Zygotic genome activation occurs shortly after fertilization in maize

Plant Cell

Volumn 29, Issue 9, 2017, Pages 2106-2125

  Chen, Junyi ^a   Strieder, Nicholas ^a   Krohn, Nadia G ^a,b   Cyprys, Philipp ^a   Sprunck, Stefanie ^a   Engelmann, Julia C ^a   Dresselhaus, Thomas ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b STATE UNIVERSITY OF MARINGÁ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; INDOLEACETIC ACID DERIVATIVE; TRANSCRIPTION FACTOR; TRANSCRIPTOME;

BODY PATTERNING; CELL CYCLE; CELL SEPARATION; CHROMATIN; CYTOLOGY; FERTILIZATION; FLOWER; GENE EXPRESSION REGULATION; GENETICS; MAIZE; METABOLISM; ORYZA; PLANT GENE; PLANT GENOME; PLANT SEED; REPRODUCIBILITY; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TIME FACTOR; ZYGOTE;

BODY PATTERNING; CELL CYCLE; CELL SEPARATION; CHROMATIN; FERTILIZATION; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENOME, PLANT; GERM CELLS, PLANT; HISTONES; INDOLEACETIC ACIDS; ORYZA; REPRODUCIBILITY OF RESULTS; SEEDS; SEQUENCE ANALYSIS, RNA; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION FACTORS; TRANSCRIPTOME; ZEA MAYS; ZYGOTE;

EID: 85032646475     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.17.00099     Document Type: Article

References (83)

1. Ahmad, K., and Henikoff, S. (2002). The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol. Cell 9: 1191-1200.
2. Amien, S., Kliwer, I., Márton, M.L., Debener, T., Geiger, D., Becker, D., and Dresselhaus, T. (2010). Defensin-like ZmES4 mediates pollen tube burst in maize via opening of the potassium channel KZM1. PLoS Biol. 8: e1000388.
3. Anderson, S.N., Johnson, C.S., Jones, D.S., Conrad, L.J., Gou, X., Russell, S.D., and Sundaresan, V. (2013). Transcriptomes of isolated Oryza sativa gametes characterized by deep sequencing: evidence for distinct sex-dependent chromatin and epigenetic states before fertilization. Plant J. 76: 729-741.
4. Autran, D., et al. (2011). Maternal epigenetic pathways control parental contributions to Arabidopsis early embryogenesis. Cell 145: 707-719.
5. Baroux, C., and Grossniklaus, U. (2015). The maternal-to-zygotic transition in flowering plants: Evidence, mechanisms, and plasticity. Curr. Top. Dev. Biol. 113: 351-371.
6. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57: 289-300.
7. Bolger, A.M., Lohse, M., and Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114-2120.
8. Borges, F., Gomes, G., Gardner, R., Moreno, N., McCormick, S., Feijó, J.A., and Becker, J.D. (2008). Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol. 148: 1168-1181.
9. Boutilier, K., Offringa, R., Sharma, V.K., Kieft, H., Ouellet, T., Zhang, L., Hattori, J., Liu, C.-M., van Lammeren, A.A.M., Miki, B.L.A., Custers, J.B.M., and van Lookeren Campagne, M.M. (2002). Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14: 1737-1749.
10. Breuninger, H., Rikirsch, E., Hermann, M., Ueda, M., and Laux, T. (2008). Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev. Cell 14: 867-876.
11. Budkevich, T.V., Timchenko, A.A., Tiktopulo, E.I., Negrutskii, B.S., Shalak, V.F., Petrushenko, Z.M., Aksenov, V.L., Willumeit, R., Kohlbrecher, J., Serdyuk, I.N., and El’skaya, A.V. (2002). Extended conformation of mammalian translation elongation factor 1A in solution. Biochemistry 41: 15342-15349.
12. Buendía-Monreal, M., Rentería-Canett, I., Guerrero-Andrade, O., Bravo-Alberto, C.E., Martínez-Castilla, L.P., García, E., and Vázquez-Ramos, J.M. (2011). The family of maize D-type cyclins: genomic organization, phylogeny and expression patterns. Physiol. Plant. 143: 297-308.
13. Chen, J., Lausser, A., and Dresselhaus, T. (2014). Hormonal responses during early embryogenesis in maize. Biochem. Soc. Trans. 42: 325-331.
14. Chen, J., Gutjahr, C., Bleckmann, A., and Dresselhaus, T. (2015). Calcium signaling during reproduction and biotrophic fungal interactions in plants. Mol. Plant 8: 595-611.
15. Chettoor, A.M., Givan, S.A., Cole, R.A., Coker, C.T., Unger-Wallace, E., Vejlupkova, Z., Vollbrecht, E., Fowler, J.E., and Evans, M.M. (2014). Discovery of novel transcripts and gametophytic functions via RNA-seq analysis of maize gametophytic transcriptomes. Genome Biol. 15: 414.
16. Chevalier, F., Perazza, D., Laporte, F., Le Hénanff, G., Hornitschek, P., Bonneville, J.-M., Herzog, M., and Vachon, G. (2008). GeBP and GeBP-like proteins are noncanonical leucine-zipper transcription factors that regulate cytokinin response in Arabidopsis. Plant Physiol. 146: 1142-1154.
17. Cordts, S., Bantin, J., Wittich, P.E., Kranz, E., Lörz, H., and Dresselhaus, T. (2001). ZmES genes encode peptides with structural homology to defensins and are specifically expressed in the female gametophyte of maize. Plant J. 25: 103-114.
18. Cui, Y., Dinman, J.D., Kinzy, T.G., and Peltz, S.W. (1998). The Mof2/ Sui1 protein is a general monitor of translational accuracy. Mol. Cell. Biol. 18: 1506-1516.
19. Dante, R.A., Larkins, B.A., and Sabelli, P.A. (2014). Cell cycle control and seed development. Front. Plant Sci. 5: 493.
20. Deal, R.B., and Henikoff, S. (2011). Histone variants and modifications in plant gene regulation. Curr. Opin. Plant Biol. 14: 116-122.
21. Del Toro-De León, G., García-Aguilar, M., and Gillmor, C.S. (2014). Non-equivalent contributions of maternal and paternal genomes to early plant embryogenesis. Nature 514: 624-627.
22. Dobin, A., Davis, C.A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., and Gingeras, T.R. (2013). STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29: 15-21.
23. Dresselhaus, T., Cordts, S., and Lörz, H. (1999a). A transcript encoding translation initiation factor eIF-5A is stored in unfertilized egg cells of maize. Plant Mol. Biol. 39: 1063-1071.
24. Dresselhaus, T., Lausser, A., and Márton, M.L. (2011). Using maize as a model to study pollen tube growth and guidance, crossincompatibility and sperm delivery in grasses. Ann. Bot. (Lond.) 108: 727-737.
25. Dresselhaus, T., Sprunck, S., and Wessel, G.M. (2016). Fertilization mechanisms in flowering plants. Curr. Biol. 26: R125-R139.
26. Dresselhaus, T., Srilunchang, K.-O., Leljak-Levanic, D., Schreiber, D.N., and Garg, P. (2006). The fertilization-induced DNA replication factor MCM6 of maize shuttles between cytoplasm and nucleus, and is essential for plant growth and development. Plant Physiol. 140: 512-527.
27. Dresselhaus, T., Cordts, S., Heuer, S., Sauter, M., Lörz, H., and Kranz, E. (1999b). Novel ribosomal genes from maize are differentially expressed in the zygotic and somatic cell cycles. Mol. Gen. Genet. 261: 416-427.
28. Dupuis, I., Roeckel, P., Matthys-Rochon, E., and Dumas, C. (1987). Procedure to isolate viable sperm cells from corn (Zea mays L.) pollen grains. Plant Physiol. 85: 876-878.
29. Engel, M.L., Chaboud, A., Dumas, C., and McCormick, S. (2003). Sperm cells of Zea mays have a complex complement of mRNAs. Plant J. 34: 697-707.
30. Friml, J., Vieten, A., Sauer, M., Weijers, D., Schwarz, H., Hamann, T., Offringa, R., and Jürgens, G. (2003). Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426: 147-153.
31. 2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell Biol. 6: 449-461.
32. Grimanelli, D., Perotti, E., Ramirez, J., and Leblanc, O. (2005). Timing of the maternal-to-zygotic transition during early seed development in maize. Plant Cell 17: 1061-1072.
33. Hecht, V., Vielle-Calzada, J.-P., Hartog, M.V., Schmidt, E.D.L., Boutilier, K., Grossniklaus, U., and de Vries, S.C. (2001). The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiol. 127: 803-816.
34. Hu, X., Cheng, X., Jiang, H., Zhu, S., Cheng, B., and Xiang, Y. (2010). Genome-wide analysis of cyclins in maize (Zea mays). Genet. Mol. Res. 9: 1490-1503.
35. Ingouff, M., Rademacher, S., Holec, S., Soljić, L., Xin, N., Readshaw, A., Foo, S.H., Lahouze, B., Sprunck, S., and Berger, F. (2010). Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Curr. Biol. 20: 2137-2143.
36. Juranicˇ, M., Srilunchang, K.O., Krohn, N.G., Leljak-Levanic´, D., Sprunck, S., and Dresselhaus, T. (2012). Germline-specific MATHBTB substrate adaptor MAB1 regulates spindle length and nuclei identity in maize. Plant Cell 24: 4974-4991.
37. Kawahara, Y., et al. (2013). Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice (N. Y.) 6: 4.
38. Kleine, T. (2012). Arabidopsis thaliana mTERF proteins: evolution and functional classification. Front. Plant Sci. 3: 233.
39. Kranz, E., Bautor, J., and Lorz, H. (1991). In vitro fertilization of single, isolated gametes of maize mediated by electrofusion. Sex. Plant Reprod. 4: 12-16.
40. Lee, M.T., Bonneau, A.R., and Giraldez, A.J. (2014). Zygotic genome activation during the maternal-to-zygotic transition. Annu. Rev. Cell Dev. Biol. 30: 581-613.
41. Lehti-Shiu, M.D., Adamczyk, B.J., and Fernandez, D.E. (2005). Expression of MADS-box genes during the embryonic phase in Arabidopsis. Plant Mol. Biol. 58: 89-107.
42. Li, L., Stoeckert, C.J., Jr., and Roos, D.S. (2003). OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13: 2178-2189.
43. Liao, Y., Smyth, G.K., and Shi, W. (2014). featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30: 923-930.
44. Lotan, T., Ohto, M., Yee, K.M., West, M.A., Lo, R., Kwong, R.W., Yamagishi, K., Fischer, R.L., Goldberg, R.B., and Harada, J.J. (1998). Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93: 1195-1205.
45. Love, M.I., Huber, W., and Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15: 550.
46. Lowe, K., et al. (2016). Morphogenic regulators Baby Boom and Wuschel improve monocot transformation. Plant Cell 28: 1998-2015.
47. Maiorano, D., Lutzmann, M., and Méchali, M. (2006). MCM proteins and DNA replication. Curr. Opin. Cell Biol. 18: 130-136.
48. Martin, M. (2011). Cutadapt removes adapter sequences from highthroughput sequencing reads. EMBnet J. 17: 10-12.
49. Márton, M.L., Cordts, S., Broadhvest, J., and Dresselhaus, T. (2005). Micropylar pollen tube guidance by egg apparatus 1 of maize. Science 307: 573-576.
50. Meijer, M., and Murray, J.A. (2001). Cell cycle controls and the development of plant form. Curr. Opin. Plant Biol. 4: 44-49.
51. Nodine, M.D., and Bartel, D.P. (2012). Maternal and paternal genomes contribute equally to the transcriptome of early plant embryos. Nature 482: 94-97.
52. Okada, T., Endo, M., Singh, M.B., and Bhalla, P.L. (2005). Analysis of the histone H3 gene family in Arabidopsis and identification of the male-gamete-specific variant AtMGH3. Plant J. 44: 557-568.
53. Ouyang, S., et al. (2007). The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res. 35: D883-D887.
54. Ouyang, X., et al. (2011). Genome-wide binding site analysis of FARRED ELONGATED HYPOCOTYL3 reveals its novel function in Arabidopsis development. Plant Cell 23: 2514-2535.
55. Petrásek, J., and Friml, J. (2009). Auxin transport routes in plant development. Development 136: 2675-2688.
56. Pintard, L., Willis, J.H., Willems, A., Johnson, J.-L.F., Srayko, M., Kurz, T., Glaser, S., Mains, P.E., Tyers, M., Bowerman, B., and Peter, M. (2003). The BTB protein MEL-26 is a substrate-specific adaptor of the CUL-3 ubiquitin-ligase. Nature 425: 311-316.
57. Ren, H., and Gray, W.M. (2015). SAUR proteins as effectors of hormonal and environmental signals in plant growth. Mol. Plant 8: 1153-1164.
58. Rieseberg, L.H., and Willis, J.H. (2007). Plant speciation. Science 317: 910-914.
59. Russell, S.D., Gou, X., Wong, C.E., Wang, X., Yuan, T., Wei, X., Bhalla, P.L., and Singh, M.B. (2012). Genomic profiling of rice sperm cell transcripts reveals conserved and distinct elements in the flowering plant male germ lineage. New Phytol. 195: 560-573.
60. Sabelli, P.A., Hoerster, G., Lizarraga, L.E., Brown, S.W., Gordon-Kamm, W.J., and Larkins, B.A. (2009). Positive regulation of minichromosome maintenance gene expression, DNA replication, and cell transformation by a plant retinoblastoma gene. Proc. Natl. Acad. Sci. USA 106: 4042-4047.
61. Sabelli, P.A., Liu, Y., Dante, R.A., Lizarraga, L.E., Nguyen, H.N., Brown, S.W., Klingler, J.P., Yu, J., LaBrant, E., Layton, T.M., Feldman, M., and Larkins, B.A. (2013). Control of cell proliferation, endoreduplication, cell size, and cell death by the retinoblastomarelated pathway in maize endosperm. Proc. Natl. Acad. Sci. USA 110: E1827-E1836.
62. Salvo, S.A.G.D., Hirsch, C.N., Buell, C.R., Kaeppler, S.M., and Kaeppler, H.F. (2014). Whole transcriptome profiling of maize during early somatic embryogenesis reveals altered expression of stress factors and embryogenesis-related genes. PLoS One 9: e111407.
63. Sauter, M., von Wiegen, P., Lörz, H., and Kranz, E. (1998). Cell cycle regulatory genes from maize are differentially controlled during fertilization and first embryonic cell division. Sex. Plant Reprod. 11: 41-48.
64. Schier, A.F. (2007). The maternal-zygotic transition: death and birth of RNAs. Science 316: 406-407.
65. Schnable, P.S., et al. (2009). The B73 maize genome: complexity, diversity, and dynamics. Science 326: 1112-1115.
66. Schon, M.A., and Nodine, M.D. (2017). Widespread contamination of Arabidopsis embryo and endosperm transcriptome data sets. Plant Cell 29: 608-617.
67. Schreiber, D.N., Bantin, J., and Dresselhaus, T. (2004). The MADS box transcription factor ZmMADS2 is required for anther and pollen maturation in maize and accumulates in apoptotic bodies during anther dehiscence. Plant Physiol. 134: 1069-1079.
68. Siller, K.H., and Doe, C.Q. (2009). Spindle orientation during asymmetric cell division. Nat. Cell Biol. 11: 365-374.
69. Thomas, J.O., and Travers, A.A. (2001). HMG1 and 2, and related ‘architectural’ DNA-binding proteins. Trends Biochem. Sci. 26: 167-174.
70. Tuteja, N., Tran, N.Q., Dang, H.Q., and Tuteja, R. (2011). Plant MCM proteins: role in DNA replication and beyond. Plant Mol. Biol. 77: 537-545.
71. Uebler, S., Márton, M.L., and Dresselhaus, T. (2015). Classification of EA1-box proteins and new insights into their role during reproduction in grasses. Plant Reprod. 28: 183-197.
72. Vandepoele, K., Raes, J., De Veylder, L., Rouzé, P., Rombauts, S., and Inzé, D. (2002). Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14: 903-916.
73. Vilella, A.J., Severin, J., Ureta-Vidal, A., Heng, L., Durbin, R., and Birney, E. (2009). EnsemblCompara GeneTrees: Complete, duplication-aware phylogenetic trees in vertebrates. Genome Res. 19: 327-335.
74. Wagner, G.P., Kin, K., and Lynch, V.J. (2012). Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples. Theory Biosci. 131: 281-285.
75. Wei, K., Chen, J., Wang, Y., Chen, Y., Chen, S., Lin, Y., Pan, S., Zhong, X., and Xie, D. (2012). Genome-wide analysis of bZIPencoding genes in maize. DNA Res. 19: 463-476.
76. Wu, R.-C., Jiang, M., Beaudet, A.L., and Wu, M.-Y. (2013). ARID4A and ARID4B regulate male fertility, a functional link to the AR and RB pathways. Proc. Natl. Acad. Sci. USA 110: 4616-4621.
77. Wuest, S.E., Vijverberg, K., Schmidt, A., Weiss, M., Gheyselinck, J., Lohr, M., Wellmer, F., Rahnenführer, J., von Mering, C., and Grossniklaus, U. (2010). Arabidopsis female gametophyte gene expression map reveals similarities between plant and animal gametes. Curr. Biol. 20: 506-512.
78. Yue, R., Tie, S., Sun, T., Zhang, L., Yang, Y., Qi, J., Yan, S., Han, X., Wang, H., and Shen, C. (2015). Genome-wide identification and expression profiling analysis of ZmPIN, ZmPILS, ZmLAX and ZmABCB auxin transporter gene families in maize (Zea mays L.) under various abiotic stresses. PLoS One 10: e0118751.
79. Zhang, Z., Li, X., Han, M., and Wu, Z. (2015). Genome-wide analysis and functional identification of the annexin gene family in maize (Zea mays L.). Plant Omics 8: 420-428.
80. Zhao, P., and Sun, M.X. (2015). The maternal-to-zygotic transition in higher plants: Available approaches, critical limitations, and technical requirements. Curr. Top. Dev. Biol. 113: 373-398.
81. Zhao, P., Begcy, K., Dresselhaus, T., and Sun, M.X. (2017). Does early embryogenesis in eudicots and monocots involve the same mechanism and molecular players? Plant Physiol. 173: 130-142.
82. Zheng, B., He, H., Zheng, Y., Wu, W., and McCormick, S. (2014). An ARID domain-containing protein within nuclear bodies is required for sperm cell formation in Arabidopsis thaliana. PLoS Genet. 10: e1004421.
83. Zhou, D.X., Bisanz-Seyer, C., and Mache, R. (1995). Molecular cloning of a small DNA binding protein with specificity for a tissuespecific negative element within the rps1 promoter. Nucleic Acids Res. 23: 1165-1169.