Science China Life Sciences

, Volume 61, Issue 2, pp 148–154 | Cite as

Grass phasiRNAs and male fertility

Review
  • 21 Downloads

Abstract

Recent studies have indicated that a special type of small noncoding RNAs, phased small-interfering RNAs (phasiRNAs) play crucial roles in many cellular processes of plant development. PhasiRNAs are generated from long RNA precursors at intervals of 21 or 24 nt in plants, and they are produced from both protein-coding gene and long noncoding RNA genes. Different from those in eudicots, grass phasiRNAs include a special class of small RNAs that are specifically expressed in reproductive organs. These grass phasiRNAs are associated with gametogenesis, especially with anther development and male fertility. In this review, we summarized current knowledge on these small noncoding RNAs in male germ cells and their possible biological functions and mechanisms in grass species.

Keywords

noncoding RNA phasiRNA crop fertility 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (91640202, 91335104) and the grants from Guangdong Province (2016A030308015) and Guangzhou (201707020018, 201710010029).

References

  1. Axtell, M.J. (2013). Classification and comparison of small RNAs from plants. Annu Rev Plant Biol 64, 137–159.CrossRefPubMedGoogle Scholar
  2. Barakat, A., Sriram, A., Park, J., Zhebentyayeva, T., Main, D., and Abbott, A. (2012). Genome wide identification of chilling responsive microRNAs in Prunus persica. BMC Genomics 13, 481.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bohmert, K., Camus, I., Bellini, C., Bouchez, D., Caboche, M., and Benning, C. (1998). AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J 17, 170–180.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Borges, F., and Martienssen, R.A. (2015). The expanding world of small RNAs in plants. Nat Rev Mol Cell Biol 16, 727–741.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Chen, L., and Liu, Y.G. (2014). Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65, 579–606.CrossRefPubMedGoogle Scholar
  6. Cui, J., You, C., and Chen, X. (2017). The evolution of microRNAs in plants. Curr Opin Plant Biol 35, 61–67.CrossRefPubMedGoogle Scholar
  7. Dukowic-Schulze, S., Sundararajan, A., Ramaraj, T., Kianian, S., Pawlowski, W.P., Mudge, J., and Chen, C. (2016). Novel meiotic miRNAs and indications for a role of phasiRNAs in meiosis. Front Plant Sci 7, 762.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Fan, Y., Yang, J., Mathioni, S.M., Yu, J., Shen, J., Yang, X., Wang, L., Zhang, Q., Cai, Z., Xu, C., Li, X., Xiao, J., Meyers, B.C., and Zhang, Q. (2016). PMS1T, producing phased small-interfering RNAs, regulates photoperiod-sensitive male sterility in rice. Proc Natl Acad Sci USA 113, 15144–15149.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Fei, Q., Xia, R., and Meyers, B.C. (2013). Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. Plant Cell 25, 2400–2415.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Fei, Q., Yang, L., Liang, W., Zhang, D., and Meyers, B.C. (2016). Dynamic changes of small RNAs in rice spikelet development reveal specialized reproductive phasiRNA pathways. J Exp Bot 67, 6037–6049.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Fu, Q., and Wang, P.J. (2014). Mammalian piRNAs. Spermatogenesis 4, e27889.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Gao, Z., Luo, X., Shi, T., Cai, B., Zhang, Z., Cheng, Z., and Zhuang, W. (2012). Identification and validation of potential conserved microRNAs and their targets in peach (Prunus persica). Mol Cells 34, 239–249.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Gou, L.T., Dai, P., Yang, J.H., Xue, Y., Hu, Y.P., Zhou, Y., Kang, J.Y., Wang, X., Li, H., Hua, M.M., Zhao, S., Hu, S.D., Wu, L.G., Shi, H.J., Li, Y., Fu, X.D., Qu, L.H., Wang, E.D., and Liu, M.F. (2014). Pachytene piRNAs instruct massive mRNA elimination during late spermiogenesis. Cell Res 24, 680–700.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Han, B.W., Wang, W., Li, C., Weng, Z., and Zamore, P.D. (2015). piRNAguided transposon cleavage initiates Zucchini-dependent, phased piRNA production. Science 348, 817–821.CrossRefPubMedPubMedCentralGoogle Scholar
  15. He, H., Yang, T.Y., Wu, W.Y., and Zheng, B.L. (2015). Small RNAs in pollen. Sci China Life Sci 58, 246–252.CrossRefPubMedGoogle Scholar
  16. Itoh, J.I., Kitano, H., Matsuoka, M., and Nagato, Y. (2000). SHOOT ORGANIZATION genes regulate shoot apical meristem organization and the pattern of leaf primordium initiation in rice. Plant Cell 12, 2161–2174.CrossRefPubMedPubMedCentralGoogle Scholar
  17. Jeong, D.H., Schmidt, S.A., Rymarquis, L.A., Park, S., Ganssmann, M., German, M.A., Accerbi, M., Zhai, J., Fahlgren, N., Fox, S.E., Garvin, D.F., Mockler, T.C., Carrington, J.C., Meyers, B.C., and Green, P.J. (2013). Parallel analysis of RNA ends enhances global investigation of microRNAs and target RNAs of Brachypodium distachyon. Genome Biol 14, R145.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Jia, J., Zhao, S., Kong, X., Li, Y., Zhao, G., He, W., Appels, R., Pfeifer, M., Tao, Y., Zhang, X., Jing, R., Zhang, C., Ma, Y., Gao, L., Gao, C., Spannagl, M., Mayer, K.F.X., Li, D., Pan, S., Zheng, F., Hu, Q., Xia, X., Li, J., Liang, Q., Chen, J., Wicker, T., Gou, C., Kuang, H., He, G., Luo, Y., Keller, B., Xia, Q., Lu, P., Wang, J., Zou, H., Zhang, R., Xu, J., Gao, J., Middleton, C., Quan, Z., Liu, G., Wang, J., Wang, J., Yang, H., Liu, X., He, Z., Mao, L., and Wang, J. (2013). Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature 496, 91–95.CrossRefPubMedGoogle Scholar
  19. Johnson, C., Kasprzewska, A., Tennessen, K., Fernandes, J., Nan, G.L., Walbot, V., Sundaresan, V., Vance, V., and Bowman, L.H. (2009). Clusters and superclusters of phased small RNAs in the developing inflorescence of rice. Genome Res 19, 1429–1440.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kantar, M., Lucas, S.J., and Budak, H. (2011). miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta 233, 471–484.CrossRefPubMedGoogle Scholar
  21. Kapoor, M., Arora, R., Lama, T., Nijhawan, A., Khurana, J.P., Tyagi, A.K., and 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 Genomics 9, 451.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Kelliher, T., and Walbot, V. (2014). Maize germinal cell initials accommodate hypoxia and precociously express meiotic genes. Plant J 77, 639–652.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Komiya, R. (2017). Biogenesis of diverse plant phasiRNAs involves an miRNA-trigger and Dicer-processing. J Plant Res 130, 17–23.CrossRefPubMedGoogle Scholar
  24. Komiya, R., Ohyanagi, H., Niihama, M., Watanabe, T., Nakano, M., Kurata, N., and Nonomura, K.I. (2014). Rice germline-specific Argonaute MEL1 protein binds to phasiRNAs generated from more than 700 lincRNAs. Plant J 78, 385–397.CrossRefPubMedGoogle Scholar
  25. Kurihara, Y., and Watanabe, Y. (2004). Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc Natl Acad Sci USA 101, 12753–12758.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Li, X., Shahid, M.Q., Xia, J., Lu, Z., Fang, N., Wang, L., Wu, J., Chen, Z., and Liu, X. (2017). Analysis of small RNAs revealed differential expressions during pollen and embryo sac development in autotetraploid rice. BMC Genomics 18, 129.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Liu, B., Chen, Z., Song, X., Liu, C., Cui, X., Zhao, X., Fang, J., Xu, W., Zhang, H., Wang, X., Chu, C., Deng, X., Xue, Y., and Cao, X. (2007). Oryza sativa Dicer-like4 reveals a key role for small interfering RNA silencing in plant development. Plant Cell 19, 2705–2718.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Liu, J., and Qu, L.J. (2008). Meiotic and mitotic cell cycle mutants involved in gametophyte development in Arabidopsis. Mol Plant 1, 564–574.CrossRefPubMedGoogle Scholar
  29. Liu, Y., Wang, Y., Zhu, Q.H., and Fan, L. (2013). Identification of phasiRNAs in wild rice (Oryza rufipogon). Plant Signal Behav 8, e25079.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Liu, X., Hao, L., Li, D., Zhu, L., and Hu, S. (2015). Long non-coding RNAs and their biological roles in plants. Genomics Proteomics Bioinformatics 13, 137–147.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Mohn, F., Handler, D., and Brennecke, J. (2015). piRNA-guided slicing specifies transcripts for Zucchini-dependent, phased piRNA biogenesis. Science 348, 812–817.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Nagasaki, H., Itoh, J., Hayashi, K., Hibara, K., Satoh-Nagasawa, N., Nosaka, M., Mukouhata, M., Ashikari, M., Kitano, H., Matsuoka, M., Nagato, Y., and 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.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Nonomura, K.I., Morohoshi, A., Nakano, M., Eiguchi, M., Miyao, A., Hirochika, H., and 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.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Reinhart, B.J., Weinstein, E.G., Rhoades, M.W., Bartel, B., and Bartel, D.P. (2002). MicroRNAs in plants. Genes Dev 16, 1616–1626.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Satoh, N., Hong, S., Nishimura, A., Matsuoka, M., Kitano, H., and Nagato, Y. (1999). Initiation of shoot apical meristem in rice: characterization of four SHOOTLESS genes. Development 126, 3629–3636.PubMedGoogle Scholar
  36. Shi, M. (1985). The discovery and study of the photosensitive recessive male-sterile rice (Oryza sativa l. Subsp. Japonica). Scient Agr Sin, 2, 006.Google Scholar
  37. Song, X., Li, P., Zhai, J., Zhou, M., Ma, L., Liu, B., Jeong, D.H., Nakano, M., Cao, S., Liu, C., Chu, C., Wang, X.J., Green, P.J., Meyers, B.C., and Cao, X. (2012a). Roles of DCL4 and DCL3b in rice phased small RNA biogenesis. Plant J 69, 462–474.CrossRefPubMedGoogle Scholar
  38. Song, X., Wang, D., Ma, L., Chen, Z., Li, P., Cui, X., Liu, C., Cao, S., Chu, C., Tao, Y., and Cao, X. (2012b). Rice RNA-dependent RNA polymerase 6 acts in small RNA biogenesis and spikelet development. Plant J 71, 378–389.PubMedGoogle Scholar
  39. Sosa-Valencia, G., Palomar, M., Covarrubias, A. A., and Reyes, J. L. (2017). The legume miR1514a modulates a NAC transcription factor transcript to trigger phasiRNA formation in response to drought. J Exp Bot 68, 2013–2026.PubMedGoogle Scholar
  40. Su, C., Yang, X., Gao, S., Tang, Y., Zhao, C., and Li, L. (2014). Identification and characterization of a subset of microRNAs in wheat (Triticum aestivum L.). Genomics 103, 298–307.CrossRefPubMedGoogle Scholar
  41. Ta, K. N., Sabot, F., Adam, H., Vigouroux, Y., De Mita, S., Ghesquiere, A., Do, N. V., Gantet, P., and Jouannic, S. (2016). miR2118-triggered phased siRNAs are differentially expressed during the panicle development of wild and domesticated African rice species. Rice (N Y) 9, 10.CrossRefPubMedCentralGoogle Scholar
  42. Walbot, V., and Egger, R.L. (2016). Pre-meiotic anther development: cell fate specification and differentiation. Annu Rev Plant Biol 67, 365–395.CrossRefPubMedGoogle Scholar
  43. Wang, L., and Wang, J.W. (2015). Coding function for non-coding RNA in plants—insights from miRNA encoded peptide (miPEP). Sci China Life Sci 58, 503–505.CrossRefPubMedGoogle Scholar
  44. 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.Google Scholar
  45. Wu, L., Zhang, Q., Zhou, H., Ni, F., Wu, X., and Qi, Y. (2009). Rice microRNA effector complexes and targets. Plant Cell 21, 3421–3435.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Xie, Z., Allen, E., Wilken, A., and Carrington, J.C. (2005). DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc Natl Acad Sci USA 102, 12984–12989.CrossRefPubMedPubMedCentralGoogle Scholar
  47. Xu, M., Li, Y., Zhang, Q., Xu, T., Qiu, L., Fan, Y., and Wang, L. (2014). Novel miRNA and phasiRNA biogenesis networks in soybean roots from two sister lines that are resistant and susceptible to SCN race 4. PLoS ONE 9, e110051.CrossRefPubMedPubMedCentralGoogle Scholar
  48. Yoshikawa, M., Peragine, A., Park, M.Y., and Poethig, R.S. (2005). A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev 19, 2164–2175.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Zhai, J., Zhang, H., Arikit, S., Huang, K., Nan, G.L., Walbot, V., and Meyers, B.C. (2015). Spatiotemporally dynamic, cell-type-dependent premeiotic and meiotic phasiRNAs in maize anthers. Proc Natl Acad Sci USA 112, 3146–3151.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Zhang, H., Xia, R., Meyers, B.C., and Walbot, V. (2015a). Evolution, functions, and mysteries of plant ARGONAUTE proteins. Curr Opin Plant Biol 27, 84–90.CrossRefPubMedGoogle Scholar
  51. Zhang, P., Kang, J.Y., Gou, L.T., Wang, J., Xue, Y., Skogerboe, G., Dai, P., Huang, D.W., Chen, R., Fu, X.D., Liu, M.F., and He, S. (2015b). MIWI and piRNA-mediated cleavage of messenger RNAs in mouse testes. Cell Res 25, 193–207.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Zhang, Y.C., Liao, J.Y., Li, Z.Y., Yu, Y., Zhang, J.P., Li, Q.F., Qu, L.H., Shu, W.S., and Chen, Y.Q. (2014). Genome-wide screening and functional analysis identify a large number of long noncoding RNAs involved in the sexual reproduction of rice. Genome Biol 15, 512.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Zheng, Y., Wang, Y., Wu, J., Ding, B., and Fei, Z. (2015). A dynamic evolutionary and functional landscape of plant phased small interfering RNAs. BMC Biol 13, 32.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Zou, C., Wang, Q., Lu, C., Yang, W., Zhang, Y., Cheng, H., Feng, X., Prosper, M.A., and Song, G. (2016). Transcriptome analysis reveals long noncoding RNAs involved in fiber development in cotton (Gossypium arboreum). Sci China Life Sci 59, 164–171.CrossRefPubMedGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Yang Yu
    • 1
  • Yanfei Zhou
    • 1
  • Yuchan Zhang
    • 1
  • Yueqin Chen
    • 1
  1. 1.Guangdong Provincial Key Laboratory of Plant Resources, State Key Laboratory for Biocontrol, School of Life SciencesSun Yat-sen UniversityGuangzhouChina

Personalised recommendations