Skip to main content
Genetics logoLink to Genetics
. 2002 Dec;162(4):1911–1925. doi: 10.1093/genetics/162.4.1911

Embryo and endosperm development is disrupted in the female gametophytic capulet mutants of Arabidopsis.

Paul E Grini 1, Gerd Jürgens 1, Martin Hülskamp 1
PMCID: PMC1462375  PMID: 12524359

Abstract

The female gametophyte of higher plants gives rise, by double fertilization, to the diploid embryo and triploid endosperm, which develop in concert to produce the mature seed. What roles gametophytic maternal factors play in this process is not clear. The female-gametophytic effects on embryo and endosperm development in the Arabidopsis mea, fis, and fie mutants appear to be due to gametic imprinting that can be suppressed by METHYL TRANSFERASE1 antisense (MET1 a/s) transgene expression or by mutation of the DECREASE IN DNA METHYLATION1 (DDM1) gene. Here we describe two novel gametophytic maternal-effect mutants, capulet1 (cap1) and capulet2 (cap2). In the cap1 mutant, both embryo and endosperm development are arrested at early stages. In the cap2 mutant, endosperm development is blocked at very early stages, whereas embryos can develop to the early heart stage. The cap mutant phenotypes were not rescued by wild-type pollen nor by pollen from tetraploid plants. Furthermore, removal of silencing barriers from the paternal genome by MET1 a/s transgene expression or by the ddm1 mutation also failed to restore seed development in the cap mutants. Neither cap1 nor cap2 displayed autonomous seed development, in contrast to mea, fis, and fie mutants. In addition, cap2 was epistatic to fis1 in both autonomous endosperm and sexual development. Finally, both cap1 and cap2 mutant endosperms, like wild-type endosperms, expressed the paternally inactive endosperm-specific FIS2 promoter GUS fusion transgene only when the transgene was introduced via the embryo sac, indicating that imprinting was not affected. Our results suggest that the CAP genes represent novel maternal functions supplied by the female gametophyte that are required for embryo and endosperm development.

Full Text

The Full Text of this article is available as a PDF (395.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams S., Vinkenoog R., Spielman M., Dickinson H. G., Scott R. J. Parent-of-origin effects on seed development in Arabidopsis thaliana require DNA methylation. Development. 2000 Jun;127(11):2493–2502. doi: 10.1242/dev.127.11.2493. [DOI] [PubMed] [Google Scholar]
  2. Amedeo P., Habu Y., Afsar K., Mittelsten Scheid O., Paszkowski J. Disruption of the plant gene MOM releases transcriptional silencing of methylated genes. Nature. 2000 May 11;405(6783):203–206. doi: 10.1038/35012108. [DOI] [PubMed] [Google Scholar]
  3. Bell C. J., Ecker J. R. Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics. 1994 Jan 1;19(1):137–144. doi: 10.1006/geno.1994.1023. [DOI] [PubMed] [Google Scholar]
  4. Berger F. Endosperm development. Curr Opin Plant Biol. 1999 Feb;2(1):28–32. doi: 10.1016/s1369-5266(99)80006-5. [DOI] [PubMed] [Google Scholar]
  5. Birchler J. A. Dosage analysis of maize endosperm development. Annu Rev Genet. 1993;27:181–204. doi: 10.1146/annurev.ge.27.120193.001145. [DOI] [PubMed] [Google Scholar]
  6. Boisnard-Lorig C., Colon-Carmona A., Bauch M., Hodge S., Doerner P., Bancharel E., Dumas C., Haseloff J., Berger F. Dynamic analyses of the expression of the HISTONE::YFP fusion protein in arabidopsis show that syncytial endosperm is divided in mitotic domains. Plant Cell. 2001 Mar;13(3):495–509. doi: 10.1105/tpc.13.3.495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bonhomme S., Horlow C., Vezon D., de Laissardière S., Guyon A., Férault M., Marchand M., Bechtold N., Pelletier G. T-DNA mediated disruption of essential gametophytic genes in Arabidopsis is unexpectedly rare and cannot be inferred from segregation distortion alone. Mol Gen Genet. 1998 Dec;260(5):444–452. doi: 10.1007/s004380050915. [DOI] [PubMed] [Google Scholar]
  8. Braselton J. P., Wilkinson M. J., Clulow S. A. Feulgen staining of intact plant tissues for confocal microscopy. Biotech Histochem. 1996 Mar;71(2):84–87. doi: 10.3109/10520299609117139. [DOI] [PubMed] [Google Scholar]
  9. Chaudhury A. M., Ming L., Miller C., Craig S., Dennis E. S., Peacock W. J. Fertilization-independent seed development in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1997 Apr 15;94(8):4223–4228. doi: 10.1073/pnas.94.8.4223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Choi Yeonhee, Gehring Mary, Johnson Lianna, Hannon Mike, Harada John J., Goldberg Robert B., Jacobsen Steven E., Fischer Robert L. DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in arabidopsis. Cell. 2002 Jul 12;110(1):33–42. doi: 10.1016/s0092-8674(02)00807-3. [DOI] [PubMed] [Google Scholar]
  11. Christensen C. A., Subramanian S., Drews G. N. Identification of gametophytic mutations affecting female gametophyte development in Arabidopsis. Dev Biol. 1998 Oct 1;202(1):136–151. doi: 10.1006/dbio.1998.8980. [DOI] [PubMed] [Google Scholar]
  12. Colombo L., Franken J., Van der Krol A. R., Wittich P. E., Dons H. J., Angenent G. C. Downregulation of ovule-specific MADS box genes from petunia results in maternally controlled defects in seed development. Plant Cell. 1997 May;9(5):703–715. doi: 10.1105/tpc.9.5.703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cordts S., Bantin J., Wittich P. E., Kranz E., Lörz H., Dresselhaus T. ZmES genes encode peptides with structural homology to defensins and are specifically expressed in the female gametophyte of maize. Plant J. 2001 Jan;25(1):103–114. doi: 10.1046/j.0960-7412.2000.00944.x. [DOI] [PubMed] [Google Scholar]
  14. Drews G. N., Lee D., Christensen C. A. Genetic analysis of female gametophyte development and function. Plant Cell. 1998 Jan;10(1):5–17. doi: 10.1105/tpc.10.1.5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Feldmann K. A., Coury D. A., Christianson M. L. Exceptional segregation of a selectable marker (KanR) in Arabidopsis identifies genes important for gametophytic growth and development. Genetics. 1997 Nov;147(3):1411–1422. doi: 10.1093/genetics/147.3.1411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Finnegan E. J., Dennis E. S. Isolation and identification by sequence homology of a putative cytosine methyltransferase from Arabidopsis thaliana. Nucleic Acids Res. 1993 May 25;21(10):2383–2388. doi: 10.1093/nar/21.10.2383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Finnegan E. J., Peacock W. J., Dennis E. S. Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8449–8454. doi: 10.1073/pnas.93.16.8449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Folkers U., Kirik V., Schöbinger U., Falk S., Krishnakumar S., Pollock M. A., Oppenheimer D. G., Day I., Reddy A. S. M., Jürgens G. The cell morphogenesis gene ANGUSTIFOLIA encodes a CtBP/BARS-like protein and is involved in the control of the microtubule cytoskeleton. EMBO J. 2002 Mar 15;21(6):1280–1288. doi: 10.1093/emboj/21.6.1280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Genger R. K., Kovac K. A., Dennis E. S., Peacock W. J., Finnegan E. J. Multiple DNA methyltransferase genes in Arabidopsis thaliana. Plant Mol Biol. 1999 Sep;41(2):269–278. doi: 10.1023/a:1006347010369. [DOI] [PubMed] [Google Scholar]
  20. Goldberg R. B., de Paiva G., Yadegari R. Plant embryogenesis: zygote to seed. Science. 1994 Oct 28;266(5185):605–614. doi: 10.1126/science.266.5185.605. [DOI] [PubMed] [Google Scholar]
  21. Grini P. E., Schnittger A., Schwarz H., Zimmermann I., Schwab B., Jürgens G., Hülskamp M. Isolation of ethyl methanesulfonate-induced gametophytic mutants in Arabidopsis thaliana by a segregation distortion assay using the multimarker chromosome 1. Genetics. 1999 Feb;151(2):849–863. doi: 10.1093/genetics/151.2.849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Grossniklaus U., Schneitz K. The molecular and genetic basis of ovule and megagametophyte development. Semin Cell Dev Biol. 1998 Apr;9(2):227–238. doi: 10.1006/scdb.1997.0214. [DOI] [PubMed] [Google Scholar]
  23. Grossniklaus U., Vielle-Calzada J. P., Hoeppner M. A., Gagliano W. B. Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science. 1998 Apr 17;280(5362):446–450. doi: 10.1126/science.280.5362.446. [DOI] [PubMed] [Google Scholar]
  24. Hong S. K., Kitano H., Satoh H., Nagato Y. How is embryo size genetically regulated in rice? Development. 1996 Jul;122(7):2051–2058. doi: 10.1242/dev.122.7.2051. [DOI] [PubMed] [Google Scholar]
  25. Howden R., Park S. K., Moore J. M., Orme J., Grossniklaus U., Twell D. Selection of T-DNA-tagged male and female gametophytic mutants by segregation distortion in Arabidopsis. Genetics. 1998 Jun;149(2):621–631. doi: 10.1093/genetics/149.2.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hülskamp M., Kopczak S. D., Horejsi T. F., Kihl B. K., Pruitt R. E. Identification of genes required for pollen-stigma recognition in Arabidopsis thaliana. Plant J. 1995 Nov;8(5):703–714. doi: 10.1046/j.1365-313x.1995.08050703.x. [DOI] [PubMed] [Google Scholar]
  27. Jeddeloh J. A., Stokes T. L., Richards E. J. Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat Genet. 1999 May;22(1):94–97. doi: 10.1038/8803. [DOI] [PubMed] [Google Scholar]
  28. Kakutani T., Jeddeloh J. A., Flowers S. K., Munakata K., Richards E. J. Developmental abnormalities and epimutations associated with DNA hypomethylation mutations. Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12406–12411. doi: 10.1073/pnas.93.22.12406. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kakutani T., Jeddeloh J. A., Richards E. J. Characterization of an Arabidopsis thaliana DNA hypomethylation mutant. Nucleic Acids Res. 1995 Jan 11;23(1):130–137. doi: 10.1093/nar/23.1.130. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kinoshita T., Yadegari R., Harada J. J., Goldberg R. B., Fischer R. L. Imprinting of the MEDEA polycomb gene in the Arabidopsis endosperm. Plant Cell. 1999 Oct;11(10):1945–1952. doi: 10.1105/tpc.11.10.1945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Kiyosue T., Ohad N., Yadegari R., Hannon M., Dinneny J., Wells D., Katz A., Margossian L., Harada J. J., Goldberg R. B. Control of fertilization-independent endosperm development by the MEDEA polycomb gene in Arabidopsis. Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):4186–4191. doi: 10.1073/pnas.96.7.4186. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Konieczny A., Ausubel F. M. A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J. 1993 Aug;4(2):403–410. doi: 10.1046/j.1365-313x.1993.04020403.x. [DOI] [PubMed] [Google Scholar]
  33. Laux T., Jurgens G. Embryogenesis: A New Start in Life. Plant Cell. 1997 Jul;9(7):989–1000. doi: 10.1105/tpc.9.7.989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Lin B. Y. Ploidy barrier to endosperm development in maize. Genetics. 1984 May;107(1):103–115. doi: 10.1093/genetics/107.1.103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Lukowitz W., Mayer U., Jürgens G. Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell. 1996 Jan 12;84(1):61–71. doi: 10.1016/s0092-8674(00)80993-9. [DOI] [PubMed] [Google Scholar]
  36. Lund G., Ciceri P., Viotti A. Maternal-specific demethylation and expression of specific alleles of zein genes in the endosperm of Zea mays L. Plant J. 1995 Oct;8(4):571–581. doi: 10.1046/j.1365-313x.1995.8040571.x. [DOI] [PubMed] [Google Scholar]
  37. Luo M., Bilodeau P., Koltunow A., Dennis E. S., Peacock W. J., Chaudhury A. M. Genes controlling fertilization-independent seed development in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1999 Jan 5;96(1):296–301. doi: 10.1073/pnas.96.1.296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Mayer U., Herzog U., Berger F., Inzé D., Jürgens G. Mutations in the pilz group genes disrupt the microtubule cytoskeleton and uncouple cell cycle progression from cell division in Arabidopsis embryo and endosperm. Eur J Cell Biol. 1999 Feb;78(2):100–108. doi: 10.1016/S0171-9335(99)80011-9. [DOI] [PubMed] [Google Scholar]
  39. Mittelsten Scheid O., Afsar K., Paszkowski J. Release of epigenetic gene silencing by trans-acting mutations in Arabidopsis. Proc Natl Acad Sci U S A. 1998 Jan 20;95(2):632–637. doi: 10.1073/pnas.95.2.632. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Nadeau J. A., Zhang X. S., Li J., O'Neill S. D. Ovule development: identification of stage-specific and tissue-specific cDNAs. Plant Cell. 1996 Feb;8(2):213–239. doi: 10.1105/tpc.8.2.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Ohad N., Margossian L., Hsu Y. C., Williams C., Repetti P., Fischer R. L. A mutation that allows endosperm development without fertilization. Proc Natl Acad Sci U S A. 1996 May 28;93(11):5319–5324. doi: 10.1073/pnas.93.11.5319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Perry S. E., Nichols K. W., Fernandez D. E. The MADS domain protein AGL15 localizes to the nucleus during early stages of seed development. Plant Cell. 1996 Nov;8(11):1977–1989. doi: 10.1105/tpc.8.11.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Ray A., Lang J. D., Golden T., Ray S. SHORT INTEGUMENT (SIN1), a gene required for ovule development in Arabidopsis, also controls flowering time. Development. 1996 Sep;122(9):2631–2638. doi: 10.1242/dev.122.9.2631. [DOI] [PubMed] [Google Scholar]
  44. Ray S. M., Park S. S., Ray A. Pollen tube guidance by the female gametophyte. Development. 1997 Jun;124(12):2489–2498. doi: 10.1242/dev.124.12.2489. [DOI] [PubMed] [Google Scholar]
  45. Ray S., Golden T., Ray A. Maternal effects of the short integument mutation on embryo development in Arabidopsis. Dev Biol. 1996 Nov 25;180(1):365–369. doi: 10.1006/dbio.1996.0309. [DOI] [PubMed] [Google Scholar]
  46. Rédei G P. Non-Mendelian Megagametogenesis in Arabidopsis. Genetics. 1965 Jun;51(6):857–872. doi: 10.1093/genetics/51.6.857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Schoof H., Lenhard M., Haecker A., Mayer K. F., Jürgens G., Laux T. The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell. 2000 Mar 17;100(6):635–644. doi: 10.1016/s0092-8674(00)80700-x. [DOI] [PubMed] [Google Scholar]
  48. Scott R. J., Spielman M., Bailey J., Dickinson H. G. Parent-of-origin effects on seed development in Arabidopsis thaliana. Development. 1998 Sep;125(17):3329–3341. doi: 10.1242/dev.125.17.3329. [DOI] [PubMed] [Google Scholar]
  49. Shimizu K. K., Okada K. Attractive and repulsive interactions between female and male gametophytes in Arabidopsis pollen tube guidance. Development. 2000 Oct;127(20):4511–4518. doi: 10.1242/dev.127.20.4511. [DOI] [PubMed] [Google Scholar]
  50. Springer P. S., Holding D. R., Groover A., Yordan C., Martienssen R. A. The essential Mcm7 protein PROLIFERA is localized to the nucleus of dividing cells during the G(1) phase and is required maternally for early Arabidopsis development. Development. 2000 May;127(9):1815–1822. doi: 10.1242/dev.127.9.1815. [DOI] [PubMed] [Google Scholar]
  51. Springer P. S., McCombie W. R., Sundaresan V., Martienssen R. A. Gene trap tagging of PROLIFERA, an essential MCM2-3-5-like gene in Arabidopsis. Science. 1995 May 12;268(5212):877–880. doi: 10.1126/science.7754372. [DOI] [PubMed] [Google Scholar]
  52. St Johnston D., Nüsslein-Volhard C. The origin of pattern and polarity in the Drosophila embryo. Cell. 1992 Jan 24;68(2):201–219. doi: 10.1016/0092-8674(92)90466-p. [DOI] [PubMed] [Google Scholar]
  53. Stewart C. N., Jr, Via L. E. A rapid CTAB DNA isolation technique useful for RAPD fingerprinting and other PCR applications. Biotechniques. 1993 May;14(5):748–750. [PubMed] [Google Scholar]
  54. Sørensen M. B., Chaudhury A. M., Robert H., Bancharel E., Berger F. Polycomb group genes control pattern formation in plant seed. Curr Biol. 2001 Feb 20;11(4):277–281. doi: 10.1016/s0960-9822(01)00072-0. [DOI] [PubMed] [Google Scholar]
  55. Vielle-Calzada J. P., Baskar R., Grossniklaus U. Delayed activation of the paternal genome during seed development. Nature. 2000 Mar 2;404(6773):91–94. doi: 10.1038/35003595. [DOI] [PubMed] [Google Scholar]
  56. Vielle-Calzada J. P., Thomas J., Spillane C., Coluccio A., Hoeppner M. A., Grossniklaus U. Maintenance of genomic imprinting at the Arabidopsis medea locus requires zygotic DDM1 activity. Genes Dev. 1999 Nov 15;13(22):2971–2982. doi: 10.1101/gad.13.22.2971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Vinkenoog R., Spielman M., Adams S., Fischer R. L., Dickinson H. G., Scott R. J. Hypomethylation promotes autonomous endosperm development and rescues postfertilization lethality in fie mutants. Plant Cell. 2000 Nov;12(11):2271–2282. doi: 10.1105/tpc.12.11.2271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Vizir I. Y., Anderson M. L., Wilson Z. A., Mulligan B. J. Isolation of deficiencies in the Arabidopsis genome by gamma-irradiation of pollen. Genetics. 1994 Aug;137(4):1111–1119. doi: 10.1093/genetics/137.4.1111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Yadegari R., Kinoshita T., Lotan O., Cohen G., Katz A., Choi Y., Katz A., Nakashima K., Harada J. J., Goldberg R. B. Mutations in the FIE and MEA genes that encode interacting polycomb proteins cause parent-of-origin effects on seed development by distinct mechanisms. Plant Cell. 2000 Dec;12(12):2367–2382. doi: 10.1105/tpc.12.12.2367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Zimmerman J. L. Somatic Embryogenesis: A Model for Early Development in Higher Plants. Plant Cell. 1993 Oct;5(10):1411–1423. doi: 10.1105/tpc.5.10.1411. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES