The OsIME4 gene identified as a key to meiosis initiation by RNA in situ hybridization. - OpacWWW

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Tytuł:: The OsIME4 gene identified as a key to meiosis initiation by RNA in situ hybridization.
Autorzy:: Zhou W; Crop Research Institute, Gansu Academy of Agricultural Sciences, Lanzhou, 730070, PR China.
Li Z; Department of Plant Genetics and Breeding, China Agricultural University, Beijing, 100094, PR China.
Zhang J; Crop Research Institute, Gansu Academy of Agricultural Sciences, Lanzhou, 730070, PR China.
Mou B; US Department of Agriculture, Agricultural Research Service, USDA-ARS), 1636 E. Alisal Street, Salinas, CA, 93905, USA.
Zhou W; Department of Plant Genetics and Breeding, China Agricultural University, Beijing, 100094, PR China.; US Department of Agriculture, Agricultural Research Service, USDA-ARS), 1636 E. Alisal Street, Salinas, CA, 93905, USA.
Źródło:: Plant biology (Stuttgart, Germany) [Plant Biol (Stuttg)] 2021 Sep; Vol. 23 (5), pp. 861-873. Date of Electronic Publication: 2021 Jun 25.
Typ publikacji:: Journal Article
Język:: English
Imprint Name(s):: Publication: Oxford, England : Wiley
Original Publication: Stuttgart : New York, NY : G. Thieme Verlag ; Thieme New York, c1999-
MeSH Terms:: Apomixis*
RNA*
In Situ Hybridization ; Meiosis ; Plant Breeding
References:: Agarwala S.D., Blitzblau H.G., Hochwagen A., Fink G.R. (2012) RNA methylation by the MIS complex regulates a cell fate decision in yeast. PLoS Genetics, 8, e1002732.
Altschul S.F., Koonin E.V. (1998) Iterated profile searches with PSI-BLAST - a tool for discovery in protein databases. Trends in Biochemical Sciences, 23, 444-447.
Anuradha S., Muniyappa K. (2005) Molecular aspects of meiotic chromosome synapsis and recombination. Progress in Nucleic Acid Research and Molecular Biology, 79, 49-132.
Bailey T.L., Boden M., Buske F.A., Frith M., Grant C.E., Clementi L., Ren J.Y., Li W.W., Noble W.S. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Research, 37, 202-208.
Bicknell R.A., Koltunow A.M. (2004) Understanding apomixis: recent advances and remaining conundrums. The Plant Cell, 16(suppl 1), S228-S245.
Bodi Z., Zhong S., Mehra S., Song J., Graham N., Li H., May S., Fray R.G. (2012) Adenosine methylation in Arabidopsis mRNA is associated with the 3' end and reduced levels cause developmental defects. Frontiers in Plant Science, 3, 48.
Bujnicki J.M., Feder M., Radlinska M., Blumenthal R.M. (2002) Structure prediction and phylogenetic analysis of a functionally diverse family of proteins homologous to the MT-A70 subunit of the human mRNA:m(6)A methyltransferase. Journal of Molecular Evolution, 55, 431-444.
Buonomo S.B., Clyne R.K., Fuchs J., Loidl J., Uhlmann F., Nasmyth K. (2000) Disjunction of homologous chromosomes in meiosis I depends on proteolytic cleavage of the meiotic cohesin Rec8 by separin. Cell, 103, 387-398.
Canaani D., Kahana C., Lavi S., Groner Y. (1979) Identification and mapping of N6-methyladenosine containing sequences in simian virus 40 RNA. Nucleic Acids Research., 6, 2879-2899.
Chen-Kiang S., Nevins J.R., Darnell J.E. (1979) N-6-methyl-adenosine in adenovirus type 2 nuclear RNA is conserved in the formation of messenger RNA. Journal of Molecular Biology., 135, 733-752.
Clancy M.J., Shambaugh M.E., Timpte C.S., Bokar J.A. (2002) Induction of sporulation in Saccharomyces cerevisiae leads to the formation of N6-methyladenosine in mRNA: a potential mechanism for the activity of the IME4 gene. Nucleic Acids Research., 30, 4509-4518.
Collins J.F., Coulson A.F.W., Lyall A. (1988) The significance of protein sequence similarities. Bioinformatics, 4, 67-71.
Cooper K.F., Mallory M.J., Egeland D.B., Jarnik M., Strich R. (2000) Ama1p is a meiosis-specific regulator of the anaphase promoting complex/cyclosome in yeast. Proceedings of the National Academy of Sciences, USA, 97, 14548-14553.
Cooper K.F., Strich R. (2011) Meiotic control of the APC/C: similarities and differences from mitosis. Cell Division, 6, 1-7.
Drinnenberg I.A., Weinberg D.E., Xie K.T., Mower J.P., Wolfe K.H., Fink G.R., Bartel D.P. (2009) RNAi in budding yeast. Science, 326, 544-550.
Fiaz S., Wang X., Younas A., Alharthi B., Riaz A., Ali H. (2021) Apomixis and strategies to induce apomixis to preserve hybrid vigor for multiple generations. GM Crops & Food, 12, 57-70.
Fülöp K., Tarayre S., Kelemen Z., Horváth G., Kevei Z., Nikovics K., Bakó L., Brown S., Kondorosi A., Kondorosi E. (2005) Arabidopsis anaphase-promoting complexes: multiple activators and wide range of substrates might keep APC perpetually busy. Cell Cycle, 4, 4084-4092.
Gelfand B., Mead J., Bruning A., Apostolopoulos N., Tadigotla V., Nagaraj V., Sengupta A.M., Vershon A.K. (2011) Regulated antisense transcription controls expression of cell-type-specific genes in yeast. Molecular and Cellular Biology, 31, 1701-1709.
Hand M.L., Koltunow A.M.G. (2014) The genetic control of apomixis: asexual seed formation. Genetics, 197, 441-450.
Hanson S.J., Wolfe K.H. (2017) An evolutionary perspective on yeast mating-type switching. Genetics, 206, 9-32.
Hashimoto S.I., Green M. (1976) Multiple methylated cap sequences in adenovirus type 2 early mRNA. Journal of Virology, 20, 425-435.
Hejátko J., Blilou I., Brewer P.B., Friml J., Scheres B., Benková E. (2006) In situ hybridization technique for mRNA detection in whole mount Arabidopsis samples. Nature Protocols, 1, 1939-1946.
Hiriart E., Verdel A. (2013) Long noncoding RNA-based chromatin control of germ cell differentiation: a yeast perspective. Chromosome Research, 21, 653-663.
Holm L.R., Thon G. (2012) New romance between RNA degradation pathways: Mmi1 and RNAi meet on heterochromatic islands. EMBO Journal, 31, 2242-2243.
Holt J.E., Stanger S.J., Nixon B., McLaughlin E.A. (2016) Non-coding RNA in spermatogenesis and epididymal maturation. Advances in Experimental Medicine & Biology, 886, 95-120.
Hongay C.F., Grisafi P.L., Galitski T., Fink G.R. (2006) Antisense transcription controls cell fate in Saccharomyces cerevisiae. Cell, 127, 735-745.
Hongay C.F., Orr-Weaver T.L. (2011) Drosophila Inducer of MEiosis 4 (IME4) is required for Notch signaling during oogenesis. Proceedings of the National Academy of Sciences, USA, 108, 14855-14860.
Ishiguro K.-I., Matsuura K., Tani N., Takeda N., Usuki S., Yamane M., Sugimoto M., Fujimura S., Hosokawa M., Chuma S., Ko M.S.H., Araki K., Niwa H. (2020) MEIOSIN directs the switch from mitosis to meiosis in mammalian germ cells. Developmental Cell, 52, 429-445.
Jin L., Lloyd R.V. (1997) In situ hybridization: methods and applications. Journal of Clinical Laboratory Analysis, 11, 2-9.
Jun-Ichi I., Ken-Ichi N., Kyoko I., Shinichiro Y., Yoshiaki I., Hiroshi Y., Hidemi K., Yasuo N. (2005) Rice plant development: from zygote to spikelet. Plant & Cell Physiology, 46, 23-47.
Kelley L.A., Mezulis S., Yates C.M., Wass M.N., Sternberg M.J. (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nature Protocols, 10, 845-858.
Kitajima T.S., Miyazaki Y., Yamamoto M., Watanabe Y. (2003) Rec8 cleavage by separase is required for meiotic nuclear divisions in fission yeast. EMBO Journal, 22, 5643-5653.
Klungland A., Dahl J.A., Greggains G., Fedorcsak P., Filipczyk A. (2016) Reversible RNA modifications in meiosis and pluripotency. Nature Methods, 14, 18-22.
Koltunow A.M., Grossniklaus U. (2003) Apomixis: a developmental perspective. Annual Review of Plant Biology, 54, 547-574.
Komiya R., Ohyanagi H., Niihama M., Watanabe T., Nakano M., Kurata N., Nonomura K. (2014) Rice germline-specific Argonaute MEL1 protein binds to phasiRNAs generated from more than 700 lincRNAs. The Plant Journal, 78, 385-397.
Kramer E.R., Scheuringer N., Podtelejnikov A.V., Mann M., Peters J.M. (2000) Mitotic regulation of the APC activator proteins CDC20 and CDH1. Molecular Biology of the Cell, 11, 1555-1569.
Lee J.H., Culver G., Carpenter S., Dobbs D. (2008) Analysis of the EIAV Rev-responsive element (RRE) reveals a conserved RNA motif required for high affinity Rev binding in both HIV-1 and EIAV. PLoS One, 3, e2272.
Lendvai A., Pettkó-Szandtner A., Csordás-Tóth E., Miskolczi P., Horváth G.V., Györgyey J., Dudits D. (2007) Dicot and monocot plants differ in retinoblastoma-related protein subfamilies. Journal of Experimental Botany, 58, 1663-1675.
Loidl J. (2016) Conservation and variability of meiosis across the eukaryotes. Annual Review of Genetics, 50, 293-316.
Marchler-Bauer A., Lu S., Anderson J.B., Chitsaz F., Derbyshire M.K., DeWeese-Scott C., Fong J.H., Geer L.Y., Geer R.C., Gonzales N.R., Gwadz M., Hurwitz D.I., Jackson J.D., Ke Z., Lanczycki C.J., Lu F., Marchler G.H., Mullokandov M., Omelchenko M.V., Robertson C.L., Song J.S., Thanki N., Yamashita R.A., Zhang D., Zhang N., Zheng C., Bryant S.H. (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Research, 39, 225-229.
Marimuthu M.P.A., Jolivet S., Ravi M., Pereira L., Davda J.N., Cromer L., Wang L., Nogue F., Chan S.W.L., Siddiqi I., Mercier R. (2011) Synthetic clonal reproduction through seeds. Science, 331, 876-876.
Mata A.T., Proença C., Ferreira A.R., Serralheiro M.L.M., Nogueira J.M.F., Araújo M.E.M. (2007) Antioxidant and antiacetylcholinesterase activities of five plants used as Portuguese food species. Food Chemistry, 103, 778-786.
Mathias J.R., Hanlon S.E., O'Flanagan R.A., Sengupta A.M., Vershon A.K. (2004) Repression of the yeast HO gene by the MATα2 and MATa1 homeodomain proteins. Nucleic Acids Research, 32, 6469-6478.
Matyskiela M.E., Morgan D.O. (2009) Analysis of activator-binding sites on the APC/C supports a cooperative substrate-binding mechanism. Molecular Cell, 34, 68-80.
Nonomura K.I., Eiguchi M., Nakano M., Takashima K., Komeda N., Fukuchi S., Miyazaki S., Miyao A., Hirochika H., Kurata N. (2011) A novel RNA-recognition-motif protein is required for premeiotic G1/S-phase transition in rice (Oryza sativa L.). PLoS Genetics, 7, e1001265.
Nonomura K., Miyoshi K., Eiguchi M., Suzuki T., Miyao A., Hirochika H., Kurata N. (2003) The MSP1 gene is necessary to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall formation in rice. The Plant Cell, 15, 1728-1739.
Oelschlaegel T., Schwickart M., Matos J., Bogdanova A., Camasses A., Havlis J., Shevchenko A., Zachariae W. (2005) The yeast APC/C subunit Mnd2 prevents premature sister chromatid separation triggered by the meiosis-specific APC/C-Ama1. Cell, 120, 773-788.
Ortet P., Bastien O. (2010) Where does the alignment score distribution shape come from? Evolutionary Bioinformatics (Online), 6, 159-187.
Otto S.P., Payseur B.A. (2019) Crossover interference: shedding light on the evolution of recombination. Annual Review of Genetics, 53, 19-44.
Pawlowski W.P., Sheehan M.J., Ronceret A. (2007) In the beginning: the initiation of meiosis. BioEssays, 29, 511-514.
Pesin J.A., Orr-Weaver T.L. (2008) Regulation of APC/C activators in mitosis and meiosis. Annual Review of Cell and Developmental Biology, 24, 475-499.
Sakakibara K., Ando S., Yip H.K., Tamada Y., Hiwatashi Y., Murata T., Deguchi H., Hasebe M., Bowman J.l. (2013) KNOX2 genes regulate the haploid-to-diploid morphological transition in land plants. Science, 339, 1067-1070.
Schwartz S., Agarwala S., Mumbach M., Jovanovic M., Mertins P., Shishkin A., Tabach Y., Mikkelsen T., Satija R., Ruvkun G., Carr S., Lander E., Fink G., Regev A. (2013) High-resolution mapping reveals a conserved, widespread, dynamic mRNA methylation program in yeast meiosis. Cell, 155, 1409-1421.
Schwartz S., Mumbach M.R., Jovanovic M., Wang T., Maciag K., Bushkin G.G., Mertins P., Ter-Ovanesyan D., Habib N., Cacchiarelli D., Sanjana N.E., Freinkman E., Pacold M.E., Satija R., Mikkelsen T.S., Hacohen N., Zhang F., Carr S.A., Lander E.S., Regev A. (2014) Perturbation of m6A writers reveals two distinct classes of mRNA methylation at internal and 5' sites. Cell Reports, 8, 284-296.
Shah J.C., Clancy M.J. (1992) IME4, a gene that mediates MAT and nutritional control of meiosis in Saccharomyces cerevisiae. Molecular and Cellular Biology, 12, 1078-1086.
Sheridan W.F., Avalkina N.A., Shamrov I.I., Batygina T.B., Golubovskaya I.N. (1996) The mac1 gene: controlling the commitment to the meiotic pathway in maize. Genetics, 142, 1009-1020.
Sheridan W.F., Golubeva E.A., Abrhamova L.I., Golubovskaya I.N. (1999) The mac1 mutation alters the developmental fate of the hypodermal cells and their cellular progeny in the maize anther. Genetics, 153, 933-941.
Smith T.F., Waterman M.S., Burks C. (1985) The statistical distribution of nucleic acid similarities. Nucleic Acids Research, 13, 645-656.
Tabach Y., Billi A.C., Hayes G.D., Newman M.A., Zuk O.R., Gabel H., Kamath R., Yacoby K., Chapman B., Garcia S.M., Borowsky M., Kim J.K., Ruvkun G. (2013) Identification of small RNA pathway genes using patterns of phylogenetic conservation and divergence. Nature, 493, 694-698.
Taylor W.R. (1986) The classification of amino acid conservation. Journal of Theoretical Biology., 119, 205-218.
Visintin R., Prinz S., Amon A. (1997) CDC20 and CDH1: a family of substrate-specific activators of APC-dependent proteolysis. Science, 278, 460-463.
Wang X., Feng J., Xue Y., Guan Z.Y., Zhang D.L., Liu Z., Gong Z., Wang Q., Huang J.B., Tang C., Zou T.T., Yin P. (2016) Structural basis of N6-adenosine methylation by the METTL3-METTL14 complex. Nature, 534, 575-578.
Wass M.N., Kelley L.A., Sternberg M.J. (2010) 3DLigandSite: predicting ligand-binding sites using similar structures. Nucleic Acids Research, 38, 469-473.
Wei C.M., Gershowitz A., Moss B. (1976) 5'-Terminal and internal methylated nucleotide sequences in HeLa cell mRNA. Biochemistry, 15, 397-401.
Wodniok S., Brinkmann H., Glöckner G., Heidel A.J., Philippe H., Melkonian M., Becker B. (2011) Origin of land plants: do conjugating green algae hold the key? BMC Evolutionary Biology, 11, 104.
Zhang B., Arun G., Mao Y.S., Lazar Z., Hung G., Bhattacharjee G., Xiao X.K., Booth C.J., Wu J., Zhang C.L., Spector D.L. (2012) The lncRNA Malat1 is dispensable for mouse development but its transcription plays a cis-regulatory role in the adult. Cell Reports, 2, 111-123.
Zheng G.Q., Dahl J.A., Niu Y.M., Fedorcsak P., Huang C.M., Li C.J., Vågbø C.B., Shi Y., Wang W.L., Song S.H., Lu Z.K., Bosmans R.P.G., Dai Q., Hao Y.J. Yang X., Zhao W.M., Tong W.M., Wang X.J., He C.(2013) ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility. Molecular Cell, 49, 18-29.
Zhong S., Li H., Bodi Z., Button J., Vespa L., Herzog M., Fray R.G. (2008) MTA is an Arabidopsis messenger RNA adenosine methylase and interacts with a homolog of a sex-specific splicing factor. The Plant Cell, 20, 1278-1288.
Grant Information:: 2020GAAS34 The Agricultural Science and Technology Innovation Program of Gansu Academy of Agricultural Sciences; 2020GAAS06 The Agricultural Science and Technology Innovation Program of Gansu Academy of Agricultural Sciences; 2019GAAS07 The Agricultural Science and Technology Innovation Program of Gansu Academy of Agricultural Sciences
Contributed Indexing:: Keywords: IME4; Meiosis; RNA in situ hybridization; antisense RNA transcript; rice
Substance Nomenclature:: 63231-63-0 (RNA)
Entry Date(s):: Date Created: 20210422 Date Completed: 20210831 Latest Revision: 20210831
Update Code:: 20240104
DOI:: 10.1111/plb.13274
PMID:: 33884735
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The formation of asexual seeds in plants holds great promise as a breeding system for one-line hybrid rice. Entry into meiosis is a key developmental decision in gametogenesis, especially in formation of asexual seeds in plants. Apomeiosis in MeMCs can be achieved by identifying and manipulating meiosis-specific genes. Using methods based on in situ hybridization and expression analysis, we identified OsIME4 (inducer of meiosis 4) sense and antisense transcripts involved in rice meiosis initiation, similar to initiation of meiosis in budding yeast. Our data suggest that the OsIME4 sense transcript, which encodes a putative mRNA N6-adenosine methyltransferase, keeps rice cells at mitosis stage through some form of epigenesis (DNA/RNA methylation), and the non-coding antisense transcript of OsIME4 converts the cell status from mitosis to meiosis by inhibiting expression (transcription and translation) of the sense transcript. We identified that the non-coding antisense transcript of OsIME4 converts archesporial cell status from mitosis to meiosis by inhibiting expression of the OsIME4 sense transcript in rice. Our results provide novel insights into meiosis initiation in rice and for engineering of apomixis in sexual crops by manipulating the OsIME4 sense and antisense transcripts, which has great promise for producing apomictic rice in the future.
(© 2021 German Society for Plant Sciences and The Royal Botanical Society of the Netherlands.)

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The OsIME4 gene identified as a key to meiosis initiation by RNA in situ hybridization.