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Transcriptome response to nitrogen starvation in rice

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Abstract

Nitrogen is an essential mineral nutrient required for plant growth and development. Insufficient nitrogen (N) supply triggers extensive physiological and biochemical changes in plants. In this study, we used Affymetrix GeneChip rice genome arrays to analyse the dynamics of rice transcriptome under N starvation. N starvation induced or suppressed transcription of 3518 genes, representing 10.88% of the genome. These changes, mostly transient, affected various cellular metabolic pathways, including stress response, primary and secondary metabolism, molecular transport, regulatory process and organismal development. 462 or 13.1% transcripts for N starvation expressed similarly in root and shoot. Comparative analysis between rice and Arabidopsis identified 73 orthologous groups that responded to N starvation, demonstrated the existence of conserved N stress coupling mechanism among plants. Additional analysis of transcription profiles of microRNAs revealed differential expression of miR399 and miR530 under N starvation, suggesting their potential roles in plant nutrient homeostasis.

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References

  • Alexa A, Rahnenfuhrer J and Lengauer T 2006 Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22 1600–1607

    Article  PubMed  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW and Lipman DJ 1990 Basic local alignment search tool. J. Mol. Biol. 215 403–410

    PubMed  CAS  Google Scholar 

  • Aung K, Lin SI, Wu CC, Huang YT, Su CL and Chiou TJ 2006 pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol. 141 1000–1011

    Article  PubMed  CAS  Google Scholar 

  • Bachmair A, Novatchkova M, Potuschak T and Eisenhaber F 2001 Ubiquitylation in plants: a post-genomic look at a post-translational modification. Trends Plant Sci. 6 463–470

    Article  PubMed  CAS  Google Scholar 

  • Bari R, Datt Pant B, Stitt M and Scheible WR 2006 PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol. 141 988–999

    Article  PubMed  CAS  Google Scholar 

  • Bartel DP 2004 MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116 281–297

    Article  PubMed  CAS  Google Scholar 

  • Berglund AC, Sjolund E, Ostlund G and Sonnhammer EL 2008 InParanoid 6: eukaryotic ortholog clusters with inparalogs. Nucleic Acids Res. 36 263–266

    Article  Google Scholar 

  • Bonnet E, Peer YV and Rouze P 2006 The small RNA world of plants. New Phytol. 171 451–468

    Article  PubMed  CAS  Google Scholar 

  • Bi Y-M, Wang RL, Zhu T and Rothstein SJ 2007 Global transcription profiling reveals differential responses to chronic nitrogen stress and putative nitrogen regulatory components in Arabidopsis. BMC Genomics 8 281–297

    Article  PubMed  Google Scholar 

  • Buhtz A, Springer F, Chappell L, Baulcombe DC and Kehr J 2008 Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J. 53 739–749

    Article  PubMed  CAS  Google Scholar 

  • Carrington JC and Ambros V 2003 Role of microRNAs in plant and animal development. Science 301 336–338

    Article  PubMed  CAS  Google Scholar 

  • Chiou TJ 2007 The role of microRNAs in sensing nutrient stress. Plant Cell Environ. 30 323–332

    Article  PubMed  CAS  Google Scholar 

  • Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF and Su CL 2006 Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18 412–421

    Article  PubMed  CAS  Google Scholar 

  • Crawford NM and Forde BG 2002 Molecular and developmental biology of inorganic nitrogen nutrition; in The arabidopsis book (eds) E Meyerowitz and C Somerville (Rockville, MD: American Society of Plant Biologists) ( http://www.aspb.org/publications/arabidopsis )

  • Doerner P 2008 Phosphate starvation signaling: a threesome controls systemic Pi homeostasis. Curr. Opin. Plant Biol. 11 1–5

    Article  Google Scholar 

  • Fang Z, Shao C, Meng Y, Wu P and Chen M 2009 Phosphate signaling in Arabidopsis and Oryza sativa. Plant Sci. 176 170–180

    Article  CAS  Google Scholar 

  • Frink CR, Waggoner PE and Ausubel JH 1999 Nitrogen fertilizer: retrospect and prospect. Proc. Natl. Acad. Sci. USA 96 1175–1180

    Article  PubMed  CAS  Google Scholar 

  • Fujii H,Chiou TJ, Lin SI, Aung K and Zhu JK 2005 A miRNA involved in phosphate-starvation response in Arabidopsis. Curr. Biol. 15 2038–2043

    Article  PubMed  CAS  Google Scholar 

  • Good AG, Shrawat AK and Muench DG 2004 Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production. Trends Plant Sci. 9 597–605

    Article  PubMed  CAS  Google Scholar 

  • Griffiths-Jones S 2006 miRBase: the microRNA sequence database. Methods Mol. Biol. 342 129–138

    PubMed  CAS  Google Scholar 

  • Guo HS, XieQ, Fei JF and Chua NH 2005 MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17 1376–1386

    Article  PubMed  CAS  Google Scholar 

  • Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF, Christie P, Goulding KWT, et al. 2010 Significant acidification in major Chinese croplands. Science 327 1008–1010

    Article  PubMed  CAS  Google Scholar 

  • Hammond JP, Bennett MJ, Bowen HC, Broadley MR, Eastwood DC, May TM, Rahn C, Swarup R, et al. 2003 Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiol. 132 578–596

    Article  PubMed  CAS  Google Scholar 

  • Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B, Zhu T, Wang X, Kreps JA, et al. 2000 Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290 2110–2113

    Article  PubMed  CAS  Google Scholar 

  • Himanen K, Vuylsteke M, Vanneste S, Vercruysse S, Boucheron E, Alard P, Chriqui D, Montagu MV, et al. 2004 Transcript profiling of early lateral root initiation. Proc. Natl. Acad. Sci. USA 101 5146–5151

    Article  PubMed  CAS  Google Scholar 

  • Hong F, Breitling R, McEntee CW, Wittner BS, Nemhauser JL and Chory J 2006 RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics 22 2825–2827

    Article  PubMed  CAS  Google Scholar 

  • Hsieh L, Lin S, Shih AC, Chen J, Lin W, Tseng C, Li W and Chiou T 2009 Uncovering small RNA-Mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol. 151 2120–2132

    Article  PubMed  Google Scholar 

  • Hubner N, Caroline AW, Zimdahl H, Petretto E, Schulz H, Maciver F, Mueller M, Hummel O, et al. 2005 Integrated transcriptional profiling and linkage analysis for identification of genes underlying disease. Nat. Genet. 37 243–253

    Article  PubMed  CAS  Google Scholar 

  • Isin EM and Guengerich FP 2007 Complex reactions catalyzed by cytochrome P450 enzymes. Biochem. Biophys. Acta 1770 314–329

    Article  PubMed  CAS  Google Scholar 

  • Jones-Rhoades MJ, Bartel B and Bartel DP 2006 MicroRNAs and their regulatory targets in plants. Annu. Rev. Plant Biol. 57 19–53

    Article  PubMed  CAS  Google Scholar 

  • Jones-Rhoades MJ and Bartel DP 2004 Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol. Cell 14 787–799

    Article  PubMed  CAS  Google Scholar 

  • Karlsson M, Elfstrand M, Stenlid J and Olson A 2008 A fungal cytochrome P450 is expressed during the interaction between the fungal pathogen Heterobasidion annosum sensulato and conifer trees. DNA Seq. 19 115–120

    Article  PubMed  CAS  Google Scholar 

  • Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D and Bohnert H 2001 Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13 889–905

    PubMed  CAS  Google Scholar 

  • Kraft E, Stone SL, Ma L, Su N, Gao Y, Lau OS, Deng XW and Callis J 2005 Genome analysis and functional characterization of the E2 and RING-type E3 ligase ubiquitination enzymes of Arabidopsis. Plant Physiol. 139 1597–1611

    Article  PubMed  CAS  Google Scholar 

  • Lee RC, Feinbaum RL and Ambros V 1993 The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75 843–854

    Article  PubMed  CAS  Google Scholar 

  • Lian X, Wang S, Zhang J, Feng Q, Zhang L, Fan D, Li X, Yuan D, et al. 2006 Expression profiles of 10,422 genes at early stage of low nitrogen stress in rice assayed using a cDNA microarray. Plant Mol Biol 60 617–631

    Article  PubMed  CAS  Google Scholar 

  • Liu B, Li P, Li X, Liu C, Cao S, Chu C and Cao X 2005 Loss of function of OsDCL1 affects microRNA accumulation and causes developmental defects in rice. Plant Physiol. 39 296–305

    Article  Google Scholar 

  • Ma L, Gao Y, Qu L, Chen Z, Li J, Zhao H and Deng XW 2002 Genomic evidence for COP1 as a repressor of light regulated gene expression and development in Arabidopsis. Plant Cell 14 2383–2398

    Article  PubMed  CAS  Google Scholar 

  • Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL and Dietrich RA 2000 The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat. Genet. 26 403–410

    Article  PubMed  CAS  Google Scholar 

  • Mallory AC, Dugas DV, Bartel DB and Bartel B 2004 MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Curr. Biol. 14 1035–1046

    Article  PubMed  CAS  Google Scholar 

  • Mallory A and Vaucheret H 2006 Functions of microRNAs and related small RNAs in plants. Nat. Gene.t S31–36

  • Martinoia E, Maeshima M and Neuhaus E 2007 Vacuolar transporters and their essential role in plant metabolism. J. Exp. Bot. 58 83–102

    Article  PubMed  CAS  Google Scholar 

  • Miller AJ and Smith SJ 1996 Nitrate transport and compartmentation in cereal root cells. J. Exp. Bot. 300 843–854

    Article  Google Scholar 

  • Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, Ortet P, Creff A, et al. 2005 A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc. Natl. Acad. Sci. USA 102 11934–11939

    Article  PubMed  CAS  Google Scholar 

  • Morant M, Bak S, Moller BL and Werck-Reichhart D 2003 Plant cytochromes P450: tools for pharmacology, plant protection and phytoremediation. Curr. Opin. Biotechnol. 14 1511–1562

    Google Scholar 

  • Morley M, Molony CM, Weber TM, Devlin JL, Ewens KG, Spielman RS and Cheung VG 2004 Genetic analysis of genome-wide variation in human gene expression. Nature 430 743–747

    Article  PubMed  CAS  Google Scholar 

  • Muller R, Morant M, Jarmer H, Nilsson L and Nielsen TH 2007 Genome-wide analysis of the Arabidopsis leaf transcriptome reveals interaction of phosphate and sugar metabolism. Plant Physiol. 143 156–171

    Article  PubMed  CAS  Google Scholar 

  • Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, et al. 2007 The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res. 35 883–887

    Article  Google Scholar 

  • Pagliarani A, Bandiera P, Ventrella V, Trombetti F, Manuzzi MP, Pirini M and Borgatti AR 2008 Response of Na -dependent ATPase activities to the contaminant ammonia nitrogen in Tapes philippinarum: Possible ATPase involvement in ammonium transport. Arch. Environ. Contam. Toxicol. 55 49–56

    Article  PubMed  CAS  Google Scholar 

  • Palenchar PM, Kouranov A, Lejay LV and Coruzzi GM 2004 Genome-wide patterns of carbon and nitrogen regulation of gene expression validate the combined carbon and nitrogen (CN)-signaling hypothesis in plants. Genome Biol 5 R91

    Article  PubMed  Google Scholar 

  • Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther D and Scheible W 2009 Identification of nutrient-responsive Arabidopsis and Rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol. 150 1541-1555

    Article  PubMed  Google Scholar 

  • Peng M, Hannam C, Gu H, Bi YM and Rothstein SJ 2007 A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts Arabidopsis adaptability to nitrogen limitation. Plant J. 50 320–337

    Article  PubMed  CAS  Google Scholar 

  • Price J, Laxmi A, St Martin KS and Jang JC 2004 Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16 2128–2150

    Article  PubMed  CAS  Google Scholar 

  • Rea PA, Li ZS, Ln YP, Drozdowicz YM and Martinoia E 1998 From vacuolar GS-X pumps to multispecific ABC transporters. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49 727–760

    Article  PubMed  CAS  Google Scholar 

  • Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, Horvitz HR and Ruvkun G 2000 The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403 901–906

    Article  PubMed  CAS  Google Scholar 

  • Remm M, Storm CE and Sonnhammer EL 2001 Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. J. Mol. Biol. 314 1041–1052

    Article  PubMed  CAS  Google Scholar 

  • Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B and Bartel DP 2002 Prediction of plant microRNA targets. Cell 110 513–520

    Article  PubMed  CAS  Google Scholar 

  • Schachtman DP and Shin R 2007 Nutrient Sensing and Signaling: NPKS. Annu. Rev. Plant Biol. 58 47–69

    Article  PubMed  CAS  Google Scholar 

  • Scheible W-R, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N, Schindelasch D, Thimm O, et al. 2004 Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, celluar growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol. 136 2483–2499

    Article  PubMed  CAS  Google Scholar 

  • Schuler MA and Werck-Reichhart D 2003 Functional genomics of P450s. Annu. Rev. Plant Biol. 54 629–667

    Article  PubMed  CAS  Google Scholar 

  • Seki M, Narusaka M, Abe H, Kasuko M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y and Shinozaki K 2001 Monitoring the expression pattern of 1,300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13 61–72

    PubMed  CAS  Google Scholar 

  • Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, et al. 2002 Monitoring the expression profiles of 7,000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J. 31 279–292

    Article  PubMed  CAS  Google Scholar 

  • Socolow RH 1999 Nitrogen management and the future of food: lessons from the management of energy and carbon. Proc. Natl. Acad. Sci. USA 96 6001–6008

    Article  PubMed  CAS  Google Scholar 

  • Stitt M and Krapp A 1999 The molecular physiological basis for the interaction between elevated carbon dioxide and nutrients. Plant Cell Environ. 22 583–622

    Article  CAS  Google Scholar 

  • Sunkar R, Chinnusamy V, Zhu J and Zhu JK 2007 Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci. 12 301–309

    Article  PubMed  CAS  Google Scholar 

  • Sunkar R, Kapoor A and Zhu JK 2006 Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18 2051–2065

    Article  PubMed  CAS  Google Scholar 

  • Sunkar R and Zhu JK 2004 Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16 2001–2019

    Article  PubMed  CAS  Google Scholar 

  • Tepperman JM, Zhu T, Chang HS, Wang X and Quail PH 2001 Multiple transcription-factor genes are early targets of phytochrome A signaling. Proc. Natl. Acad. Sci. USA 98 9437–9442

    Article  PubMed  CAS  Google Scholar 

  • Tsai CJ, Harding SA, Tschaplinski TJ, Lindroth RL and Yuan Y 2006 Genome-wide analysis of the structural genes regulating defense phenylpropanoid metabolism in Populus. New Phytol. 172 47–62

    Article  PubMed  CAS  Google Scholar 

  • Uhde-Stone C, Gilbert G, Johnson JMF, Litjens R, Zinn KE, Temple SJ, Vance CP and Allan DL 2003 Acclimation of white lupin to phosphorus deficiency involves enhanced expression of genes related to organic acid metabolism. Plant Soil 248 99–116

    Article  CAS  Google Scholar 

  • Vaucheret H, Vazquez F, Crete P and Bartel DP 2004 The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev. 18 1187–1197

    Article  PubMed  CAS  Google Scholar 

  • Wang R and Crawford NM 1996 Genetic identification of a gene involved in constitutive, high affinity, nitrate transport in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 93 9297–9301

    Article  PubMed  CAS  Google Scholar 

  • Wang R, Guegler K, LaBrie ST and Crawford NM 2000 Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes that are induced by nitrate. Plant Cell 12 1491–1510

    PubMed  CAS  Google Scholar 

  • Wang R, Okamoto M, Xing X and Crawford NM 2003 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. 132 556–567

    Article  PubMed  CAS  Google Scholar 

  • Wang R, Tischner R, Gutierrez RA, Hoffman M, Xing X, Chen M, Coruzzi G and Crawford NM 2004 Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol. 136 2512–2522

    Article  PubMed  CAS  Google Scholar 

  • Wang YH, Garvin DF and Kochian LV 2001 Nitrate-induced genes in tomato roots. Array analysis reveals novel genes that may play a role in nitrogen nutrition. Plant Physiol. 127 345–359

    Article  PubMed  CAS  Google Scholar 

  • Wang YH, Garvin DF and Kochian LV 2002 Rapid induction of regulatory and transporter genes in response to phosphorus, potassium, and iron deficiencies in tomato roots: evidence for cross talk and root/rhizosphere-mediated signals. Plant Physiol. 130 1361–1370

    Article  PubMed  CAS  Google Scholar 

  • Wasaki J, Yonetani R, Kuroda S, Shinano T, Yazaki J, Fujii F, Shimbo K, Yamamoto K, et al. 2003 Transcriptomic analysis of metabolic changes by phosphorus stress in rice plant roots. Plant Cell Environ. 26 1515–1523

    Article  CAS  Google Scholar 

  • Werck-Reichhart D and Feyereisen R 2000 Cytochromes P450: A success story. Genome Biol. 3003 1–9

    Google Scholar 

  • Wu P, Ma L, Hou X, Wang M, Wu Y, Liu F and Deng XW 2003 Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol. 132 1260–1271

    Article  PubMed  CAS  Google Scholar 

  • Wu ZJ, Irizarry RA, Gentleman R, Martinez-Murillo F and Spencer F 2004 A model-based background adjustment for oligonucleotide expression arrays. J. Am. Stat.Assn. 99 909–917

    Article  Google Scholar 

  • Yamasaki H, Abdel-Ghany SE, Cohu CM, Kobayashi Y, Shikanai T and Pilon M 2007 Regulation of copper homeostasis by micro-RNA in Arabidopsis. J. Biol. Chem. 282 16369–16378

    Article  PubMed  CAS  Google Scholar 

  • Yoshida S, Forno DA, Cook JH and Gomez KA 1976 Laboratory manual for physiological studies of rice 3rd edition (Manila: International Rice Research Institute)

    Google Scholar 

  • Yuan H and Liu D 2008 Signaling components involved in plant responses to phosphate starvation. J. Integr. Plant Biol. 50 849–859

    Article  PubMed  CAS  Google Scholar 

  • Zhang B, Pan X, Cannon CH, Cobb GP, Anderson TA 2006a Conservation and divergence of plant microRNA genes. Plant J. 46 243–259

    Article  PubMed  CAS  Google Scholar 

  • Zhang B, Pan X, Cobb GP and Anderson TA 2006b Plant microRNA: A small regulatory molecule with big impact. Dev. Biol. 289 3–16

    Article  PubMed  CAS  Google Scholar 

  • Zhang H and Forde B 1998 An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279 407–409

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y 2005 miRU: an automated plant miRNA target prediction server. Nucleic Acids Res. 33 W701–704

    Article  PubMed  CAS  Google Scholar 

  • Zhu T 2003 Global analysis of gene expression using Gene Chip microarrays. Curr. Opin. Plant Biol. 6 1–8

    Article  Google Scholar 

  • Zhu T, Budworth P, Han B, Brown D, Chang HS, Zou G and Wang X 2001 Toward elucidating the global gene expression patterns of developing Arabidopsis: parallel analysis of 8,300 gene by a high-density oligonucleotide probe array. Plant Physiol. Biochem. 39 221–242

    Article  CAS  Google Scholar 

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Acknowledgements

This research was supported in part by grants from the National Basic Research Program of China (2011CB100304), the National High Technology Research and Development Program of China (2010AA101802), the National Natural Science Foundation of China (31000932), the Special Fund for Agro-scientific Research in the Public Interest (201003016) and the Gates Foundation.

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Authors and Affiliations

  1. National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Wuhan, China

    Hongmei Cai, Yongen Lu, Weibo Xie & Xingming Lian

  2. Microelement Research Center, College of Resources and Environment, Huazhong Agricultural University, Wuhan, 430070, China

    Hongmei Cai

  3. Syngenta Biotechnology Inc, 3054 Cornwallis Road, Research Triangle Park, NC, 27709, USA

    Tong Zhu

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  1. Hongmei Cai
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Corresponding editor: Utpal Nath

[Cai H, Lu Y, Xie W, Zhu T and Lian X 2012 Transcriptome response to nitrogen starvation in rice. J. Biosci. 37 1–17] DOI 10.1007/s12038-012-9242-2

Hongmei Cai and Yongen Lu contributed equally to this paper.

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Cai, H., Lu, Y., Xie, W. et al. Transcriptome response to nitrogen starvation in rice. J Biosci 37, 731–747 (2012). https://doi.org/10.1007/s12038-012-9242-2

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