Apomictic and Sexual Germline Development Differ with Respect to Cell Cycle, Transcriptional, Hormonal and Epigenetic Regulation

PLoS Genetics

Volumn 10, Issue 7, 2014, Pages

  Schmidt, Anja ^a   Schmid, Marc W ^a   Klostermeier, Ulrich C ^b   Qi, Weihong ^c   Guthörl, Daniela ^a   Sailer, Christian ^a   Waller, Manuel ^a   Rosenstiel, Philip ^b   Grossniklaus, Ueli ^a  

^a Botanical Institute of the University of Basel   (Switzerland)

^b UNIVERSITY OF KIEL   (Germany)

^c FUNCTIONAL GENOMICS CENTER ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

PHYTOHORMONE; SPERMIDINE;

APOMICTIC DEVELOPMENT; APOMICTIC INITIAL CELL; APOMIXIS; ARABIDOPSIS THALIANA; ARTICLE; BOECHERA GUNNISONIANA; CELL CYCLE REGULATION; CONTROLLED STUDY; EPIGENETICS; GAMETOPHYTE; GENE EXPRESSION; GENE ONTOLOGY; GERM LINE; LASER MICRODISSECTION; MEGASPORE MOTHER CELL; MEIOSIS; MICROARRAY ANALYSIS; NONHUMAN; OVULE; PLANT CELL; PLANT DEVELOPMENT; PLANT REPRODUCTION; POLYAMINE METABOLISM; RNA SEQUENCE; SEQUENCE HOMOLOGY; SEXUAL DEVELOPMENT; SIGNAL TRANSDUCTION; SOMATIC EMBRYOGENESIS; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; UPREGULATION; ARABIDOPSIS; CELL CYCLE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETIC TRANSCRIPTION; GENETICS; GERM CELL; GROWTH, DEVELOPMENT AND AGING; PLANT SEED; REPRODUCTION;

APOMIXIS; ARABIDOPSIS; CELL CYCLE; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, PLANT; GERM CELLS; MEIOSIS; REPRODUCTION; SEEDS; SEXUAL DEVELOPMENT; TRANSCRIPTION, GENETIC;

EID: 84905455425     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004476     Document Type: Article

References (98)

1. Nogler GA (1984) Gametophytic apomixis. In: Embryology of Angiosperms. Edited by Johri BM. Berlin: Springer; pp. 475-518.
2. Savidan Y, (2000) Apomixis: Genetics and breeding. Plant Breeding Reviews 18: 13-86.
3. Spillane C, Steimer A, Grossniklaus U, (2001) Apomixis in agriculture: The quest for clonal seeds. Sex Plant Reprod 14: 179-87.
4. Bicknell RA, Koltunow AM, (2004) Understanding apomixis: Recent advances and remaining conundrums. Plant Cell 16: 228-245.
5. Spillane C, Curtis MD, Grossniklaus U, (2004) Apomixis technology development- virgin births in farmers' fields? Nat Biotechnol 22: 687-691.
6. Koltunow A, Grossniklaus U, (2003) Apomixis: A developmental perspective. Annu Rev Plant Biol 54: 547-574.
7. Grossniklaus U (2001) From sexuality to apomixis: molecular and genetic approaches. In: The Flowering of Apomixis: From Mechanisms to Genetic Engineering. Edited by Savidan Y, Carman J, Dresselhaus T. Mexico DF: CIMMYT; pp.168-211.
8. Sprunck S, Gross-Hardt R, (2011) Nuclear behavior, cell polarity, and cell specification in the female gametophyte. Sex Plant Reprod 24: 123-136.
9. Koltunow AM, (1993) Apomixis: Embryo sacs and embryos formed without meiosis or fertilization in ovules. Plant Cell 5: 1425-1437.
10. Rodkienwicz B, (1970) Callose in cell walls during megasporogenesis in angiosperms. Planta 93: 39-47.
11. Wüst SE, Vijverberg K, Schmidt A, Weiss M, Gheyselinck J, et al. (2010) Arabidopsis female gametophyte gene expression map reveals similarities between plant and animal gametes. Curr Biol 20: 506-512.
12. Schmidt A, Wüst SE, Vijverberg K, Baroux C, Kleen D, et al. (2011) Transcriptome analysis of the Arabidopsis megaspore mother cell uncovers the importance of RNA helicases for plant germline development. PLoS Biol 9: e1001155.
13. Schmid MW, Schmidt A, Klostermeier UC, Barann M, Rosenstiel P, et al. (2012) A powerful method for transcriptional profiling of specific cell types in eukaryotes: laser-assisted microdissection and RNA sequencing. PLoS ONE 7: e29685.
14. Grossniklaus U, Nogler GA, van Dijk PJ, (2001) How to avoid sex: the genetic control of gametophytic apomixis. Plant Cell 2001 13: 1491-1498.
15. Savidan Y, (1982) Nature et hérédité de l' apomixie chez Panicum maximum Jacq. Trav. & Doc. Orstom 153: 1-159.
16. Nogler GA, (1984) Genetics of apospory in apomictic Ranunculus auricomus. V Conclusion Bot Helv 94: 411-422.
17. Sherwood RT, Berg CC, Young BA, (1994) Inheritance of apospory in buffelgrass. Crop Sci 34: 1490-1494.
18. Grimanelli D, Leblanc O, Espinosa E, Perotti E, González de León D, et al. (1998) Mapping diplosporous apomixis in tetraploid Tripsacum: one gene or several genes? Heredity 80: 33-39.
19. Ozias-Akins P, Roche D, Hanna WW, (1998) Tight clustering and hemizygosity of apomixis-linked molecular markers in Pennisetum squamulatum implies genetic control of apospory by a divergent locus that may have no allelic form in sexual genotypes. Proc Natl Acad Sci U S A 95: 5127-5132.
20. Noyes RD, Rieseberg LH, (2000) Two independent loci control agamospermy (apomixis) in the triploid flowering plant Erigeron annuus. Genetics 155: 379-390.
21. Valle CB, Miles JW (2001) Breeding of apomictic species. In: The Flowering of Apomixis: From Mechanisms to Genetic Engineering. Edited by Savidan Y, Carman J, Dresselhaus T. Mexico DF: CIMMYT; pp. 137-152.
22. Cáceres ME, Matzk F, Busti A, Pupilli F, Arcioni S, (2001) Apomixis and sexuality in Paspalum simplex: characterization of the mode of reproduction in segregating progenies by different methods. Sex Plant Reprod 14: 201-206.
23. van Dijk PJ, Bakx-Schotman JM, (2004) Formation of unreduced megaspores (diplospory) in apomictic dandelions (Taraxacum officinale, s.l.) is controlled by a sex-specific dominant locus. Genetics 166: 483-492.
24. Koltunow AM, Johnson SD, Rodrigues JC, Okada T, Hu Y, Tsuchiya T, et al. (2011) Sexual reproduction is the default mode in apomictic Hieracium subgenus Pilosella, in which two dominant loci function to enable apomixis. Plant J 66: 890-902.
25. Schranz ME, Kantama L, de Jong H, Mitchell-Olds T, (2006) Asexual reproduction in a close relative of Arabidopsis: a genetic investigation of apomixis in Boechera (Brassicaceae). New Phytol 171: 425-438.
26. Grimanelli D, Leblanc O, Perotti E, Grossniklaus U, (2001) Developmental genetics of gametophytic apomixis. Trends Genet 17: 597-604.
27. Sharbel TF, Voigt ML, Corral JM, Thiel T, Varshney A, et al. (2009) Molecular signatures of apomictic and sexual ovules in the Boechera holboellii complex. Plant J 104: 14026-14031.
28. Sharbel TF, Voigt ML, Corral JM, Galla G, Kumlehn J, et al. (2010) Apomictic and sexual ovules of Boechera display heterochronic global gene expression patterns. Plant Cell 22: 655-671.
29. Leblanc O, Armstead I, Pessino S, Ortiz JP, Evans C, et al. (1997) Non-radioactive mRNA fingerprinting to visualise gene expression in mature ovaries of Brachiaria hybrids derived from B. brizantha, an apomictic tropical forage. Plant Sci 126: 49-58.
30. Rodrigues JC, Carbral GB, Dusi DM, de Mello LV, Rigden DJ, et al. (2003) Identification of differentially expressed cDNA sequences in ovaries of sexual and apomictic plants of Brachiaria brizantha. Plant Mol Biol 53: 745-757.
31. Okada T, Hu Y, Tucker MR, Taylor JM, Johnson SD, et al. (2013) Enlarging cells initiating apomixis in Hieracium praealtum transition to an embryo sac program prior to entering mitosis. Plant Physiol 163: 216-31.
32. Vielle-Calzada JP, Nuccio ML, Budiman MA, Burson BL, Hussey MA, et al. (1996) Comparative gene expression in sexual and apomictic ovaries of Pennisetum ciliare (L.) Link. Plant Mol Biol 32: 1085-1092.
33. Sahu PP, Gupta S, Malaviya DR, Roy AK, Kaushal P, et al. (2012) Transcriptome analysis of differentially expressed genes during embryo sac development in apomeiotic non-parthenogenetic interspecific hybrid of Pennisetum glaucum. Mol Biotechnol 51: 262-271.
34. Pessino SC, Espinoza F, Martinez EJ, Ortiz JP, Valle EM, et al. (2001) Isolation of cDNA clones differentially expressed in flowers of apomictic and sexual Paspalum notatum. Hereditas 134: 35-42.
35. Polegri L, Calderini O, Arcioni S, Pupilli F, (2010) Specific expression of apomixis-linked alleles revealed by comparative transcriptomic analysis of sexual and apomictic Paspalum simplex Morong flowers. J Exp Bot 61: 1869-83.
36. Ochogavía AC, Seijo JG, González AM, Podio M, Duarte Silveira E, et al. (2011) Characterization of retrotransposon sequences expressed in inflorescences of apomictic and sexual Paspalum notatum plants. Sex Plant Reprod 24: 231-246.
37. Barcaccia G, Varotto S, Meneghetti S, Albertini E, Porceddu A, et al. (2001) Analysis of gene expression during flowering in apomeiotic mutants of Medicago spp.: cloning ESTs and candidate genes for apomeiosis. Sex Plant Reprod 14: 233-238.
38. Chen L, Miyazaki C, Kojima A, Saito A, Adachi T, (1999) Isolation and characterization of a gene expressed during early embryo sac development in apomictic Guinea grass (Panicum maximum). J Plant Physiol 154: 55-62.
39. Albertini E, Marconi G, Barcaccia G, Raggi L, Falcinelli M, (2004) Isolation of candidate genes for apomixis in Poa pratensis L. Plant Mol Biol 56: 879-894.
40. Albertini E, Marconi G, Reale L, Barcaccia G, Porceddu A, et al. (2005) SERK and APOSTART. Candidate genes for apomixis in Poa pratensis. Plant Physiol 138: 2185-2199.
41. Tucker MR, Araujo AC, Paech NA, Hecht V, Schmidt ED, et al. (2003) Sexual and apomictic reproduction in Hieracium subgenus pilosella are closely interrelated developmental pathways. Plant Cell 15: 1524-1537.
42. Olmedo-Monfil V, Durán-Figueroa N, Arteaga-Vázquez M, Demesa-Arévalo E, Autran D, et al. (2010) Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464: 628-632.
43. Garcia-Aguilar M, Michaud C, Leblanc O, Grimanelli D, (2010) Inactivation of a DNA methylation pathway in maize reproductive organs results in apomixis-like phenotypes. Plant Cell 22: 3249-3267.
44. Singh M, Goel S, Meeley RB, Dantec C, Parrinello H, et al. (2011) Production of viable gametes without meiosis in maize deficient for an ARGONAUTE protein. Plant Cell 23: 443-458.
45. Ravi M, Marimuthu MP, Siddiqi I, (2008) Gamete formation without meiosis in Arabidopsis. Nature 451: 1121-1124.
46. d'Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, et al. (2009) Turning meiosis into mitosis. PLoS Biol 7: e1000124.
47. Matzk F, Meister A, Schubert I, (2010) An efficient screen for reproductive pathways using mature seeds of monocots and dicots. Plant J 21: 97-108.
48. Roy BA, (1995) The breeding system of six species of Arabis (Brassicaceae). Am J Bot 82: 869-877.
49. Taskin KM, Turgut K, Scott RJ, (2004) Apomictic development in Arabis gunnisoniana. Isr J Plant Sci 52: 155-160.
50. Aliyu OM, Schranz ME, Sharbel TF, (2010) Quantitative variation for apomictic reproduction in the genus Boechera (Brassicaceae). Am J Bot 97: 1719-1731.
51. Johnston AJ (2007) Functional genomics of sexual and asexual reproduction in Arabidopsis and relatives. PhD Thesis, University of Zürich, Switzerland.
52. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnol 29: 644-654.
53. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, et al. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
54. Kent WJ, (2002) BLAT-the BLAST-like alignment tool. Genome Res 12: 656-664.
55. Bar-Or C, Czosnek H, Koltai H, (2007) Cross-species microarray hybridizations: a developing tool for studying species diversity. Trends Genet 23: 200-207.
56. Tang F, Barbacioru C, Wang Y, Nordman E, Lee C, et al. (2009) mRNA-Seq whole-transcriptome analysis of a single cell. Nat Methods 6: 377-382.
57. Tarazona S, García-Alcalde F, Dopazo J, Ferrer A, Conesa A, (2011) Differential expression in RNA-seq: a matter of depth. Genome Res 21: 2213-2223.
58. Robinson MD, McCarthy DJ, Smyth GK, (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
59. Wijnker E, Schnittger A, (2013) Control of the meiotic cell division program in plants. Plant Reprod 26: 143-158.
60. Vandepoele K, Raes J, De Veylder L, Rouzé P, Rombauts S, et al. (2002) Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14: 903-916.
61. Gutierrez C, (2009) The Arabidopsis cell division cycle. Arabidopsis Book 7: e0120.
62. Nodine MD, Bartel DP, (2010) MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev 24: 2678-2692.
63. Chen C, Farmer AD, Langley RJ, Mudge J, Crow JA, et al. (2010) Meiosis-specific gene discovery in plants: RNA-Seq applied to isolated Arabidopsis male meiocytes. BMC Plant Biol 10: 280.
64. Torti S, Fornara F, Vincent C, Andrés F, Nordström K, et al. (2012) Analysis of the Arabidopsis shoot meristem transcriptome during floral transition identifies distinct regulatory patterns and a leucine-rich repeat protein that promotes flowering. Plant Cell 24: 444-462.
65. Filichkin SA, Priest HD, Givan SA, Shen R, Bryant DW, (2010) Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res 20: 45-58.
66. Lister R, O'Malley RC, Tonti-Filippini J, Gregory BG, Berry CC, et al. (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133: 523-536.
67. Koszegi D, Johnston AJ, Rutten T, Czihal A, Altschmied L, et al. (2011) Members of the RKD transcription factor family induce an egg cell-like gene expression program. Plant J 67: 280-91.
68. Imai A, Matsuyama T, Hanzawa Y, Akiyama T, Tamaoki M, et al. (2004) Spermidine synthase genes are essential for survival of Arabidopsis. Plant Physiol 135: 1565-1573.
69. Wu XB, Wang J, Liu JH, Deng XX, (2009) Involvement of polyamine biosynthesis in somatic embryogenesis of Valencia sweet orange (Citrus sinensis) induced by glycerol. J Plant Physiol 166: 52-62.
70. De-la-Peña C, Galaz-Avalos RM, Loyola-Vargas VM, (2008) Possible role of light and polyamines in the onset of somatic embryogenesis of Coffea canephora. Mol Biotechnol 39: 215-24.
71. Dutra NT, Silveira V, de Azevedo IG, Gomes-Neto LR, Façanha AR, et al. (2013) Polyamines affect the cellular growth and structure of pro-embryogenic masses in Araucaria angustifolia embryogenic cultures through the modulation of proton pump activities and endogenous levels of polyamines. Physiol Plant 148: 121-32.
72. Ha HC, Sirisoma NS, Kuppusamy P, Zweier JL, Woster PM, et al. (1998) The natural polyamine spermidine functions directly as free radical scavenger. Proc Natl Acad Sci USA 95: 11140-11145.
73. Hörandl E, Hadacek F, (2013) The oxidative damage initiation hypothesis for meiosis. Plant Reprod DOI 10.1007s0049701302347/s00497-013-0234-7.
74. Martin MV, Fiol DF, Sundaresan V, Zabaleta EJ, Pagnussat GC, (2013) oiwa, a female gametophytic mutant impaired in a mitochondrial manganese-superoxide dismutase, reveals crucial roles for reactive oxygen species during embryo sac development and fertilization in Arabidopsis. Plant Cell 25: 1573-1591.
75. Conner JA, Goel S, Gunawan G, Cordonnier-Pratt MM, Johnson VE, et al. (2008) Sequence analysis of bacterial artificial chromosome clones from the apospory-specific genomic region of Pennisetum and Cenchrus. Plant Physiol 147: 1396-1411.
76. Guilfoyle TJ, Ulmasov T, Hagen G, (1998) The ARF family of transcription factors and their role in plant hormone-responsive transcription. Cell Mol Life Sci 54: 619-627.
77. Rademacher EH, Möller B, Lokerse AS, Llavata-Peris CI, van den Berg W, et al. (2011) A cellular expression map of the Arabidopsis AUXIN RESPONSE FACTOR gene family. Plant J 68: 597-606.
78. Craig KL, Tyers M, (1999) The F-box: a new motif for ubiquitin dependent proteolysis in cell cycle regulation and signal transduction. Prog Biophys Mol Biol 72: 299-328.
79. Lechner E, Achard P, Vansiri A, Potuschak T, Genschik P, (2006) F-box proteins everywhere. Curr Opin Plant Biol 9: 631-638.
80. Amiteye S, Corral JM, Vogel H, Sharbel TF, (2011) Analysis of conserved microRNAs in floral tissues of sexual and apomictic Boechera species. BMC Genomics 12: 500.
81. Schallau A, Arzenton F, Johnston AJ, Hähnel U, Koszegi D, et al. (2010) Identification and genetic analysis of the APOSPORY locus in Hypericum perforatum L. Plant J 62: 773-784.
82. Mladek C, Guger K, Hauser MT, (2003) Identification and characterization of the ARIADNE gene family in Arabidopsis. A group of putative E3 ligases. Plant Physiol 131: 27-40.
83. Marimuthu MP, Jolivet S, Ravi M, Pereira L, Davda JN, et al. (2011) Synthetic clonal reproduction through seeds. Science 331: 876.
84. Crismani W, Girard C, Mercier R, (2013) Tinkering with meiosis. J Exp Bot 64: 55-65.
85. Cook GS, Grønlund AL, Siciliano I, Spadafora N, Amini M, et al. (2013) Plant WEE1 kinase is cell cycle regulated and removed at mitosis via the 26S proteasome machinery. J Exp Bot 64: 2093-2106.
86. Heckmann S, Lermontova I, Berckmans B, De Veylder L, Bäumlein H, et al. (2011) The E2F transcription factor family regulates CENH3 expression in Arabidopsis thaliana. Plant J 68: 646-656.
87. Zeng Y, Conner J, Ozias-Akins P, (2011) Identification of ovule transcripts from the Apospory-Specific Genomic Region (ASGR)-carrier chromosome. BMC Genomics 12: 206.
88. Grossniklaus U, Schneitz K, (1998) The molecular and genetic basis of ovule and megagametophyte development. Semin Cell Dev Biol 9: 227-238.
89. Tucker MR, Okada T, Johnson SD, Takaiwa F, Koltunow AM, (2012) Sporophytic ovule tissues modulate the initiation and progression of apomixis in Hieracium. J Exp Bot 63: 3229-3241.
90. Vielle-Calzada J-P, Thomas J, Spillane C, Coluccio A, Hoeppner MA, Grossniklaus U, (1999) Maintenance of genomic imprinting at the Arabidopsis MEDEA locus requires zygotic DDM1 activity. Genes Dev 13: 2971-2982.
91. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
92. Paradis E, Claude J, Strimmer K, (2004) APE: Analysis of phylogenetics and evolution in the R language. Bioinformatics 20: 289-290.
93. Langmead B, Trapnell C, Pop M, Salzberg SL, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
94. Robinson MD, Oshlack A, (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 11: R25.
95. Wüst SE, O'Maoileidigh DS, Rae L, Kwasniewska K, Raganelli A, Hanczaryk K, et al. (2012) Molecular basis for the specification of floral organs by APETALA3 and PISTILLATA. Proc Natl Acad Sci U S A 109: 13452-13457.
96. Alexa A, Rahnenführer J (2009) Gene set enrichment analysis with topGO. (www.bioconductor.org).
97. Warnes G, Bolker B, Lumley T (2010) gplots: Various R programming tools for plotting data. (www.bioconductor.org).
98. Anders S, Huber W, (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106.