A Germ Cell Specific Gene of the ARGONAUTE Family is Essential for the Progression of Premeiotic Mitosis and Meiosis During Sporogenesis in Rice

Overview

Journal Plant Cell

Publisher Oxford University Press

Specialties Biology
Cell Biology

Date 2007 Aug 7

PMID 17675402

Citations 181

Authors

Ken-Ichi Nonomura

Akane Morohoshi

Mutsuko Nakano

Mitsugu Eiguchi

Akio Miyao

Hirohiko Hirochika

Nori Kurata

Affiliations

Soon will be listed here.

Abstract

The rice (Oryza sativa) genome contains 18 copies of genes of the ARGONAUTE (AGO) family. Although AGO members play important roles in RNA-mediated silencing during plant development, a family member that is specifically involved in sexual reproduction has not been identified in plants. We identified the rice AGO gene MEIOSIS ARRESTED AT LEPTOTENE1 (MEL1) from the analysis of seed-sterile mutants. In the mel1 mutant, chromosome condensation was arrested at early meiotic stages and irregularly sized, multinucleated, and vacuolated pollen mother cells (PMCs) frequently appeared in developing anthers. In addition, histone H3 lysine-9 dimethylation of pericentromeres was rarely reduced and modification of the nucleolar-organizing region was altered in mel1 mutant PMCs. The mutation also affected female germ cell development. These results indicate that the germ cell-specific rice MEL1 gene regulates the cell division of premeiotic germ cells, the proper modification of meiotic chromosomes, and the faithful progression of meiosis, probably via small RNA-mediated gene silencing, but not the initiation and establishment of germ cells themselves.

Citing Articles

Recent Progress on Plant Apomixis for Genetic Improvement.

Xue L, Zhang Y, Wei F, Shi G, Tian B, Yuan Y Int J Mol Sci. 2024; 25(21).

PMID: 39518931 PMC: 11545481. DOI: 10.3390/ijms252111378.

The biogenesis, regulation and functions of transitive siRNA in plants.

Tan H, Liu Y, Guo H Acta Biochim Biophys Sin (Shanghai). 2024; 57(1):131-147.

PMID: 39376148 PMC: 11802348. DOI: 10.3724/abbs.2024160.

Hormonal influence on maize inflorescence development and reproduction.

Chaudhry A, Chen Z, Gallavotti A Plant Reprod. 2024; 37(4):393-407.

PMID: 39367960 PMC: 11511735. DOI: 10.1007/s00497-024-00510-0.

Genome-wide identification of gene families related to miRNA biogenesis in L. and their possible role during heat stress.

Lopez-Virgen A, Dautt-Castro M, Ulloa-Llanes L, Casas-Flores S, Contreras-Vergara C, Hernandez-Onate M PeerJ. 2024; 12:e17737.

PMID: 39035161 PMC: 11260077. DOI: 10.7717/peerj.17737.

Lectin Receptor-Like Protein Kinase OsNRFG6 is Required for Embryo Sac Development and Fertilization in Neo-Tetraploid Rice.

Zhao C, Li Q, Ge Q, Chen R, Yu H, Wu J Rice (N Y). 2024; 17(1):41.

PMID: 38916708 PMC: 11199475. DOI: 10.1186/s12284-024-00720-0.

References

Yamazaki M, Tsugawa H, Miyao A, Yano M, Wu J, Yamamoto S . The rice retrotransposon Tos17 prefers low-copy-number sequences as integration targets. Mol Genet Genomics. 2001; 265(2):336-44. DOI: 10.1007/s004380000421. View

Reiser L, Fischer R . The Ovule and the Embryo Sac. Plant Cell. 1993; 5(10):1291-1301. PMC: 160362. DOI: 10.1105/tpc.5.10.1291. View

Nonomura K, Miyoshi K, Eiguchi M, Suzuki T, Miyao A, Hirochika H . 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. Plant Cell. 2003; 15(8):1728-39. PMC: 167165. DOI: 10.1105/tpc.012401. View

Nishimura A, Ito M, Kamiya N, Sato Y, Matsuoka M . OsPNH1 regulates leaf development and maintenance of the shoot apical meristem in rice. Plant J. 2002; 30(2):189-201. DOI: 10.1046/j.1365-313x.2002.01279.x. View

Carmell M, Xuan Z, Zhang M, Hannon G . The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev. 2002; 16(21):2733-42. DOI: 10.1101/gad.1026102. View

Tsuji H, Aya K, Ueguchi-Tanaka M, Shimada Y, Nakazono M, Watanabe R . GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers. Plant J. 2006; 47(3):427-44. DOI: 10.1111/j.1365-313X.2006.02795.x. View

Nonomura K, Nakano M, Eiguchi M, Suzuki T, Kurata N . PAIR2 is essential for homologous chromosome synapsis in rice meiosis I. J Cell Sci. 2006; 119(Pt 2):217-25. DOI: 10.1242/jcs.02736. View

Saitou N, Nei M . The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987; 4(4):406-25. DOI: 10.1093/oxfordjournals.molbev.a040454. View

Lynn K, Fernandez A, Aida M, Sedbrook J, Tasaka M, Masson P . The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development. 1999; 126(3):469-81. DOI: 10.1242/dev.126.3.469. View

10.

Wu H, Cheun A . Programmed cell death in plant reproduction. Plant Mol Biol. 2001; 44(3):267-81. DOI: 10.1023/a:1026536324081. View

11.

Katz A, Oliva M, Mosquna A, Hakim O, Ohad N . FIE and CURLY LEAF polycomb proteins interact in the regulation of homeobox gene expression during sporophyte development. Plant J. 2004; 37(5):707-19. DOI: 10.1111/j.1365-313x.2003.01996.x. View

12.

Schiefthaler U, Balasubramanian S, Sieber P, Chevalier D, Wisman E, Schneitz K . Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1999; 96(20):11664-9. PMC: 18091. DOI: 10.1073/pnas.96.20.11664. View

13.

Volpe T, Kidner C, Hall I, Teng G, Grewal S, Martienssen R . Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science. 2002; 297(5588):1833-7. DOI: 10.1126/science.1074973. View

14.

Peragine A, Yoshikawa M, Wu G, Albrecht H, Poethig R . SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev. 2004; 18(19):2368-79. PMC: 522987. DOI: 10.1101/gad.1231804. View

15.

Kaneko M, Inukai Y, Ueguchi-Tanaka M, Itoh H, Izawa T, Kobayashi Y . Loss-of-function mutations of the rice GAMYB gene impair alpha-amylase expression in aleurone and flower development. Plant Cell. 2003; 16(1):33-44. PMC: 301393. DOI: 10.1105/tpc.017327. View

16.

Scott R, Spielman M, Dickinson H . Stamen structure and function. Plant Cell. 2004; 16 Suppl:S46-60. PMC: 2643399. DOI: 10.1105/tpc.017012. View

17.

Itoh J, Nonomura K, Ikeda K, Yamaki S, Inukai Y, Yamagishi H . Rice plant development: from zygote to spikelet. Plant Cell Physiol. 2005; 46(1):23-47. DOI: 10.1093/pcp/pci501. View

18.

Zhao D, Speal B, Ma H . The excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev. 2002; 16(15):2021-31. PMC: 186413. DOI: 10.1101/gad.997902. View

19.

Hirochika H, Sugimoto K, Otsuki Y, Tsugawa H, Kanda M . Retrotransposons of rice involved in mutations induced by tissue culture. Proc Natl Acad Sci U S A. 1996; 93(15):7783-8. PMC: 38825. DOI: 10.1073/pnas.93.15.7783. View

20.

Cox D, Chao A, Baker J, Chang L, Qiao D, Lin H . A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev. 1998; 12(23):3715-27. PMC: 317255. DOI: 10.1101/gad.12.23.3715. View