Cross-talk between sporophyte and gametophyte generations is promoted by CHD3 chromatin remodelers in Arabidopsis thaliana

Genetics

Volumn 203, Issue 2, 2016, Pages 817-829

  Carter, Benjamin ^a   Henderson, James T ^a   Svedin, Elisabeth ^a   Fiers, Martijn ^b   McCarthy, Kyle ^a   Smith, Amanda ^a   Guo, Changhua ^b   Bishop, Brett ^a   Zhang, Heng ^a   Riksen, Tjitske ^b   Shockley, Allison ^a   Dilkes, Brian P ^a   Boutilier, Kim ^b   Ogas, Joe ^a  

^a PURDUE UNIVERSITY   (United States)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Ovule; PICKLE; PKR2; Pollen tube; Seed size

Indexed keywords

PICKLE PROTEIN; PICKLE RELATED 2 PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; ARABIDOPSIS PROTEIN; DNA HELICASE; PKL PROTEIN, ARABIDOPSIS;

ARABIDOPSIS THALIANA; ARTICLE; CHROMATIN; DEVELOPMENTAL DISORDER; EMBRYO DEVELOPMENT; ENDOSPERM; FEMALE; FEMALE GAMETOPHYTE; GENETIC ANALYSIS; INTEGUMENT; MALE; NONHUMAN; OVULE DEVELOPMENT; PHENOTYPE; PLANT DEVELOPMENT; PLANT GENETICS; PLANT REPRODUCTION; POLLEN TUBE; POLLEN TUBE GROWTH; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; SEED SIZE; SIGNAL TRANSDUCTION; SPOROPHYTE; ARABIDOPSIS; FLOWER; GENETIC EPIGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DNA HELICASES; ENDOSPERM; EPIGENESIS, GENETIC; GERM CELLS, PLANT;

EID: 84976896639     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.115.180141     Document Type: Article

References (73)

1. Aichinger, E., C. B. Villar, S. Farrona, J. C. Reyes, L. Hennig et al., 2009 CHD3 proteins and polycomb group proteins antagonistically determine cell identity in Arabidopsis. PLoS Genet. 5: e1000605.
2. Aichinger, E., C. B. Villar, R. Di Mambro, S. Sabatini, and C. Kohler, 2011 The CHD3 chromatin remodeler PICKLE and polycomb group proteins antagonistically regulate meristem activity in the Arabidopsis root. Plant Cell 23: 1047–1060.
3. Beale, K. M., A. R. Leydon, and M. A. Johnson, 2012 Gamete fusion is required to block multiple pollen tubes from entering an Arabidopsis ovule. Curr. Biol. 22: 1090–1094.
4. Bencivenga, S., L. Colombo, and S. Masiero, 2011 Cross talk between the sporophyte and the megagametophyte during ovule development. Sex. Plant Reprod. 24: 113–121.
5. Bouyer, D., F. Roudier, M. Heese, E. D. Andersen, D. Gey et al., 2011 Polycomb repressive complex 2 controls the embryo-to-seedling phase transition. PLoS Genet. 7: e1002014.
6. Cheng, C. Y., and J. J. Kieber, 2013 The role of cytokinin in ovule development in Arabidopsis. Plant Signal. Behav. 8: e23393.
7. Chevalier, E., A. Loubert-Hudon, E. L. Zimmerman, and D. P. Matton, 2011 Cell-cell communication and signalling pathways within the ovule: from its inception to fertilization. New Phytol. 192: 13–28.
8. Christensen, C. A., E. J. King, J. R. Jordan, and G. N. Drews, 1997 Megagametogenesis in Arabidopsis wild type and the Gf mutant. Sex. Plant Reprod. 10: 49–64.
9. Clark, K. A., and P. J. Krysan, 2010 Chromosomal translocations are a common phenomenon in Arabidopsis thaliana T-DNA insertion lines. Plant J. 64: 990–1001.
10. Crawford, B. C., and M. F. Yanofsky, 2008 The formation and function of the female reproductive tract in flowering plants. Curr. Biol. 18: R972–R978.
11. Crawford, B. C., and M. F. Yanofsky, 2011 HALF FILLED promotes reproductive tract development and fertilization efficiency in Arabidopsis thaliana. Development 138: 2999–3009.
12. Crawford, B. C., G. Ditta, and M. F. Yanofsky, 2007 The NTT gene is required for transmitting-tract development in carpels of Arabidopsis thaliana. Curr. Biol. 17: 1101–1108.
13. Dean Rider, Jr., S., J. T. Henderson, R. E. Jerome, H. J. Edenberg, J. Romero-Severson et al., 2003 Coordinate repression of regulators of embryonic identity by PICKLE during germination in Arabidopsis. Plant J. 35: 33–43.
14. Dilkes, B. P. and L. Comai, 2004 A differential dosage hypothesis for parental effects in seed development. Plant Cell 16: 3174–3180.
15. Dilkes, B. P., M. Spielman, R. Weizbauer, B. Watson, D. Burkart- Waco et al., 2008 The maternally expressed WRKY transcription factor TTG2 controls lethality in interploidy crosses of Arabidopsis. PLoS Biol. 6: 2707–2720.
16. Dresselhaus, T., and N. Franklin-Tong, 2013 Male-female cross-talk during pollen germination, tube growth and guidance, and double fertilization. Mol. Plant 6: 1018–1036.
17. Ebel, C., L. Mariconti, and W. Gruissem, 2004 Plant retinoblastoma homologues control nuclear proliferation in the female gametophyte. Nature 429: 776–780.
18. Elwell, A. L., D. S. Gronwall, N. D. Miller, E. P. Spalding, and T. L. Brooks, 2011 Separating parental environment from seed size effects on next generation growth and development in Arabidopsis. Plant Cell Environ. 34: 291–301.
19. Erilova, A., L. Brownfield, V. Exner, M. Rosa, D. Twell et al., 2009 Imprinting of the polycomb group gene MEDEA serves as a ploidy sensor in Arabidopsis. PLoS Genet. 5: e1000663.
20. Eshed, Y., S. F. Baum, and J. L. Bowman, 1999 Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell 99: 199–209.
21. Eshed, Y., S. F. Baum, J. V. Perea, and J. L. Bowman, 2001 Establishment of polarity in lateral organs of plants. Curr. Biol. 11: 1251–1260.
22. Gehring, M., 2013 Genomic imprinting: insights from plants. Annu. Rev. Genet. 47: 187–208.
23. Gonzalez-Reig, S., J. J. Ripoll, A. Vera, M. F. Yanofsky, and A. Martinez-Laborda, 2012 Antagonistic gene activities determine the formation of pattern elements along the mediolateral axis of the Arabidopsis fruit. PLoS Genet. 8: e1003020.
24. Gremski, K., G. Ditta, and M. F. Yanofsky, 2007 The HECATE genes regulate female reproductive tract development in Arabidopsis thaliana. Development 134: 3593–3601.
25. Grossniklaus, U., J. P. Vielle-Calzada, M. A. Hoeppner, and W. B. Gagliano, 1998 Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science 280: 446–450.
26. Henderson, J. T., H. C. Li, S. D. Rider, A. P. Mordhorst, J. Romero- Severson et al., 2004 PICKLE acts throughout the plant to repress expression of embryonic traits and may play a role in gibberellin-dependent responses. Plant Physiol. 134: 995–1005.
27. Herridge, R. P., R. C. Day, S. Baldwin, and R. C. Macknight, 2011 Rapid analysis of seed size in Arabidopsis for mutant and QTL discovery. Plant Methods 7: 3.
28. Hsu, S. C., M. F. Belmonte, J. J. Harada, and K. Inoue, 2010 Indispensable roles of plastids in Arabidopsis thaliana embryogenesis. Curr. Genomics 11: 338–349.
29. Jiang, H., and C. Kohler, 2012 Evolution, function, and regulation of genomic imprinting in plant seed development. J. Exp. Bot. 63: 4713–4722.
30. Jiang, L., S. L. Yang, L. F. Xie, C. S. Puah, X. Q. Zhang et al., 2005 VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell 17: 584–596.
31. Jing, Y., D. Zhang, X. Wang, W. Tang, W. Wang et al., 2013 Arabidopsis chromatin remodeling factor PICKLE interacts with transcription factor HY5 to regulate hypocotyl cell elongation. Plant Cell 25: 242–256.
32. Johnston, A. J., P. Meier, J. Gheyselinck, S. E. Wuest, M. Federer et al., 2007 Genetic subtraction profiling identifies genes essential for Arabidopsis reproduction and reveals interaction between the female gametophyte and the maternal sporophyte. Genome Biol. 8: R204.
33. Josefsson, C., B. Dilkes, and L. Comai, 2006 Parent-dependent loss of gene silencing during interspecies hybridization. Curr. Biol. 16: 1322–1328.
34. Karimi, M., D. Inze, and A. Depicker, 2002 GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7: 193–195.
35. Kasahara, R. D., D. Maruyama, Y. Hamamura, T. Sakakibara, D. Twell et al., 2012 Fertilization recovery after defective sperm cell release in Arabidopsis. Curr. Biol. 22: 1084–1089.
36. Katz, A., M. Oliva, A. Mosquna, O. Hakim, and N. Ohad, 2004 FIE and CURLY LEAF polycomb proteins interact in the regulation of homeobox gene expression during sporophyte development. Plant J. 37: 707–719.
37. Khan, N., R. H. Kazmi, L. A. Willems, A. W. van Heusden, W. Ligterink et al., 2012 Exploring the natural variation for seedling traits and their link with seed dimensions in tomato. PLoS One 7: e43991.
38. Kohler, C., L. Hennig, R. Bouveret, J. Gheyselinck, U. Grossniklaus et al., 2003a Arabidopsis MSI1 is a component of the MEA/FIE Polycomb group complex and required for seed development. EMBO J. 22: 4804–4814.
39. Kohler, C., L. Hennig, C. Spillane, S. Pien, W. Gruissem et al., 2003b The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1. Genes Dev. 17: 1540–1553.
40. Kradolfer, D., L. Hennig, and C. Kohler, 2013 Increased maternal genome dosage bypasses the requirement of the FIS polycomb repressive complex 2 in Arabidopsis seed development. PLoS Genet. 9: e1003163.
41. Kunieda, T., N. Mitsuda, M. Ohme-Takagi, S. Takeda, M. Aida et al., 2008 NAC family proteins NARS1/NAC2 and NARS2/NAM in the outer integument regulate embryogenesis in Arabidopsis. Plant Cell 20: 2631–2642.
42. Lafos, M., P. Kroll, M. L. Hohenstatt, F. L. Thorpe, O. Clarenz et al., 2011 Dynamic regulation of H3K27 trimethylation during arabidopsis differentiation. PLoS Genet. 7: e1002040.
43. Le, B. H., C. Cheng, A. Q. Bui, J. A. Wagmaister, K. F. Henry et al., 2010 Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc. Natl. Acad. Sci. USA 107: 8063–8070.
44. Lee, E. C., D. Yu, J. Martinez de Velasco, L. Tessarollo, D. A. Swing et al., 2001 A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73: 56–65.
45. Leshem, Y., C. Johnson, S. E. Wuest, X. Song, Q. A. Ngo et al., 2012 Molecular characterization of the glauce mutant: a central cell-specific function is required for double fertilization in Arabidopsis. Plant Cell 24: 3264–3277.
46. Leydon, A. R., A. Chaibang, and M. A. Johnson, 2014 Interactions between pollen tube and pistil control pollen tube identity and sperm release in the Arabidopsis female gametophyte. Biochem. Soc. Trans. 42: 340–345.
47. Li, H. C., K. Chuang, J. T. Henderson, S. D. Rider Jr., Y. Bai et al., 2005 PICKLE acts during germination to repress expression of embryonic traits. Plant J. 44: 1010–1022.
48. Li, J., X. Nie, J. L. Tan, and F. Berger, 2013 Integration of epigenetic and genetic controls of seed size by cytokinin in Arabidopsis. Proc. Natl. Acad. Sci. USA 110: 15479–15484.
49. Luo, M., P. Bilodeau, E. S. Dennis, W. J. Peacock, and A. Chaudhury, 2000 Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. Proc. Natl. Acad. Sci. USA 97: 10637–10642.
50. Ma, H., and V. Sundaresan, 2010 Development of flowering plant gametophytes. Curr. Top. Dev. Biol. 91: 379–412.
51. Maruyama, D., Y. Hamamura, H. Takeuchi, D. Susaki, M. Nishimaki et al., 2013 Independent control by each female gamete prevents the attraction of multiple pollen tubes. Dev. Cell 25: 317–323.
52. Ngo, Q. A., H. Vogler, D. S. Lituiev, A. Nestorova, and U. Grossniklaus, 2014 A calcium dialog mediated by the FERONIA signal transduction pathway controls plant sperm delivery. Dev. Cell 29: 491– 500.
53. Niklas, K. J., and U. Kutschera, 2010 The evolution of the land plant life cycle. New Phytol. 185: 27–41.
54. Ogas, J., J. C. Cheng, Z. R. Sung, and C. Somerville, 1997 Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle mutant. Science 277: 91–94.
55. Ogas, J., S. Kaufmann, J. Henderson, and C. Somerville, 1999 PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc. Natl. Acad. Sci. USA 96: 13839–13844.
56. Ohad, N., L. Margossian, Y. C. Hsu, C. Williams, P. Repetti et al., 1996 A mutation that allows endosperm development without fertilization. Proc. Natl. Acad. Sci. USA 93: 5319–5324.
57. Parcy, F., C. Valon, M. Raynal, P. Gaubier-Comella, M. Delseny et al., 1994 Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6: 1567–1582.
58. Park, S. O., Z. Zheng, D. G. Oppenheimer, and B. A. Hauser, 2005 The PRETTY FEW SEEDS2 gene encodes an Arabidopsis homeodomain protein that regulates ovule development. Development 132: 841–849.
59. Perruc, E., N. Kinoshita, and L. Lopez-Molina, 2007 The role of chromatin-remodeling factor PKL in balancing osmotic stress responses during Arabidopsis seed germination. Plant J. 52: 927–936.
60. Peterson, R., J. P. Slovin, and C. Chen, 2010 A simplified method for differential staining of aborted and non-aborted pollen grains. International Journal of Plant Biology 1: e13.
61. Schmid, M., T. S. Davison, S. R. Henz, U. J. Pape, M. Demar et al., 2005 A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37: 501–506.
62. Scott, R., M. Spielman, J. Bailey, and H. G. Dickinson, 1998 Parent-of-origin effects on seed development in Arabidopsis thaliana. Development 125: 3329–3341.
63. Shi, D. Q., and W. C. Yang, 2011 Ovule development in Arabidopsis: progress and challenge. Curr. Opin. Plant Biol. 14: 74–80.
64. Shirzadi, R., E. D. Andersen, K. N. Bjerkan, B. M. Gloeckle, M. Heese et al., 2011 Genome-wide transcript profiling of endosperm without paternal contribution identifies parent-of-origin-dependent regulation of AGAMOUS-LIKE36. PLoS Genet. 7: e1001303.
65. Soriano, M., H. Li, C. Jacquard, G. C. Angenent, J. Krochko et al., 2014 Plasticity in cell division patterns and auxin transport dependency during in vitro embryogenesis in Brassica napus. Plant Cell 26: 2568–2581.
66. Vielle-Calzada, J. P., E. Hernandez-Lagana, D. Rodriguez-Leal, I. Rodriguez-Arevalo, G. Leon-Martinez et al., 2012 Reproductive versatility and the epigenetic control of female gametogenesis. Cold Spring Harb. Symp. Quant. Biol. 77: 17–21.
67. Xiao, W., R. C. Brown, B. E. Lemmon, J. J. Harada, R. B. Goldberg et al., 2006 Regulation of seed size by hypomethylation of maternal and paternal genomes. Plant Physiol. 142: 1160–1168.
68. Xu, J., H. Y. Zhang, C. H. Xie, H. W. Xue, P. Dijkhuis et al., 2005 EMBRYONIC FACTOR 1 encodes an AMP deaminase and is essential for the zygote to embryo transition in Arabidopsis. Plant J. 42: 743–756.
69. Xu, M., T. Hu, M. R. Smith, and R. S. Poethig, 2016 Epigenetic regulation of vegetative phase change in Arabidopsis. Plant Cell 28: 28–41.
70. Zhang, D., Y. Jing, Z. Jiang, and R. Lin, 2014 The chromatin-remodeling factor PICKLE integrates brassinosteroid and gibberellin signaling during skotomorphogenic growth in Arabidopsis. Plant Cell 26: 2472–2485.
71. Zhang, H., S. D. Rider Jr., J. T. Henderson, M. Fountain, K. Chuang et al., 2008 The CHD3 remodeler PICKLE promotes trimethylation of histone H3 lysine 27. J. Biol. Chem. 283: 22637–22648.
72. Zhang, H., B. Bishop, W. Ringenberg, W. M. Muir, and J. Ogas, 2012 The CHD3 remodeler PICKLE associates with genes enriched for trimethylation of histone H3 lysine 27. Plant Physiol. 159: 418–432.
73. Zhang, H., A. Chaudhury, and X. Wu, 2013 Imprinting in plants and its underlying mechanisms. J. Genet. Genomics 40: 239–247.