Abstract
Analysis of spatial and temporal gene expression pattern is instrumental to elucidation of gene networks and molecular mechanisms of tissue development. It also holds great value to applied research by providing tissue-specific (TS) promoter candidates for transgenic studies. Here, we present a large-scale systematic discovery of tissue-specific genes in maize. Profiles of TS genes were generated from a maize transcriptome atlas, with 71, 539, 23, 352, 51, and 287 genes showing expression specificity in the root, leaf, cob, endosperm, silk, and anther. Functional annotations and enrichment analysis of these TS genes identified pathways overrepresented for each tissue. Tissue specificity was experimentally confirmed by RT-PCR, mRNA in situ hybridization, and transgenic expression of promoter-fluorescent proteins. Two significantly enriched binding motifs, CATTGYCG and KGGTATCA, were identified from the promoter analysis of the anther- and endosperm-specifically expressed genes. Further, co-expression analysis on a broader set of maize germplasms identified molecular networks of TS genes and revealed a number of novel transcripts including non-coding RNA expressing the same pattern with the TS genes from B73. Our global analysis of maize TS transcriptomes could shed light on the molecular mechanisms of tissue specificity and facilitate transgenic studies by providing a valuable resource of TS promoter candidates.
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References
Anderson TJ, Lamsal BP (2011) Review: Zein extraction from corn, corn products, and coproducts and modifications for various applications: a review. Cereal Chem 88:159–173
Bailey TL (2011) DREME: motif discovery in transcription factor ChIP-seq data. Bioinformatics 27:1653–1659
Belmonte MF et al (2013) Comprehensive developmental profiles of gene activity in regions and subregions of the Arabidopsis seed. Proc Natl Acad Sci 110:E435–E444
Brown AP et al (2012) Tissue-specific whole transcriptome sequencing in castor, directed at understanding triacylglycerol lipid biosynthetic pathways. PLoS One 7:e30100
Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, Rinn JL (2011) Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 25:1915–1927
Chávez-Bárcenas AT, Valdez-Alarcón JJ, Martínez-Trujillo M, Chen L, Xoconostle-Cázares B, Lucas WJ, Herrera-Estrella L (2000) Tissue-specific and developmental pattern of expression of the rice sps1 gene. Plant Physiol 124:641–654
Chen M-X et al (2014) Strong seed-specific protein expression from the Vigna radiata storage protein 8SGα promoter in transgenic Arabidopsis seeds. J Biotechnol 174:49–56
Childs KL, Davidson RM, Buell CR (2011) Gene coexpression network analysis as a source of functional annotation for rice genes. PloS one 6:e22196
Christensen AH, Sharrock RA, Quail PH (1992) Maize polyubiquitin genes: structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation. Plant Mol Biol 18:675–689
Coen ES, Romero J, Doyle S, Elliott R, Murphy G, Carpenter R (1990) Floricaula: a homeotic gene required for flower development in Antirrhinum majus. Cell 63:1311–1322
Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676
Cook M, Thilmony R (2012) The OsGEX2 gene promoter confers sperm cell expression in transgenic rice. Plant Mol Biol Report 30:1138–1148
Cox MP, Peterson DA, Biggs PJ (2010) SolexaQA: at-a-glance quality assessment of Illumina second-generation sequencing data. BMC bioinformatics 11:485
de Pater S, Pham K, Memelink J, Kijne J (1996) Binding specificity and tissue-specific expression pattern of the Arabidopsis bZIP transcription factor TGA2. Mol Gen Genet MGG 250:237–239
Diaz I, Vicente‐Carbajosa J, Abraham Z, Martínez M, Moneda IL, Carbonero P (2002) The GAMYB protein from barley interacts with the DOF transcription factor BPBF and activates endosperm‐specific genes during seed development. Plant J 29:453–464
Diaz I, Martinez M, Isabel‐Lamoneda I, Rubio‐Somoza I, Carbonero P (2005) The DOF protein SAD, interacts with GAMYB in plant nuclei and activates transcription of endosperm‐specific genes during barley seed development. Plant J 42:652–662
Dobrin R et al (2009) Multi-tissue coexpression networks reveal unexpected subnetworks associated with disease. Genome Biol 10:R55
Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70. doi:10.1093/nar/gkq310
Dutt M, Ananthakrishnan G, Jaromin M, Brlansky R, Grosser J (2012) Evaluation of four phloem-specific promoters in vegetative tissues of transgenic citrus plants. Tree Physiol 32:83–93
Dutt M, Dhekney SA, Soriano L, Kandel R, Grosser JW (2014) Temporal and spatial control of gene expression in horticultural crops. Horticulture Research. 1.
Fagerberg L et al (2014) Analysis of the human tissue-specific expression by genome-wide integration of transcriptomics and antibody-based proteomics. Mol Cell Proteomics 13:397–406
Geng L, Duan X, Liang C, Shu C, Song F, Zhang J (2014) Mining tissue-specific contigs from peanut (Arachis hypogaea L.) for promoter cloning by deep transcriptome sequencing. Plant Cell Physiol 55:1793–1801
Gubler F, Raventos D, Keys M, Watts R, Mundy J, Jacobsen JV (1999) Target genes and regulatory domains of the GAMYB transcriptional activator in cereal aleurone. Plant J 17:1–9
Gupta S, Stamatoyannopoulos JA, Bailey TL, Noble WS (2007) Quantifying similarity between motifs. Genome Biol 8:R24
Hirsch CN et al (2014) Insights into the maize pan-genome and pan-transcriptome. Online 26:121–135
Hochholdinger F, Wulff D, Reuter K, Park WJ, Feix G (2000) Tissue-specific expression of AUX1 in maize roots. J Plant Physiol 157:315–319
Ishida Y, Hiei Y, Komari T (2007) Agrobacterium-mediated transformation of maize. Nat Protoc 2:1614–1621
Joshi JB et al. (2015) A maize α-zein promoter drives an endosperm-specific expression of transgene in rice. Physiology and Molecular Biology of Plants 21:35-42
Kathuria H, Giri J, Tyagi H, Tyagi AK (2007) Advances in transgenic rice biotechnology. Crit Rev Plant Sci 26:65–103
Kong L, Zhang Y, Ye Z-Q, Liu X-Q, Zhao S-Q, Wei L, Gao G (2007) CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res 35:W345–W349
Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC bioinformatics 9:559
Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25
Larkins BA, Pedersen K, Marks MD, Wilson DR (1984) The zein proteins of maize endosperm. Trends Biochem Sci 9:306–308
Law M et al (2015) Automated update, revision, and quality control of the maize genome annotations using MAKER-P improves the B73 RefGen_v3 gene models and identifies new genes. Plant Physiol 167:25–39
Li H et al (2013) Genome-wide association study dissects the genetic architecture of oil biosynthesis in maize kernels. Nat Genet 45:43–50
Liang S, Li Y, Be X, Howes S, Liu W (2006) Detecting and profiling tissue-selective genes. Physiol Genomics 26:158–162
Lightfoot DJ, Orford SJ, Timmis JN (2013) Identification and characterisation of cotton boll wall-specific gene promoters for future transgenic cotton varieties. Plant Mol Biol Report 31:174–184
Lin F, Jiang L, Liu Y, Lv Y, Dai H, Zhao H (2014) Genome-wide identification of housekee** genes in maize. Plant Mol Biol 86:543–554
Melzer R, Verelst W, Theißen G (2009) The class E floral homeotic protein SEPALLATA3 is sufficient to loop DNA in ‘floral quartet’-like complexes in vitro. Nucleic Acids Res 37:144–157
Nain V, Verma A, Kumar N, Sharma P, Ramesh B, Kumar PA (2008) Cloning of an ovule specific promoter from Arabidopsis thaliana and expression of beta-glucuronidase. Indian J Exp Biol 46:207
Odell JT, Nagy F, Chua N-H (1985) Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. Nature 313:810–812
Opsahl‐Ferstad HG, Deunff EL, Dumas C, Rogowsky PM (1997) ZmEsr, a novel endosperm‐specific gene expressed in a restricted region around the maize embryo. Plant J 12:235–246
Porto MS, Pinheiro MPN, Batista VGL, Dos Santos RC, de Albuquerque Melo Filho P, de Lima LM (2014) Plant promoters: an approach of structure and function. Molecular biotechnology 56:38–49
Rahim MA, Busatto N, Trainotti L (2014) Regulation of anthocyanin biosynthesis in peach fruits. Planta 240:913–929
Rosa BA, Jasmer DP, Mitreva M (2014) Genome-wide tissue-specific gene expression, co-expression and regulation of co-expressed genes in adult nematode Ascaris suum. PLoS Negl Trop Dis 8:e2678
Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods in Molecular Biology 132:365-386
Shannon P et al (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504
Smale ST, Kadonaga JT (2003) The RNA polymerase II core promoter. Annu Rev Biochem 72:449–479
Smirnova OG, Ibragimova SS, Kochetov AV (2012) Simple database to select promoters for plant transgenesis. Transgenic Res 21:429–437
Subramanian S, Hu X, Lu G, Odelland JT, Yu O (2004) The promoters of two isoflavone synthase genes respond differentially to nodulation and defense signals in transgenic soybean roots. Plant Mol Biol 54:623–639
Trapnell C et al (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515
Turcich MP, Hamilton DA, Mascarenhas JP (1993) Isolation and characterization of pollen-specific maize genes with sequence homology to ragweed allergens and pectate lyases. Plant Mol Biol 23:1061–1065
Vicente-Carbajosa J, Moose SP, Parsons RL, Schmidt RJ (1997) A maize zinc-finger protein binds the prolamin box in zein gene promoters and interacts with the basic leucine zipper transcriptional activator Opaque2. Proc Natl Acad Sci 94:7685–7690
Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63
**ao S-J, Zhang C, Zou Q, Ji Z-L (2010) TiSGeD: a database for tissue-specific genes. Bioinformatics 26:1273–1275
Ye R, Zhou F, Lin Y (2012) Two novel positive cis-regulatory elements involved in green tissue-specific promoter activity in rice (Oryza sativa L ssp.). Plant Cell Rep 31:1159–1172
Yin T et al (2009) Two negative cis-regulatory regions involved in fruit-specific promoter activity from watermelon (Citrullus vulgaris S.). J Exp Bot 60:169–185
Acknowledgments
This work was supported by a grant from Natural Science Foundation of Jiangsu Province, China (BK20141385), Natural Science Foundation of China (31271728), and Jiangsu Agriculture Science and Technology Innovation Fund [CX(14)5054].
Authors’ Contributions
H.Z. and F.L. conceived, designed, and conducted the experiments. H.B., H.X.D., and J.Y. helped in conducting the experiments. F.L. and H.B. analyzed the data and results. F.L., Y.H.L., and H.Z. wrote the manuscript. All authors read and approved the final manuscript.
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Feng Lin and Huabin Bao contributed equally to this work.
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Supplementary Table S1
The list of 1323 tissue-specific gene candidates with average FPKM detected in three RNA-seq datasets. (XLSX 82 kb)
Supplementary Table S2
Non-coding predictions of 389 unannotated TS transcripts with sequences. (XLSX 23 kb)
Supplementary Table S3
Functions enriched in each tissue analyzed by using SEA tool. (XLSX 11 kb)
Supplementary Table S4
Electronic northern analysis of predicted genes queried to EST libraries. (XLSX 19 kb)
Supplementary Table S5
The list of 270 genes clustered into six modules with co-expression in seed. (XLSX 18 kb)
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Lin, F., Bao, H., Yang, J. et al. Genome-Wide Discovery of Tissue-Specific Genes in Maize. Plant Mol Biol Rep 34, 1204–1214 (2016). https://doi.org/10.1007/s11105-016-1001-3
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DOI: https://doi.org/10.1007/s11105-016-1001-3