Gametocidal genes: from a discovery to the application in wheat breeding

. 2024 ; 15 () : 1396553. [epub] 20240422

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid38711610

Some species of the genus Aegilops, a wild relative of wheat, carry chromosomes that after introducing to wheat exhibit preferential transmission to progeny. Their selective retention is a result of the abortion of gametes lacking them due to induced chromosomal aberrations. These chromosomes are termed Gametocidal (Gc) and, based on their effects, they are categorized into three types: mild, intense or severe, and very strong. Gc elements within the same homoeologous chromosome groups of Aegilops (II, III, or IV) demonstrate similar Gc action. This review explores the intriguing dynamics of Gc chromosomes and encompasses comprehensive insights into their source species, behavioral aspects, mode of action, interactions, suppressions, and practical applications of the Gc system in wheat breeding. By delving into these areas, this work aims to contribute to the development of novel plant genetic resources for wheat breeding. The insights provided herein shed light on the utilization of Gc chromosomes to produce chromosomal rearrangements in wheat and its wild relatives, thereby facilitating the generation of chromosome deletions, translocations, and telosomic lines. The Gc approach has significantly advanced various aspects of wheat genetics, including the introgression of novel genes and alleles, molecular markers and gene mapping, and the exploration of homoeologous relationships within Triticeae species. The mystery lies in why gametes possessing Gc genes maintain their normality while those lacking Gc genes suffer abnormalities, highlighting an unresolved research gap necessitating deeper investigation.

Zobrazit více v PubMed

Aldrich J. C., Leibholz A., Cheema M. S., Ausiό J., Ferree P. M. (2017). A “selfish” B chromosome induces genome elimination by disrupting the histone code in the jewel wasp Nasonia vitripennis. Sci. Rep. 7, 42551. doi:  10.1038/srep42551 PubMed DOI PMC

Ashida T., Nasuda S., Sato K., Endo T. R. (2007). Dissection of barley chromosome 5H in common wheat. Genes Genet. Syst. 82, 123–133. doi:  10.1266/ggs.82.123 PubMed DOI

Badaeva E. D., Amosova A. V., Samatadze T. E., Zoshchuk S. A., Shostak N. G., Chikida N. N., et al. (2004). Genome differentiation in DOI

Badaeva E. D., Friebe B., Gill B. S. (1996). Genome differentiation in PubMed DOI

Blavet N., Yang H., Su H., Solanský P., Douglas R. N., Karafiátová M., et al. (2021). Sequence of the supernumerary B chromosome of maize provides insight into its drive mechanism and evolution. PNAS 118, 1–11. doi:  10.1073/pnas.2104254118 PubMed DOI PMC

Boehm J., Cai X. (2024). Enrichment and diversification of the wheat genome via alien introgression. Plants 13, 339. doi:  10.3390/plants13030339 PubMed DOI PMC

Cameron D. R., Moav R. M. (1957). Inheritance in PubMed DOI PMC

Chen P., Liu W., Yuan J., Wang X., Zhou B., Wang S., et al. (2005). Development and characterization of wheat- PubMed DOI

Chen Q., Cao A., Qi Z., Zhang W., Chen P. (2008). Structural Changes of 2V Chromosome of PubMed DOI

Cherif-Mouaki S., Said M., Alvarez J. B., Cabrera A. (2011). Sub-arm location of prolamin and EST-SSR loci on chromosome 1H(ch) from DOI

Copete-Parada A., Palomino C., Cabrera A. (2021). Development and characterization of wheat- DOI

Crow J. F. (1983). Hybrid dysgenesis and the P factor in Drosophila. Japanese J. Genet. 58, 621–625. doi:  10.1266/jjg.58.621 DOI

de Las Heras J. I., King I. P., Parker J. S. (2001). 5-azacytidine induces chromosomal breakage in the root tips of wheat carrying the cuckoo chromosome 4SL from PubMed DOI

Durante M., Formenti S. C. (2018). Radiation-induced chromosomal aberrations and immunotherapy: micronuclei, cytosolic DNA, and interferon-production pathway. Front. Oncol. 8. doi:  10.3389/fonc.2018.00192 PubMed DOI PMC

Endo T. R. (1979). Selective gametocidal action of a chromosome of

Endo T. R. (1982). Gametocidal chromosomes of three DOI

Endo T. R. (1985). Two types of gametocidal chromosome of DOI

Endo T. R. (1988. a). “Chromosome mutations induced by gametocidal chromosomes in common wheat,” in Proceedings of the seventh international wheat genetics symposium, Cambridge, UK, 13-19 July 1988, CABI Digital Library. 259–265.

Endo T. R. (1988. b). Induction of chromosomal structural changes by a chromosome of PubMed DOI

Endo T. R. (1990). Gametocidal chromosomes and their induction of chromosome mutations in wheat. Japanese J. Genet. 65, 135–152. doi:  10.1266/jjg.65.135 DOI

Endo T. R. (2007). The gametocidal chromosome as a tool for chromosome manipulation in wheat. Chromosome Res. 15, 67–75. doi:  10.1007/s10577-006-1100-3 PubMed DOI

Endo T. R. (2015). “Gametocidal Genes,” in Alien Introgression in Wheat: Cytogenetics, Molecular Biology, and Genomics. Eds. Molnár-Láng M., Ceoloni C., Doležel J. (Springer International Publishing, Cham: ), 121–131. doi:  10.1007/978-3-319-23494-6_5 DOI

Endo T. R., Gill B. S. (1996). The deletion stocks of common wheat. J. Heredity 87, 295–307. doi:  10.1093/oxfordjournals.jhered.a023003 DOI

Endo T. R., Katayama Y. (1978). Finding of a selectively retained chromosome of

Endo T. R., Tsunewaki K. (1975). Sterility of common wheat with DOI

Farkas A., Gaál E., Ivanizs L., Blavet N., Said M., Holušová K., et al. (2023). Chromosome genomics facilitates the marker development and selection of wheat- PubMed DOI PMC

Feldman M. (1979). “New evidence on the origin of the B genome of wheat,” in Proceedings of the Fifth International Wheat Genetics Symposium, New Delhi, India: Indian Society of Genetics & Plant Breeding, February 23-28, 1978. 120–132.

Finch R. A., Miller T. E., Bennett M. D. (1984). “Cuckoo” DOI

Friebe B., Kynast R. G., Gill B. S. (2000). Gametocidal factor-induced structural rearrangements in rye chromosomes added to common wheat. Chromosome Res. 8, 501–511. doi:  10.1023/A:1009219722418 PubMed DOI

Friebe B., Schubert V., Blüthner W. D., Hammer K. (1992). C-banding pattern and polymorphism of PubMed DOI

Friebe B. R., Tuleen N. A., Gill B. S. (1999). Development and identification of a complete set of DOI

Friebe B., Zhang P., Gill B. S., Nasuda S. (2003). Characterization of a knock-out mutation at the PubMed DOI

Gill K. S., Gill B. S., Endo T. R., Boyko E. V. (1996). Identification and high-density mapping of gene-rich regions in chromosome group 5 of wheat. Genetics 143, 1001–1012. doi:  10.1093/genetics/143.2.1001 PubMed DOI PMC

Guo W., Comai L., Henry I. M. (2021). Chromoanagenesis from radiation-induced genome damage in PubMed DOI PMC

Haapaniemi E., Botla S., Persson J., Schmierer B., Taipale J. (2018). CRISPR–Cas9 genome editing induces a p53-mediated DNA damage response. Nat. Med. 24, 927–930. doi:  10.1038/s41591-018-0049-z PubMed DOI

Hajjar R., Hodgkin T. (2007). The use of wild relatives in crop improvement: a survey of developments over the last 20 years. Euphytica 156, 1–13. doi:  10.1007/s10681-007-9363-0 DOI

Han H., Bai L., Su J., Zhang J., Song L., Gao A., et al. (2014). Genetic rearrangements of six wheat– PubMed DOI PMC

Houben A. (2017). B chromosomes – A matter of chromosome drive. Front. Plant Sci. 8. doi:  10.3389/fpls.2017.00210 PubMed DOI PMC

Ishihara A., Mizuno N., Islam R. A. K. M., Doležel J., Endo T. R., Nasuda S. (2014). Dissection of barley chromosomes 1H and 6H by the gametocidal system. Genes Genet. Syst. 89, 203–214. doi:  10.1266/ggs.89.203 PubMed DOI

Jones R. N. (1995). B chromosomes in plants. NewPhytol 131, 411–434. doi:  10.1111/j.1469-8137.1995.tb03079.x PubMed DOI

Jones N., Houben A. (2003). B chromosomes in plants: escapees from the A chromosome genome? Trends Plant Sci. 8, 417–423. doi:  10.1016/S1360-1385(03)00187-0 PubMed DOI

Jones R. N., Viegas W., Houben A. (2008). A century of B chromosomes in plants: so what? Ann. Bot. 101, 767–775. doi:  10.1093/aob/mcm167 PubMed DOI PMC

Karafiátová M., Bednářová M., Said M., Čížková J., Holušová K., Blavet N., et al. (2021). The B chromosome of PubMed DOI PMC

Kibirige-Sebunya I., Knott D. R. (1983). Transfer of stem rust resistance to wheat from an DOI

Kidwell M. G. (1983). Evolution of hybrid dysgenesis determinants in PubMed DOI PMC

Kihara H. (1959). Fertility and morphological variation in the substitution backcrosses of the hybrid

Kim S. H., Kim S. W., Ryu J., Kang S.-Y., Kang B.-C., Kim J.-B. (2020). Dark/light treatments followed by γ-irradiation increase the frequency of leaf-color mutants in cymbidium. Plants 9, 532. doi:  10.3390/plants9040532 PubMed DOI PMC

Kim Y. J., Lee J. W., Cho Y. H., Choi Y. J., Lee Y., Chung H. W. (2022). Chromosome damage in relation to recent radiation exposure and radiation quality in nuclear power plant workers. Toxics 10, 94. doi:  10.3390/toxics10020094 PubMed DOI PMC

King J., Grewal S., Yang C.-Y., Hubbart S., Scholefield D., Ashling S., et al. (2017). A step change in the transfer of interspecific variation into wheat from PubMed DOI PMC

King J., Grewal S., Yang C., Hubbart Edwards S., Scholefield D., Ashling S., et al. (2018). Introgression of PubMed DOI PMC

King I. P., Koebner R. M. D., Schlegel R., Reader S. M., Miller T. E., Law C. N. (1991. a). Exploitation of a preferentially transmitted chromosome from DOI

King I. P., Laurie D. A. (1993). Chromosome damage in early embryo and endosperm development in crosses involving the preferentially transmitted 4S1 chromosome of DOI

King I. P., Miller T. E., Koebner R. M. D. (1991. b). Determination of the transmission frequency of chromosome 4S (l) of PubMed DOI

Kishii M. (2019). An update of recent use of PubMed DOI PMC

Knight E., Binnie A., Draeger T., Moscou M., Rey M.-D., Sucher J., et al. (2015). Mapping the ‘breaker’ element of the gametocidal locus proximal to a block of sub-telomeric heterochromatin on the long arm of chromosome 4Ssh of PubMed DOI PMC

Kosicki M., Tomberg K., Bradley A. (2018). Repair of double-strand breaks induced by CRISPR–Cas9 leads to large deletions and complex rearrangements. Nat. Biotechnol. 36, 765–771. doi:  10.1038/nbt.4192 PubMed DOI PMC

Kota R. S., Dvorak J. (1988). Genomic instability in wheat induced by chromosome 6b(s) of PubMed DOI PMC

Kwiatek M., Majka M., Ślusarkiewicz-Jarzina A., Ponitka A., Pudelska H., Belter J., et al. (2016). Transmission of the PubMed DOI PMC

Kwiatek M. T., Wiśniewska H., Ślusarkiewicz-Jarzina A., Majka J., Majka M., Belter J., et al. (2017). Gametocidal factor transferred from Aegilops geniculata Roth can be adapted for large-scale chromosome manipulations in cereals. Front. Plant Sci. 8. doi:  10.3389/fpls.2017.00409 PubMed DOI PMC

Kynast R. G., Friebe B., Gill B. S. (2000). Fate of multicentric and ring chromosomes induced by a new gametocidal factor located on chromosome 4Mg of PubMed DOI

Lapitan N. L. V., Sears R. G., Gill B. S. (1984). Translocations and other karyotypic structural changes in wheat x rye hybrids regenerated from tissue culture. Theoret. Appl. Genet. 68, 547–554. doi:  10.1007/BF00285012 PubMed DOI

Li H.-J., Guo B.-H., Li Y.-W., Du L.-Q., Jia X., Chu C.-C. (2000). Molecular cytogenetic analysis of intergeneric chromosomal translocations between wheat ( PubMed DOI

Liu C., Guo W., Wang Y., Fu B., Doležel J., Liu Y., et al. (2023). Introgression of sharp eyespot resistance from DOI

Liu W.-H., Luan Y., Wang J.-C., Wang X.-G., Su J.-J., Zhang J.-P., et al. (2010). Production and identification of wheat – PubMed DOI

Loegering W. Q., Sears E. R. (1963). Distorted inheritance of stem-rust resistance of timstein wheat caused by a pollen-killing gene. Can. J. Genet. Cytol. 5, 65–72. doi:  10.1139/g63-010 DOI

Luan Y., Wang X., Liu W., Li C., Zhang J., Gao A., et al. (2010). Production and identification of wheat- PubMed DOI

Lyttle T. W. (1993). Cheaters sometimes prosper: distortion of mendelian segregation by meiotic drive. Trends Genet. 9, 205–210. doi:  10.1016/0168-9525(93)90120-7 PubMed DOI

Ma W., Gabriel T. S., Martis M. M., Gursinsky T., Schubert V., Vrána J., et al. (2017). Rye B chromosomes encode a functional Argonaute-like protein with PubMed DOI

Maan S. S. (1975). Exclusive preferential transmission of an alien chromosome in common wheat. Crop Sci. 15, cropsci1975.0011183X001500030002x. doi:  10.2135/cropsci1975.0011183X001500030002x DOI

Manabe M., Ino T., Kasaya M., Takumi S., Mori N., Ohtsuka I., et al. (1999). Segregation distortion through female gametophytes in interspecific hybrids of tetraploid wheat as revealed by RAPD analysis. Hereditas 131, 47–53. doi:  10.1111/j.1601-5223.1999.00047.x DOI

Marais G. F., Pretorius Z. A. (1996). Gametocidal effects and resistance to wheat leaf rust and stem rust in derivatives of a DOI

Masoudi-Nejad A., Nasuda S., Bihoreau M.-T., Waugh R., Endo T. R. (2005). An alternative to radiation hybrid mapping for large-scale genome analysis in barley. Mol. Genet. Genomics 274, 589–594. doi:  10.1007/s00438-005-0052-1 PubMed DOI

Mattera M. G., Ávila C. M., Atienza S. G., Cabrera A. (2015). Cytological and molecular characterization of wheat- DOI

McClintock B. (1941). The stability of broken ends of chromosomes in PubMed DOI PMC

Miller T. E., Hutchinson J., Chapman V. (1982). Investigation of a preferentially transmitted PubMed DOI

Moav J., Moav R., Zohary D. (1968). Spontaneous morphological alterations of chromosomes in PubMed DOI PMC

Molnár I., Benavente E., Molnár-Láng M. (2009). Detection of intergenomic chromosome rearrangements in irradiated PubMed DOI

Molnár I., Cifuentes M., Schneider A., Benavente E., Molnár-Láng M. (2011). Association between simple sequence repeat-rich chromosome regions and intergenomic translocation breakpoints in natural populations of allopolyploid wild wheats. Ann. Bot. 107, 65–76. doi:  10.1093/aob/mcq215 PubMed DOI PMC

Molnár I., Vrána J., Burešová V., Cápal P., Farkas A., Darkó É., et al. (2016). Dissecting the U, M, S and C genomes of wild relatives of bread wheat ( PubMed DOI

Molnár-Láng M., Novotny C., Linc G., Naoy E. D. (2005). Changes in the meiotic pairing behaviour of a winter wheat-winter barley hybrid maintained for a long term in tissue culture, and tracing the barley chromatin in the progeny using GISH and SSR markers. Plant Breed. 124, 247–252. doi:  10.1111/j.1439-0523.2005.01097.x DOI

Nasuda S., Friebe B., Gill B. S. (1998). Gametocidal genes induce chromosome breakage in the interphase prior to the first mitotic cell division of the male gametophyte in wheat. Genetics 149, 1115–1124. doi:  10.1093/genetics/149.2.1115 PubMed DOI PMC

Nasuda S., Kikkawa Y., Ashida T., Islam A. K. M. R., Sato K., Endo T. R. (2005). Chromosomal assignment and deletion mapping of barley EST markers. Genes Genet. Syst. 80, 357–366. doi:  10.1266/ggs.80.357 PubMed DOI

Niranjana M. (2017). Gametocidal genes of PubMed DOI

Niranjana M., Vinod, Sharma J. B., Mallick N., Tomar S. M. S., Jha S. K. (2017). Cytogenetic analysis and mapping of leaf rust resistance in PubMed DOI

Nomura T., Ishihara A., Imaishi H., Ohkawa H., Endo T. R., Iwamura H. (2003). Rearrangement of the genes for the biosynthesis of benzoxazinones in the evolution of Triticeae species. Planta 217, 776–782. doi:  10.1007/s00425-003-1040-5 PubMed DOI

Ochoa V., Madrid E., Said M., Rubiales D., Cabrera A. (2015). Molecular and cytogenetic characterization of a common wheat- DOI

Palomino C., Cabrera A. (2019). Development of wheat— DOI

Qi L., Echalier B., Friebe B., Gill B. S. (2003). Molecular characterization of a set of wheat deletion stocks for use in chromosome bin mapping of ESTs. Funct. Integr. Genomics 3, 39–55. doi:  10.1007/s10142-002-0063-5 PubMed DOI

Qi L., Friebe B., Zhang P., Gill B. S. (2007). Homoeologous recombination, chromosome engineering and crop improvement. Chromosome Res. 15, 3–19. doi:  10.1007/s10577-006-1108-8 PubMed DOI

Rick C. M. (1966). Abortion of male and female gametes in the tomato determined by allelic interaction. Genetics 53, 85–96. doi:  10.1093/genetics/53.1.85 PubMed DOI PMC

Said M., Cabrera A. (2009). A physical map of chromosome 4Hch from DOI

Said M., Holušová K., Farkas A., Ivanizs L., Gaál E., Cápal P., et al. (2021). Development of DNA Markers From Physically Mapped Loci in PubMed DOI PMC

Said M., Kubaláková M., Karafiátová M., Molnár I., Doležel J., Vrána J. (2019. a). Dissecting the complex genome of crested wheatgrass by chromosome flow sorting. Plant Genome 12, 180096. doi:  10.3835/plantgenome2018.12.0096 PubMed DOI

Said M., Parada A. C., Gaál E., Molnár I., Cabrera A., Doležel J., et al. (2019. b). Uncovering homeologous relationships between tetraploid PubMed DOI PMC

Said M., Recio R., Cabrera A. (2012). Development and characterisation of structural changes in chromosome 3Hch from DOI

Sakai K., Nasuda S., Sato K., Endo T. R. (2009). Dissection of barley chromosome 3H in common wheat and a comparison of 3H physical and genetic maps. Genes Genet. Syst. 84, 25–34. doi:  10.1266/ggs.84.25 PubMed DOI

Sakata M., Nasuda S., Endo T. R. (2010). Dissection of barley chromosome 4H in common wheat by the gametocidal system and cytological mapping of chromosome 4H with EST markers. Genes Genet. Syst. 85, 19–29. doi:  10.1266/ggs.85.19 PubMed DOI

Sandler L., Hiraizumi Y., Sandler I. (1959). Meiotic drive in natural populations of PubMed DOI PMC

Sandler L., Novitski E. (1957). Meiotic drive as an evolutionary force. Am. Nat. 91, 105–110. doi:  10.1086/281969 DOI

Sano Y. (1990). The genic nature of gamete eliminator in rice. Genetics 125, 183–191. doi:  10.1093/genetics/125.1.183 PubMed DOI PMC

Schmidt C., Schindele P., Puchta H. (2020). From gene editing to genome engineering: restructuring plant chromosomes via CRISPR/Cas. aBIOTECH 1, 21–31. doi:  10.1007/s42994-019-00002-0 PubMed DOI PMC

Schubert I., Pecinka A., Meister A., Schubert V., Klatte M., Jovtchev G. (2004). DNA damage processing and aberration formation in plants. Cytogenetic Genome Res. 104, 104–108. doi:  10.1159/000077473 PubMed DOI

Serizawa N., Nasuda S., Shi F., Endo T. R., Prodanovic S., Schubert I., et al. (2001). Deletion-based physical mapping of barley chromosome 7H. Theor. Appl. Genet. 103, 827–834. doi:  10.1007/s001220100703 DOI

Serra H., Svačina R., Baumann U., Whitford R., Sutton T., Bartoš J., et al. (2021). PubMed DOI PMC

Shi F., Endo T. R. (1999). Genetic induction of structural changes in barley chromosomes added to common wheat by a gametocidal chromosome derived from DOI

Silver L. M. (1985). MOUSE tau HAPLOTYPES. Annu. Rev. Genet. 19, 179–208. doi:  10.1146/annurev.ge.19.120185.001143 PubMed DOI

Silver L. M. (1993). The peculiar journey of a selfish chromosome: mouse PubMed DOI

Svačina R., Karafiátová M., Malurová M., Serra H., Vítek D., Endo T. R., et al. (2020). Development of deletion lines for chromosome 3D of bread wheat. Front. Plant Sci. 10. doi:  10.3389/fpls.2019.01756 PubMed DOI PMC

Symington L. S. (2016). Mechanism and regulation of DNA end resection in eukaryotes. Crit. Rev. Biochem. Mol. Biol. 51, 195–212. doi:  10.3109/10409238.2016.1172552 PubMed DOI PMC

Szakács E., Molnár-Láng M. (2010). Molecular cytogenetic evaluation of chromosome instability in PubMed DOI

Taketa S., Kato J., Takeda K. (1995). High crossability of wild barley ( PubMed DOI

Tsujimoto H. (1995). Gametocidal genes in wheat and its relatives. IV. Functional relationships between six gametocidal genes. Genome 38, 283–289. doi:  10.1139/g95-035 PubMed DOI

Tsujimoto H. (2005). Gametocidal genes in wheat as the inducer of chromosome breakage. Wheat Inf Serv. 100, 33–48.

Tsujimoto H., Noda K. (1989). Structure of chromosome 5A of wheat speltoid mutants induced by the gametocidal genes of DOI

Tsujimoto H., Noda K. (1990). Deletion mapping by gametocidal genes in common wheat: position of speltoid suppression ( DOI

Tsujimoto H., Tsunewaki K. (1984). Gametocidal genes in wheat and its relatives. I. Genetic analyses in common wheat of a gametocidal gene derived from DOI

Tsujimoto H., Tsunewaki K. (1985. a). Gametocidal genes in wheat and its relatives. II. Suppressor of the chromosome 3C gametocidal gene of DOI

Tsujimoto H., Tsunewaki K. (1985. b). Hybrid dysgenesis in common wheat caused by gametocidal genes. Japanese J. Genet. 60, 565–578. doi:  10.1266/jjg.60.565 DOI

Tsujimoto H., Tsunewaki K. (1988). Gametocidal genes in wheat and its relatives. III. Chromosome location and effects of two DOI

Tsujimoto H., Yamada T., Sasakuma T. (1997). Molecular structure of a wheat chromosome end healed after gametocidal gene-induced breakage. Proc. Natl. Acad. Sci. 94, 3140–3144. doi:  10.1073/pnas.94.7.3140 PubMed DOI PMC

Tsunewaki K. (2015). “Prof. H. Kihara’s Genome Concept and Advancements in Wheat Cytogenetics in His School,” in Advances in Wheat Genetics: From Genome to Field. Eds. Ogihara Y., Takumi S., Handa H. (Springer Japan, Tokyo: ), 3–11. doi:  10.1007/978-4-431-55675-6_1 DOI

Türkösi E., Ivanizs L., Farkas A., Gaál E., Kruppa K., Kovács P., et al. (2022). Transfer of the PubMed DOI PMC

Türkösi E., Szakács É., Ivanizs L., Farkas A., Gaál E., Said M., et al. (2024). A chromosome arm from PubMed DOI PMC

Werner J. E., Kota R. S., Gill B. S., Endo T. R. (1992). Distribution of telomeric repeats and their role in the healing of broken chromosome ends in wheat. Genome 35, 844–848. doi:  10.1139/g92-128 DOI

Yamano S., Nitta M., Tsujimoto H., Ishikawa G., Nakamura T., Endo T. R., et al. (2010). Molecular mapping of the suppressor gene PubMed DOI

Zhang H.-B., Dvořák J. (1990). Characterization and distribution of an interspersed repeated nucleotide sequence from PubMed DOI

Zhang R., Sun B., Chen J., Cao A., Xing L., Feng Y., et al. (2016). PubMed DOI

Zuo E., Huo X., Yao X., Hu X., Sun Y., Yin J., et al. (2017). CRISPR/Cas9-mediated targeted chromosome elimination. Genome Biol. 18, 224. doi:  10.1186/s13059-017-1354-4 PubMed DOI PMC

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...