The differential transcription network between embryo and endosperm in the early developing

Plant Physiology

Volumn 162, Issue 1, 2013, Pages 440-455

  Lu, Xiaoduo ^a,c   Chen, Dijun ^b,d,e   Shu, Defeng ^a   Zhang, Zhao ^b   Wang, Weixuan ^c,f   Klukas, Christian ^e   Chen, Ling ling ^d   Fan, Yunliu ^c,f   Chen, Ming ^b   Zhang, Chunyi ^c,f  

^a Qilu Normal University   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c INSTITUTE OF PLANT PROTECTION   (China)

^d HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^e LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^f Sciences/National Key Facility for Crop Gene Resources and Genetic Improvement   (China)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME; VEGETABLE PROTEIN;

ALTERNATIVE RNA SPLICING; ARTICLE; ENDOSPERM; EXON; GENE EXPRESSION REGULATION; GENE LIBRARY; GENE REGULATORY NETWORK; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIGH THROUGHPUT SEQUENCING; INTRON; MAIZE; PLANT SEED; SEQUENCE ANALYSIS; TRANS SPLICING;

ALTERNATIVE SPLICING; ENDOSPERM; EXONS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENE LIBRARY; GENE REGULATORY NETWORKS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; INTRONS; PLANT PROTEINS; SEEDS; SEQUENCE ANALYSIS, RNA; TRANS-SPLICING; TRANSCRIPTOME; ZEA MAYS;

ZEA MAYS;

EID: 84877017150     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.214874     Document Type: Article

References (99)

1. Aanes H, Winata CL, Lin CH, Chen JP, Srinivasan KG, Lee SG, Lim AY, Hajan HS, Collas P, Bourque G, et al (2011) Zebrafish mRNA sequencing deciphers novelties in transcriptome dynamics during maternal to zygotic transition. Genome Res 21: 1328-1338
2. Abbe EC, Stein OL (1954) The growth of the shoot apex in maize: embryogeny. Am J Bot 41: 285-293
3. Agarwal P, Kapoor S, Tyagi AK (2011) Transcription factors regulating the progression of monocot and dicot seed development. Bioessays 33: 189-202
4. Barbazuk WB, Fu Y, McGinnis KM (2008) Genome-wide analyses of alternative splicing in plants: opportunities and challenges. Genome Res 18: 1381-1392
5. Barthole G, Lepiniec L, Rogowsky PM, Baud S (2012) Controlling lipid accumulation in cereal grains. Plant Sci 185-186: 33-39
6. Bemer M, Heijmans K, Airoldi C, Davies B, Angenent GC (2010) An atlas of type I MADS box gene expression during female gametophyte and seed development in Arabidopsis. Plant Physiol 154: 287-300
7. Black DL (2003) Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 72: 291-336
8. Blencowe BJ (2006) Alternative splicing: new insights from global analyses. Cell 126: 37-47
9. Brooks AN, Yang L, Duff MO, Hansen KD, Park JW, Dudoit S, Brenner SE, Graveley BR (2011) Conservation of an RNA regulatory map between Drosophila and mammals. Genome Res 21: 193-202
10. Bruno VM, Wang Z, Marjani SL, Euskirchen GM, Martin J, Sherlock G, Snyder M (2010) Comprehensive annotation of the transcriptome of the human fungal pathogen Candida albicans using RNA-seq. Genome Res 20: 1451-1458
11. Chaudhury AM, Koltunow A, Payne T, Luo M, Tucker MR, Dennis ES, Peacock WJ (2001) Control of early seed development. Annu Rev Cell Dev Biol 17: 677-699
12. Cloonan N, Forrest AR, Kolle G, Gardiner BB, Faulkner GJ, Brown MK, Taylor DF, Steptoe AL, Wani S, Bethel G, et al (2008) Stem cell transcriptome profiling via massive-scale mRNA sequencing. Nat Methods 5: 613-619
13. Daines B, Wang H, Wang L, Li Y, Han Y, Emmert D, Gelbart W, Wang X, Li W, Gibbs R, et al (2011) The Drosophila melanogaster transcriptome by paired-end RNA sequencing. Genome Res 21: 315-324
14. de Araujo PG, Rossi M, de Jesus EM, Saccaro NL Jr, Kajihara D, Massa R, de Felix JM, Drummond RD, Falco MC, Chabregas SM, et al (2005) Transcriptionally active transposable elements in recent hybrid sugarcane. Plant J 44: 707-717
15. de Hoon MJ, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20: 1453-1454
16. Dembinsky D, Woll K, Saleem M, Liu Y, Fu Y, Borsuk LA, Lamkemeyer T, Fladerer C, Madlung J, Barbazuk B, et al (2007) Transcriptomic and proteomic analyses of pericycle cells of the maize primary root. Plant Physiol 145: 575-588
17. Diboll AG (1968) Fine structural development of the megagametophyte of Zea mays following fertilization. Am J Bot 55: 797-806
18. 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
19. Feng S, Jacobsen SE, Reik W (2010) Epigenetic reprogramming in plant and animal development. Science 330: 622-627
20. Filichkin SA, Priest HD, Givan SA, Shen R, Bryant DW, Fox SE, Wong WK, Mockler TC (2010) Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res 20: 45-58
21. Fu J, Thiemann A, Schrag TA, Melchinger AE, Scholten S, Frisch M (2010) Dissecting grain yield pathways and their interactions with grain dry matter content by a two-step correlation approach with maize seedling transcriptome. BMC Plant Biol 10: 63
22. Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM, Yang L, Artieri CG, van Baren MJ, Boley N, Booth BW, et al (2011) The developmental transcriptome of Drosophila melanogaster. Nature 471: 473-479
23. Hehenberger E, Kradolfer D, Köhler C (2012) Endosperm cellularization defines an important developmental transition for embryo development. Development 139: 2031-2039
24. Hsieh TF, Ibarra CA, Silva P, Zemach A, Eshed-Williams L, Fischer RL, Zilberman D (2009) Genome-wide demethylation of Arabidopsis endosperm. Science 324: 1451-1454
25. Hueros G, Gomez E, Cheikh N, Edwards J, Weldon M, Salamini F, Thompson RD (1999a) Identification of a promoter sequence from the BETL1 gene cluster able to confer transfer-cell-specific expression in transgenic maize. Plant Physiol 121: 1143-1152
26. Hueros G, Royo J, Maitz M, Salamini F, Thompson RD (1999b) Evidence for factors regulating transfer cell-specific expression in maize endosperm. Plant Mol Biol 41: 403-414
27. Hueros G, Varotto S, Salamini F, Thompson RD (1995) Molecular characterization of BET1, a gene expressed in the endosperm transfer cells of maize. Plant Cell 7: 747-757
28. Huh JH, Bauer MJ, Hsieh TF, Fischer R (2007) Endosperm gene imprinting and seed development. Curr Opin Genet Dev 17: 480-485
29. Ingram GC, Boisnard-Lorig C, Dumas C, Rogowsky PM (2000) Expression patterns of genes encoding HD-ZipIV homeo domain proteins define specific domains in maize embryos and meristems. Plant J 22: 401-414
30. Ingram GC, Magnard JL, Vergne P, Dumas C, Rogowsky PM (1999) ZmOCL1, an HDGL2 family homeobox gene, is expressed in the outer cell layer throughout maize development. Plant Mol Biol 40: 343-354
31. Isshiki M, Morino K, Nakajima M, Okagaki RJ, Wessler SR, Izawa T, Shimamoto K (1998) A naturally occurring functional allele of the rice waxy locus has a GT to TT mutation at the 59 splice site of the first intron. Plant J 15: 133-138
32. Jin P, Guo T, Becraft PW (2000) The maize CR4 receptor-like kinase mediates a growth factor-like differentiation response. Genesis 27: 104-116
33. Kakumanu A, Ambavaram MM, Klumas C, Krishnan A, Batlang U, Myers E, Grene R, Pereira A (2012) Effects of drought on gene expression in maize reproductive and leaf meristem tissue revealed by RNA-Seq. Plant Physiol 160: 846-867
34. Kalsotra A, Cooper TA (2011) Functional consequences of developmentally regulated alternative splicing. Nat Rev Genet 12: 715-729
35. Kang IH, Steffen JG, Portereiko MF, Lloyd A, Drews GN (2008) The AGL62 MADS domain protein regulates cellularization during endosperm development in Arabidopsis. Plant Cell 20: 635-647
36. Keren H, Lev-Maor G, Ast G (2010) Alternative splicing and evolution: diversification, exon definition and function. Nat Rev Genet 11: 345-355
37. Kerstetter RA, Laudencia-Chingcuanco D, Smith LG, Hake S (1997) Lossof-function mutations in the maize homeobox gene, knotted1, are defective in shoot meristem maintenance. Development 124: 3045-3054
38. Kim D, Salzberg SL (2011) TopHat-Fusion: an algorithm for discovery of novel fusion transcripts. Genome Biol 12: R72
39. Kodrzycki R, Boston RS, Larkins BA (1989) The opaque-2 mutation of maize differentially reduces zein gene transcription. Plant Cell 1: 105-114
40. Kowles R, Phillips R (1988) Endosperm development in maize. Int Rev Cytol 112: 97-136
41. Lammeren AAM (1986) Developmental morphology and cytology of the young maize embryo (Zea mays L.). Acta Bot Neerl 35: 169-188
42. 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
43. Le BH, Cheng C, Bui AQ, Wagmaister JA, Henry KF, Pelletier J, Kwong L, Belmonte M, Kirkbride R, Horvath S, et al (2010) Global analysis of gene activity during Arabidopsis seed development and identification of seedspecific transcription factors. Proc Natl Acad Sci USA 107: 8063-8070
44. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows- Wheeler transform. Bioinformatics 25: 1754-1760
45. Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta SL, Kebrom TH, Provart N, Patel R, Myers CR, et al (2010) The developmental dynamics of the maize leaf transcriptome. Nat Genet 42: 1060-1067
46. Lister R, O'Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, Ecker JR (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133: 523-536
47. Liu PP, Montgomery TA, Fahlgren N, Kasschau KD, Nonogaki H, Carrington JC (2007) Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J 52: 133-146
48. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408
49. Lopes FR, Carazzolle MF, Pereira GA, Colombo CA, Carareto CM (2008) Transposable elements in Coffea (Gentianales: Rubiacea) transcripts and their role in the origin of protein diversity in flowering plants. Mol Genet Genomics 279: 385-401
50. Lopes MA, Larkins BA (1993) Endosperm origin, development, and function. Plant Cell 5: 1383-1399
51. Lu T, Lu G, Fan D, Zhu C, Li W, Zhao Q, Feng Q, Zhao Y, Guo Y, Li W, et al (2010) Function annotation of the rice transcriptome at singlenucleotide resolution by RNA-seq. Genome Res 20: 1238-1249
52. Lu X, Li Y, Su Y, Liang Q, Meng H, Li S, Shen S, Fan Y, Zhang C (2012) An Arabidopsis gene encoding a C2H2-domain protein with alternatively spliced transcripts is essential for endosperm development. J Exp Bot 63: 5935-5944
53. Macknight R, Duroux M, Laurie R, Dijkwel P, Simpson G, Dean C (2002) Functional significance of the alternative transcript processing of the Arabidopsis floral promoter FCA. Plant Cell 14: 877-888
54. Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y (2008) RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 18: 1509-1517
55. Marquez Y, Brown JW, Simpson C, Barta A, Kalyna M (2012) Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis. Genome Res 22: 1184-1195
56. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628
57. Mosher RA, Melnyk CW, Kelly KA, Dunn RM, Studholme DJ, Baulcombe DC (2009) Uniparental expression of PolIV-dependent siRNAs in developing endosperm of Arabidopsis. Nature 460: 283-286
58. Mosher RA, Melnyk CW (2010) siRNAs and DNA methylation: seedy epigenetics. Trends Plant Sci 15: 204-210
59. Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, Snyder M (2008) The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320: 1344-1349
60. Nilsen TW, Graveley BR (2010) Expansion of the eukaryotic proteome by alternative splicing. Nature 463: 457-463
61. Ohtsu K, Smith MB, Emrich SJ, Borsuk LA, Zhou R, Chen T, Zhang X, Timmermans MC, Beck J, Buckner B, et al (2007) Global gene expression analysis of the shoot apical meristem of maize (Zea mays L.). Plant J 52: 391-404
62. Olsen OA (2004) Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell (Suppl) 16: S214-S227
63. Olsen OA, Linnestad C, Nichols SE (1999) Developmental biology of the cereal endosperm. Trends Plant Sci 4: 253-257
64. Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 40: 1413-1415
65. Picault N, Chaparro C, Piegu B, Stenger W, Formey D, Llauro C, Descombin J, Sabot F, Lasserre E, Meynard D, et al (2009) Identification of an active LTR retrotransposon in rice. Plant J 58: 754-765
66. Prioul JL, Méchin V, Lessard P, Thévenot C, Grimmer M, Chateau-Joubert S, Coates S, Hartings H, Kloiber-Maitz M, Murigneux A, et al (2008) A joint transcriptomic, proteomic and metabolic analysis of maize endosperm development and starch filling. Plant Biotechnol J 6: 855-869
67. Randolph L (1936) Developmental morphology of the caryopsis in maize. J Agric Res 53: 881-916
68. Reddy AS (2007) Alternative splicing of pre-messenger RNAs in plants in the genomic era. Annu Rev Plant Biol 58: 267-294
69. Saldanha AJ (2004) Java Treeview: extensible visualization of microarray data. Bioinformatics 20: 3246-3248
70. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326: 1112-1115
71. Schruff MC, Spielman M, Tiwari S, Adams S, Fenby N, Scott RJ (2006) The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development 133: 251-261
72. Seo PJ, Kim MJ, Ryu JY, Jeong EY, Park CM (2011) Two splice variants of the IDD14 transcription factor competitively form nonfunctional heterodimers which may regulate starch metabolism. Nat Commun 2: 303
73. Sibout R, Sukumar P, Hettiarachchi C, Holm M, Muday GK, Hardtke CS (2006) Opposite root growth phenotypes of hy5 versus hy5 hyh mutants correlate with increased constitutive auxin signaling. PLoS Genet 2: e202
74. Smith LG, Jackson D, Hake S (1995) Expression of knotted1 marks shoot meristem formation during maize embryogenesis. Dev Genet 16: 344-348
75. Sossountzov L, Ruiz-Avila L, Vignols F, Jolliot A, Arondel V, Tchang F, Grosbois M, Guerbette F, Miginiac E, Delseny M, et al (1991) Spatial and temporal expression of a maize lipid transfer protein gene. Plant Cell 3: 923-933
76. Sreenivasulu N, Usadel B, Winter A, Radchuk V, Scholz U, Stein N, Weschke W, Strickert M, Close TJ, Stitt M, et al (2008) Barley grain maturation and germination: metabolic pathway and regulatory network commonalities and differences highlighted by new MapMan/PageMan profiling tools. Plant Physiol 146: 1738-1758
77. Stein LD, Mungall C, Shu S, Caudy M, Mangone M, Day A, Nickerson E, Stajich JE, Harris TW, Arva A, et al (2002) The generic genome browser: a building block for a model organism system database. Genome Res 12: 1599-1610
78. Stone SL, Kwong LW, Yee KM, Pelletier J, Lepiniec L, Fischer RL, Goldberg RB, Harada JJ (2001) LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proc Natl Acad Sci USA 98: 11806-11811
79. Sultan M, Schulz MH, Richard H, Magen A, Klingenhoff A, Scherf M, Seifert M, Borodina T, Soldatov A, Parkhomchuk D, et al (2008) A global view of gene activity and alternative splicing by deep sequencing of the human transcriptome. Science 321: 956-960
80. Takacs EM, Li J, Du C, Ponnala L, Janick-Buckner D, Yu J, Muehlbauer GJ, Schnable PS, Timmermans MC, Sun Q, et al (2012) Ontogeny of the maize shoot apical meristem. Plant Cell 24: 3219-3234
81. Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37: 914-939
82. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111
83. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515
84. Vernoud V, Hajduch M, Khaled A-S, Depège N, Rogowsky PM (2005) Maize embryogenesis. Maydica 50: 469-484
85. Vicient CM, Jääskeläinen MJ, Kalendar R, Schulman AH (2001) Active retrotransposons are a common feature of grass genomes. Plant Physiol 125: 1283-1292
86. Wang BB, Brendel V (2006) Genomewide comparative analysis of alternative splicing in plants. Proc Natl Acad Sci USA 103: 7175-7180
87. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456: 470-476
88. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10: 57-63
89. Wetterbom A, Ameur A, Feuk L, Gyllensten U, Cavelier L (2010) Identification of novel exons and transcribed regions by chimpanzee transcriptome sequencing. Genome Biol 11: R78
90. Wilhelm BT, Landry JR (2009) RNA-Seq-quantitative measurement of expression through massively parallel RNA-sequencing. Methods 48: 249-257
91. Wilhelm BT, Marguerat S, Watt S, Schubert F, Wood V, Goodhead I, Penkett CJ, Rogers J, Bähler J (2008) Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature 453: 1239-1243
92. Woo YM, Hu DW, Larkins BA, Jung R (2001) Genomics analysis of genes expressed in maize endosperm identifies novel seed proteins and clarifies patterns of zein gene expression. Plant Cell 13: 2297-2317
93. Xing H, Pudake RN, Guo G, Xing G, Hu Z, Zhang Y, Sun Q, Ni Z (2011) Genome-wide identification and expression profiling of auxin response factor (ARF) gene family in maize. BMC Genomics 12: 178
94. Zhang CQ, Xu Y, Lu Y, Yu HX, Gu MH, Liu QQ (2011a) The WRKY transcription factor OsWRKY78 regulates stem elongation and seed development in rice. Planta 234: 541-554
95. Zhang G, Guo G, Hu X, Zhang Y, Li Q, Li R, Zhuang R, Lu Z, He Z, Fang X, et al (2010) Deep RNA sequencing at single base-pair resolution reveals high complexity of the rice transcriptome. Genome Res 20: 646-654
96. Zhang H, Zhu JK (2011) RNA-directed DNA methylation. Curr Opin Plant Biol 14: 142-147
97. Zhang M, Zhao H, Xie S, Chen J, Xu Y, Wang K, Zhao H, Guan H, Hu X, Jiao Y, et al (2011b) Extensive, clustered parental imprinting of proteincoding and noncoding RNAs in developing maize endosperm. Proc Natl Acad Sci USA 108: 20042-20047
98. Zhang XC, Gassmann W (2007) Alternative splicing and mRNA levels of the disease resistance gene RPS4 are induced during defense responses. Plant Physiol 145: 1577-1587
99. Zhang XN, Mount SM (2009) Two alternatively spliced isoforms of the Arabidopsis SR45 protein have distinct roles during normal plant development.Plant Physiol 150: 1450-1458