Skip to main content
Log in

Loss of function of Oryza sativa Argonaute 18 induces male sterility and reduction in phased small RNAs

  • Original Article
  • Published:
Plant Reproduction Aims and scope Submit manuscript

Key message

In this manuscript, we show that Oryza sativa indica Argonaute protein AGO18 is required for male gametophyte development likely to through a small RNA-mediated mechanism.

Abstract

Monocots have evolved unique gene silencing pathways due to the presence of unique members of Dicer-like and Argonaute (AGO) family members. Among the monocot AGO homologs, AGO18 occupies a unique position. Previous reports have implicated this protein in viral resistance as well as in gametogenesis, likely through its competition with AGO1 clade members for micro(mi)RNAs and other small (s)RNAs. Although expression of rice AGO18 in specific stages of male gametogenesis has been documented, its major functions in plant development remain poorly understood. Here, we show that Oryza sativa indica AGO18 is involved in male gametophyte development. Knockdown (KD) of AGO18 in transgenic rice lines resulted in stunted plants that are male sterile, whereas their carpels were functional. Transcriptome analysis revealed downregulation of several pollen development-associated genes in KD lines. sRNA sequencing in vegetative and reproductive tissues of KD lines indicated reduction of miRNAs and phased secondary sRNAs implicated in male gametophyte development. Our results indicate a distinct role for rice AGO18 in male fertility.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adam H, Marguerettaz M, Qadri R, Adroher B, Richaud F, Collin M, Thuillet AC, Vigouroux Y, Laufs P, Tregear JW, Jouannic S (2011) Divergent expression patterns of miR164 and CUP-SHAPED COTYLEDON genes in palms and other monocots: Implication for the evolution of meristem function in angiosperms. Mol Biol Evol 28:1439–1454

    CAS  PubMed  Google Scholar 

  • Arikit S, Zhai J, Meyers BC (2013) Biogenesis and function of rice small RNAs from non-coding RNA precursors. Curr Opin Plant Biol 16:170–179

    CAS  PubMed  Google Scholar 

  • Axtell MJ (2013) ShortStack: comprehensive annotation and quantification of small RNA genes. RNA 19:740–751

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363

    CAS  PubMed  Google Scholar 

  • Bian H, Xie Y, Guo F, Han N, Ma S, Zeng Z, Wang J, Yang Y, Zhu M (2012) Distinctive expression patterns and roles of the miRNA393/TIR1 homolog module in regulating flag leaf inclination and primary and crown root growth in rice (Oryza sativa). New Phytol 196:149–161

    CAS  PubMed  Google Scholar 

  • Bologna NG, Voinnet O (2014) The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annu Rev Plant Biol 65:473–503

    CAS  PubMed  Google Scholar 

  • Bonnet E, He Y, Billiau K, Van de Peer Y (2010) TAPIR, a web server for the prediction of plant microRNA targets, including target mimics. Bioinformatics 26:1566–1568

    CAS  PubMed  Google Scholar 

  • Borges F, Pereira PA, Slotkin RK, Martienssen RA, Becker JD (2011) MicroRNA activity in the Arabidopsis male germline. J Exp Bot 62:1611–1620

    CAS  PubMed  PubMed Central  Google Scholar 

  • Canales C, Bhatt AM, Scott R, Dickinson H (2002) EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr Biol 12:1718–1727

    CAS  PubMed  Google Scholar 

  • Cao P, Jung KH, Choi D, Hwang D, Zhu J, Ronald PC (2012) The rice oligonucleotide array database: an atlas of rice gene expression. Rice 5:17

    PubMed  PubMed Central  Google Scholar 

  • Chen L, Liu Y-G (2014) Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65:579–606

    CAS  PubMed  Google Scholar 

  • Du P, Wu J, Zhang J, Zhao S, Zheng H, Gao G, Wei L, Li Y (2011) Viral infection induces expression of novel phased microRNAs from conserved cellular microRNA precursors. PLoS Pathog 7(8):e1002176

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, Alexander AL, Carrington JC (2006) Regulation of AUXIN RESPONSE FACTOR 3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 16:939–944

    CAS  PubMed  Google Scholar 

  • Fang X, Qi Y (2016) RNAi in plants: an argonaute-centered view. Plant Cell 28:272–285

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fei Q, Yang L, Liang W, Zhang D, Meyers BC (2016) Dynamic changes of small RNAs in rice spikelet development reveal specialized reproductive phasiRNA pathways. J Exp Bot 67:6037–6049

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fujioka T, Kaneko F, Kazama T, Suwabe K, Suzuki G, Makino A, Mae T, Endo M, Kawagishi-Kobayashi M, Watanabe M (2008) Identification of small RNAs in late developmental stage of rice anthers. Genes Genet Syst 83:281–284

    CAS  PubMed  Google Scholar 

  • García-Pérez RD, Houdt HV, Depicker A (2004) Spreading of post-transcriptional gene silencing along the target gene promotes systemic silencing. Plant J 38:594–602

    PubMed  Google Scholar 

  • Gillmor CS, Silva-Ortega CO, Willmann MR, Buendia-Monreal M, Poethig RS (2014) The Arabidopsis Mediator CDK8 module genes CCT (MED12) and GCT (MED13) are global regulators of developmental phase transitions. Development 141:4580–4589

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guo JX, Liu YG (2012) Molecular control of male reproductive development and pollen fertility in rice. J Integr Plant Biol 54:967–978

    CAS  PubMed  Google Scholar 

  • Hiei Y, Komari T, Kubo T (1997) Transformation of rice mediated by Agrobacterium tumefaciens. Plant Mol Biol 35:205–218

    CAS  PubMed  Google Scholar 

  • Itoh JI, Nonomura KI, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, Kitano H, Nagato Y (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol 46:23–47

    CAS  PubMed  Google Scholar 

  • Jeong D-H, Park S, Zhai J, Gurazada SGR, De Paoli E, Meyers BC, Green PJ (2011) Massive analysis of rice small RNAs: mechanistic implications of regulated MicroRNAs and variants for differential target RNA cleavage. Plant Cell 23:4185–4207

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X, Qian Q, Li J (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42:541–544

    CAS  PubMed  Google Scholar 

  • Johnson C, Kasprzewska A, Tennessen K, Fernandes J, Nan GL, Walbot V, Sundaresan V, Vance V, Bowman LH (2009) Clusters and superclusters of phased small RNAs in the developing inflorescence of rice. Genome Res 19:1429–1440

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jung KH, Han MJ, Lee YS, Kim YW, Hwang I, Kim MJ, Kim YK, Nahm BH, An G (2005) Rice undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 17:2705–2722

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kapoor M, Arora R, Lama T, Nijhawan A, Khurana JP, Tyagi AK, Kapoor S (2008) Genome-wide identification, organization and phylogenetic analysis of dicer-like, argonaute and RNA-dependent RNA polymerase gene families and their expression analysis during reproductive development and stress in rice. BMC Genom 9:451–468

    Google Scholar 

  • Komiya R (2017) Biogenesis of diverse plant phasiRNAs involves an miRNA-trigger and Dicer-processing. J Plant Res 130:17–23

    CAS  PubMed  Google Scholar 

  • Komiya R, Ohyanagi H, Niihama M, Watanabe T, Nakano M, Kurata N, Nonomura KI (2014) Rice germline-specific Argonaute MEL1 protein binds to phasiRNAs generated from more than 700 lincRNAs. Plant J 78:385–397

    CAS  PubMed  Google Scholar 

  • Lee DY, An G (2012) Two AP2 family genes, SUPERNUMERARY BRACT (SNB) and OsINDETERMINATE SPIKELET 1 (OsIDS1), synergistically control inflorescence architecture and floral meristem establishment in rice. Plant J 69:445–461

    CAS  PubMed  Google Scholar 

  • Li N, Zhang D-S, Liu H-S, Yin CS, Li XX, Liang WQ, Yuan Z, Xu B, Chu HW, Wang J, Wen TQ, Huang H, Luo D, Ma H, Zhang DB (2006) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18:2999–3014

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H, Jia S, Shen D, Liu J, Li J, Zhao H, Han S, Wang Y (2012) Four AUXIN RESPONSE FACTOR genes downregulated by microRNA167 are associated with growth and development in Oryza sativa. Funct Plant Biol 39:736–744

    CAS  PubMed  Google Scholar 

  • Mallory A, Vaucheret H (2010) Form, function, and regulation of ARGONAUTE proteins. Plant Cell 22:3879–3889

    CAS  PubMed  PubMed Central  Google Scholar 

  • Margis R, Fusaro AF, Smith NA, Curtin SJ, Watson JM, Finnegan EJ, Waterhouse PM (2006) The evolution and diversification of Dicers in plants. FEBS Lett 580:2442–2450

    CAS  PubMed  Google Scholar 

  • Mi S, Cai T, Hu Y, Chen Y, Hodges E, Ni F, Wu L, Li S, Zhou H, Long C, Chen S, Hannon GJ, Qi Y (2008) Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide. Cell 133:116–127

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miura K, Ikeda M, Matsubara A, Song X-J, Ito M, Asano K, Matsuoka M, Kitano H, Ashikari M (2010) OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42:545–549

    CAS  PubMed  Google Scholar 

  • Moxon S, Schwach F, Dalmay T, MacLean D, Studholme DJ, Moulton V (2008) A toolkit for analysing large-scale plant small RNA datasets. Bioinformatics 24:2252–2253

    CAS  PubMed  Google Scholar 

  • Nagasaki H, Itoh J, Hayashi K, Hibara K, Satoh-Nagasawa N, Nosaka M, Mukouhata M, Ashikari M, Kitano H, Matsuoka M, Nagato Y, Sato Y (2007) The small interfering RNA production pathway is required for shoot meristem initiation in rice. Proc Natl Acad Sci USA 104:14867–14871

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nishimura A, Ito M, Kamiya N, Sato Y, Matsuoka M (2002) OsPNH1 regulates leaf development and maintenance of the shoot apical meristem in rice. Plant J 30:189–201

    CAS  PubMed  Google Scholar 

  • Nonomura K-I, 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. Plant Cell 15:1728–1739

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nonomura K-I, Morohoshi A, Nakano M, Eiguchi M, Miyao A, Hirochika H, Kurata N (2007) 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 19:2583–2594

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oliver C, Santos JL, Pradillo M (2014) On the role of some ARGONAUTE proteins in meiosis and DNA repair in Arabidopsis thaliana. Front Plant Sci 5:177

    PubMed  PubMed Central  Google Scholar 

  • Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16:1616–1626

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110:513–520

    CAS  PubMed  Google Scholar 

  • Rogers K, Chen X (2013) Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25:2383–2399

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ru P, Xu L, Ma H, Huang H (2006) Plant fertility defects induced by the enhanced expression of microRNA167. Cell Res 16:457–465

    CAS  PubMed  Google Scholar 

  • Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18:1121–1133

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shikata M, Koyama T, Mitsuda N, Ohme-Takagi M (2009) Arabidopsis SBP-Box genes SPL10, SPL11 and SPL2 control morphological change in association with shoot maturation in the reproductive phase. Plant Cell Physiol 50:2133–2145

    CAS  PubMed  Google Scholar 

  • Shivaprasad PV, Chen H-M, Patel K, Bond DM, Santos BACM, Baulcombe DC (2012) A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell 24:859–874

    CAS  PubMed  PubMed Central  Google Scholar 

  • Song X, Li P, Zhai J, Zhou M, Ma L, Liu B, Jeong DH, Nakano M, Cao S, Liu C, Chu C, Wang XJ, Green PJ, Meyers BC, Cao X (2011) Roles of DCL4 and DCL3b in rice phased small RNA biogenesis. Plant J 69:462–474

    PubMed  Google Scholar 

  • Song X, Wang D, Ma L, Chen Z, Li P, Cui X, Liu C, Cao S, Chu C, Tao Y, Cao X (2012) Rice RNA-dependent RNA polymerase 6 acts in small RNA biogenesis and spikelet development. Plant J 71:378–389

    CAS  PubMed  Google Scholar 

  • Stocks MB, Moxon S, Mapleson D, Woolfenden HC, Mohorianu I, Folkes L, Schwach F, Dalmay T, Moulton V (2012) The UEA sRNA workbench: a suite of tools for analysing and visualizing next generation sequencing microRNA and small RNA datasets. Bioinformatics 28:2059–2061

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun W, Xiang X, Zhai L, Zhang D, Cao Z, Liu L, Zhang Z (2017) AGO18b negatively regulates determinacy of spikelet meristems on the tassel central spike in maize. J Integr Plant Biol 20:65–78

    Google Scholar 

  • Sun W, Chen D, Xue Y, Zhai L, Zhang D, Cao Z, Liu L, Cheng C, Zhang Y, Zhang Z (2019) Genome-wide identification of AGO18b bound miRNAs and phasiRNAs in maize by cRIP-seq. BMC Genom 20:656

    Google Scholar 

  • Ta KN, Sabot F, Adam H, Vigouroux Y, De Mita S, Ghesquière A, Do NV, Gantet P, Jouannic S (2016) miR2118-triggered phased siRNAs are differentially expressed during the panicle development of wild and domesticated African rice species. Rice 9:10

    CAS  PubMed  PubMed Central  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuji H, Aya K, Ueguchi-Tanaka M, Shimada Y, Nakazono M, Watanabe R, Nishizawa NK, Gomi K, Shimada A, Kitano H, Ashikari M, Matsuoka M (2006) GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers. Plant J 47:427–444

    CAS  PubMed  Google Scholar 

  • Tucker MR, Okada T, Hu Y, Scholefield A, Taylor JM, Koltunow AMG (2012) Somatic small RNA pathways promote the mitotic events of megagametogenesis during female reproductive development in Arabidopsis. Development 139:1399–1404

    CAS  PubMed  Google Scholar 

  • Vaucheret H (2008) Plant ARGONAUTES. Trends Plant Sci 13:350–358

    CAS  PubMed  Google Scholar 

  • Wang H, Wang H (2015) The miR156/SPL module, a regulatory hub and versatile toolbox, gears up crops for enhanced agronomic traits. Mol Plant 8:677–688

    CAS  PubMed  Google Scholar 

  • Wang L, Zhang Q (2017) Boosting rice yield by fine-tuning SPL gene expression. Trends Plant Sci 22:643–646

    CAS  PubMed  Google Scholar 

  • Wang L, Sun S, Jin J, Fu D, Yang X, Weng X, Xu C, Li X, Xiao J, Zhang Q (2015) Coordinated regulation of vegetative and reproductive branching in rice. Proc Natl Acad Sci USA 112:15504–15509

    CAS  PubMed  PubMed Central  Google Scholar 

  • Warthmann N, Chen H, Ossowski S, Weigel D, Herve P (2008) Highly specific gene silencing by artificial miRNAs in rice. PLoS ONE 3:e1829

    PubMed  PubMed Central  Google Scholar 

  • Willmann MR, Poethig RS (2007) Conservation and evolution of miRNA regulatory programs in plant development. Curr Opin Plant Biol 10:503–511

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu M-F, Tian Q, Reed JW (2006) Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133:4211–4218

    CAS  PubMed  Google Scholar 

  • Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS (2009a) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138:750–759

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu L, Zhang Q, Zhou H, Ni F, Wu X, Qi Y (2009b) Rice microRNA effector complexes and targets. Plant Cell 21:3421–3435

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu J, Yang Z, Wang Y, Zheng L, Ye R, Ji Y, Zhao S, Ji S, Liu R, Xu L, Zheng H, Zhou Y, Zhang X, Cao X, Xie L, Wu Z, Qi Y, Li Y (2015) Viral-inducible Argonaute18 confers broad-spectrum virus resistance in rice by sequestering a host microRNA. eLife 4:e05733

    PubMed Central  Google Scholar 

  • Xia K, Wang R, Ou X, Fang Z, Tian C, Duan J, Wang Y, Zhang M (2012) OsTIR1 and OsAFB2 downregulation via OsmiR393 overexpression leads to more tillers, early flowering and less tolerance to salt and drought in rice. PLoS ONE 7:e30039

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xie K, Wu C, Xiong L (2006) Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol 142:280–293

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang L, Qian X, Chen M, Fei Q, Meyers BC, Liang W, Zhang D (2016) Regulatory role of OsTDL1A-MSP1 signaling in specifying anther cell identity in rice. Plant Physiol 171:2085–2100

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang X, Li G, Tian Y, Song Y, Liang W, Zhang D (2018) A rice glutamyl-tRNA synthetase modulates early anther cell division and patterning. Plant Physiol 177:728–744

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yao M, Ai TB, Mao Q, Chen F, Li FS, Tang L (2018) Down-regulation of OsAGO17 by artificial microRNA caused pollen abortion, resulting in reduction of grain yield in rice. Electron J Biotechnol 35:25–32

    CAS  Google Scholar 

  • Yue E, Li C, Li Y, Liu Z, Xu JH (2017) MiR529a modulates panicle architecture through regulating SQUAMOSA PROMOTER BINDING-LIKE genes in rice (Oryza sativa). Plant Mol Biol 94:469–480

    CAS  PubMed  Google Scholar 

  • Zhai L, Sun W, Zhang K, Jia H, Liu L, Liu Z, Teng F, Zhang Z (2014) Identification and characterization of Argonaute gene family and meiosis-enriched Argonaute during sporogenesis in maize. J Integr Plant Biol 56:1042–1052

    CAS  PubMed  Google Scholar 

  • Zhai J, Zhang H, Arikit S, Huang K, Nan G-L, Walbot V, Meyers BC (2015) Spatiotemporally dynamic, cell-type-dependent premeiotic and meiotic phasiRNAs in maize anthers. Proc Natl Acad Sci USA 112:3146–3151

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhai L, Teng F, Zheng K, Xiao J, Deng W, Sun W (2019) Expression analysis of Argonaute genes in maize (Zea mays L.) in response to abiotic stress. Hereditas. https://doi.org/10.1186/s41065-019-0102-z

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Henderson IR, Lu C, Green PJ, Jacobsen SE (2007) Role of RNA polymerase IV in plant small RNA metabolism. Proc Natl Acad Sci USA 104:4536–4541

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Xia R, Meyers BC, Walbot V (2015) Evolution, functions, and mysteries of plant ARGONAUTE proteins. Curr Opin Plant Biol 27:84–90

    CAS  PubMed  Google Scholar 

  • Zhao DZ, Wang GF, Speal B, Ma H (2002) 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 16:2021–2031

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao X, De Palma J, Oane R, Gamuyao R, Luo M, Chaudhury A, Hervé P, Xue Q, Bennett J (2008) OsTDL1A binds to the LRR domain of rice receptor kinase MSP1, and is required to limit sporocyte numbers. Plant J 54:375–387

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng S, Li J, Ma L, Wang H, Zhou H, Ni E, Jiang D, Liu Z, Zhuang C (2018) OsAGO2 controls ROS production and the initiation of tapetal PCD by epigenetically regulating OsHXK1 expression in rice anthers. Proc Natl Acad Sci USA 116:7549–7558

    Google Scholar 

Download references

Acknowledgements

The authors acknowledge access to radiation laboratory, central imaging, greenhouse and sequencing facilities from the host Institute. sRNA and RNA-seq was performed at Genotypic Technologies, Bangalore. Thanks to Prof. K. Veluthambi for PB1 seeds and Agrobacterium strain LBA4404 (pSB1), and N. D. Sunitha for comments. Thanks to Rahul Raj Singh for help with subcloning.

Funding

PVS acknowledges support from Ramanujan Fellowship (SR/S2/RJN-109/2012, Department of Science and Technology, Government of India). PVS Lab is supported by NCBS-TIFR core funding and grants (BT/PR12394/AGIII/103/891/2014; BT/IN/Swiss/47/JGK/2018-19; BT/PR25767/GET/119/151/2017) from the Department of Biotechnology, Government of India. SD and KP were supported partially through DBT-Research Associateship. SC acknowledges a research fellowship from DBT.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to P. V. Shivaprasad.

Ethics declarations

Conflict of interest

Authors declare that they have no conflict of interests.

Additional information

Communicated by Venkatesan Sundaresan.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 725 kb)

Supplementary material 2 (PDF 1190 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Das, S., Swetha, C., Pachamuthu, K. et al. Loss of function of Oryza sativa Argonaute 18 induces male sterility and reduction in phased small RNAs. Plant Reprod 33, 59–73 (2020). https://doi.org/10.1007/s00497-020-00386-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00497-020-00386-w

Keywords

Navigation