Does early embryogenesis in eudicots and monocots involve the same mechanism and molecular players?

Plant Physiology

Volumn 173, Issue 1, 2017, Pages 130-142

  Zhao, Peng ^a   Begcy, Kevin ^b   Dresselhaus, Thomas ^b   Sun, Meng Xiang ^a  

^a WUHAN UNIVERSITY   (China)

^b UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

INDOLEACETIC ACID DERIVATIVE; PHYTOHORMONE;

ANGIOSPERM; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL DIVISION; CELL LINEAGE; EMBRYOLOGY; GENE REGULATORY NETWORK; GENETICS; GENOME IMPRINTING; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; PLANT GENOME; ZYGOTE;

CELL COMMUNICATION; CELL DIFFERENTIATION; CELL DIVISION; CELL LINEAGE; GENE REGULATORY NETWORKS; GENOME, PLANT; GENOMIC IMPRINTING; INDOLEACETIC ACIDS; MAGNOLIOPSIDA; PLANT GROWTH REGULATORS; ZYGOTE;

EID: 85008677038     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.16.01406     Document Type: Article

References (92)

1. Abiko M, Maeda H, Tamura K, Hara-Nishimura I, Okamoto T (2013) Gene expression profiles in rice gametes and zygotes: identification of gamete-enriched genes and up- or down-regulated genes in zygotes after fertilization. J Exp Bot 64: 1927–1940
2. Anderson SN, Johnson CS, Jones DS, Conrad LJ, Gou X, Russell SD, 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
3. Autran D, Baroux C, Raissig MT, Lenormand T, Wittig M, Grob S, Steimer A, Barann M, Klostermeier UC, Leblanc O, et al (2011) Maternal epigenetic pathways control parental contributions to Arabidopsis early embryogenesis. Cell 145: 707–719
4. Bakos F, Szabó L, Olmedilla A, Barnabás B (2009) Histological comparison between wheat embryos developing in vitro from isolated zygotes and those developing in vivo. Sex Plant Reprod 22: 15–25
5. Baroux C, Grossniklaus U (2015) The maternal-to-zygotic transition in flowering plants: Evidence, mechanisms, and plasticity. Curr Top Dev Biol 113: 351–371
6. Bayer M, Nawy T, Giglione C, Galli M, Meinnel T, Lukowitz W (2009) Paternal control of embryonic patterning in Arabidopsis thaliana. Science 323: 1485–1488
7. Breuninger H, Rikirsch E, Hermann M, Ueda M, Laux T (2008) Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev Cell 14: 867–876
8. Carraro N, Forestan C, Canova S, Traas J, Varotto S (2006) ZmPIN1a and ZmPIN1b encode two novel putative candidates for polar auxin transport and plant architecture determination of maize. Plant Physiol 142: 254–264
9. Chandler J, Nardmann J, Werr W (2008) Plant development revolves around axes. Trends Plant Sci 13: 78–84
10. Chaw SM, Chang CC, Chen HL, Li WH (2004) Dating the monocot-dicot divergence and the origin of core eudicots using whole chloroplast genomes. J Mol Evol 58: 424–441
11. Chen J, Lausser A, Dresselhaus T (2014) Hormonal responses during early embryogenesis in maize. Biochem Soc Trans 42: 325–331
12. Chen Q, Yan M, Cao Z, Li X, Zhang Y, Shi J, Feng GH, Peng H, Zhang X, Zhang Y, et al (2016) Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science 351: 397–400
13. Costa LM, Marshall E, Tesfaye M, Silverstein KA, Mori M, Umetsu Y, Otterbach SL, Papareddy R, Dickinson HG, Boutiller K, et al (2014) Central cell-derived peptides regulate early embryo patterning in flowering plants. Science 344: 168–172
14. Del ToroDe Leon G, Garcia-Aguilar M, Gillmor CS (2014) Non-equivalent contributions of maternal and paternal genomes to early plant embryogenesis. Nature 514: 624–627
15. Dresselhaus T, Cordts S, Heuer S, Sauter M, Lörz H, Kranz E (1999) Novel ribosomal genes from maize are differentially expressed in the zygotic and somatic cell cycles. Mol Gen Genet 261: 416–427
16. Dresselhaus T, Srilunchang KO, Leljak-Levanic D, Schreiber DN, 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
17. Floyd SK, Lerner VT, Friedman WE (1999) A developmental and evolutionary analysis of embryology in Platanus (platanaceae), abasal eudicot. Am J Bot 86: 1523–1537
18. Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426: 147–153
19. Gehring M, Missirian V, Henikoff S (2011) Genomic analysis of parent-of-origin allelic expression in Arabidopsis thaliana seeds. PLoS One 6: e23687
20. Gooh K, Ueda M, Aruga K, Park J, Arata H, Higashiyama T, Kurihara D (2015) Live-cell imaging and optical manipulation of Arabidopsis early embryogenesis. Dev Cell 34: 242–251
21. Guo L, Jiang L, Zhang Y, Lu XL, Xie Q, Weijers D, Liu CM (2016) The anaphase-promoting complex initiates zygote division in Arabidopsis through degradation of cyclin B1. Plant J 86: 161–174
22. Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, Laux T (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131: 657–668
23. Hamann T, Benkova E, Bäurle I, Kientz M, Jürgens G (2002) The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev 16: 1610–1615
24. Hamann T, Mayer U, Jürgens G (1999) The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo. Development 126: 1387–1395
25. Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17: 1405–1411
26. Hsieh TF, Shin J, Uzawa R, Silva P, Cohen S, Bauer MJ, Hashimoto M, Kirkbride RC, Harada JJ, Zilberman D, et al (2011) Regulation of imprinted gene expression in Arabidopsis endosperm. Proc Natl Acad Sci USA 108: 1755–1762
27. Huang S, Hill RD, Stasolla C (2014a) Plant hemoglobin participation in cell fate determination. Plant Signal Behav 9: e29485
28. Huang S, Hill RD, Wally OSD, Dionisio G, Ayele BT, Jami SK, Stasolla C (2014b) Hemoglobin control of cell survival/death decision regulates in vitro plant embryogenesis. Plant Physiol 165: 810–825
29. Jahnke S, Scholten S (2009) Epigenetic resetting of a gene imprinted in plant embryos. Curr Biol 19: 1677–1681
30. Jenik PD, Gillmor CS, Lukowitz W (2007) Embryonic patterning in Arabidopsis thaliana. Annu Rev Cell Dev Biol 23: 207–236
31. Jeong S, Palmer TM, Lukowitz W (2011) The RWP-RK factor GROUNDED promotes embryonic polarity by facilitating YODA MAP kinase signaling. Curr Biol 21: 1268–1276
32. Jullien PE, Susaki D, Yelagandula R, Higashiyama T, Berger F (2012) DNA methylation dynamics during sexual reproduction in Arabidopsis thaliana. Curr Biol 22: 1825–1830
33. Juranic M, Srilunchang KO, Krohn NG, Leljak-Levanic D, Sprunck S, Dresselhaus T (2012) Germline-specific MATH-BTB substrate adaptor MAB1 regulates spindle length and nuclei identity in maize. Plant Cell 24: 4974–4991
34. Kankel MW, Ramsey DE, Stokes TL, Flowers SK, Haag JR, Jeddeloh JA, Riddle NC, Verbsky ML, Richards EJ (2003) Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163: 1109–1122
35. Lau S, Slane D, Herud O, Kong J, Jürgens G (2012) Early embryogenesis in flowering plants: setting up the basic body pattern. Annu Rev Plant Biol 63: 483–506
36. Lee MT, Bonneau AR, Giraldez AJ (2014) Zygotic genome activation during the maternal-to-zygotic transition. Annu Rev Cell Dev Biol 30: 581–613
37. Leljak-Levanic D, Juranic M, Sprunck S (2013) De novo zygotic transcription in wheat (Triticum aestivum L.) includes genes encoding small putative secreted peptides and a protein involved in proteasomal degradation. Plant Reprod 26: 267–285
38. Liu Y, Li X, Zhao J, Tang X, Tian S, Chen J, Shi C, Wang W, Zhang L, Feng X, Sun MX (2015) Direct evidence that suspensor cells have embryogenic potential that is suppressed by the embryo proper during normal embryogenesis. Proc Natl Acad Sci USA 112: 12432–12437
39. Locascio A, Roig-Villanova I, Bernardi J, Varotto S (2014) Current perspectives on the hormonal control of seed development in Arabidopsis and maize: a focus on auxin. Front Plant Sci 5: 412
40. Lukowitz W, Roeder A, Parmenter D, Somerville C (2004) A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 116: 109–119
41. Luo A, Shi C, Zhang L, Sun MX (2014) The expression and roles of parent-of-origin genes in early embryogenesis of angiosperms. Front Plant Sci 5: 729
42. Luo M, Taylor JM, Spriggs A, Zhang H, Wu X, Russell S, Singh M, Koltunow A (2011) A genome-wide survey of imprinted genes in rice seeds reveals imprinting primarily occurs in the endosperm. PLoS Genet 7: e1002125
43. Ma L, Xin H, Qu L, Zhao J, Yang L, Zhao P, Sun M (2011) Transcription profile analysis reveals that zygotic division results in uneven distribution of specific transcripts in apical/basal cells of tobacco. PLoS One 6: e15971
44. Mathieu O, Reinders J, Caikovski M, Smathajitt C, Paszkowski J (2007) Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation. Cell 130: 851–862
45. Mayer KF, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95: 805–815
46. Mayer U, Buttner G, Jürgens G (1993) Apical-basal pattern-formation in the Arabidopsis embryo - studies on the role of the gnom gene. Development 117: 149–162
47. Meyer S, Scholten S (2007) Equivalent parental contribution to early plant zygotic development. Curr Biol 17: 1686–1691
48. Mol R, Matthysrochon E, Dumas C (1994) The kinetics of cytological events during double fertilization in Zea mays L. Plant J 5: 197–206
49. Nardmann J, Zimmermann R, Durantini D, Kranz E, Werr W (2007) WOX gene phylogeny in Poaceae: a comparative approach addressing leaf and embryo development. Mol Biol Evol 24: 2474–2484
50. Ning J, Peng XB, Qu LH, Xin HP, Yan TT, Sun M (2006) Differential gene expression in egg cells and zygotes suggests that the transcriptome is restructed before the first zygotic division in tobacco. FEBS Lett 580: 1747–1752
51. Nodine MD, Bartel DP (2012) Maternal and paternal genomes contribute equally to the transcriptome of early plant embryos. Nature 482: 94–97
52. Okamoto T, Scholten S, Lörz H, Kranz E (2005) Identification of genes that are up- or down-regulated in the apical or basal cell of maize two-celled embryos and monitoring their expression during zygote development by a cell manipulation- and PCR-based approach. Plant Cell Physiol 46: 332–338
53. Peters JM (2006) The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat Rev Mol Cell Biol 7: 644–656
54. Quint M, Drost HG, Gabel A, Ullrich KK, Bönn M, Grosse I (2012) A transcriptomic hourglass in plant embryogenesis. Nature 490: 98–101
55. Rademacher EH, Lokerse AS, Schlereth A, Llavata-Peris CI, Bayer M, Kientz M, Freire Rios A, Borst JW, Lukowitz W, Jurgens G, Weijers D (2012) Different auxin response machineries control distinct cell fates in the early plant embryo. Dev Cell 22: 211–222
56. Raissig MT, Bemer M, Baroux C, Grossniklaus U (2013) Genomic imprinting in the Arabidopsis embryo is partly regulated by PRC2. PLoS Genet 9: e1003862
57. Ronceret A, Gadea-Vacas J, Guilleminot J, Lincker F, Delorme V, Lahmy S, Pelletier G, Chabouté ME, Devic M (2008) The first zygotic division in Arabidopsis requires de novo transcription of thymidylate kinase. Plant J 53: 776–789
58. Sanmartín M, Sauer M, Muñoz A, Zouhar J, Ordóñez A, van de Ven WTG, Caro E, de la Paz Sánchez M, Raikhel NV, Gutiérrez C, et al (2011) A molecular switch for initiating cell differentiation in Arabidopsis. Curr Biol 21: 999–1008
59. Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446: 811–814
60. Sato A, Toyooka K, Okamoto T (2010) Asymmetric cell division of rice zygotes located in embryo sac and produced by in vitro fertilization. Sex Plant Reprod 23: 211–217
61. Sauter M, von Wiegen P, Lörz H, 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
62. Scholten S, Lörz H, Kranz E (2002) Paternal mRNA and protein synthesis coincides with male chromatin decondensation in maize zygotes. Plant J 32: 221–231
63. Schwartz BW, Yeung EC, Meinke DW (1994) Disruption of morphogenesis and transformation of the suspensor in abnormal suspensor mutants of Arabidopsis. Development 120: 3235–3245
64. Sharma U, Conine CC, Shea JM, Boskovic A, Derr AG, Bing XY, Belleannee C, Kucukural A, Serra RW, Sun F, et al (2016) Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science 351: 391–396
65. Siklenka K, Erkek S, Godmann M, Lambrot R, McGraw S, Lafleur C, Cohen T, Xia J, Suderman M, Hallett M, et al (2015) Disruption of histone methylation in developing sperm impairs offspring health transgenerationally. Science 350: aab2006
66. Smith LG, Jackson D, Hake S (1995) Expression of Knotted1 marks shoot meristem formation during maize embryogenesis. Dev Genet 16: 344–348
67. Souter M, Lindsey K (2000) Polarity and signalling in plant embryogenesis. J Exp Bot 51: 971–983
68. Sprunck S, Baumann U, Edwards K, Langridge P, Dresselhaus T (2005) The transcript composition of egg cells changes significantly following fertilization in wheat (Triticum aestivum L.). Plant J 41: 660–672
69. Srilunchang KO, Krohn NG, Dresselhaus T (2010) DiSUMO-like DSUL is required for nuclei positioning, cell specification and viability during female gametophyte maturation in maize. Development 137: 333–345
70. Tadros W, Lipshitz HD (2009) The maternal-to-zygotic transition: a play in two acts. Development 136: 3033–3042
71. ten Hove CA, Lu KJ, Weijers D (2015) Building a plant: cell fate specification in the early Arabidopsis embryo. Development 142: 420–430
72. Torres-Ruiz RA, Jürgens G (1994) Mutations in the FASS gene uncouple pattern formation and morphogenesis in Arabidopsis development. Development 120: 2967–2978
73. Ueda M, Zhang Z, Laux T (2011) Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 links zygote polarity to embryo development. Dev Cell 20: 264–270
74. Vernon DM, Meinke DW (1994) Embryogenic transformation of the suspensor in twin, a polyembryonic mutant of Arabidopsis. Dev Biol 165: 566–573
75. Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19: 63–73
76. Waters AJ, Makarevitch I, Eichten SR, Swanson-Wagner RA, Yeh CT, Xu W, Schnable PS, Vaughn MW, Gehring M, Springer NM (2011) Parent-of-origin effects on gene expression and DNA methylation in the maize endosperm. Plant Cell 23: 4221–4233
77. Wu JJ, Peng XB, Li WW, He R, Xin HP, Sun MX (2012) Mitochondrial GCD1 dysfunction reveals reciprocal cell-to-cell signaling during the maturation of Arabidopsis female gametes. Dev Cell 23: 1043–1058
78. Xiao W, Custard KD, Brown RC, Lemmon BE, Harada JJ, Goldberg RB, Fischer RL (2006) DNA methylation is critical for Arabidopsis embryogenesis and seed viability. Plant Cell 18: 805–814
79. Xu J, Zhang HY, Xie CH, Xue HW, Dijkhuis P, Liu CM (2005) EMBRYONIC FACTOR 1 encodes an AMP deaminase and is essential for the zygote to embryo transition in Arabidopsis. Plant J 42: 743–756
80. Yadegari R, Paiva G, Laux T, Koltunow AM, Apuya N, Zimmerman JL, Fischer RL, Harada JJ, Goldberg RB (1994) Cell differentiation and morphogenesis are uncoupled in Arabidopsis raspberry embryos. Plant Cell 6: 1713–1729
81. Yi J, Lee YS, Lee DY, Cho MH, Jeon JS, An G (2016) OsMPK6 plays a critical role in cell differentiation during early embryogenesis in Oryza sativa. J Exp Bot 67: 2425–2437
82. Yu D, Jiang L, Gong H, Liu CM(2012) EMBRYONIC FACTOR 19 encodes a pentatricopeptide repeat protein that is essential for the initiation of zygotic embryogenesis in Arabidopsis. J Integr Plant Biol 54: 55–64
83. Yu HS, Russell SD (1994) Occurrence of mitochondria in the nuclei of tobacco sperm cells. Plant Cell 6: 1477–1484
84. Yu TY, Shi DQ, Jia PF, Tang J, Li HJ, Liu J, Yang WC (2016) The Arabidopsis receptor kinase ZAR1 is required for zygote asymmetric division and its daughter cell fate. PLoS Genet 12: e1005933
85. Zhang JZ, Somerville CR (1997) Suspensor-derived polyembryony caused by altered expression of valyl-tRNA synthetase in the twn2 mutant of Arabidopsis. Proc Natl Acad Sci USA 94: 7349–7355
86. Zhang M, Zhao H, Xie S, Chen J, Xu Y, Wang K, Zhao H, Guan H, Hu X, Jiao Y, et al (2011) Extensive, clustered parental imprinting of protein-coding and noncoding RNAs in developing maize endosperm. Proc Natl Acad Sci USA 108: 20042–20047
87. Zhao J, Xin H, Cao L, Huang X, Shi C, Zhao P, Fu Y, Sun MX (2016) NtDRP is necessary for accurate zygotic division orientation and differentiation of basal cell lineage toward suspensor formation. New Phytol 212: 598–612
88. Zhao J, Xin H, Qu L, Ning J, Peng X, Yan T, Ma L, Li S, Sun MX (2011) Dynamic changes of transcript profiles after fertilization are associated with de novo transcription and maternal elimination in tobacco zygote, and mark the onset of the maternal-to-zygotic transition. Plant J 65: 131–145
89. Zhao P, Sun MX (2015) The maternal-to-zygotic transition in higher plants: available approaches, critical limitations, and technical requirements. Curr Top Dev Biol 113: 373–398
90. Zhao P, Zhou XM, Zhang LY, Wang W, Ma LG, Yang LB, Peng XB, Bozhkov PV, Sun MX (2013) A bipartite molecular module controls cell death activation in the basal cell lineage of plant embryos. PLoS Biol 11: e1001655
91. Zimmermann R, Werr W (2005) Pattern formation in the monocot embryo as revealed by NAM and CUC3 orthologues from Zea mays L. Plant Mol Biol 58: 669–685
92. Zimmermann R, Werr W (2007) Transcription of the putative maize or-thologue of the Arabidopsis DORNROSCHEN gene marks early asymmetry in the proembryo and during leaf initiation in the shoot apical meristem. Gene Expr Patterns 7: 158–164