Plant Reproduction

, Volume 26, Issue 3, pp 267–285 | Cite as

De novo zygotic transcription in wheat (Triticum aestivum L.) includes genes encoding small putative secreted peptides and a protein involved in proteasomal degradation

  • Dunja Leljak-Levanić
  • Martina Juranić
  • Stefanie Sprunck
Original Article

Abstract

Wheat is one of the world’s most important crops, and increasing grain yield is a major challenge for the future. Still, our knowledge about the molecular machineries responsible for early post-fertilization events such as zygotic reprogramming, the initial cell-specification events during embryogenesis, and the intercellular communication between the early embryo and the developing endosperm is very limited. Here, we describe the identification of de novo transcribed genes in the wheat zygote. We used wheat ovaries of defined post-fertilization stages to isolate zygotes and early embryos, and identified genes that are specifically induced in these particular stages. Importantly, we observed that some of the zygotic-induced genes encode proteins with similarity to secreted signaling peptides such as TAPETUM DETERMINANT 1 and EGG APPARATUS 1, and to MATH-BTB proteins which are known substrate-binding adaptors for the Cullin3-based ubiquitin E3 ligase. This suggests that both cell–cell signaling and targeted proteasomal degradation may be important molecular events during zygote formation and the progression of early embryogenesis.

Keywords

Wheat Zygote Proembryo Cell–cell communication Cell specification Polarity EA1 TPD1 MATH-BTB 

Supplementary material

497_2013_229_MOESM1_ESM.docx (107 kb)
Supplementary material 1 (DOCX 107 kb)
497_2013_229_MOESM2_ESM.xlsx (32 kb)
Supplementary material 2 (XLSX 33 kb)
497_2013_229_MOESM3_ESM.pdf (176 kb)
Supplementary material 3 (PDF 176 kb)
497_2013_229_MOESM4_ESM.pdf (100 kb)
Supplementary material 4 (PDF 99 kb)

References

  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(7):1927–1940PubMedCrossRefGoogle Scholar
  2. Amien S, Kliwer I, Márton ML, Debener T, Geiger D, Becker D, Dresselhaus T (2010) Defensin-like ZmES4 mediates pollen tube burst in maize via opening of the potassium channel KZM1. PLoS Biol 8:e1000388PubMedCrossRefGoogle Scholar
  3. Autran D, Baroux C, Raissig MT, Lenormand T, Wittig M, Grob S, Steimer A, Barann M, Klostermeier UC, Leblanc O, Vielle-Calzada JP, Rosenstiel P, Grimanelli D, Grossniklaus U (2011) Maternal epigenetic pathways control parental contributions to Arabidopsis early embryogenesis. Cell 145(5):707–719PubMedCrossRefGoogle Scholar
  4. Baroux C, Autran D, Gillmor CS, Grimanelli D, Grossniklaus U (2008) The maternal to zygotic transition in animals and plants. Cold Spring Harb Symp Quant Biol 73:89–100PubMedCrossRefGoogle Scholar
  5. Bayer M, Nawy T, Giglione C, Galli M, Meinnel T, Lukowitz W (2009) Paternal control of embryonic patterning in Arabidopsis thaliana. Science 323(5920):1485–1488PubMedCrossRefGoogle Scholar
  6. Canales C, Bhatt AM, Scott R, Dickinson H (2002) EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr Biol 12(20):1718–1727PubMedCrossRefGoogle Scholar
  7. Domoki M, Szűcs A, Jäger K, Bottka S, Barnabás B, Fehér A (2013) Identification of genes preferentially expressed in wheat egg cells and zygotes. Plant Cell Rep 32(3):339–348PubMedCrossRefGoogle Scholar
  8. 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 261:416–427PubMedCrossRefGoogle Scholar
  9. Fiume E, Fletcher JC (2012) Regulation of Arabidopsis embryo and endosperm development by the polypeptide signaling molecule CLE8. Plant Cell 24(3):1000–1012PubMedCrossRefGoogle Scholar
  10. Gingerich DJ, Gagne JM, Salter DW, Hellmann H, Estelle M, Ma LG, Vierstra RD (2005) Cullins 3a and 3b assemble with members of the broad complex/tramtrack/brica-brac (BTB) protein family to form essential ubiquitin-protein ligases (E3s) in Arabidopsis. J Biol Chem 280:18810–18821PubMedCrossRefGoogle Scholar
  11. Grimanelli D, Perotti E, Ramirez J, Leblanc O (2005) Timing of the maternal-to-zygotic transition during early seed development in maize. Plant Cell 17(4):1061–1072PubMedCrossRefGoogle Scholar
  12. He Y-C, He Y-Q, Qu L-H, Sun M-X, Yang H-Y (2007) Tobacco zygotic embryogenesis in vitro: the original cell wall of the zygote is essential for maintenance of cell polarity, the apical–basal axis and typical suspensor formation. Plant J 49:515–527PubMedCrossRefGoogle Scholar
  13. Jeong S, Palmer TM, Lukowitz W (2011) The RWP-RK factor GROUNDED promotes embryonic polarity by facilitating YODA MAP kinase signaling. Curr Biol 21(15):1268PubMedCrossRefGoogle Scholar
  14. Jia G, Liu X, Owen HA, Zhao D (2008) Signaling of cell fate determination by the TPD1 small protein and EMS1 receptor kinase. PNAS 105(6):2220–2225PubMedCrossRefGoogle Scholar
  15. Juranić M, Srilunchang KO, Krohn NG, Leljak-Levanić D, Sprunck S, Dresselhaus T (2012) Germline-specific MATH-BTB substrate adaptor MAB1 regulates spindle length and nuclei identity in maize. Plant Cell 24(12):4974–4991PubMedCrossRefGoogle Scholar
  16. Jürgens G (2001) Apical-basal pattern formation in Arabidopsis embryogenesis. EMBO J 20(14):3609–3616PubMedCrossRefGoogle Scholar
  17. Karimi M, Inze D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7:193–195PubMedCrossRefGoogle Scholar
  18. Katsir L, Davies KA, Bergmann DC, Laux T (2011) Peptide signaling in plant development. Curr Biol 21(9):R356–R364PubMedCrossRefGoogle Scholar
  19. Kim HJ, Oh SA, Brownfield L, Hong SH, Ryu H, Hwang I, Twell D, Nam HG (2008) Control of plant germline proliferation by SCF(FBL17) degradation of cell cycle inhibitors. Nature 455(7216):1134–1137PubMedCrossRefGoogle Scholar
  20. Kranz E, Vonwiegen P, Lorz H (1995) Early cytological events after induction of cell-division in egg cells and zygote development following in vitro fertilization with Angiosperm gametes. Plant J 8(1):9–23CrossRefGoogle Scholar
  21. Krasowska J, Olasek M, Bzowska A, Clark PL, Wielgus-Kutrowska B (2010) The comparison of aggregation and folding of enhanced green fluorescent protein (EGFP) by spectroscopic studies. Spectrosc-Int J 24(3–4):343–348CrossRefGoogle Scholar
  22. Krohn NG, Lausser A, Juranic M, Dresselhaus T (2012) Egg cell signaling by the secreted peptide ZmEAL1 controls antipodal cell fate. Dev Cell 23(1):219–225PubMedCrossRefGoogle Scholar
  23. Kumlehn J, Lörz H, Kranz E (1999) Monitoring individual development of isolated wheat zygotes: a novel approach to study early embryogenesis. Protoplasma 208(1–4):156–162CrossRefGoogle Scholar
  24. Lau S, Slane D, Herud O, Kong JX, Jurgens G (2012) Early embryogenesis in flowering plants: setting up the basic body pattern. Annu Rev Plant Biol 63:483–506PubMedCrossRefGoogle Scholar
  25. Laux T, Wurschum T, Breuninger H (2004) Genetic regulation of embryonic pattern formation. Plant Cell 16:S190–S202PubMedCrossRefGoogle Scholar
  26. Lechner E, Leonhardt N, Eisler H, Parmentier Y, Alioua M, Jacquet H, Leung J, Genschik P (2011) MATH/BTB CRL3 receptors target the homeodomain-leucine zipper ATHB6 to modulate abscisic acid signaling. Dev Cell 21(6):1116–1128PubMedCrossRefGoogle Scholar
  27. Leljak-Levanić D, Horvat T, Martinčić J, Bauer N (2012) A novel bipartite nuclear localization signal guides BPM1 protein to nucleolus suggesting its Cullin3 independent function. PLoS ONE 7:e51184PubMedCrossRefGoogle Scholar
  28. Lukowitz W, Roeder A, Parmenter D, Somerville C (2004) A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 116(1):109–119PubMedCrossRefGoogle Scholar
  29. Maerki S, Olma MH, Staubli T, Steigemann P, Gerlich DW, Quadroni M, Sumara I, Peter M (2009) The Cul3–KLHL21 E3 ubiquitin ligase targets Aurora B to midzone microtubules in anaphase and is required for cytokinesis. J Cell Biol 187(6):791–800PubMedCrossRefGoogle Scholar
  30. Maraschin SF, de Priester W, Spaink HP, Wang M (2005) Androgenic switch: an example of plant embryogenesis from the male gametophyte perspective. J Exp Bot 56(417):1711–1726PubMedCrossRefGoogle Scholar
  31. Marshall E, Costa LM, Gutierrez-Marcos J (2011) Cysteine-rich peptides (CRPs) mediate diverse aspects of cell–cell communication in plant reproduction and development. J Exp Bot 62(5):1677–1686PubMedCrossRefGoogle Scholar
  32. Márton ML, Cordts S, Broadhvest J, Dresselhaus T (2005) Micropylar pollen tube guidance by egg apparatus 1 of maize. Science 307(5709):573–576PubMedCrossRefGoogle Scholar
  33. Márton ML, Fastner A, Uebler S, Dresselhaus T (2012) Overcoming hybridization barriers by the secretion of the maize pollen tube attractant ZmEA1 from Arabidopsis ovules. Curr Biol 22(13):1194–1198PubMedCrossRefGoogle Scholar
  34. Meyer S, Scholten S (2007) Equivalent parental contribution to early plant zygotic development. Curr Biol 17:1686–1691PubMedCrossRefGoogle Scholar
  35. Muralla R, Lloyd J, Meinke D (2011) Molecular foundations of reproductive lethality in Arabidopsis thaliana. PLoS One 6(12):e28398PubMedCrossRefGoogle Scholar
  36. Nelson BK, Cai X, Nebenführ A (2007) A multi-color set of in vivo organelle markers for colocalization studies in Arabidopsis and other plants. Plant J 51:1126–1136PubMedCrossRefGoogle Scholar
  37. Ning J, Peng XB, Qu LH, Xin HP, Yan TT, Sun MX (2006) Differential gene expression in egg cells and zygotes suggests that the transcriptome is restructed before the first zygotic division in tobacco. FEBS Lett 580:1747–1752PubMedCrossRefGoogle Scholar
  38. Nodine MD, Bartel DP (2012) Maternal and paternal genomes contribute equally to the transcriptome of early plant embryos. Nature 482:94–97PubMedCrossRefGoogle Scholar
  39. Nodine MD, Bryan AC, Racolta A, Jerosky KV, Tax FE (2011) A few standing for many: embryo receptor-like kinases. Trends Plant Sci 16(4):211–217PubMedCrossRefGoogle Scholar
  40. Okuda S, Tsutsui H, Shiina K, Sprunck S, Takeuchi H, Yui R, Kasahara RD, Hamamura Y, Mizukami A, Susaki D, Kawano N, Sakakibara T, Namiki S, Itoh K, Otsuka K, Matsuzaki M, Nozaki H, Kuroiwa T, Nakano A, Kanaoka MM, Dresselhaus T, Sasaki N, Higashiyama T (2009) Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature 458:357–361PubMedCrossRefGoogle Scholar
  41. Palotta MA, Graham RD, Langridge P, Sparrow DHB, Barker SJ (2000) RFLP mapping of manganese efficiency in barley. Theor Appl Genet 101:1100–1108CrossRefGoogle Scholar
  42. Pang SZ, DeBoer DL, Wan Y, Ye G, Layton JG, Neher MK, Armstrong CL, Fry JE, Hinchee MA, Fromm ME (1996) An improved green fluorescent protein gene as a vital marker in plants. Plant Physiol 112:893–900PubMedCrossRefGoogle Scholar
  43. Peris CIL, Rademacher EH, Weijers D (2010) Chapter One-Green beginnings—pattern formation in the early plant embryo. Curr Top Dev Biol 91:1–27PubMedCrossRefGoogle Scholar
  44. Pillot M, Baroux C, Vazquez MA, Autran D, Leblanc O, Vielle-Calzada JP, Grossniklaus U, Grimanelli D (2010) Embryo and endosperm inherit distinct chromatin and transcriptional states from the female gametes in Arabidopsis. Plant Cell 22(2):307–320PubMedCrossRefGoogle Scholar
  45. Pintard L, Willi JH, Willems A, Johnson JLF, Srayko M, Kurz T, Glaser S, Mains PE, Tyers M, Bowerman B, Peter M (2003) The BTB protein MEL-26 is a substrate-specific adaptor of the CUL-3 ubiquitin-ligase. Nature 425:311–316PubMedCrossRefGoogle Scholar
  46. Pintard L, Willems A, Peter M (2004) Cullin-based ubiquitin ligases: Cul3-BTB complexes join the family. EMBO J 23(8):1681–1687PubMedCrossRefGoogle Scholar
  47. Ronceret A, Gadea-Vacas J, Guilleminot J, Lincker F, Delorme V, Lahmy S, Pelletier G, Chaboute ME, Devic M (2008) The first zygotic division in Arabidopsis requires de novo transcription of thymidylate kinase. Plant J 53(5):776–789PubMedCrossRefGoogle Scholar
  48. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  49. Schier AF (2007) The maternal-zygotic transition: death and birth of RNAs. Science 316(5823):406–407PubMedCrossRefGoogle Scholar
  50. Scholten S, Lörz H, Kranz E (2002) Paternal mRNA and protein synthesis coincides with male chromatin decondensation in maize zygotes. Plant J 32:221–231PubMedCrossRefGoogle Scholar
  51. Sivaramakrishna D (1977) Size relationships of apical call and basal cell in two-celled embryos in angiosperms. Can J Bot 56:1434–1438CrossRefGoogle Scholar
  52. 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 41:660–672PubMedCrossRefGoogle Scholar
  53. Sprunck S, Rademacher S, Vogler F, Gheyselinck J, Grossniklaus U, Dresselhaus T (2012) Egg cell–secreted EC1 triggers sperm cell activation during double fertilization. Science 338:1093–1097PubMedCrossRefGoogle Scholar
  54. Stitzel M, Seydoux G (2007) Regulation of the oocyte-to-zygote transition. Science 316(5823):407–408PubMedCrossRefGoogle Scholar
  55. Stogios PJ, Downs GS, Jauhal JJS, Nandra SK, Prive GG (2005) Sequence and structural analysis of BTB domain proteins. Genome Biol 6:R82PubMedCrossRefGoogle Scholar
  56. Sumara I, Maerki S, Peter M (2008) E3 ubiquitin ligases and mitosis: embracing the complexity. Trends Cell Biol 18(2):84–94PubMedCrossRefGoogle Scholar
  57. Sun MX, Zhao J, Xin HP, Qu LH, Ning J, Peng XB, Yan TT, Ma LG, Li SS (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(1):131–145PubMedCrossRefGoogle Scholar
  58. Tadros W, Lipshitz HD (2009) The maternal-to-zygotic transition: a play in two acts. Development 136:3033–3042PubMedCrossRefGoogle Scholar
  59. Takeuchi H, Higashiyama T (2012) A species-specific cluster of defensin-like genes encodes diffusible pollen tube attractants in Arabidopsis. PLoS Biol 10(12):e1001449PubMedCrossRefGoogle Scholar
  60. Tian Q, Olsen L, Sun B, Lid SE, Brown RC, Lemmon BE, Fosnes K, Gruis DF, Opsahl-Sorteberg HG, Otegui MS, Olsen OA (2007) Subcellular localization and functional domain studies of DEFECTIVE KERNEL1 in maize and Arabidopsis suggest a model for aleurone cell fate specification involving CRINKLY4 and SUPERNUMERARY ALEURONE LAYER1. Plant Cell 19(10):3127–3145PubMedCrossRefGoogle Scholar
  61. Van Norman JM, Breakfield NW, Benfey PN (2011) Intercellular communication during plant development. Plant Cell 23(3):855–864PubMedCrossRefGoogle Scholar
  62. Vernoud V, Hajduch M, Khaled A-S, Depège N, Rogowsky PM (2005) Maize embryogenesis. Maydica 50:469–483Google Scholar
  63. Vielle-Calzada JP, Baskar R, Grossniklaus U (2000) Delayed activation of the paternal genome during seed development. Nature 404(6773):91–94PubMedCrossRefGoogle Scholar
  64. Waki T, Hiki T, Watanabe R, Hashimoto T, Nakajima K (2011) The Arabidopsis RWP-RK protein RKD4 triggers gene expression and pattern formation in early embryogenesis. Curr Biol 21(15):1277–1281PubMedCrossRefGoogle Scholar
  65. Wang MM, Zhang Y, Wang J, Wu XL, Guo XQ (2007) A novel MAP kinase gene in cotton (Gossypium hirsutum L.), GhMAPK, is involved in response to diverse environmental stresses. J Biochem Mol Biol 40(3):325–332PubMedCrossRefGoogle Scholar
  66. Wang CJR, Nan G-L, Kelliher T, Timofejeva L, Vernoud V, Golubovskaya IN, Harper L, Egger R, Walbot V, Cande WZ (2012) Maize multiple archesporial cells 1 (mac1), an ortholog of rice TDL1A, modulates cell proliferation and identity in early anther development. Development 139:2594–2603PubMedCrossRefGoogle Scholar
  67. Weber H, Bernhardt A, Dieterle M, Han P, Hano P, Mutlu A, Estelle M, Genschik P, Hellmann H (2005) Arabidopsis AtCUL3a and AtCUL3b form complexes with members of the BTB/POZ-MATH protein family. Plant Physiol 13:83–93CrossRefGoogle Scholar
  68. Weijers D, Geldner N, Offringa R, Jurgens G (2001) Seed development—early paternal gene activity in Arabidopsis. Nature 414(6865):709–710PubMedCrossRefGoogle Scholar
  69. Wendrich JR, Weijers D (2013) The Arabidopsis embryo as a miniature morphogenesis model. New Phytol 199(1):14–25PubMedCrossRefGoogle Scholar
  70. Willemsen V, Scheres B (2004) Mechanisms of pattern formation in plant embryogenesis. Annu Rev Genet 38:587–614PubMedCrossRefGoogle Scholar
  71. Xin HP, Zhao J, Sun MX (2012) The maternal-to-zygotic transition in higher plants. J Integr Plant Biol 54(9):610–615PubMedCrossRefGoogle Scholar
  72. 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(5):743–756PubMedCrossRefGoogle Scholar
  73. Yang SL, Xiea LF, Mao HZ, Puah CS, Yang WC, Jiang LX, Sundaresan V, Ye D (2003) TAPETUM DETERMINANT1 is required for cell specialization in the Arabidopsis anther. Plant Cell 15(12):2792–2804PubMedCrossRefGoogle Scholar
  74. Yang SL, Jiang L, Puah CS, Xie L-F, Zhang X-Q, Chen L-Q, Yang W-C, Ye D et al (2005) Overexpression of TAPETUM DETERMINANT1 alters the cell fates in the Arabidopsis carpel and tapetum via genetic interaction with EXCESS MICROSPOROCYTES1/EXTRA SPOROGENOUS CELLS. Plant Physiol 139:186–191PubMedCrossRefGoogle Scholar
  75. Zhang ZJ, Laux T (2011) The asymmetric division of the Arabidopsis zygote: from cell polarity to an embryo axis. Sex Plant Reprod 24:161–169PubMedCrossRefGoogle Scholar
  76. Zhao DZ, Wang GF, Speal B, Ma H (2002) The EXCESS MICROSPOROCYTES1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Gene Dev 16(15):2021–2031PubMedCrossRefGoogle Scholar
  77. Zhao J, Xin H, Qu L, Ning J, Peng X, Yan T, Ma L, Li S, Sun M-X (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 65:131–145PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Dunja Leljak-Levanić
    • 1
  • Martina Juranić
    • 1
  • Stefanie Sprunck
    • 2
  1. 1.Department of Molecular Biology, Faculty of Science and MathematicsUniversity of ZagrebZagrebCroatia
  2. 2.Cell Biology and Plant Biochemistry, Biochemie-Zentrum RegensburgUniversity of RegensburgRegensburgGermany

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