheat seedlings. Biotechnology and Applied Biochemistry 63, 220–229.
Nitrate reductase, nitrite reductase, glutamine synthetase, and glutamate synthase expression and activity in response to different nitrogen sources in nitrogen-starved wheat seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXptFOlsLY%3D&md5=a07d8335937132ab7c586f2d3752bbdcCAS |

Barton KE, Koricheva J (2010) The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. American Naturalist 175, 481–493.
The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis.Crossref | GoogleScholarGoogle Scholar |

Bassard JE, Møller BL, Laursen T (2017) Assembly of dynamic P450-mediated metabolons – order versus chaos. Current Molecular Biology Reports 3, 37–51.
Assembly of dynamic P450-mediated metabolons – order versus chaos.Crossref | GoogleScholarGoogle Scholar |

Blomstedt CK, Gleadow RM, O’Donnell NH, Naur P, Jensen K, Laursen T, Olsen CE, Stuart P, Hamill JD, Møller BL, Neale AD (2012) A combined biochemical screen and TILLING approach identifies mutations in Sorghum bicolor (L.) Moench resulting in acyanogenic forage production. Plant Biotechnology Journal 10, 54–66.
A combined biochemical screen and TILLING approach identifies mutations in Sorghum bicolor (L.) Moench resulting in acyanogenic forage production.Crossref | GoogleScholarGoogle Scholar |

Blomstedt C, O’Donnell N, Bjarnholt N, Neale AD, Hamill JD, Møller BL, Gleadow R (2016) Metabolic consequences of knocking out UGT85B1, the gene encoding the glucosyltransferase required for synthesis of dhurrin in Sorghum bicolor (L.) Moench. Plant & Cell Physiology 57, 373–386.
Metabolic consequences of knocking out UGT85B1, the gene encoding the glucosyltransferase required for synthesis of dhurrin in Sorghum bicolor (L.) Moench.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtlGru7jJ&md5=ccc809ac077b2e523746c63a0d03d8d2CAS |

Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends in Ecology & Evolution 20, 441–448.
Facing herbivory as you grow up: the ontogeny of resistance in plants.Crossref | GoogleScholarGoogle Scholar |

Briggs MA, Schultz JC (1990) Chemical defense production in Lotus corniculatus L. II. Trade-offs among growth, reproduction and defense. Oecologia 83, 32–37.
Chemical defense production in Lotus corniculatus L. II. Trade-offs among growth, reproduction and defense.Crossref | GoogleScholarGoogle Scholar |

Burke JJ, Chen J, Burow G, Mechref Y, Rosenow D, Payton P, Xin Z, Hayes CM (2013) Leaf dhurrin content is a quantitative measure of the level of pre- and postflowering drought tolerance in sorghum. Crop Science 53, 1056–1065.

Burke JJ, Payton P, Chen JP, Xin ZG, Burow G, Hayes C (2015) Metabolic responses of two contrasting sorghums to water-deficit stress. Crop Science 55, 344–353.
Metabolic responses of two contrasting sorghums to water-deficit stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXntFOqsw%3D%3D&md5=d3c8537b92efdecb36c5ef1c329001eeCAS |

Burns AE, Gleadow RM, Woodrow IE (2002) Light alters the allocation of nitrogen to cyanogenic glycosides in Eucalyptus cladocalyx. Oecologia 133, 288–294.
Light alters the allocation of nitrogen to cyanogenic glycosides in Eucalyptus cladocalyx.Crossref | GoogleScholarGoogle Scholar |

Busk PK, Møller BL (2002) Dhurrin synthesis in sorghum is regulated at the transcriptional level and induced by nitrogen fertilization in older plants. Plant Physiology 129, 1222–1231.
Dhurrin synthesis in sorghum is regulated at the transcriptional level and induced by nitrogen fertilization in older plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsFajsbg%3D&md5=a5aa961f4ae45f19e6a49a205da12e0fCAS |

Cipollini D, Walters D, Voelckel C (2014) Costs of resistance in plants: from theory to evidence. In ‘Insect–plant interactions. Vol. 47’. (Eds C Voelckel, G Jander) pp. 263–307. (John Wiley & Sons Ltd: Chichester, UK)

Coley PD (1988) Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defense. Oecologia 74, 531–536.
Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defense.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC1czotValug%3D%3D&md5=11fe9b0f5e1daf27151672c204c6902fCAS |

Del Cueto J, Ionescu IA, Pičmanová M, Gericke O, Motawia MS, Olsen CE, Campoy JA, Dicenta F, Møller BL, Sánchez-Pérez R (2017) Cyanogenic glucosides and derivatives in almond and sweet cherry flower buds from dormancy to flowering. Frontiers in Plant Science 8, 800
Cyanogenic glucosides and derivatives in almond and sweet cherry flower buds from dormancy to flowering.Crossref | GoogleScholarGoogle Scholar |

Finnie JW, Windsor PA, Kessell AE (2011) Neurological diseases of ruminant livestock in Australia. II. toxic disorders and nutritional deficiencies. Australian Veterinary Journal 89, 247–253.
Neurological diseases of ruminant livestock in Australia. II. toxic disorders and nutritional deficiencies.Crossref | GoogleScholarGoogle Scholar |

Gelli M, Duo Y, Konda AR, Zhang C, Holding D, Dweikat I (2014) Identification of differentially expressed genes between sorghum genotypes with contrasting nitrogen stress tolerance by genome-wide transcriptional profiling. BMC Genomics 15, 179
Identification of differentially expressed genes between sorghum genotypes with contrasting nitrogen stress tolerance by genome-wide transcriptional profiling.Crossref | GoogleScholarGoogle Scholar |

Gleadow RM, Møller BL (2014) Cyanogenic glucosides- synthesis, physiology and plasticity. Annual Review of Plant Biology 65, 155–185.
Cyanogenic glucosides- synthesis, physiology and plasticity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFWhtrrE&md5=96881c99a2794174a5a1fedb34816132CAS |

Gleadow R, Rowan K (1982) Invasion by Pittosporum undulatum of the forests of central Victoria. III. Effects of temperature and light on growth and drought resistance. Australian Journal of Botany 30, 347–357.
Invasion by Pittosporum undulatum of the forests of central Victoria. III. Effects of temperature and light on growth and drought resistance.Crossref | GoogleScholarGoogle Scholar |

Gleadow RM, Woodrow IE (2000a) Polymorphism in cyanogenic glycoside content and cyanogenic β-glucosidase activity in natural populations of Eucalyptus cladocalyx. Australian Journal of Plant Physiology 27, 693–699.

Gleadow RM, Woodrow IE (2000b) Temporal and spatial variation in cyanogenic glycosides in Eucalyptus cladocalyx. Tree Physiology 20, 591–598.
Temporal and spatial variation in cyanogenic glycosides in Eucalyptus cladocalyx.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjvFSgtbo%3D&md5=1374e939584c8b9f64424b2f022fbb88CAS |

Gleadow RM, Bjarnholt N, Jørgensen K, Fox J, Miller RM (2012) Detection, identification and quantitative measurement of cyanogenic glycosides. In ‘Research methods in plant science: soil allelochemicals. Vol. 1’. (Eds SS Narwal, L Szajdak, DA Sampietro) pp. 283–310. (International Allelopathy Foundation, Studium Press: Houston, TX, USA)

Gleadow RM, Ottman MJ, Kimball BA, Wall GW, Pinter P, LaMorte RL, Leavitt SW (2016) Drought-induced changes in nitrogen partitioning between cyanide and nitrate in leaves and stems of sorghum grown at elevated CO2 are age dependent. Field Crops Research 185, 97–102.
Drought-induced changes in nitrogen partitioning between cyanide and nitrate in leaves and stems of sorghum grown at elevated CO2 are age dependent.Crossref | GoogleScholarGoogle Scholar |

Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. The Quarterly Review of Biology 67, 283–335.
The dilemma of plants: to grow or defend.Crossref | GoogleScholarGoogle Scholar |

Ionescu IA, López-Ortega G, Burow M, Bayo-Canha A, Junge A, Gericke O, Møller BL, Sánchez-Pérez R (2017a) Transcriptome and metabolite changes during hydrogen cyanamide-induced floral bud break in sweet cherry. Frontiers in Plant Science 8, 1233
Transcriptome and metabolite changes during hydrogen cyanamide-induced floral bud break in sweet cherry.Crossref | GoogleScholarGoogle Scholar |

Ionescu IA, Møller BL, Sánchez-Pérez R (2017b) Chemical control of flowering time. Journal of Experimental Botany 68, 369–382.
Chemical control of flowering time.Crossref | GoogleScholarGoogle Scholar |

Jenrich R, Trompetter I, Bak S, Olsen CE, Møller BL, Piotrowski M (2007) Evolution of heteromeric nitrilase complexes in Poaceae with new functions in nitrile metabolism. Proceedings of the National Academy of Sciences of the United States of America 104, 18848–18853.
Evolution of heteromeric nitrilase complexes in Poaceae with new functions in nitrile metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtl2ks77J&md5=ac0e6df251f21ae8edf2684c1dc44932CAS |

Jones DA (1998) Why are so many food plants cyanogenic? Phytochemistry 47, 155–162.
Why are so many food plants cyanogenic?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXislChtg%3D%3D&md5=387b7bd74647e4e7ee61dd18022f925aCAS |

Jørgensen K, Bak S, Busk PK, Sørensen C, Olsen CE, Puonti-Kaerlas J, Møller BL (2005) Cassava plants with a depleted cyanogenic glucoside content in leaves and tubers. Distribution of cyanogenic glucosides, their site of synthesis and transport, and blockage of the biosynthesis by RNA interference technology. Plant Physiology 139, 363–374.
Cassava plants with a depleted cyanogenic glucoside content in leaves and tubers. Distribution of cyanogenic glucosides, their site of synthesis and transport, and blockage of the biosynthesis by RNA interference technology.Crossref | GoogleScholarGoogle Scholar |

Kakes P (1989) An analysis of the costs and benefits of the cyanogenic system in Trifolium repens L. Theoretical and Applied Genetics 77, 111–118.
An analysis of the costs and benefits of the cyanogenic system in Trifolium repens L.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2c7mvVKntg%3D%3D&md5=5115a302a7369fcb353557551b318f77CAS |

Koch B, Sibbesen O, Svendsen I, Møller BL (1995) The primary sequence of cytochrome P450tyr, the multifunctional N-hydroxylase catalyzing the conversion of L-tyrosine to p-hydroxyphenylacetaldehyde oxime in the biosynthesis of the cyanogenic glucoside dhurrin in Sorghum bicolor (L.) Moench. Archives of Biochemistry and Biophysics 323, 177–186.
The primary sequence of cytochrome P450tyr, the multifunctional N-hydroxylase catalyzing the conversion of L-tyrosine to p-hydroxyphenylacetaldehyde oxime in the biosynthesis of the cyanogenic glucoside dhurrin in Sorghum bicolor (L.) Moench.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXoslyksr0%3D&md5=dc4d2d750b69b5db2c3486c63e0d29bbCAS |

Kongsawadworakul P, Viboonjun U, Romruensukharom P, Chantuma P, Ruderman S, Chrestin H (2009) The leaf, inner bark and latex cyanide potential of Hevea brasiliensis: evidence for involvement of cyanogenic glucosides in rubber yield. Phytochemistry 70, 730–739.
The leaf, inner bark and latex cyanide potential of Hevea brasiliensis: evidence for involvement of cyanogenic glucosides in rubber yield.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms1yht7k%3D&md5=994dc280840532431b4cbda910ecdbe5CAS |

Kumagai E, Araki T, Hamaoka N, Ueno O (2011) Ammonia emission from rice leaves in relation to photorespiration and genotypic differences in glutamine synthetase activity. Annals of Botany 108, 1381–1386.
Ammonia emission from rice leaves in relation to photorespiration and genotypic differences in glutamine synthetase activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlGktLrP&md5=4b1ae32ce7bc01460893a787dba69d0cCAS |

Laing WA, Martínez-Sánchez M, Wright MA, Bulley SM, Brewster D, Dare AP, Rassam M, Wang D, Storey R, Macknight RC, Hellens RP (2015) An upstream open reading frame is essential for feedback regulation of ascorbate biosynthesis in Arabidopsis. The Plant Cell 27, 772–786.
An upstream open reading frame is essential for feedback regulation of ascorbate biosynthesis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXntFOmsLk%3D&md5=9b81532a7520a0e94c4fef6dceb1ceb0CAS |

Laursen T, Borch J, Knudsen C, Bavishi K, Torta F, Martens HJ, Silvestro D, Hatzakis NS, Wenk MR, Dafforn TR, Olsen CE, Motawia MS, Hamberger B, Møller BL, Bassard JE (2016) Characterization of a dynamic metabolon producing the defense compound dhurrin in sorghum. Science 354, 890–893.
Characterization of a dynamic metabolon producing the defense compound dhurrin in sorghum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhvFGrtb7I&md5=6289648c1086f13f2f6c882b65d0e20bCAS |

McAllister CH, Beatty PH, Good AG (2012) Engineering nitrogen use efficient crop plants: the current status. Plant Biotechnology Journal 10, 1011–1025.
Engineering nitrogen use efficient crop plants: the current status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXkvVWrtQ%3D%3D&md5=1f884400175ab80aab3d31b3c3ff1529CAS |

Miller RE, Gleadow RM, Cavagnaro TR (2014) Age versus stage: does ontogeny modify the effect of phosphorus and arbuscular mycorrhizas on above- and below-ground defence in forage sorghum? Plant, Cell & Environment 37, 929–942.
Age versus stage: does ontogeny modify the effect of phosphorus and arbuscular mycorrhizas on above- and below-ground defence in forage sorghum?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjslWlsr4%3D&md5=ac0917e89776016435cb9c798da51bf8CAS |

Møller BL (2010) Dynamic metabolons. Science 330, 1328–1329.
Dynamic metabolons.Crossref | GoogleScholarGoogle Scholar |

Neilson EH, Goodger JQD, Woodrow IE, Møller BL (2013) Plant chemical defense: at what cost? Trends in Plant Science 18, 250–258.
Plant chemical defense: at what cost?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXisVGrtro%3D&md5=11af393d32c7134a50f99790647b881dCAS |

Neilson EH, Edwards AM, Blomstedt CK, Berger B, Møller BL, Gleadow RM (2015) Utilization of a high-throughput shoot imaging system to examine the dynamic phenotypic responses of a C4 cereal crop plant to nitrogen and water deficiency over time. Journal of Experimental Botany 66, 1817–1832.
Utilization of a high-throughput shoot imaging system to examine the dynamic phenotypic responses of a C4 cereal crop plant to nitrogen and water deficiency over time.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVGjsrnE&md5=39298d32509291db18f6a0fbe261c67fCAS |

Nielsen LJ, Stuart P, Pičmanová M, Rasmussen S, Olsen CE, Harholt J, Møller BL, Bjarnholt N (2016) Dhurrin metabolism in the developing grain of Sorghum bicolor (L. Moench) investigated by metabolite profiling and novel clustering analyses of time-resolved transcriptomic data. BMC Genomics 17, 1021–1044.
Dhurrin metabolism in the developing grain of Sorghum bicolor (L. Moench) investigated by metabolite profiling and novel clustering analyses of time-resolved transcriptomic data.Crossref | GoogleScholarGoogle Scholar |

O’Donnell NH (2012) Regulation of synthesis of cyanogenic glycosides. PhD thesis, School of Biological Sciences, Monash University.

O’Donnell NH, Møller BL, Neale AD, Hamill JD, Blomstedt CK, Gleadow RM (2013) Effects of PEG-induced osmotic stress on growth and dhurrin levels of forage sorghum. Plant Physiology and Biochemistry 73, 83–92.
Effects of PEG-induced osmotic stress on growth and dhurrin levels of forage sorghum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvV2qu7jO&md5=233942b1451f5aa6b5a7d55df4d7d40eCAS |

Paolacci AR, Tanzarella OA, Porceddu E, Ciaffi M (2009) Identification and validation of reference genes for quantitative RT-PCR normalization in wheat. BMC Molecular Biology 10, 11
Identification and validation of reference genes for quantitative RT-PCR normalization in wheat.Crossref | GoogleScholarGoogle Scholar |

Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob-ur-Rahman M, Ware D, Westhoff P, Mayer KFX, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457, 551–556.
The Sorghum bicolor genome and the diversification of grasses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOmsb4%3D&md5=a43b91f5744855e4aec5e002859d2102CAS |

Pičmanová M, Neilson EH, Motawia MS, Olsen CE, Agerbirk N, Gray CJ, Flitsch S, Meier S, Silvestro D, Jørgensen K, Sánchez-Pérez R, Møller BL, Bjarnholt N (2015) A recycling pathway for cyanogenic glycosides evidenced by the comparative metabolic profiling in three cyanogenic plant species. The Biochemical Journal 469, 375–389.
A recycling pathway for cyanogenic glycosides evidenced by the comparative metabolic profiling in three cyanogenic plant species.Crossref | GoogleScholarGoogle Scholar |

Rasmann S, Chassin E, Bilat J, Glauser G, Reymond P (2015) Trade-off between constitutive and inducible resistance against herbivores is only partially explained by gene expression and glucosinolate production. Journal of Experimental Botany 66, 2527–2534.
Trade-off between constitutive and inducible resistance against herbivores is only partially explained by gene expression and glucosinolate production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtlWnt7jL&md5=89362ff6787cb363ede32c91382619b6CAS |

Selmar D, Kleinwächter M (2013) Stress enhances the synthesis of secondary plant products: the impact of stress-related over-reduction on the accumulation of natural products. Plant & Cell Physiology 54, 817–826.
Stress enhances the synthesis of secondary plant products: the impact of stress-related over-reduction on the accumulation of natural products.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXptFCjsbk%3D&md5=7a05621917a9e9050052f1b79c9cdefbCAS |

Siegień I, Bogatek R (2006) Cyanide action in plants – from toxic to regulatory. Acta Physiologiae Plantarum 28, 483–497.
Cyanide action in plants – from toxic to regulatory.Crossref | GoogleScholarGoogle Scholar |

Simon J, Gleadow RM, Woodrow IE (2010) Allocation of resources to chemical defence and plant functional traits is constrained by soil N. Tree Physiology 30, 1111–1117.
Allocation of resources to chemical defence and plant functional traits is constrained by soil N.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFKhtLbF&md5=c1e49fcf0c909a84350bafd176b5f2bcCAS |

Stitt M, Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant, Cell & Environment 22, 583–621.
The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXksVartLo%3D&md5=8562e2bf39768b28538ce84ec38484e4CAS |

Ullmann-Zeunert L, Stanton MA, Wielsch N, Bartram S, Hummert C, Svatoš A, Baldwin IT, Groten K (2013) Quantification of growth–defense trade-offs in a common currency: nitrogen required for phenolamide biosynthesis is not derived from ribulose-1,5-bisphosphate carboxylase/oxygenase turnover. The Plant Journal 75, 417–429.
Quantification of growth–defense trade-offs in a common currency: nitrogen required for phenolamide biosynthesis is not derived from ribulose-1,5-bisphosphate carboxylase/oxygenase turnover.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFGmsrjJ&md5=7ba13f69d75a7f161fc7dc61cd0f3364CAS |

Vanderlip RL, Reeves HE (1972) Growth stages of sorghum. Agronomy Journal 64, 13–17.
Growth stages of sorghum.Crossref | GoogleScholarGoogle Scholar |

White AC, Rogers A, Rees M, Osborne CP (2016) How can we make crop plants grow faster? A source–sink perspective on growth rate. Journal of Experimental Botany 67, 31–45.
How can we make crop plants grow faster? A source–sink perspective on growth rate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtlWiu7%2FM&md5=e812dc36ef50627f3c3f3389cf27a440CAS |

Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Annual Review of Plant Biology 63, 153–182.
Plant nitrogen assimilation and use efficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xos1ams7w%3D&md5=333e2d79c5805361a00f92a821148ebfCAS |

Yu X-Z, Zhang F-Z (2012) Activities of nitrate reductase and glutamine synthetase in rice seedlings during cyanide metabolism. Journal of Hazardous Materials 225–226, 190–194.
Activities of nitrate reductase and glutamine synthetase in rice seedlings during cyanide metabolism.Crossref | GoogleScholarGoogle Scholar |

Züst T, Agrawal AA (2017) Trade-offs between plant growth and defense against insect herbivory: an emerging mechanistic synthesis. Annual Review of Plant Biology 68, 513–534.
Trade-offs between plant growth and defense against insect herbivory: an emerging mechanistic synthesis.Crossref | GoogleScholarGoogle Scholar |