Review
Special Issue: Noncoding and small RNAs
Plant ARGONAUTES

https://doi.org/10.1016/j.tplants.2008.04.007Get rights and content

ARGONAUTE (AGO) proteins are integral players in all known small RNA-directed regulatory pathways. Eukaryotes produce numerous types of small RNAs, such as microRNAs (miRNA), small interfering RNAs (siRNA), PIWI-interacting RNAs (piRNAs), scanRNAs and 21U-RNAs, and these RNA species associate with different types of AGO family members, such as AGO, PIWI and group 3 proteins. Small RNA-guided AGO proteins regulate gene expression at various levels, including internal genomic DNA sequence elimination (in ciliates), translational repression (animals), and RNA cleavage (all eukaryotes), which in some cases is followed by DNA methylation and chromatin remodeling. The plant model species Arabidopsis contains ten AGO proteins belonging to three phylogenetic clades. This review covers our current knowledge of plant AGO functions during miRNA- and siRNA-mediated regulation of development and stress responses, siRNA-mediated antiviral immune response, and siRNA-mediated regulation of chromatin structure and transposons.

Section snippets

History of ARGONAUTE nomenclature

Proteins of the ARGONAUTE (AGO) family were referred to first as PAZ proteins because of a unique domain in the central part of the three founding members of the family: Drosophila P ELEMENT-INDUCED WIMPY TESTIS (PIWI), Arabidopsis ARGONAUTE1 (AGO1) and Arabidopsis ZWILLE (ZLL). To distinguish AGO proteins from DICER proteins, which later were also found to harbour a PAZ domain, AGO proteins were renamed PPD (PAZ PIWI DOMAINS) proteins, owing to the presence of a PIWI domain, which is not found

Diversity of ARGONAUTE proteins among kingdoms

Although all AGO proteins harbour PAZ, MID (middle) and PIWI domains (see below), they are divided into three groups on the basis of both their phylogenetic relationships and their capacity to bind to small RNAs (see Box 1 for a description of the different classes of eukaryotic small RNAs, and Box 2 for a thorough description of plant small RNAs) 1, 2. Group 1 members bind to microRNAs (miRNAs) and small interfering RNAs (siRNAs) and are referred to as AGO proteins. Group 2 members bind to

Domains and activities of ARGONAUTE proteins

AGOs are large proteins (ca 90–100 kDa) consisting of one variable N-terminal domain and conserved C-terminal PAZ, MID and PIWI domains 1, 2. Experiments with bacterial and animal AGO proteins have elucidated the roles of these three domains in small RNA pathways 6, 7. The MID domain binds to the 5′ phosphate of small RNAs, whereas the PAZ domain recognizes the 3′ end of small RNAs 1, 2. The PIWI domain adopts a folded structure similar to that of RNaseH enzymes and exhibits endonuclease

Functions of plant AGO proteins

Phylogenic analyses group plant AGO proteins in three clades (Figure 1). Arabidopsis exhibits an equal distribution of its ten members within the three clades: AtAGO1, AtAGO5 and AtAGO10 within the first clade; AtAGO2, AtAGO3 and AtAGO7 within the second clade; and AtAGO4, AtAGO6, AtAGO8 and AtAGO9 within the third clade [4]. By contrast, rice exhibits an expanded first clade (12 members), an equivalent second clade (three members), and a reduced third clade (two members) [5].

Conclusions

Despite the fact that AGO proteins were first discovered in plants ten years ago, only some members of the Arabidopsis AGO family have been analyzed in depth, and the functions of half of the family remain unexplored. Therefore, many fundamental questions about the functions of this large conserved gene family remain unanswered in plants:

  • (i)

    What is the reason for the absence of PIWI or group 3 proteins in plants? Do plant AGO members perform functions similar to those of PIWI proteins during

Acknowledgements

I thank Allison Mallory for critically reading the manuscript, and I apologize to colleagues whose work could not be fully cited owing to space constraints.

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