Maize Maintains Growth in Response to Decreased Nitrate Supply Through a Highly Dynamic and Developmental Stage-specific Transcriptional Response

Overview

Journal Plant Biotechnol J

Specialties Biology
Biotechnology

Date 2015 Jun 4

PMID 26038196

Citations 7

Authors

Darren Plett

Ute Baumann

Andreas W Schreiber

Luke Holtham

Elena Kalashyan

John Toubia

John Nau

Mary Beatty

Antoni Rafalski

Kanwarpal S Dhugga

Mark Tester

Trevor Garnett

Brent N Kaiser

Affiliations

Soon will be listed here.

Abstract

Elucidation of the gene networks underlying the response to N supply and demand will facilitate the improvement of the N uptake efficiency of plants. We undertook a transcriptomic analysis of maize to identify genes responding to both a non-growth-limiting decrease in NO3- provision and to development-based N demand changes at seven representative points across the life cycle. Gene co-expression networks were derived by cluster analysis of the transcript profiles. The majority of NO3--responsive transcription occurred at 11 (D11), 18 (D18) and 29 (D29) days after emergence, with differential expression predominating in the root at D11 and D29 and in the leaf at D18. A cluster of 98 probe sets was identified, the expression pattern of which is similar to that of the high-affinity NO3- transporter (NRT2) genes across the life cycle. The cluster is enriched with genes encoding enzymes and proteins of lipid metabolism and transport, respectively. These are candidate genes for the response of maize to N supply and demand. Only a few patterns of differential gene expression were observed over the entire life cycle; however, the composition of the classes of the genes differentially regulated at individual time points was unique, suggesting tightly controlled regulation of NO3--responsive gene expression.

Citing Articles

Physiological response to low-nitrogen stress and comprehensive evaluation in four rice varieties.

Zhang Y, Cai H, You E, Qiao X, Gao Z, Chen G Photosynthetica. 2024; 62(3):252-262.

PMID: 39649354 PMC: 11622558. DOI: 10.32615/ps.2024.028.

Root phenotypes for improved nitrogen capture.

Lynch J, Galindo-Castaneda T, Schneider H, Sidhu J, Rangarajan H, York L Plant Soil. 2024; 502(1-2):31-85.

PMID: 39323575 PMC: 11420291. DOI: 10.1007/s11104-023-06301-2.

Hydroponic cultivation conditions allowing the reproducible investigation of poplar root suberization and water transport.

Grunhofer P, Guo Y, Li R, Lin J, Schreiber L Plant Methods. 2021; 17(1):129.

PMID: 34911563 PMC: 8672600. DOI: 10.1186/s13007-021-00831-5.

Integration of the metabolome and transcriptome reveals the mechanism of resistance to low nitrogen supply in wild bermudagrass (Cynodon dactylon (L.) Pers.) roots.

Li D, Liu J, Zong J, Guo H, Li J, Wang J BMC Plant Biol. 2021; 21(1):480.

PMID: 34674655 PMC: 8532362. DOI: 10.1186/s12870-021-03259-0.

The expression patterns and putative function of nitrate transporter 2.5 in plants.

Liu R, Jia T, Cui B, Song J Plant Signal Behav. 2020; 15(12):1815980.

PMID: 32867594 PMC: 7671049. DOI: 10.1080/15592324.2020.1815980.

References

Maldonado A, Doerner P, Dixon R, Lamb C, Cameron R . A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature. 2002; 419(6905):399-403. DOI: 10.1038/nature00962. View

Wang Y, Hsu P, Tsay Y . Uptake, allocation and signaling of nitrate. Trends Plant Sci. 2012; 17(8):458-67. DOI: 10.1016/j.tplants.2012.04.006. View

Sturn A, Quackenbush J, Trajanoski Z . Genesis: cluster analysis of microarray data. Bioinformatics. 2002; 18(1):207-8. DOI: 10.1093/bioinformatics/18.1.207. View

Krouk G, Mirowski P, LeCun Y, Shasha D, Coruzzi G . Predictive network modeling of the high-resolution dynamic plant transcriptome in response to nitrate. Genome Biol. 2010; 11(12):R123. PMC: 3046483. DOI: 10.1186/gb-2010-11-12-r123. View

Amiour N, Imbaud S, Clement G, Agier N, Zivy M, Valot B . The use of metabolomics integrated with transcriptomic and proteomic studies for identifying key steps involved in the control of nitrogen metabolism in crops such as maize. J Exp Bot. 2012; 63(14):5017-33. DOI: 10.1093/jxb/ers186. View

Wang L, Xie W, Chen Y, Tang W, Yang J, Ye R . A dynamic gene expression atlas covering the entire life cycle of rice. Plant J. 2009; 61(5):752-66. DOI: 10.1111/j.1365-313X.2009.04100.x. View

Gutierrez R, Lejay L, Dean A, Chiaromonte F, Shasha D, Coruzzi G . Qualitative network models and genome-wide expression data define carbon/nitrogen-responsive molecular machines in Arabidopsis. Genome Biol. 2007; 8(1):R7. PMC: 1839130. DOI: 10.1186/gb-2007-8-1-r7. View

Chomczynski P . A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Biotechniques. 1993; 15(3):532-4, 536-7. View

Nakamichi N, Kiba T, Henriques R, Mizuno T, Chua N, Sakakibara H . PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell. 2010; 22(3):594-605. PMC: 2861452. DOI: 10.1105/tpc.109.072892. View

10.

Druka A, Muehlbauer G, Druka I, Caldo R, Baumann U, Rostoks N . An atlas of gene expression from seed to seed through barley development. Funct Integr Genomics. 2006; 6(3):202-11. DOI: 10.1007/s10142-006-0025-4. View

11.

Sylvester-Bradley R, Kindred D . Analysing nitrogen responses of cereals to prioritize routes to the improvement of nitrogen use efficiency. J Exp Bot. 2009; 60(7):1939-51. DOI: 10.1093/jxb/erp116. View

12.

Scheible W, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N . Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol. 2004; 136(1):2483-99. PMC: 523316. DOI: 10.1104/pp.104.047019. View

13.

Chanda B, Xia Y, Mandal M, Yu K, Sekine K, Gao Q . Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nat Genet. 2011; 43(5):421-7. DOI: 10.1038/ng.798. View

14.

Wang R, Okamoto M, Xing X, Crawford N . Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1,000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiol. 2003; 132(2):556-67. PMC: 166997. DOI: 10.1104/pp.103.021253. View

15.

Sekhon R, Lin H, Childs K, Hansey C, Buell C, de Leon N . Genome-wide atlas of transcription during maize development. Plant J. 2011; 66(4):553-63. DOI: 10.1111/j.1365-313X.2011.04527.x. View

16.

Schluter U, Mascher M, Colmsee C, Scholz U, Brautigam A, Fahnenstich H . Maize source leaf adaptation to nitrogen deficiency affects not only nitrogen and carbon metabolism but also control of phosphate homeostasis. Plant Physiol. 2012; 160(3):1384-406. PMC: 3490595. DOI: 10.1104/pp.112.204420. View

17.

Ranathunge K, Schreiber L, Franke R . Suberin research in the genomics era--new interest for an old polymer. Plant Sci. 2011; 180(3):399-413. DOI: 10.1016/j.plantsci.2010.11.003. View

18.

Schmid M, Davison T, Henz S, Pape U, Demar M, Vingron M . A gene expression map of Arabidopsis thaliana development. Nat Genet. 2005; 37(5):501-6. DOI: 10.1038/ng1543. View

19.

Liseron-Monfils C, Lewis T, Ashlock D, McNicholas P, Fauteux F, Stromvik M . Promzea: a pipeline for discovery of co-regulatory motifs in maize and other plant species and its application to the anthocyanin and phlobaphene biosynthetic pathways and the Maize Development Atlas. BMC Plant Biol. 2013; 13:42. PMC: 3658923. DOI: 10.1186/1471-2229-13-42. View

20.

Bi Y, Meyer A, Downs G, Shi X, El-Kereamy A, Lukens L . High throughput RNA sequencing of a hybrid maize and its parents shows different mechanisms responsive to nitrogen limitation. BMC Genomics. 2014; 15:77. PMC: 3912931. DOI: 10.1186/1471-2164-15-77. View