Skip to main content
SpringerLink
Log in

Down-regulation of nitrogen/carbon metabolism coupled with coordinative hormone modulation contributes to developmental inhibition of the maize ear under nitrogen limitation

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Developmental inhibition of the maize ear by nitrogen limitation is due to overall down-regulation of nitrogen/carbon metabolism, coordinative hormonal modulation, and probable early senescence.

The kernel number is primarily determined from 2 weeks pre-silking to 3 weeks post-silking, largely depending on dynamic nitrogen (N) and carbohydrate metabolism and accumulation in the maize ear. Underlying physiological and molecular mechanisms of kernel abortion caused by N limitation needs to be further investigated. Using a widely grown maize hybrid ZD958, we found that the N deficient ear was shorter, with less biomass accumulation, lower N concentrations, and overall lower concentrations of N assimilates and soluble sugars at 1- or 2-week after silking. Such negative alterations were probably due to significant decreases in activities of nitrate reductase, glutamine synthetase, sucrose phosphate synthetase, and sucrose synthetase in the N deficient maize ear especially after silking. Compensatory up-regulation of corresponding gene expression, together with co-downregulation of gene expression and enzyme activities in certain circumstances, suggested regulatory complexity and mechanistic differentiation from gene expression to functioning at physiological and molecular levels in quickly developing maize ear in counteracting N deficiency. Importantly, auxin, gibberellin, cytokinin, and abscisic acid may act in a coordinative manner to negatively modulate ear development under N limitation, as indicated by their concentration variations and substantial up-regulation of IAA14, GA2-ox1, and CKX12. Lastly, early senescence may occur in the low-N ear driven by interplay of hormone functioning and senescence-related gene regulation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

GA:

Gibberellin

GS:

Glutamine synthetase

NR:

Nitrate reductase

NUtE:

Nitrogen utilization efficiency

OAS:

One week after silking

OBS:

One week before silking

SPS:

Sucrose phosphate synthetase

SS:

Sucrose synthetase

TAS:

Two weeks after silking

ZR:

Zeatin-riboside

References

  • Aloni R, Aloni E, Langhans M, Ullrich CI (2006) Role of auxin in regulating Arabidopsis flower development. Planta 223(2):315–328

    Article  CAS  PubMed  Google Scholar 

  • Alonso-Ramírez A, Rodríguez D, Reyes D et al (2009) Evidence for a role of gibberellins in salicylic acid-modulated early plant responses to abiotic stress in Arabidopsis seeds. Plant Physiol 150(3):1335–1344

    Article  PubMed  PubMed Central  Google Scholar 

  • Andrade FH, Echarte L, Rizalli R et al (2002) Kernel number prediction in maize under nitrogen or water stress. Crop Sci 42(4):1173–1179

    Article  Google Scholar 

  • Ashikari M, Sakakibara H, Lin S et al (2005) Cytokinin oxidase regulates rice grain production. Science 309(5735):741–745

    Article  CAS  PubMed  Google Scholar 

  • Below FE, Christensen LE, Redd AJ, Hageman RH (1981) Availability of reduced N and carbohydrate for ear development of maize. Plant Physiol 68(5):1186–1190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Below FE, Cazetta JO, Seebauer JR (2000) Carbon/nitrogen interactions during ear and kernel development of maize. In: Westgate M, Boote K (eds) Physiology and modeling kernel set in maize. Crop Science Society of America and American Society of Agronomy special publication number 29, Madison, pp 15–24

  • Beveridge CA, Murfet IC, Kerhoas L et al (1997) The shoot controls zeatin riboside export from pea roots. Evidence from the branching mutant rms4. Plant J 11(2):339–345

    Article  CAS  Google Scholar 

  • Busov VB, Meilan R, Pearce DW et al (2003) Activation tagging of a dominant gibberellin catabolism gene (GA 2-oxidase) from poplar that regulates tree stature. Plant Physiol 132(3):1283–1291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calatayud A, Roca D, Gorbe E, Martínez PF (2007) Light acclimation in rose (Rosa hybrida cv. Grand Gala) leaves after pruning: effects on chlorophyll a fluorescence, nitrate reductase, ammonium and carbohydrates. Sci Hortic-Amsterdam 111(2):152–159

    Article  CAS  Google Scholar 

  • Campbell WH (1999) Nitrate reductase structure, function and regulation: bridging the gap between biochemistry and physiology. Ann Rev Plant Physiol Plant Mol Biol 50:277–303

    Article  CAS  Google Scholar 

  • Cañas RA, Quilleré I, Christ A et al (2009) Nitrogen metabolism in the developing ear of maize (Zea mays): analysis of two lines contrasting in their mode of nitrogen management. New Phytol 184(2):340–352

    Article  PubMed  Google Scholar 

  • Cañas RA, Quilleré I, Lea PJ, Hirel B (2010) Analysis of amino acid metabolism in the ear of maize mutants deficient in two cytosolic glutamine synthetase isoenzymes highlights the importance of asparagine for nitrogen translocation within sink organs. Plant Biotechnol J 8(9):966–978

    Article  PubMed  Google Scholar 

  • Chin TY, Beevers L (1970) Changes in endogenous growth regulators in nasturtium leaves during senescence. Planta 92(2):178–188

    Article  CAS  PubMed  Google Scholar 

  • Chourey PS, Taliercio EW, Carlson SJ, Ruan YL (1998) Genetic evidence that the two isozymes of sucrose synthase present in developing maize endosperm are critical, one for cell wall integrity and the other for starch biosynthesis. Mol Gen Genet 259(1):88–96

    Article  CAS  PubMed  Google Scholar 

  • Denance N, Szurek B, Noeel LD (2014) Emerging functions of nodulin-like proteins in non-nodulating plant species. Plant Cell Physiol 55(3):469–474

    Article  CAS  PubMed  Google Scholar 

  • Fischer WN, André B, Rentsch D et al (1998) Amino acid transport in plants. Trends Plant Sci 3(5):188–195

    Article  Google Scholar 

  • Forde BG (2002) Local and long-range signaling pathways regulating plant responses to nitrate. Annu Rev Plant Biol 53(1):203–224

    Article  CAS  PubMed  Google Scholar 

  • Forde BG, Lea PJ (2007) Glutamate in plants: metabolism, regulation, and signalling. J Exp Bot 58(9):2339–2358

    Article  CAS  PubMed  Google Scholar 

  • Gaur VS, Singh US, Gupta AK, Kumar A (2012) Influence of different nitrogen inputs on the members of ammonium transporter and glutamine synthetase genes in two rice genotypes having differential responsiveness to nitrogen. Mol Biol Rep 39(8):8035–8044

    Article  CAS  PubMed  Google Scholar 

  • Gebril S, Seger M, Villanueva FM et al (2015) Transgenic alfalfa (Medicago sativa) with increased sucrose phosphate synthase activity shows enhanced growth when grown under N2-fixing conditions. Planta 242(4):1009–1024

    Article  CAS  PubMed  Google Scholar 

  • Goodall AJ, Kumar P, Tobin AK (2013) Identification and expression analyses of cytosolic glutamine synthetase genes in barley (Hordeum vulgare L.). Plant Cell Physiol 54(4):492–505

    Article  CAS  PubMed  Google Scholar 

  • Gosti F, Beaudoin N, Serizet C et al (1999) ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell 11(10):1897–1909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gowri G, Kenis JD, Ingemarsson B et al (1992) Nitrate reductase transcript is expressed in the primary response of maize to environmental nitrate. Plant Mol Biol 18(1):55–64

    Article  CAS  PubMed  Google Scholar 

  • Hirel B, Bertin P, Quilleré I et al (2001) Towards a better understanding of the genetic and physiological basis for nitrogen use efficiency in maize. Plant Physiol 125(3):1258–1270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hubbard NL, Huber SC, Pharr DM (1989) Sucrose phosphate synthase and acid invertase as determinants of sucrose concentration in developing muskmelon (Cucumis melo L.) fruits. Plant Physiol 91(4):1527–1534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Husted S, Hebbern CA, Mattsson M, Schjoerring JK (2000) A critical experimental evaluation of methods for determination of NH4 + in plant tissue, xylem sap and apoplastic fluid. Physiol Plantarum 109(2):167–179

    Article  CAS  Google Scholar 

  • Kant S, Bi YM, Rothstein SJ (2011) Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency. J Exp Bot 62(4):1499–1509

    Article  CAS  PubMed  Google Scholar 

  • Khan NA, Mir R, Khan M, Javid S (2002) Effects of gibberellic acid spray on nitrogen yield efficiency of mustard grown with different nitrogen levels. Plant Growth Regul 38(3):243–247

    Article  CAS  Google Scholar 

  • Kiba T, Kudo T, Kojima M, Sakakibara H (2011) Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. J Exp Bot 62(4):1399–1409

    Article  CAS  PubMed  Google Scholar 

  • Laporte MM, Galagan JA, Shapiro JA et al (1997) sucrose-phophate synthase activity and yield analysis of tomato plants transformed with maize sucrose-phophate synthase. Planta 203(2):253–259

    Article  CAS  Google Scholar 

  • Lemcoff JH, Loomis RS (1994) Nitrogen and density influences on silk emergence, endosperm development, and grain yield in maize (Zea mays L.). Field Crop Res 38(2):63–72

    Article  Google Scholar 

  • Li J, Baroja-Fernández E, Bahaji A et al (2013) Enhancing sucrose synthase activity results in increased levels of starch and ADP-glucose in maize (Zea mays L.) seed endosperms. Plant Cell Physiol 54(2):282–294

    Article  CAS  PubMed  Google Scholar 

  • Liao C, Peng Y, Ma W et al (2012) Proteomic analysis revealed nitrogen-mediated metabolic, developmental, and hormonal regulation of maize (Zea mays L.) ear growth. J Exp Bot 63(14):5275–5288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408

    Article  CAS  PubMed  Google Scholar 

  • Lu Y, Sasaki Y, Li X et al (2015) ABI1 regulates carbon/nitrogen-nutrient signal transduction independent of ABA biosynthesis and canonical ABA signalling pathways in Arabidopsis. J Exp Bot 66(9):2763–2771

    Article  PubMed  Google Scholar 

  • Lunn JE, Hatch MD (1997) The role of sucrose-phosphate synthase in the control of photosynthates partitioning in Zea mays leaves. Aust J Plant Physiol 24(1):1–8

    Article  CAS  Google Scholar 

  • Marsch-Martinez N, de Folter S (2016) Hormonal control of the development of the gynoecium. Curr Opin Plant Biol 29:104–114

    Article  CAS  PubMed  Google Scholar 

  • Martin A, Lee J, Kichey T et al (2006) Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of kernel production. Plant Cell 18(11):3252–3274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Micallef BJ, Haskins KA, Vanderveer PJ et al (1995) Altered photosynthesis, flowering, and fruiting in transgenic tomato plants that have an increased capacity for sucrose synthesis. Planta 196(2):327–334

    Article  CAS  Google Scholar 

  • Miller AJ, Cramer MD (2004) Root nitrogen acquisition and assimilation. Plant Soil 274:1–36

    Article  Google Scholar 

  • Muhitch MJ (2003) Distribution of the glutamine synthetase isozyme GS (p1) in maize (Zea mays). J Plant Physiol 160(6):601–605

    Article  CAS  PubMed  Google Scholar 

  • Murata Y, Pei Z, Mori IC et al (2001) Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell 13(11):2513–2523

    CAS  PubMed  PubMed Central  Google Scholar 

  • O’Neal D, Joy KW (1973) Glutamine synthetase of pea leaves. I. Purification, stabilisation and pH optima. Arch Biochem Biophys 159(1):113–122

    Article  PubMed  Google Scholar 

  • O’Donnell PJ, Schmelz EA, Moussatche P et al (2003) Susceptible to intolerance a range of hormonal actions in a susceptible Arabidopsis pathogen response. Plant J 33(2):245–257

    Article  PubMed  Google Scholar 

  • Okumoto S, Koch W, Tegeder M et al (2004) Root phloem-specific expression of the plasma membrane amino acid proton cotransporter AAP3. J Exp Bot 55(406):2155–2168

    Article  CAS  PubMed  Google Scholar 

  • Ortega JL, Temple SJ, Sengupta-Gopalan C (2001) Constitutive overexpression of cytosolic glutamine synthetase (GS1) gene in transgenic alfalfa demonstrates that GS1 may be regulated at the level of RNA stability and protein turnover. Plant Physiol 126(1):109–121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan X, Hasan MM, Li Y et al (2015) Asymmetric transcriptomic signatures between the cob and florets in the maize ear under optimal-and low-nitrogen conditions at silking, and functional characterization of amino acid transporters ZmAAP4 and ZmVAAT3. J Exp Bot 66(20):6149–6166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pasternak TP, Prinsen E, Ayaydin F et al (2002) The role of auxin, pH, and stress in the activation of embryogenic cell division in leaf protoplast-derived cells of alfalfa. Plant Physiol 129(4):1807–1819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plackett AR, Thomas SG, Wilson ZA, Hedden P (2011) Gibberellin control of stamen development: a fertile field. Trends Plant Sci 16(10):568–578

    Article  CAS  PubMed  Google Scholar 

  • Reed JW (2001) Roles and activities of Aux/IAA proteins in Arabidopsis. Trends Plant Sci 6(9):420–425

    Article  CAS  PubMed  Google Scholar 

  • Rosen H (1957) A modified ninhydrin colorimetric analysis for amino acids. Arch Biochem Biophys 67(1):10–15

    Article  CAS  PubMed  Google Scholar 

  • Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57:431–449

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto T, Kobayashi M, Itoh H et al (2001) Expression of a gibberellin 2-oxidase gene around the shoot apex is related to phase transition in rice. Plant Physiol 125(3):1508–1516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santner A, Calderon-Villalobos LIA, Estelle M (2009) Plant hormones are versatile chemical regulators of plant growth. Nat Chem Biol 5(5):301–307

    Article  CAS  PubMed  Google Scholar 

  • Schomburg FM, Bizzell CM, Lee DJ et al (2003) Overexpression of a novel class of gibberellin 2-oxidases decreases gibberellin levels and creates dwarf plants. Plant Cell 15(1):151–163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seebauer JR, Moose SP, Fabbri BJ et al (2004) Amino acid metabolism in maize earshoots. Implications for assimilate preconditioning and nitrogen signaling. Plant Physiol 136(4):4326–4334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Šmehilová M, Galuszka P, Bilyeu KD et al (2009) Subcellular localization and biochemical comparison of cytosolic and secreted cytokinin dehydrogenase enzymes from maize. J Exp Bot 60(9):2701–2712

    Article  PubMed  Google Scholar 

  • Stitt M (1999) Nitrate regulation of metabolism and growth. Curr Opin Plant Biol 2(3):178–186

    Article  CAS  PubMed  Google Scholar 

  • Sugiharto B, Sugiyama T (1992) Effects of nitrate and ammonium on gene expression of phosphoeno/pyruvate carboxylase and nitrogen metabolism in maize leaf tissue during recovery from nitrogen stress. Plant Physiol 98(4):1403–1408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swank JC, Below FE, Lambert RJ, Hageman RH (1982) Interaction of carbon and nitrogen metabolism in the productivity of maize. Plant Physiol 70(4):1185–1190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taiz L, Zeiger E (2006) Plant physiology. Sinauer Associates, Sunderland

    Google Scholar 

  • Takei K, Sakakibara H, Taniguchi M, Sugiyama T (2001) Nitrogen-dependent accumulation of cytokinins in root and the translocation to leaf: implication of cytokinin species that induces gene expression of maize response regulator. Plant Cell Physiol 42(1):85–93

    Article  CAS  PubMed  Google Scholar 

  • Thomsen HC, Eriksson D, Møller IS, Schjoerring JK (2014) Cytosolic glutamine synthetase: a target for improvement of crop nitrogen use efficiency? Trends Plant Sci 19(10):656–663

    Article  CAS  PubMed  Google Scholar 

  • Tian Q, Chen F, Liu J et al (2008) Inhibition of maize root growth by high nitrate supply is correlated with reduced IAA levels in roots. J Plant Physiol 165(9):942–951

    Article  CAS  PubMed  Google Scholar 

  • Tollenaar M, Dwyer L, Stewart D (1992) Ear and kernel formation in maize hybrids representing three decades of grain yield improvement in Ontario. Crop Sci 32(2):432–438

    Article  Google Scholar 

  • Ueno O, Yoshimura Y, Sentoku N (2005) Variation in the activity of some enzymes of photorespiratory metabolism in C4 grasses. Ann Bot (Lond) 96(5):863–869

    Article  CAS  Google Scholar 

  • Uhart SA, Andrade FH (1995) Nitrogen deficiency in maize: II. Carbon-nitrogen interaction effects on kernel number and grain yield. Crop Sci 35(5):1384–1389

    Article  Google Scholar 

  • Vettakkorumakankav NN, Falk D, Saxena P, Fletcher RA (1999) A crucial role for gibberellins in stress protection of plants. Plant Cell Physiol 40(5):542–548

    Article  CAS  Google Scholar 

  • Wagner BM, Beck E (1993) Cytokinins in the perennial herb Urtica dioica L. as influenced by its nitrogen status. Planta 190(4):511–518

    Article  CAS  Google Scholar 

  • Wang Y, Deng D, Ding H et al (2013) Gibberellin biosynthetic deficiency is responsible for maize dominant Dwarf11 (D11) mutant phenotype: physiological and transcriptomic evidence. PLoS One 8(6):e66466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wardlaw IF, Willenbrink J (1994) Carbohydrate storage and mobilisation by the culm of wheat between heading and grain maturity: the relation to sucrose synthase and sucrose-phosphate synthase. J Plant Physiol 21(3):255–271

    CAS  Google Scholar 

  • Weiler EW, Jourdan PS, Conrad W (1981) Levels of indole-3-acetic acid in intact and decapitated coleoptiles as determined by a specific and highly sensitive solid-phase enzyme immunoassay. Planta 153(6):561–571

    Article  CAS  PubMed  Google Scholar 

  • Worrell AC, Bruneau JM, Summerfelt K et al (1991) Expression of a maize sucrose phosphate synthase in tomato alters leaf carbohydrate partitioning. Plant Cell 3(10):1121–1130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zalewski W, Galuszka P, Gasparis S et al (2010) Silencing of the HvCKX1 gene decreases the cytokinin oxidase/dehydrogenase level in barley and leads to higher plant productivity. J Exp Bot 61(6):1839–1851

    Article  CAS  PubMed  Google Scholar 

  • Zieserl JF, Rivenbark WL, Hageman RH (1963) Nitrate reductase activity, protein content, and yield of four maize hybrids at varying plant populations. Crop Sci 3(1):27–32

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank the NSFC Grant (31471928), the program for New Century Excellent Talents in University (NCET-12-0521), the CAU Innovation Grant (2016QC101) and the Innovative Group Grant of the NSFC (31421092) for financial support.

Author information

Authors and Affiliations

  1. Department of Plant Nutrition, China Agricultural University, Beijing, 100193, China

    Jiaojiao Yu, Jienan Han, Ruifeng Wang & Xuexian Li

  2. The Key Laboratory of Plant-Soil Interactions, MOE, Beijing, China

    Jiaojiao Yu, Jienan Han, Ruifeng Wang & Xuexian Li

Authors
  1. Jiaojiao Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jienan Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ruifeng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xuexian Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xuexian Li.

Electronic supplementary material

Below is the link to the electronic supplementary material.

425_2016_2499_MOESM1_ESM.docx

Supplementary material 1 (DOCX 22 kb) Supplementary Fig. S1 ABA responsive elements (ABRE) in the 5’ untranslated regions of ATA15, nodulin like, and STO. The 1499-bp sequence immediately upstream of the start codon (ATG) was analyzed for senescence-related cis-elements. ABREs were highlighted in red

Supplementary material 2 (DOCX 18 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yu, J., Han, J., Wang, R. et al. Down-regulation of nitrogen/carbon metabolism coupled with coordinative hormone modulation contributes to developmental inhibition of the maize ear under nitrogen limitation. Planta 244, 111–124 (2016). https://doi.org/10.1007/s00425-016-2499-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-016-2499-1

Keywords

Search

Navigation