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Digital gene expression analysis reveals nitrogen fertilizer increases panicle size by repressing Hd3a signaling in rice

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Abstract

Nitrogen fertilizer significantly increases spikelet number and grain yield in rice. Although many transcriptome analyses of rice have been conducted, this is the first study to examine differential gene expression in young panicles of rice in response to nitrogen fertilizer. Digital gene expression tag profiling is a revolutionary approach for gene expression analysis. Here, differential gene expression was analyzed in young panicles that received different applications of fertilizer. Digital gene expression analysis identified hundreds of genes that significantly differed in their expression level after the plants received nitrogen treatment. Of note, nitrogen fertilizer significantly reduced several major photoperiod sensitivity regulators that trigger flowering in rice. Quantitative reverse transcription polymerase chain reaction analysis also showed that the expression of two florigen genes, Heading date 3a (Hd3a) and RICE FLOWERING LOCUS T 1 (RFT1), was repressed in leaves by nitrogen fertilizer. In addition, the expression of two important genes that control panicle size, OsEATB and DENSE AND ERECT PANICLE1 (DEP1), was significantly promoted by nitrogen fertilizer. The identification of novel differentially expressed genes provides new insights into the profound impacts of nitrogen fertilizer on panicle development and may suggest new strategies to improve yield in rice.

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References

  • Andres F, Galbraith DW, Talon M, Domingo C (2009) Analysis of PHOTOPERIOD SENSITIVITY5 sheds light on the role of phytochromes in photoperiodic flowering in rice. Plant Physiol 151:681–690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chakravorty D, Trusov Y, Zhang W, Acharya BR, Sheahan MB, McCurdy DW, Assmann SM, Botella JR (2011) An atypical heterotrimeric g-protein gamma-subunit is involved in guard cell K(+)-channel regulation and morphological development in Arabidopsis thaliana. Plant J 67:840–851

    Article  CAS  PubMed  Google Scholar 

  • Ding C, You J, Chen L, Wang S, Ding Y (2014) Nitrogen fertilizer increases spikelet number per panicle by enhancing cytokinin synthesis in rice. Plant Cell Rep 33:363–371

    Article  CAS  PubMed  Google Scholar 

  • Eveland AL, Satoh-Nagasawa N, Goldshmidt A, Meyer S, Beatty M, Sakai H, Ware D, Jackson D (2010) Digital gene expression signatures for maize development. Plant Physiol 154:1024–1039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furukawa T, Sakaguchi N, Shimada H (2006) Two OsGASR genes, rice GAST homologue genes that are abundant in proliferating tissues, show different expression patterns in developing panicles. Genes Genet Syst 81:171–180

    Article  CAS  PubMed  Google Scholar 

  • Gao X, Chen Z, Zhang J, Li X, Chen G, Li X, Wu C (2012) OsLIS-L1 encoding a lissencephaly type-1-like protein with WD40 repeats is required for plant height and male gametophyte formation in rice. Planta 235:713–727

    Article  CAS  PubMed  Google Scholar 

  • Gao H, Jin M, Zheng XM, Chen J, Yuan D, Xin Y, Wang M, Huang D, Zhang Z, Zhou K, Sheng P, Ma J, Ma W, Deng H, Jiang L, Liu S, Wang H, Wu C, Yuan L, Wan J (2014) Days to heading 7, a major quantitative locus determining photoperiod sensitivity and regional adaptation in rice. Proc Natl Acad Sci USA 111:16337–16342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hao QN, Zhou XA, Sha AH, Wang C, Zhou R, Chen SL (2011) Identification of genes associated with nitrogen-use efficiency by genome-wide transcriptional analysis of two soybean genotypes. BMC Genom 12:525

    Article  CAS  Google Scholar 

  • Huang X, Qian Q, Liu Z, Sun H, He S, Luo D, Xia G, Chu C, Li J, Fu X (2009) Natural variation at the DEP1 locus enhances grain yield in rice. Nat Genet 41:494–497

    Article  CAS  PubMed  Google Scholar 

  • Jain M, Nijhawan A, Arora R, Agarwal P, Ray S, Sharma P, Kapoor S, Tyagi AK, Khurana JP (2007) F-box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiol 143:1467–1483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jan A, Kitano H, Matsumoto H, Komatsu S (2006) The rice OsGAE1 is a novel gibberellin-regulated gene and involved in rice growth. Plant Mol Biol 62:439–452

    Article  CAS  PubMed  Google Scholar 

  • Kim SK, Yun CH, Lee JH, Jang YH, Park HY, Kim JK (2008) OsCO3, a CONSTANS-LIKE gene, controls flowering by negatively regulating the expression of FT-like genes under SD conditions in rice. Planta 228:355–365

    Article  CAS  PubMed  Google Scholar 

  • Komiya R, Ikegami A, Tamaki S, Yokoi S, Shimamoto K (2008) Hd3a and RFT1 are essential for flowering in rice. Development 135:767–774

    Article  CAS  PubMed  Google Scholar 

  • Lee YS, Jeong DH, Lee DY, Yi J, Ryu CH, Kim SL, Jeong HJ, Choi SC, Jin P, Yang J, Cho LH, Choi H, An G (2010) OsCOL4 is a constitutive flowering repressor upstream of Ehd1 and downstream of OsphyB. Plant J 63:18–30

    CAS  PubMed  Google Scholar 

  • Lian X, Wang S, Zhang J, Feng Q, Zhang L, Fan D, Li X, Yuan D, Han B, Zhang Q (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  CAS  PubMed  Google Scholar 

  • Licausi F, Ohme-Takagi M, Perata P (2013) APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol 199:639–649

    Article  CAS  PubMed  Google Scholar 

  • Osugi A, Itoh H, Ikeda-Kawakatsu K, Takano M, Izawa T (2011) Molecular dissection of the roles of phytochrome in photoperiodic flowering in rice. Plant Physiol 157:1128–1137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng M, Bi YM, Zhu T, Rothstein SJ (2007) Genome-wide analysis of Arabidopsis responsive transcriptome to nitrogen limitation and its regulation by the ubiquitin ligase gene NLA. Plant Mol Biol 65:775–797

    Article  CAS  PubMed  Google Scholar 

  • Qi W, Sun F, Wang Q, Chen M, Huang Y, Feng YQ, Luo X, Yang J (2011) Rice ethylene-response AP2/ERF factor OsEATB restricts internode elongation by down-regulating a gibberellin biosynthetic gene. Plant Physiol 157:216–228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rieu I, Powers SJ (2009) Real-time quantitative RT–PCR: design, calculations, and statistics. Plant Cell 21:1031–1033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen Y, Jiang Z, Yao X, Zhang Z, Lin H, Zhao M, Liu H, Peng H, Li S, Pan G (2012) Genome expression profile analysis of the immature maize embryo during dedifferentiation. PLoS ONE 7:e32237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun H, Qian Q, Wu K, Luo J, Wang S, Zhang C, Ma Y, Liu Q, Huang X, Yuan Q, Han R, Zhao M, Dong G, Guo L, Zhu X, Gou Z, Wang W, Wu Y, Lin H, Fu X (2014) Heterotrimeric G proteins regulate nitrogen-use efficiency in rice. Nat Genet 46:652–656

    Article  CAS  PubMed  Google Scholar 

  • Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K (2007) Hd3a protein is a mobile flowering signal in rice. Science 316:1033–1036

    Article  CAS  PubMed  Google Scholar 

  • Tamura W, Kojima S, Toyokawa A, Watanabe H, Tabuchi-Kobayashi M, Hayakawa T, Yamaya T (2011) Disruption of a novel NADH-glutamate synthase2 gene caused marked reduction in spikelet number of rice. Front Plant Sci 2:57

    Article  PubMed  PubMed Central  Google Scholar 

  • Taoka K, Ohki I, Tsuji H, Furuita K, Hayashi K, Yanase T, Yamaguchi M, Nakashima C, Purwestri YA, Tamaki S, Ogaki Y, Shimada C, Nakagawa A, Kojima C, Shimamoto K (2011) 14-3-3 proteins act as intracellular receptors for rice Hd3a florigen. Nature 476:332–335

    Article  CAS  PubMed  Google Scholar 

  • Urano D, Jones AM (2014) Heterotrimeric G protein-coupled signaling in plants. Annu Rev Plant Biol 65:365–384

    Article  CAS  PubMed  Google Scholar 

  • Wan L, Zhang J, Zhang H, Zhang Z, Quan R, Zhou S, Huang R (2011) Transcriptional activation of OsDERF1 in OsERF3 and OsAP2-39 negatively modulates ethylene synthesis and drought tolerance in rice. PLoS ONE 6:e25216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang R, Guegler K, LaBrie ST, Crawford NM (2000) Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate. Plant Cell 12:1491–1509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei X, Xu J, Guo H, Jiang L, Chen S, Yu C, Zhou Z, Hu P, Zhai H, Wan J (2010) DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiol 153:1747–1758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weng X, Wang L, Wang J, Hu Y, Du H, Xu C, Xing Y, Li X, Xiao J, Zhang Q (2014) Grain number, plant height, and heading date7 is a central regulator of growth, development, and stress response. Plant Physiol 164:735–747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X, Zhang Q (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40:761–767

    Article  CAS  PubMed  Google Scholar 

  • Yadav DK, Islam SM, Tuteja N (2012) Rice heterotrimeric G-protein gamma subunits (RGG1 and RGG2) are differentially regulated under abiotic stress. Plant Signal Behav 7:733–740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yaish MW, El-kereamy A, Zhu T, Beatty PH, Good AG, Bi Y-M, Rothstein SJ (2010) The APETALA-2-like transcription factor OsAP2-39 controls key interactions between abscisic acid and gibberellin in rice. PLoS Genet 6:e1001098

    Article  PubMed  PubMed Central  Google Scholar 

  • Yoshida H, Horie T, Shiraiwa T (2006) A model explaining genotypic and environmental variation of rice spikelet number per unit area measured by cross-locational experiments in Asia. Field Crops Res 97:337–343

    Article  Google Scholar 

  • Yoshida A, Ohmori Y, Kitano H, Taguchi-Shiobara F, Hirano HY (2012) Aberrant spikelet and panicle1, encoding a TOPLESS-related transcriptional co-repressor, is involved in the regulation of meristem fate in rice. Plant J 70:327–339

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (Grant Numbers 31401324), the Fundamental Research Funds for the Central Universities (Grant Numbers KJQN201504), and the National High Technology Research and Development Program of China (863 Program, Grant Number 2014AA10A605-1).

Author contributions

C.D., S.W., and Y.D. conceived and designed the experiments. C.D. performed the experiments and analyzed the data. C.D., Y.W. and S.Y. wrote the paper.

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Correspondence to Yanfeng Ding.

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Ding, C., Wang, Y., You, S. et al. Digital gene expression analysis reveals nitrogen fertilizer increases panicle size by repressing Hd3a signaling in rice. Plant Growth Regul 79, 47–54 (2016). https://doi.org/10.1007/s10725-015-0108-0

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  • DOI: https://doi.org/10.1007/s10725-015-0108-0

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