Sexual polyploidization in plants – cytological mechanisms and molecular regulation

Abstract

Summary In the plant kingdom, events of whole genome duplication or polyploidization are generally believed to occur via alterations of the sexual reproduction process. Thereby, diploid pollen and eggs are formed that contain the somatic number of chromosomes rather than the gametophytic number. By participating in fertilization, these so‐called 2n gametes generate polyploid offspring and therefore constitute the basis for the establishment of polyploidy in plants. In addition, diplogamete formation, through meiotic restitution, is an essential component of apomixis and also serves as an important mechanism for the restoration of F 1 hybrid fertility. Characterization of the cytological mechanisms and molecular factors underlying 2n gamete formation is therefore not only relevant for basic plant biology and evolution, but may also provide valuable cues for agricultural and biotechnological applications (e.g. reverse breeding, clonal seeds). Recent data have provided novel insights into the process of 2n pollen and egg formation and have revealed multiple means to the same end. Here, we summarize the cytological mechanisms and molecular regulatory networks underlying 2n gamete formation, and outline important mitotic and meiotic processes involved in the ectopic induction of sexual polyploidization. Contents Summary 670 I. Introduction 670 II. General mechanisms of 2n gamete formation 671 III. Cytological processes leading to meiotic restitution 672 IV. Genetic control of 2n gamete formation 675 V. Conclusions and future directions 680 Acknowledgements 680 References 680

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101. 101.

     Li J, Lee GI, Van Doren SR, Walker JC. The FHA domain mediates phosphoprotein interactions. Journal of Cell Science. 2000;113:4143-4149.

     Not in our library10.1242/jcs.113.23.4143

102. 102.

     Li XY, Sakashita G, Matsuzaki H, Sugimoto K, Kimura K, Hanaoka F, Taniguchi H, Furukawa K, Urano T. Direct association with inner centromere protein (INCENP) activates the novel chromosomal passenger protein, Aurora-C. Journal of Biological Chemistry. 2004;279:47201-47211.

     Not in our library10.1074/jbc.m403029200

103. 103.

     Li YH, Shen YA, Cai C, Zhong CC, Zhu L, Yuan M, Ren HY. The Type II Arabidopsis Formin14 interacts with microtubules and microfilaments to regulate cell division. Plant Cell. 2010;22:2710-2726.

     Not in our library10.1105/tpc.110.075507

104. 104.

     Li Z, Larson-Rabin Z, Masson PH, Day CD. FZR2/CCS52A1 mediated endoreduplication in Arabidopsis development. Plant Signaling & Behavior. 2009;4:451-453.

     Not in our library10.4161/psb.4.5.8480

105. 105.

     Lim KB, Ramanna MS, de Jong JH, Jacobsen E, van Tuyl JM. Indeterminate meiotic restitution (IMR): a novel type of meiotic nuclear restitution mechanism detected in interspecific lily hybrids by GISH. Theoretical and Applied Genetics. 2001;103:219-230.

     Not in our library

106. 106.

     Lim KB, Shen TM, Barba-Gonzalez R, Ramanna MS, Van Tuyl JM. Occurrence of SDR 2N-gametes in Lilium hybrids. Breeding Science. 2004;54:13-18.

     Not in our library

107. 107.

     Lopez-Lavalle LAB, Orjeda G. Occurrence and cytological mechanism of 2n pollen formation in a tetraploid accession of Ipomoea batatas (sweet potato). Journal of Heredity. 2002;93:185-192.

     Not in our library10.1093/jhered/93.3.185

108. 108.

     Lu CS, Bridgen MP. Chromosome doubling and fertility study of Alstroemeria aurea × A. caryophyllaea. Euphytica. 1997;94:75-81.

     Not in our library

109. 109.

     Lutes AA, Neaves WB, Baumann DP, Wiegraebe W, Baumann P. Sister chromosome pairing maintains heterozygosity in parthenogenetic lizards. Nature. 2010;464:283-286.

     Not in our library10.1038/nature08818

110. 110.

     Ma JB, Ye KQ, Patel DJ. Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature. 2004;429:318-322.

     Not in our library10.1038/nature02519

111. 111.

     Magnard JL, Yang M, Chen YCS, Leary M, McCormick S. The Arabidopsis gene tardy asynchronous meiosis is required for the normal pace and synchrony of cell division during male meiosis. Plant Physiology. 2001;127:1157-1166.

     Not in our library

112. 112.

     Magyar Z, Horvath B, Khan S, Mohammed B, Henriques R, De Veylder L, Bako L, Scheres B, Bogre L. Arabidopsis E2FA stimulates proliferation and endocycle separately through RBR-bound and RBR-free complexes. EMBO Journal. 2012;31:1480-1493.

     Not in our library10.1038/emboj.2012.13

113. 113.

     Malapeira J, Moldon A, Hidalgo E, Smith GR, Nurse P, Ayte J. A meiosis-specific cyclin regulated by splicing is required for proper progression through meiosis. Molecular and Cellular Biology. 2005;25:6330-6337.

     Not in our library10.1128/mcb.25.15.6330-6337.2005

114. 114.

     Mariani A, Tavoletti S, Veronesi F. Abnormal microsporogenesis in five alfalfa (Medicago sativa) mutants producing 4n pollen. Theoretical and Applied Genetics. 1993;85:873-881.

     Not in our library10.1007/bf00225032

115. 115.

     Marston AL, Amon A. Meiosis: cell-cycle controls shuffle and deal. Nature Reviews Molecular Cell Biology. 2004;5:983-997.

     Not in our library10.1038/nrm1526

116. 116.

     Mason AS, Nelson MN, Yan GJ, Cowling WA. Production of viable male unreduced gametes in Brassica interspecific hybrids is genotype specific and stimulated by cold temperatures. BMC Plant Biology. 2011;11:103.

     Not in our library10.1186/1471-2229-11-103

117. 117.

     McCoy TJ. The inheritance of 2n pollen formation in diploid alfalfa Medicago sativa. Canadian Journal of Genetics and Cytology. 1982;24:315-323.

     Not in our library

118. 118.

     Mercier R, Vezon D, Bullier E, Motamayor JC, Sellier A, Lefevre F, Pelletier G, Horlow C. SWITCH1 (SWI1): a novel protein required for the establishment of sister chromatid cohesion and for bivalent formation at meiosis. Genes & Development. 2001;15:1859-1871.

     Not in our library10.1101/gad.203201

119. 119.

     Meyuhas O. Physiological roles of ribosomal protein S6: one of its kind. International Review of Cell and Molecular Biology. 2008;268:1-37.

     Not in our library10.1016/s1937-6448(08)00801-0

120. 120.

     Modzelewski AJ, Holmes RJ, Hilz S, Grimson A, Cohen PE. AGO4 regulates entry into meiosis and influences silencing of sex chromosomes in the male mouse germline. Developmental Cell. 2012;23:251-264.

     Not in our library10.1016/j.devcel.2012.07.003

121. 121.

     Mok D, Peloquin SJ. The inheritance of three mechanisms of diplandroid (2n pollen) formation in diploid potatoes. Heredity. 1975a;35:1-8.

     Not in our library

122. 122.

     Mok D, Peloquin SJ. Three mechanisms of 2n pollen formation in diploid potatoes. Canadian Journal of Genetics and Cytology. 1975b;17:217-225.

     Not in our library

123. 123.

     Motamayor JC, Vezon D, Bajon C, Sauvanet A, Grandjean O, Marchand M, Bechtold N, Pelletier G, Horlow C. Switch (swi1), an Arabidopsis thaliana mutant affected in the female meiotic switch. Sexual Plant Reproduction. 2000;12:209-218.

     Not in our library

124. 124.

     Muller S, Smertenko A, Wagner V, Heinrich M, Hussey PJ, Hauser MT. The plant microtubule-associated protein AtMAP65-3/PLE is essential for cytokinetic phragmoplast function. Current Biology. 2004;14:412-417.

     Not in our library10.1016/j.cub.2004.02.032

125. 125.

     Naumova TN, van der Laak J, Osadtchiy J, Matzk F, Kravtchenko A, Bergervoet J, Ramulu KS, Boutilier K. Reproductive development in apomictic populations of Arabis holboellii (Brassicaceae). Sexual Plant Reproduction. 2001;14:195-200.

     Not in our library10.1007/s00497-001-0118-0

126. 126.

     Neaves WB, Baumann P. Unisexual reproduction among vertebrates. Trends in Genetics. 2011;27:81-88.

     Not in our library10.1016/j.tig.2010.12.002

127. 127.

     Nguyen HG, Ravid K. Tetraploidy/aneuploidy and stem cells in cancer promotion: the role of chromosome passenger proteins. Journal of Cellular Physiology. 2006;208:12-22.

     Not in our library10.1002/jcp.20565

128. 128.

     Nishihama R, Ishikawa M, Araki S, Soyano T, Asada T, Machida Y. The NPK1 mitogen-activated protein kinase kinase kinase is a regulator of cell-plate formation in plant cytokinesis. Genes & Development. 2001;15:352-363.

     Not in our library10.1101/gad.863701

129. 129.

     Nishihama R, Soyano T, Ishikawa M, Araki S, Tanaka H, Asada T, Irie K, Ito M, Terada M, Banno H, et al. Expansion of the cell plate in plant cytokinesis requires a kinesin-like protein/MAPKKK complex. Cell. 2002;109:87-99.

     Not in our library10.1016/s0092-8674(02)00691-8

130. 130.

     Nonomura KI, Morohoshi A, Nakano M, Eiguchi M, Miyao A, Hirochika H, Kurata N. A germ cell-specific gene of the ARGONAUTE family is essential for the progression of premeiotic mitosis and meiosis during sporogenesis in rice. Plant Cell. 2007;19:2583-2594.

     Not in our library10.1105/tpc.107.053199

131. 131.

     Ortiz R. Occurrence and inheritance of 2n pollen in Musa. Annals of Botany. 1997;79:449-453.

     Not in our library

132. 132.

     Ortiz R, Peloquin SJ. Breeding for 2n-egg production in haploid-X species 2x-potato hybrids. American Potato Journal. 1991;68:691-703.

     Not in our library

133. 133.

     Otto SP, Whitton J. Polyploidy: incidence and evolution. Annual Review of Genetics. 2000;34:401-437.

     Not in our library10.1146/annurev.genet.34.1.401

134. 134.

     Ozias-Akins P. Apomixis: developmental characteristics and genetics. Critical Reviews in Plant Sciences. 2006;25:199-214.

     Not in our library

135. 135.

     Ozias-Akins P, van Dijk PJ. Mendelian genetics of apomixis in plants. Annual Review of Genetics. 2007;41:509-537.

     Not in our library10.1146/annurev.genet.40.110405.090511

136. 136.

     Ozias-Akins P, Roche D, Hanna WW. Tight clustering and hemizygosity of apomixis-linked molecular markers in Pennisetum squamulatum genetic control of apospory by a divergent locus that may have no allelic form in sexual genotypes. Proceedings of the National Academy of Sciences, USA. 1998;95:5127-5132.

     Not in our library10.1073/pnas.95.9.5127

137. 137.

     Pagliarini MS, Takayama SY, de Freitas PM, Carraro LR, Adamowski EV, Silva N, Batista LAR. Failure of cytokinesis and 2n gamete formation in Brazilian accessions of Paspalum. Euphytica. 1999;108:129-135.

     Not in our library

138. 138.

     Parrott WA, Smith RR. Production of 2n pollen in red-clover. Crop Science. 1984;24:469-472.

     Not in our library

139. 139.

     Parrott WA, Smith RR. Recurrent selection for 2n pollen formation in red-clover. Crop Science. 1986;26:1132-1135.

     Not in our library

140. 140.

     Pecrix Y, Rallo G, Folzer H, Cigna M, Gudin S, Le Bris M. Polyploidization mechanisms: temperature environment can induce diploid gamete formation in Rosa sp. Journal of Experimental Botany. 2011;62:3587-3597.

     Not in our library10.1093/jxb/err052

141. 141.

     Peloquin SJ, Boiteux LS, Carputo D. Meiotic mutants in potato: valuable variants. Genetics. 1999;153:1493-1499.

     Not in our library10.1093/genetics/153.4.1493

142. 142.

     Peloquin SJ, Boiteux LS, Simon PW, Jansky SH. A chromosome-specific estimate of transmission of heterozygosity by 2n gametes in potato. Journal of Heredity. 2008;99:177-181.

     Not in our library10.1093/jhered/esm110

143. 143.

     Pfeiffer TW, Bingham ET. Abnormal meiosis in alfalfa, Medicago sativa – cytology of 2n egg and 4n pollen formation. Canadian Journal of Genetics and Cytology. 1983;25:107-112.

     Not in our library

144. 144.

     Ramanna MS. First division restitution gametes through fertile desynaptic mutants of potato. Euphytica. 1983;32:337-350.

     Not in our library

145. 145.

     Ramanna MS, Jacobsen E. Relevance of sexual polyploidization for crop improvement – a review. Euphytica. 2003;133:3-18.

     Not in our library

146. 146.

     Ramanna MS, Kuipers AGJ, Jacobsen E. Occurrence of numerically unreduced (2n) gametes in Alstroemeria interspecific hybrids and their significance for sexual polyploidisation. Euphytica. 2003;133:95-106.

     Not in our library

147. 147.

     Ramsey J, Schemske DW. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annual Review of Ecology and Systematics. 1998;29:467-501.

     Not in our library

148. 148.

     Ravi M, Marimuthu MPA, Siddiqi I. Gamete formation without meiosis in Arabidopsis. Nature. 2008;451:1121-U1110.

     Not in our library10.1038/nature06557

149. 149.

     Reddy TV, Kaur J, Agashe B, Sundaresan V, Siddiqi I. The DUET gene is necessary for chromosome organization and progression during male meiosis in Arabidopsis and encodes a PHD finger protein. Development. 2003;130:5975-5987.

     Not in our library10.1242/dev.00827

150. 150.

     Resnick TD, Dej KJ, Xiang Y, Hawley RS, Ahn C, Orr-Weaver TL. Mutations in the chromosomal passenger complex and the condensin complex differentially affect synaptonemal complex disassembly and metaphase I configuration in Drosophila female meiosis. Genetics. 2009;181:875-887.

     Not in our library10.1534/genetics.108.097741

151. 151.

     Rhoades MM, Dempsey E. Induction of chromosome doubling at meiosis by the elongate gene in maize. Genetics. 1966;54:505-522.

     Not in our library10.1093/genetics/54.2.505

152. 152.

     Rim YW, Beuselinck PR. Cytology of 2N pollen formation and pollen morphology in diploid Lotus tenuis (Fabaceae). American Journal of Botany. 1996;83:1057-1062.

     Not in our library

153. 153.

     Santos MA, van de Werken C, de Vries M, Jahr H, Vromans MJM, Laven JSE, Fauser BC, Kops GJ, Lens SM, Baart EB. A role for Aurora C in the chromosomal passenger complex during human preimplantation embryo development. Human Reproduction. 2011;26:1868-1881.

     Not in our library10.1093/humrep/der111

154. 154.

     Sasabe M, Kosetsu K, Hidaka M, Murase A, Machida Y. Arabidopsis thaliana MAP65-1 and MAP65-2 function redundantly with MAP65-3/PLEIADE in cytokinesis downstream of MPK4. Plant Signaling & Behavior. 2011;6:743-747.

     Not in our library10.4161/psb.6.5.15146

155. 155.

     Schnittger A, Schobinger U, Stierhof YD, Hulskamp M. Ectopic B-type cyclin expression induces mitotic cycles in endoreduplicating Arabidopsis trichomes. Current Biology. 2002;12:415-420.

     Not in our library10.1016/s0960-9822(02)00693-0

156. 156.

     Scott RJ, Spielman M, Bailey J, Dickinson HG. Parent-of-origin effects on seed development in Arabidopsis thaliana. Development. 1998;125:3329-3341.

     Not in our library10.1242/dev.125.17.3329

157. 157.

     Seal AG, Ferguson AR, de Silva HN, Zhang JL. The effect of 2n gametes on sex ratios in Actinidia. Sexual Plant Reproduction. 2012;25:197-203.

     Not in our library10.1007/s00497-012-0191-6

158. 158.

     Shamina NV, Shatskaya OA. Two novel meiotic restitution mechanisms in haploid maize (Zea mays L.). Russian Journal of Genetics. 2011;47:438-445.

     Not in our library

159. 159.

     Shamina NV, Zharkov NA, Omelyanchuk LV. Feed-back regulation of successive meiotic cytokinesis. Cell Biology International. 2009;33:393-401.

     Not in our library10.1016/j.cellbi.2009.01.011

160. 160.

     Sharbel TF, Mitchell-Olds TM, Dobes C, Kantama L, de Jong H. Biogeographic distribution of polyploidy and B chromosomes in the apomictic Boechera holboellii complex. Cytogenetic and Genome Research. 2005;109:283-292.

     Not in our library10.1159/000082411

161. 161.

     Sharbel TF, Voigt ML, Mitchell-Olds T, Kantama L, de Jong H. Is the aneuploid chromosome in an apomictic Boechera holboellii a genuine B chromosome? Cytogenetic and Genome Research. 2004;106:173-183.

     Not in our library10.1159/000079284

162. 162.

     Siddiqi I, Ganesh G, Grossniklaus U, Subbiah V. The dyad gene is required for progression through female meiosis in Arabidopsis. Development. 2000;127:197-207.

     Not in our library10.1242/dev.127.1.197

163. 163.

     Silkova OG, Dobrovolskaya OB, Shchapova AI, Shumny VK. Features of the regulation of meiotic restitution in androgenic haploids of wheat–rye substitution lines 2R(2D)(1), 2R(2D)(3), and 6R(6A) (Triticum aestivum L., cultivar Saratovskaya 29/Secale cereale L., cultivar Onokhoiskaya). Russian Journal of Genetics. 2009;45:1062-1066.

     Not in our library

164. 164.

     Silkova OG, Shchapova AI, Kravtsova LA. Mechanisms of meiotic restitution and their genetic regulation in wheat–rye polyhaploids. Russian Journal of Genetics. 2003;39:1271-1280.

     Not in our library

165. 165.

     Singh M, Goel S, Meeley RB, Dantec C, Parrinello H, Michaud C, Leblanc O, Grimanelli D. Production of viable gametes without meiosis in maize deficient for an ARGONAUTE protein. Plant Cell. 2011;23:443-458.

     Not in our library10.1105/tpc.110.079020

166. 166.

     Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, Zheng CF, Sankoff D, dePamphilis CW, Wall PK, Soltis PS. Polyploidy and angiosperm diversification. American Journal of Botany. 2009;96:336-348.

     Not in our library10.3732/ajb.0800079

167. 167.

     Song JJ, Smith SK, Hannon GJ, Joshua-Tor L. Crystal structure of argonaute and its implications for RISC slicer activity. Science. 2004;305:1434-1437.

     Not in our library10.1126/science.1102514

168. 168.

     Souter EW, Dawe JC, Peloquin SJ. 2n pollen formation via parallel spindles in the potato cultivar Sebago. American Potato Journal. 1980;57:449-455.

     Not in our library

169. 169.

     Soyano T, Nishihama R, Morikiyo K, Ishikawa M, Machida Y. NQK1/NtMEK1 is a MAPKK that acts in the NPK1 MAPKKK-mediated MAPK cascade and is required for plant cytokinesis. Genes & Development. 2003;17:1055-1067.

     Not in our library10.1101/gad.1071103

170. 170.

     Spielman M, Preuss D, Li FL, Browne WE, Scott RJ, Dickinson HG. TETRASPORE is required for male meiotic cytokinesis in Arabidopsis thaliana. Development. 1997;124:2645-2657.

     Not in our library10.1242/dev.124.13.2645

171. 171.

     Stelly DM, Peloquin SJ. Formation of 2n megagametophytes in diploid tuber-bearing Solanums. American Journal of Botany. 1986;73:1351-1363.

     Not in our library

172. 172.

     Stern BM. FEARless in meiosis. Molecular Cell. 2003;11:1123-1125.

     Not in our library10.1016/s1097-2765(03)00194-1

173. 173.

     Strasburger E. Sexuelle und apogame Fortpflanzung bei Urticaceen. Jahrbuch der Wissenschaftlichen Botanik. 1910;47:245-288.

     Not in our library

174. 174.

     Strompen G, El Kasmi F, Richter S, Lukowitz W, Assaad FF, Jurgens G, Mayer U. The Arabidopsis HINKEL gene encodes a kinesin-related protein involved in cytokinesis and is expressed in a cell cycle-dependent manner. Current Biology. 2002;12:153-158.

     Not in our library10.1016/s0960-9822(01)00655-8

175. 175.

     Takahashi Y, Soyano T, Kosetsu K, Sasabe M, Machida Y. HINKEL kinesin, ANP MAPKKKs and MKK6/ANQ MAPKK, which phosphorylates and activates MPK4 MAPK, constitute a pathway that is required for cytokinesis in Arabidopsis thaliana. Plant and Cell Physiology. 2010;51:1766-1776.

     Not in our library10.1093/pcp/pcq135

176. 176.

     Takahashi Y, Soyano T, Sasabe M, Machida Y. A MAP kinase cascade that controls plant cytokinesis. Journal of Biochemistry. 2004;136:127-132.

     Not in our library10.1093/jb/mvh118

177. 177.

     Tanaka H, Ishikawa M, Kitamura S, Takahashi Y, Soyano T, Machida C, Machida Y. The AtNACK1HINKEL and STUDTETRASPOREAtNACK2 genes, which encode functionally redundant kinesins, are essential for cytokinesis in Arabidopsis. Genes to Cells. 2004;9:1199-1211.

     Not in our library10.1111/j.1365-2443.2004.00798.x

178. 178.

     Tanaka S, Tak YS, Araki H. The role of CDK in the initiation step of DNA replication in eukaryotes. Cell Division. 2007;2.

     Not in our library10.1186/1747-1028-2-16

179. 179.

     Tavoletti S. Cytological mechanisms of 2n egg formation in a diploid genotype of Medicago sativa subsp. falcata. Euphytica. 1994;75:1-8.

     Not in our library

180. 180.

     Tavoletti S, Mariani A, Veronesi F. Cytological analysis of macro- and microsporogenesis of a diploid alfalfa clone producing male and female 2n gametes. Crop Science. 1990;31:1258-1263.

     Not in our library

181. 181.

     Tavoletti S, Mariani A, Veronesi F. Phenotypic recurrent selection for 2n-pollen and 2n-egg production in diploid alfalfa. Euphytica. 1991;57:97-102.

     Not in our library

182. 182.

     Teoh SB. Polyploid spore formation in diploid orchid species. Genetica. 1984;63:53-59.

     Not in our library

183. 183.

     Thomson T, Lin HF. The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annual Review of Cell and Developmental Biology. 2009;25:355-376.

     Not in our library10.1146/annurev.cellbio.24.110707.175327

184. 184.

     Unhavaithaya Y, Hao Y, Beyret E, Yin H, Kuramochi-Miyagawa S, Nakano T, Lin HF. MILI, a PIWI-interacting RNA-binding protein, is required for germ line stem cell self-renewal and appears to positively regulate translation. Journal of Biological Chemistry. 2009;284:6507-6519.

     Not in our library10.1074/jbc.m809104200

185. 185.

     Van de Peer Y, Maere S, Meyer A. OPINION the evolutionary significance of ancient genome duplications. Nature Reviews Genetics. 2009;10:725-732.

     Not in our library10.1038/nrg2600

186. 186.

     Vanstraelen M, Baloban M, Da Ines O, Cultrone A, Lammens T, Boudolf V, Brown SC, De Veylder L, Mergaert P, Kondorosi E. APC/CCCS52A complexes control meristem maintenance in the Arabidopsis root. Proceedings of the National Academy of Sciences, USA. 2009;106:11806-11811.

     Not in our library10.1073/pnas.0901193106

187. 187.

     Veilleux R. Diploid and polyploid gametes in crop plants: mechanisms of formation and utilization in plant breeding. Plant Breeding Review. 1985;3:252-288.

     Not in our library

188. 188.

     Veilleux RE, Lauer FI. Variation for 2n pollen production in clones of Solanum phureja Juz and Buk. Theoretical and Applied Genetics. 1981;59:95-100.

     Not in our library10.1007/bf00285897

189. 189.

     Vijverberg K, Milanovic-Ivanovic S, Bakx-Schotman T, van Dijk PJ. Genetic fine-mapping of DIPLOSPOROUS in Taraxacum (dandelion; Asteraceae) indicates a duplicated DIP-gene. BMC Plant Biology. 2010;10:154.

     Not in our library10.1186/1471-2229-10-154

190. 190.

     Wagenaar EB. Meiotic restitution and the origin of polyploidy. II. Prolonged duration of metaphase I as causal factor of restitution induction. Canadian Journal of Genetics and Cytology. 1968;10:844-852.

     Not in our library

191. 191.

     Wang GF, Kong HZ, Sun YJ, Zhang XH, Zhang W, Altman N, dePamphilis CW, Ma H. Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins. Plant Physiology. 2004;135:1084-1099.

     Not in our library10.1104/pp.104.040436

192. 192.

     Watanabe K, Peloquin SJ. Cytological basis of 2n pollen formation in a wide-range of 2x, 4x, and 6x taxa from tuber-bearing Solanum species. Genome. 1993;36:8-13.

     Not in our library10.1139/g93-002

193. 193.

     Weinberg RA. The retinoblastoma protein and cell-cycle control. Cell. 1995;81:323-330.

     Not in our library10.1016/0092-8674(95)90385-2

194. 194.

     Wendel JF. Genome evolution in polyploids. Plant Molecular Biology. 2000;42:225-249.

     Not in our library

195. 195.

     Werner JE, Peloquin SJ. Inheritance and two mechanisms of 2n egg formation in 2x potatoes. Journal of Heredity. 1990;81:371-374.

     Not in our library

196. 196.

     Werner JE, Peloquin SJ. Occurrence and mechanisms of 2n egg formation in 2x potato. Genome. 1991;34:975-982.

     Not in our library

197. 197.

     Winkler H. Über die experimentelle Erzeugung von Pflanzen mit abweichenden Chromosomenzahlen. Zeitschrift für Botanik. 1916;8:417-531.

     Not in our library

198. 198.

     Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB, Rieseberg LH. The frequency of polyploid speciation in vascular plants. Proceedings of the National Academy of Sciences, USA. 2009;106:13875-13879.

     Not in our library10.1073/pnas.0811575106

199. 199.

     Xu SJ, Dong YS. Fertility and meiotic mechanisms of hybrids between chromosome autoduplication tetraploid wheats and Aegilops species. Genome. 1992;35:379-384.

     Not in our library

200. 200.

     Xu SJ, Joppa LR. First-division restitution in hybrids of Langdon durum disomic substitution lines with rye and Aegilops squarrosa. Plant Breeding. 2000;119:233-241.

     Not in our library

201. 201.

     Yang CY, Spielman M, Coles JP, Li Y, Ghelani S, Bourdon V, Brown RC, Lemmon BE, Scott RJ, Dickinson HG. TETRASPORE encodes a kinesin required for male meiotic cytokinesis in Arabidopsis. Plant Journal. 2003;34:229-240.

     Not in our library10.1046/j.1365-313x.2003.01713.x

202. 202.

     Yang KT, Li SK, Chang CC, Tang CJC, Lin YN, Lee SC, Tang TK. Aurora-C kinase deficiency causes cytokinesis failure in meiosis I and production of large polyploid oocytes in mice. Molecular Biology of the Cell. 2010;21:2371-2383.

     Not in our library10.1091/mbc.e10-02-0170

203. 203.

     Yoshikawa H, Morishima K, Fujimoto T, Saito T, Kobayashi T, Yamaha E, Arai K. Chromosome doubling in early spermatogonia produces diploid spermatozoa in a natural clonal fish. Biology of Reproduction. 2009;80:973-979.

     Not in our library10.1095/biolreprod.108.075150

204. 204.

     Zeng QN, Chen JG, Ellis BE. AtMPK4 is required for male-specific meiotic cytokinesis in Arabidopsis. Plant Journal. 2011;67:895-906.

     Not in our library10.1111/j.1365-313x.2011.04642.x

205. 205.

     Zhang HS, Postigo AA, Dean DC. Active transcriptional repression by the Rb-E2F complex mediates G1 arrest triggered by p16(INK4a), TGF beta, and contact inhibition. Cell. 1999;97:53-61.

     Not in our library10.1016/s0092-8674(00)80714-x

206. 206.

     Zhang JF, Wei ZZ, Li D, Li BL. Using SSR markers to study the mechanism of 2n pollen formation in Populus × euramericana (Dode) Guinier and P. × popularis. Annals of Forest Science. 2009;66:506.

     Not in our library

207. 207.

     Zhang LQ, Chen QJ, Yuan ZW, Xiang ZG, Zheng YL, Liu DC. Production of aneuhaploid and euhaploid sporocytes by meiotic restitution in fertile hybrids between durum wheat Langdon chromosome substitution lines and Aegilops tauschii. Journal of Genetics and Genomics. 2008;35:617-623.

     Not in our library10.1016/s1673-8527(08)60082-x

208. 208.

     Zhang LQ, Yen Y, Zheng YL, Liu DC. Meiotic restriction in emmer wheat is controlled by one or more nuclear genes that continue to function in derived lines. Sexual Plant Reproduction. 2007;20:159-166.

     Not in our library

209. 209.

     Zhang ZH, Kang XY. Cytological characteristics of numerically unreduced pollen production in Populus tomentosa Carr. Euphytica. 2010;173:151-159.

     Not in our library

210. 210.

     Zhou SJ, Ramanna MS, Visser RGF, van Tuyl JM. Analysis of the meiosis in the F(1) hybrids of Longiflorum × Asiatic (LA) of lilies (Lilium) using genomic in situ hybridization. Journal of Genetics and Genomics. 2008;35:687-695.

     Not in our library10.1016/s1673-8527(08)60091-0

Cited by papers we hold 6

• Homoeologous Exchanges, Segmental Allopolyploidy, and Polyploid Genome Evolution · 2020
  No notice
• The Rise of Apomixis in Natural Plant Populations · 2019
  Not checked
• Transient Activation of Apomixis in Sexual Neotriploids May Retain Genomically Altered States and Enhance Polyploid Establishment · 2018
  Not checked
• Comparative Genome Analysis Reveals Divergent Genome Size Evolution in a Carnivorous Plant Genus · 2015
  Not checked
• Tangled up in two: a burst of genome duplications at the end of the Cretaceous and the consequences for plant evolution · 2014
  No notice
• Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous–Paleogene boundary · 2014
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.