Nuclear functions of AGO1 · 2019/1/3 · uclear functions of plant AGO proteins 72 were first described for AGO4 (Zilberman et al., 2003) and AGO6 (Zheng et al., 2007; McCue et

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Running title: 1

Nuclear functions of AGO1 2

Corresponding author details: 3

Jakub Dolata 4

Department of Gene Expression, Institute of Molecular Biology and Biotechnology, Faculty of Biology, 5

Adam Mickiewicz University, Umultowska 89, 61-614 Poznan, Poland 6

Email: [email protected] 7

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Correspondence may also be addressed to: 9

Artur Jarmolowski 10

Department of Gene Expression, Institute of Molecular Biology and Biotechnology, Faculty of Biology, 11

Adam Mickiewicz University, Umultowska 89, 61-614 Poznan, Poland 12

Email: [email protected] 13

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Novel nuclear functions of Arabidopsis ARGONAUTE1: beyond RNA interference 16

Mateusz Bajczyk, Susheel Sagar Bhat, Lukasz Szewc, Zofia Szweykowska-Kulinska, Artur Jarmolowski* 17

and Jakub Dolata* 18

Department of Gene Expression, Institute of Molecular Biology and Biotechnology Faculty of Biology, 19

Adam Mickiewicz University, Poznan, Poland 20

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One-sentence summary 23

AGO1 activity is not limited to the cytoplasm and has been found to be associated with the 24

regulation of gene expression in the nucleus and to be tightly associated with chromatin and 25

transcription. 26

Funding 27

This project was supported by the Polish National Science Centre (UMO-2017/25/B/NZ1/00603 to JD, 28

UMO-2013/10/A/NZ1/00557 to AJ, UMO-2016/23/B/NZ9/00862 to ZSK, UMO-29

2017/27/N/NZ1/00202 to SSB, UMO-2014/13/N/NZ1/00049 to MB, UMO-2015/19/N/NZ1/01997 to 30

LS) and the KNOW Poznan RNA Centre (01/KNOW2/2014). 31

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Corresponding author email 33

Jakub Dolata: [email protected] 34

Artur Jarmolowski: [email protected] 35

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Plant Physiology Preview. Published on January 3, 2019, as DOI:10.1104/pp.18.01351

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Introduction 39

Argonaute (AGO) proteins, key factors in the RNA interference (RNAi) pathway, are involved 40

in the regulation of gene expression at the transcriptional, posttranscriptional and translational levels 41

and play roles in genome integrity maintenance (Hutvagner and Simard, 2008; Meister, 2013; 42

Kalantari et al., 2016; Carbonell, 2017; Ma et al., 2017). AGO proteins, found in all eukaryotes 43

(excluding Saccharomyces cerevisiae) as well as in bacteria and archaea (Drinnenberg et al., 2009; 44

Meister, 2013; Swarts et al., 2014), are classified into three paralogous groups: (1) AGO-like proteins, 45

which account for most AGO proteins and are similar to Arabidopsis thaliana AGO1; (2) PIWI-like 46

proteins, homologous to Drosophila melanogaster PIWI and exclusively expressed in animal germ 47

cells; and (3) AGOs expressed in only Caenorhabditis elegans (Hutvagner and Simard, 2008; Zhang et 48

al., 2015; Ma et al., 2017). The number of genes encoding AGO proteins varies among species, 49

ranging from one in Schizosaccharomyces pombe to 27 in C. elegans (Carmell et al., 2002). All AGO 50

proteins are evolutionarily conserved in structure and function (Hock and Meister, 2008), which 51

emphasizes their importance in cellular metabolism and development. 52

In eukaryotes, AGO family proteins possess four characteristic domains: N-terminal, PAZ 53

(PIWI-AGO-Zwille), MID and PIWI (Hutvagner and Simard, 2008; Zhang et al., 2014). The PAZ domain 54

anchors the 3' end of the guide strand of a small RNA (sRNA) duplex (Ma et al., 2004), whereas the 55

MID-PIWI domain creates a binding pocket for the 5’ end of the sRNA duplex guide strand (Boland et 56

al., 2011). Moreover, the PIWI domain shows similarity to RNase H and is essential for target 57

cleavage (Song et al., 2004; Parker et al., 2005). Finally, the N-terminal domain fragment (DUF1785) 58

was recently described as being important for RNA duplex unwinding (Derrien et al., 2018). 59

The AGO proteins mediate posttranscriptional gene silencing (PTGS). Based on microRNA 60

(miRNA) or small interfering RNA (siRNA) sequence complementarity, RNA-induced silencing complex 61

(RISC) is guided to a target RNA, which leads to its cleavage (predominantly in plants) (Baumberger 62

and Baulcombe, 2005) or translation inhibition (Brodersen et al., 2008; Guo et al., 2010). However, 63

AGO proteins also exhibit an sRNA-independent target recognition mechanism, as suggested for C. 64

elegans, mammalian cells (Leung et al., 2011; Friend et al., 2012) and D. melanogaster (Pinder and 65

Smibert, 2013). In A. thaliana, ten AGO family members are expressed (Vaucheret, 2008; Borges and 66

Martienssen, 2015), with the most prominent being AGO1, the main component of the miRNA-67

guided cytoplasmic RISC. 68

Other members of the AGO family were found to be associated with chromatin and involved 69

in histone modification and DNA methylation in transcriptional gene silencing (reviewed (Castel and 70

Martienssen, 2013; Martienssen and Moazed, 2015). The nuclear functions of plant AGO proteins 71

were first described for AGO4 (Zilberman et al., 2003) and AGO6 (Zheng et al., 2007; McCue et al., 72

2015). A. thaliana AGO4 binds 24-nt siRNAs, which are most likely generated in the nucleus by DCL3 73

in the RNA polymerase IV (RNAPIV) and RNA-dependent RNA polymerase 2 (RDR2)-dependent 74

pathway (reviewed in (Wendte and Pikaard, 2017). Binding of the siRNA-AGO4 complex to RNA 75

polymerase V (RNAPV) nascent transcripts leads to recruitment of the DNA methyltransferase DRM2 76

and induces de novo DNA methylation (m5C) at specific loci (Wierzbicki et al., 2008; Bohmdorfer et 77

al., 2014; Zhong et al., 2014), leading to transcriptional silencing. The introduction of a methyl group 78

at cytosine residues requires assistance from the SWI/SNF chromatin remodeling complex (Zhu et al., 79

2013) and is accompanied by histone modifications, such as H3 and H4 deacetylation, H3K9 80

methylation (H3K9me) and H3K4 demethylation (reviewed in (Matzke and Mosher, 2014). Similarly, 81 https://plantphysiol.orgDownloaded on November 29, 2020. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


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Arabidopsis AGO6 is related to the RNA-directed DNA methylation (RdDM) pathway and may act 82

redundantly (Zheng et al., 2007) or interdependently with (Duan et al., 2015) AGO4. 83

Moreover, Arabidopsis AGO6 exhibits a specific expression pattern (shoot and root 84

meristem) (Havecker et al., 2010; Eun et al., 2011) and participates in the methylation of 85

transcriptionally active transposons (McCue et al., 2015). In S. pombe, the AGO-containing RNA-86

induced transcriptional silencing (RITS) complex is required for the formation of constitutive 87

heterochromatin at pericentromeric regions, stimulating histone H3K9me (Partridge et al., 2002). In 88

C. elegans, the nuclear RNAi pathway is also involved in transcription silencing by promoting H3K9me 89

(Gu et al., 2012), which protects germline cells from transposon activity (Vastenhouw and Plasterk, 90

2004). 91

In worms, AGO family proteins are involved in not only transcriptional suppression but also 92

positive regulation of the transcription of target genes required for spermatogenesis (Conine et al., 93

2013; Seth et al., 2013), and in D. melanogaster, heterochromatin formation is dependent on RNAi 94

and AGO proteins (Pal-Bhadra et al., 2002; Pal-Bhadra et al., 2004). High-throughput RNA-seq and 95

ChIP-seq studies on flies revealed that AGO2 represses transcription by binding to chromatin, but this 96

mechanism could be independent of its catalytic activity (Taliaferro et al., 2013). Moreover, 97

Drosophila AGO2 was found to corelate with transcriptionally active regions of the genome and 98

thought to be involved in the control of RNA polymerase II (RNAPII) processivity (Cernilogar et al., 99

2011). In human cells, AGO1 directs transcriptional gene silencing by associating with targeted 100

promoters (Kim et al., 2006). However, it is also involved in the initiation of transcription and 101

interacts directly with RNAPII (Huang et al., 2013). 102

Recent studies show that the action of Arabidopsis AGO1 is not limited to the cytoplasm, as it 103

is also involved in the regulation of gene expression in the nucleus, where it is tightly associated with 104

chromatin (Dolata et al., 2016; Schalk et al., 2017; Liu et al., 2018). Here, we summarize recent 105

findings on the nuclear function of Arabidopsis AGO1 and provide ideas and directions for future 106

studies. 107

108

miRNA loading into AGO1 in the nucleus 109

In contrast to animal cells, wherein miRNA biogenesis occurs in both the nucleus and the cytoplasm, 110

in plant cells, miRNA production occurs entirely in the nucleus (Stepien et al., 2017). miRNA/miRNA* 111

duplexes are generated in two cleavage reactions, both of which are catalyzed by the endonuclease 112

DICER-LIKE 1 (DCL1) (Kurihara and Watanabe, 2004). The 2’ OH groups of the 3’ terminal nucleotides 113

of both duplex strands generated in these reactions are methylated by the methylase HUA 114

ENHANCER 1 (HEN1) (Park et al., 2002), which protects them from uridylation and subsequent 115

degradation (Yu et al., 2005). Interestingly, miRNA and miRNA* accumulate asymmetrically, as one 116

strand remains more abundant than the other, and this effect is correlated with the formation of a 117

functional RISC, initiated by AGO1 loading (traditionally thought to occur in the cytoplasm) in which 118

the guide strand (miRNA) is retained inside this effector ribonucleoprotein complex, while the 119

passenger strand (miRNA*) is removed by unwinding and degradation (Iki et al., 2010). 120

Until recently, very little was known about the exact site at which plant sRNA duplex loading 121

occurs. According to previously published data, miRNA/miRNA* duplexes are exported to the 122

cytoplasm by HASTY (HST) (Papp et al., 2003; Park et al., 2005; Pontes et al., 2013), an ortholog of 123

human Exportin 5 (Exp5) (Yi et al., 2005) after completing biogenesis in the nucleus. However, this is 124

not a general mechanism as HST has been reported to be required for the export of only some 125 https://plantphysiol.orgDownloaded on November 29, 2020. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


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specific miRNAs (Park et al., 2005). Additionally, in contradiction to the current model of miRNA 126

biogenesis in plants, data showing that the miRNA biogenesis machinery is necessary for 127

miRNA/miRNA* duplex formation and RISC loading is already present in the nucleus have been 128

reported; Fang and Spector showed that AGO1 and HYL1 (HYPONASTIC LEAVES 1), a double-stranded 129

RNA-binding protein involved in primary transcript (pri-miRNA) processing and loading AGO1 with 130

miRNAs (Vazquez et al., 2004) are present in Dicing bodies (D-bodies) (Fang and Spector, 2007), 131

nuclear structures involved in miRNA biogenesis in plants. HYL1 is an important factor for strand 132

selection during AGO1 loading with miRNAs (Eamens et al., 2009). These observations are considered 133

the first clue indicating that miRNA is loaded to AGO1 in the nucleus. Moreover, Pontes and 134

colleagues showed that DCL1 colocalizes in nuclear D-bodies with HEN1 (Pontes et al., 2013). 135

Recently published data reshaped the miRNA biogenesis model and shed new light on the 136

RISC-loading process in plants. Fascinatingly, a conserved coiled structure, termed an N-coil, deemed 137

to have an important function, was observed at the AGO1 N-terminal domain. The N- and C-terminal 138

regions of the N-coil possess both a nuclear localization signal (NLS) and a nuclear export signal 139

(NES), indicating that AGO1 is a nuclear-cytoplasmic shuttling protein (Bologna et al., 2018). The 140

prevalent presence of AGO1 in the cytoplasm results from the dominance of the NES over the NLS, 141

which is recognized in the nucleus by the evolutionarily conserved CRM1/EXPORTIN1 (EXPO1) 142

protein (Kudo et al., 1999). However, according to Bologna and coworkers (Bologna et al., 2018), the 143

nuclear localization of AGO1 is necessary for the loading and translocation of most methylated, 144

mature miRNAs from the nucleus to the cytoplasm. In the cytoplasm, the NES element on the surface 145

of unloaded AGO1 is unrecognizable, and the exposed NLS results in the translocation of AGO1 to the 146

nucleus. Upon sRNA duplex binding in the nucleus, the NES element is exposed and begins to 147

dominate over the NLS, resulting in the translocation of loaded AGO1 back to the cytoplasm. 148

When present in the nucleus, AGO1 undergoes two major conformational changes during 149

RISC formation. One change occurs before the loading of miRNA/miRNA* duplexes and requires the 150

molecular chaperone Hsp90, which binds to AGO1 in the form of a dimer, and it is a common feature 151

of plant and animal RISC formation process (Iwasaki et al., 2010). In the presence of ATP, Hsp90 152

mediates the conformational opening of AGO1, enabling the fit of sRNA duplexes. In Arabidopsis and 153

tobacco (Nicotiana tabacum), cyclophilin 40/SQUINT cochaperones assist Hsp90 in the loading of the 154

siRNA duplex into AGO (Iki et al., 2012). Additionally, unlike in animals, in plants, the RNA duplex 155

binding does not require energy generated from ATP hydrolysis, but hydrolysis is still required 156

afterward for the dissociation of AGO1 from the Hsp90 dimer. Dissociation enforces a second 157

conformational change that promotes unwinding and passenger strand ejection (Rohl et al., 2013). 158

Alteration of the NES element accessibility in AGO1 highly resembles the regulation of AGO4 159

nuclear localization in the RNA-directed DNA methylation (RdDM) pathway in plants (Ye et al., 2012). 160

siRNAs must be loaded into the AGO4 protein to form AGO4/siRNA complexes, which occurs in the 161

cytoplasm and triggers conformational changes in AGO4, exposing an initially hidden NLS and 162

consequently allowing translocation to the nucleus. Assembly of the AGO4 complex before entry into 163

the nucleus and selective transport may function as a quality control step before the nuclear RNAi 164

process occurs (Ye et al., 2012), and a similar process could be applicable to the loading of miRNA 165

into AGO1. 166

Bologna and colleagues have shown the importance of the NES for AGO1 function (AGO1 167

with mutated NES could not be transported to the cytoplasm). AGO1-mNES could not rescue the 168

defects in ago1 mutants (Bologna et al., 2018), an observation similar to that made for cleavage 169

activity mutants (Carbonell et al., 2012). However, the significance of AGO1 NLS remains unclear 170 https://plantphysiol.orgDownloaded on November 29, 2020. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


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since AGO-mNLS shows only reduced nuclear localization (Bologna et al., 2018). The molecular 171

phenotype of nuclear AGO1-depleted plants is not known and requires further investigation. 172

173

ARGONAUTE1 regulates protein-coding gene transcription 174

A. thaliana AGO1 has been predominantly studied for its function in the cytoplasm in the PTGS 175

pathway (Morel et al., 2002; Baumberger and Baulcombe, 2005; Brodersen et al., 2008; Li et al., 176

2013; Arribas-Hernandez et al., 2016). Although AGO1 nuclear localization in A. thaliana was 177

reported several years ago (Fang and Spector, 2007; Wang et al., 2011), a function of chromatin-178

associated AGO1 was described much later (Dolata et al., 2016). Data recently published by Liu and 179

colleagues (Liu et al., 2018) provide a model for AGO1 functioning as a positive regulator of 180

transcription in Arabidopsis. Using the Chip-seq approach, the authors identified more than 900 181

AGO1-enriched sites in the A. thaliana genome, which correspond mostly to genomic regions 182

containing transcription start sites (TSS) and transcription termination sites (TTS). 183

This AGO1 enrichment corresponds to the known total RNAPII distribution profile (Adelman 184

and Lis, 2012; Hajheidari et al., 2013). Arabidopsis AGO1 was shown to coimmunoprecipitate with 185

RNAPII complex subunits, and AGO1 depletion in the ago1-36 mutant induced a genome-wide 186

decreased chromatin-associated accumulation of total RNAPII as well as that of its phosphorylated 187

forms (P-Ser5 and P-Ser2), whereas the overall abundance of RNAPII in the cell did not decrease (Liu 188

et al., 2018). These results support previously published data showing a reduced RNAPII occupancy at 189

some MIR genes of the ago1-11 mutant (Dolata et al., 2016). Liu and colleagues suggest that in 190

contrast to the cytoplasmic AGO1 pool, chromatin-associated AGO1 stimulates gene expression by 191

assisting in the recruitment of RNAPII, and the presence of AGO1 on chromatin positively correlates 192

with the expression levels of target genes. Moreover, the levels of nascent and mature transcripts 193

encoded by AGO1-bound genes are predominantly reduced in the ago1-36 mutant (Liu et al., 2018). 194

For more than 50% of AGO1-bound genes, corresponding sRNAs associated with nuclear 195

AGO1 have been identified (Liu et al., 2018). These sRNAs are 21 nt in length and contain the 5’ 196

uridine, which is consistent with the known AGO1-binding preference (Mi et al., 2008) and most 197

likely produced by DCL1 with assistance from HYL1 (Liu et al., 2018). The association of AGO1 with 198

chromatin was previously shown to be impaired in the HYL1-knockout mutant (hyl1-2) or upon 199

alteration of the HYL1 phosphorylation status (in the cpl1-7 mutant) (Dolata et al., 2016). 200

Interestingly, the nuclear fraction of sRNAs bound to AGO1 is depleted in miRNAs and enriched in 201

trans-acting siRNAs (tasiRNAs) (Liu et al., 2018), which coincides with previous observations of AGO1 202

being detected on TAS1 and TAS2 loci but not on the TAS3 gene (Dolata et al., 2016). Finally, both 203

sRNA binding and the ribonuclease activity of AGO1 have been shown to be required for its 204

interaction with chromatin (Liu et al., 2018), which contrasts with the results of studies on flies 205

(Taliaferro et al., 2013). 206

In human cells, nuclear AGO1/AGO2 copurifies with many RNA-binding proteins, splicing 207

factors, histones and chromatin-related proteins (Ameyar-Zazoua et al., 2012; Batsche and Ameyar-208

Zazoua, 2015) and interacts with RNAPII (Huang et al., 2013). In A. thaliana, FLAG-AGO1 209

coimmunoprecipitates with GFP-tagged SWI/SNF complex subunits (SWI3B, SWI3D and BSH) (Liu et 210

al., 2018). Similar results showing the interaction of AGO2 with SWI/SNF components in an 211

DNA/RNA-independent manner have been reported in HeLa cells (Carissimi et al., 2015). Liu and 212

colleagues have demonstrated that the binding of AGO1 to its chromatin targets is affected in 213

Arabidopsis SWI/SNF subunit mutants, whereas SWI3B recruitment to chromatin is not changed 214 https://plantphysiol.orgDownloaded on November 29, 2020. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


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upon depletion of AGO1. These data suggest that SWI/SNF components are required for the AGO1-215

chromatin association (Liu et al., 2018). However, recent data show that the main ATPase of 216

SWI/SNF, BRM (CHR2), cotranscriptionally inhibits pri-miRNA processing (Wang et al., 2018). These 217

observations raise the question of whether impaired AGO1/chromatin binding in the brm-4 mutant 218

(Liu et al., 2018) could be the result of misregulated sRNA production. 219

AGO1/chromatin binding was shown to be enhanced under biotic and abiotic stresses 220

(Dolata et al., 2016; Liu et al., 2018), and a binding preference to stress-related genes was found 221

among AGO1 chromatin targets (Liu et al., 2018). Interestingly, studies on the influence of the 222

jasmonic acid derivative methyl jasmonate (MeJA) on root growth have shown that its inhibitory 223

effect is reduced in ago1 mutants. Moreover, AGO1 binding to chromatin is induced by MeJA and 224

correlates with elevated target gene expression (Liu et al., 2018). 225 226 Cotranscriptional regulation of miRNA biogenesis by Argonaute1 227

While RNA processing and maturation are known to occur cotranscriptionally in eukaryotic cells 228

(Bentley, 2014; Herzel et al., 2017; Grasser and Grasser, 2018), knowledge of cotranscriptional 229

processes in plants is still limited. Several studies have shown functional correlations among mRNA 230

transcription, splicing, and 5’- and 3’-end processing events in both animals and plants (Geraldo et 231

al., 2009; Liu et al., 2012; Dolata et al., 2015; Li et al., 2016). Similarly, the biogenesis of noncoding 232

RNAs, especially miRNAs, is known to occur cotranscriptionally in both human and animal cells 233

(Morlando et al., 2012; Dhir et al., 2015; Yin et al., 2015; Church et al., 2017). In plants, this field is 234

rather underinvestigated and requires further study. In Arabidopsis, miRNA biogenesis processes, 235

including (i) the amount and activity of various proteins involved in miRNA biogenesis (for review: 236

Rogers and Chen, 2013; Achkar, Cambiagno and Manavella, 2016; Dolata et al., 2018), (ii) the 237

influence of splicing and polyadenylation (Bielewicz et al., 2013; Knop et al., 2016; Stepien et al., 238

2017), (iii) alternative stem-loop structure formation (Iki et al., 2018), (iv) miRNA modifications (Bhat 239

et al., 2016), and (v) miRNA stability (Zhao et al., 2012), are highly regulated. Modulation of pri-240

miRNA processing based on secondary structure has also been recently shown (Wang et al., 2018). 241

Demonstrating a role of CHROMATIN REMODELING FACTOR 2 (CHR2) in unwinding pri-miRNA stem 242

and loop structures in association with Serrate (SE), Wang and colleagues provided evidence of 243

cotranscriptional pri-miRNA processing, as CHR2 also plays a role in SE-independent transcription. 244

Upon the application of different environmental stresses, which alter these regulatory 245

processes, the levels of mature miRNA expression are barely correlated with the expression levels of 246

MIR pri-miRNAs (Barciszewska-Pacak et al., 2015). The role of AGO1 in miRNA biogenesis, especially 247

under stress conditions, was investigated by Dolata and colleagues (Dolata et. al., 2016), who 248

identified some MIR genes (MIR161 and MIR173) that had decreased pri-miRNA levels and increased 249

miRNA accumulation under salinity stress. The increased levels of miRNA161 and miRNA173 (but not 250

the corresponding miRNAs*) were shown to result from AGO1-mediated stabilization, which is 251

consistent with previously published data (Vaucheret et al., 2006; Vaucheret, 2009). While the exact 252

mechanism by which specific miRNAs are preferentially bound and stabilized by RISC under stress 253

conditions is currently unknown, Iki and colleagues (Iki et al., 2018) may have shed some light on this 254

phenomenon, as they showed that the structural flexibility of the pre-miRNA domain within 255

Arabidopsis pri-miR168a could generate different miRNA/miRNA* duplexes with different AGO1-256

binding preferences. 257

While loading could be one aspect underlying the enrichment of some miRNAs under stress 258

conditions, the degradation of other miRNAs could also contribute to this selectivity. Recently, an 259 https://plantphysiol.orgDownloaded on November 29, 2020. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


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association between the miRNA/miRNA* degradation pathway and AGO1 was also established. A 3’-260

5’ exoribonuclease, ATRM2, was shown to selectively degrade miRNA/miRNA* duplexes and partially 261

colocalize with AGO1 in the cytoplasm, and this colocalization was enhanced under heat stress 262

(Wang et al., 2018). The authors suggested that the association with AGO1 may be important for 263

strand selection during degradation and could play a role in modulating miRNA biogenesis in 264

response to environmental conditions. Both miRNA161 and miRNA173 were previously shown to 265

respond to various stresses, including viral infection and drought (Hajdarpasic and Ruggenthaler, 266

2012). Moreover, in addition to targeting protein-coding transcripts, both miRNAs have been shown 267

to be involved in the generation of secondary siRNAs, including TAS1a/b/c- and TAS2-derived 268

tasiRNAs (Rhoades et al., 2002; Allen et al., 2005; Khraiwesh et al., 2012), indicating their importance 269

and potentially explaining the precise and complicated pathways underlying their regulation. 270

Although stabilization or lack thereof can explain the up- or downregulation of mature 271

miRNAs, changes in pri-miRNA levels potentially suggest a role of AGO1 in transcription. This 272

transcriptional/cotranscriptional role of AGO1 in A. thaliana was suggested based on an observation 273

that AGO1 binds to chromatin in close proximity of the MIR161 and MIR173 genes (Dolata et al. 274

2016). AGO1 enrichment on these two MIR genes was observed upon salt stress treatment and 275

correlated with decreased RNAPII occupancy. However, reduced RNAPII levels were limited to MIR 276

gene body regions and not to their promoters. These results together with those of studies on MIR 277

promoter activity indicate that this regulation likely occurs at the elongation/termination phase of 278

transcription. Moreover, the overaccumulation of nonpolyadenylated MIR transcripts indicates that 279

the presence of AGO1 on the gene body causes RNAPII to pause and/or terminate transcription 280

prematurely. Changes in the RNAPII distribution at MIR loci and alterations in pri-miRNA levels under 281

salt stress conditions were far smaller in the ago1-11 background than in the wild-type background, 282

suggesting that AGO1 plays a negative role in cotranscriptional miRNA biogenesis under salt stress. 283

These results contrasted with those indicating the transcriptional role of AGO1, as demonstrated by 284

Liu and colleagues (Liu et. al., 2018). 285

AGO-dependent posttranscriptional processing of miRNA precursors has also been shown in 286

human cells, albeit with AGO2 as the main player. AGO2-cleaved precursor miRNAs (ac-pre-miRNAs) 287

are products of AGO2-mediated pre-miRNA cleavage and endogenous products of miRNA biogenesis 288

(Diederichs and Haber, 2007). On the other hand, certain Arabidopsis pri-miRNAs could be the 289

targets of their own miRNAs (German et al., 2008). German and colleagues suggest that the interplay 290

between polyadenylation and degradation machinery could lead to several different mechanisms by 291

which pri-miRNAs are processed. Recent studies revealed that the binding of AGO1 to MIR genes is 292

RNA-dependent (Dolata et al., 2016). To test whether the association of AGO1 with chromatin 293

requires sRNAs, the Arabidopsis hyl1-2 mutant was analyzed, in which the loading of miRNAs onto 294

AGO1 is known to be hampered (Eamens et al., 2009). As expected, under salt stress, the association 295

of AGO1 with chromatin was weaker in hyl1-2 mutant plants compared to that in wild-type plants. 296

This information in combination with previous results showing colocalization of AGO1 with HYL1 in D-297

bodies (Fang and Spector, 2007) also indicates that AGO1 could act during early stages of miRNA 298

biogenesis. 299

300

Role of ARGONAUTE1 in RNA-mediated DNA repair 301

DNA double-stranded breaks (DSBs) are caused by reactive oxygen species, ionizing radiation, or 302

failed DNA replication and underlie serious DNA damage, as they cause mutations and genome 303 https://plantphysiol.orgDownloaded on November 29, 2020. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.


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instability and may lead to cell death. Therefore, quick repair of DSBs is important for the 304

maintenance of cellular genome integrity and excludes harmful mutations (Iyama and Wilson, 2013). 305

In eukaryotes, DSBs are repaired by two major pathways: homologous recombination (HR) and 306

nonhomologous end-joining (NHEJ). In the HR pathway, DNA is repaired using sister chromatids as a 307

template, which accurately restores the DNA sequence. NHEJ involves joining of two double-308

stranded DNA strains by DNA synthesis and ligation (Iyama and Wilson, 2013). Wei and colleagues 309

(Wei et al., 2012) elucidated the role of sRNAs in DSB repair via the HR pathway in both HeLa cells 310

and Arabidopsis and showed that knocking down Dicer and AGO2 in human cells reduced the DSB 311

repair efficiency (Wei et al., 2012). The main sRNA-processing enzymes Dicer and DROSHA have also 312

been shown to be involved in activating a response to DNA damage upon genotoxic stress in fly and 313

human cells (Francia et al., 2012; Michalik et al., 2012). Wei and colleagues (Wei et al., 2012) showed 314

that RNAPIV, RDRs and Dicer-like proteins (DCL2, DCL3, DCL4) are required for the proper biogenesis 315

of DSB-induced sRNAs (diRNAs) in Arabidopsis. 316

These diRNAs are incorporated into AGO2 and interact with RNAPV scaffold transcripts to 317

recruit DSB repair proteins to the DSB sites. Therefore, Arabidopsis mutants of proteins involved in 318

diRNA biogenesis reduce the efficiency of DSB repair (Wei et al., 2012). Human AGO2 was later 319

shown to interact with the Rad51 recombinase (Gao et al., 2014), and Rad51 mediates dsDNA 320

ligation during HR (San Filippo et al., 2008). Moreover, AGO2 together with sRNA recruit Rad51 to 321

DSB sites, and the efficiency of HR depends on the association of AGO2 with sRNA (Gao et al., 2014). 322

Further genetic studies have provided evidence that diRNAs are involved in not only HR but also the 323

NHEJ repair pathway in plants (Qi et al., 2016), and Oliver and colleagues showed that Arabidopsis 324

AGO9 is involved in somatic DNA repair (Oliver et al., 2014). The role of AGO9 in the repair of 325

damaged DNA remains unknown, but it very likely acts by associating with sRNAs. In addition to 326

Arabidopsis AGO2 and AGO9, AGO1 was recently shown to be involved in the RNA-mediated DNA 327

repair pathway by forming a complex with DNA damage binding protein 2 (DDB2), the stability of 328

which is mediated by DNA and sRNAs (Schalk et al., 2017). Using DDB2 with a mutated DNA-binding 329

domain, the authors first showed that AGO1-DDB2 did not form, and this complex was shown to be 330

less stable in RNAPV and DCL4 mutants, suggesting that the interactions between AGO1 and DDB2 331

are mediated by sRNAs. 332

Further experiments have revealed that the AGO1-DDB2 complex is involved in DNA repair 333

after UV-C irradiation. Cyclobutane pyrimidine dimers (CPDs) are a major form of UV-induced DNA 334

lesions that alter the structure of DNA and inhibit transcription and replication. Schalk and colleagues 335

described plant UV-induced sRNAs (uviRNAs). Most uviRNAs associated with the AGO1-DDB2 336

complex are complementary to the DNA strand enriched in CPDs, and the biogenesis of uviRNAs 337

requires transcription to be carried out by RNAPIV. RDR2 produces dsRNAs, which are processed by 338

DCL4 into 21-nt RNAs (Schalk et al., 2017). These data confirm that DNA repair strongly relies on 339

sRNAs produced by PTGS and RNA-dependent DNA repair pathway (Wei et al., 2012; Oliver et al., 340

2014). DDB2 is a key factor for the recognition of DNA damage in the global genome repair (GGR) 341

pathway and for the repair of DNA lesions via nucleotide excision repair (Scharer, 2013; Schalk et al., 342

2017). 343

Similar to the observed accumulation of AGO1 upon salt stress (Dolata et al., 2016), 344

accumulation of AGO1 together with DDB2 in the nucleus has been associated with UV-C irradiation 345

(Schalk et al., 2017) and observed in the chromatin fraction. However, the levels of both proteins 346

decrease very quickly, suggesting that the AGO1-DDB2 complex is transient and short-lived, existing 347

for only a short period after UV-C stress. The ATR (Ataxia telangiectasia-mutated and RAD3-like) 348 https://plantphysiol.orgDownloaded on November 29, 2020. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.

https://www.uniprot.org/uniprot/A0A1R7T394


9

protein is important for transmitting DNA damage signals to downstream elements, and the AGO1-349

DDB2 complex stability has been shown to be ATR-dependent. Furthermore, in an atr loss-of-350

function mutant, this complex occupies chromatin for a longer time, demonstrating that the ATR-351

mediated signaling of DNA damage is important for release of the AGO1-DDB2 complex from 352

chromatin (Schalk et al., 2017). After detection of DNA damage, DDB2 must be released from 353

chromatin, allowing downstream players to bind and proceed to the next step of DNA repair in the 354

GGR pathway (Chen et al., 2001; Molinier et al., 2008). 355

Finally, the role of AGO1 in DNA repair in the response to UV stress is detectable at the 356

morphological level. The ago1-27 mutant is more sensitive to UV-C during a period of recovery in the 357

dark, which manifests as reduced root growth after UV-C treatment. Moreover, UV irradiation has a 358

positive effect on recruitment of the AGO1-DDB2 complex to CPD-enriched DNA damage sites (Schalk 359

et al., 2017). Therefore, it is possible that after UV stress, numerous uviRNAs are produced by 360

RNAPV, RDR2, and DCL4, and these uviRNAs increase the stabilization of AGO1 and thus lead to the 361

increased occupancy of AGO1-DDB2 complexes on many damaged chromatin sites. 362

363

Future perspectives 364

Studies published in the past few years decisively highlight the various important roles of AGO1 in 365

the plant cell nucleus, but these data indicate only the outline of possible mechanisms. Nevertheless, 366

many efforts have been exerted to describe the pathways driven by chromatin-associated AGO1 in 367

Arabidopsis in detail. The biological relevance of AGO1 in the nucleus is still an open question, since 368

published data point to certain (stress) conditions for its action (see Outstanding Questions). It is 369

possible that nuclear AGO1 partially overlaps in function with its strictly nuclear homologs. However, 370

severe phenotypes of ago1 knockout mutants in comparison to mutants of proteins acting upstream 371

in the PTGS pathway suggest a much wider role for AGO1. Moreover, available data are based on 372

studies in vegetative tissues and might be the tip of the iceberg. Alternatively, nuclear AGO1 373

functions potentially could be much more prominent in meristematic (Kidner and Martienssen, 2005) 374

tissues, in generative tissues or even specialized cells (Grant-Downton et al., 2009; Borges et al., 375

2011), where small RNA pathways are highly active and play distinct but very important roles (Slotkin 376

et al., 2009; Calarco et al., 2012; Borges et al., 2018). 377

An important question that remains unanswered is how AGO1 is recruited to chromatin. 378

Several possibilities for this phenomenon must be considered, beginning with sequence-specific site 379

recognition in the native transcripts via AGO1-associated sRNAs (Allo et al., 2009; Liu et al., 2012) 380

and/or recruitment to specific histone modifications or chromatin-binding proteins (Ameyar-Zazoua 381

et al., 2012; Taliaferro et al., 2013), as shown in animals. Furthermore, it is important to know how 382

AGO1 binding affects transcription, as it may stimulate specific chromatin modifications and impact 383

the ability of RNAPII to bind to promoter regions (Chu et al., 2010; Hu et al., 2012; Huang et al., 384

2013). Moreover, local changes in histone markers may result in RNAPII elongation rate alterations 385

and alternative splice site selection (Allo et al., 2009; Ameyar-Zazoua et al., 2012). 386

The presence of sRNA-loaded AGO1 in the nucleus raises the question of which factors are 387

responsible for deciding whether this complex is exported to the cytoplasm or retained in the 388

nucleus. Until now, no sRNA sequence-based preferences have been found in plants (Bologna et al., 389

2018; Liu et al., 2018), although these preferences have been elucidated in human cells (Hwang et 390

al., 2007). It is possible that retainment of AGO1 in the nucleus requires the binding of some 391

additional factors or specific sRNA modifications. The list of potential AGO1/AGO2 nuclear 392



10

interactors in mammalian cells is broad, suggesting the existence of such interactions in the plant 393

nucleus as well (Ameyar-Zazoua et al., 2012). 394

Interestingly, in Arabidopsis germ line cells, several miRNA-targeted transcripts derived from 395

reactivated transposable elements (TEs) that trigger easiRNA (epigenetically activated sRNA) 396

production have been observed (Creasey et al., 2014; Borges et al., 2018), suggesting that nuclear 397

AGO1 is also involved in protecting the genome from TE-mediated epigenomic instability. Finally, the 398

potential presence of AGO1 in the nucleolus and its association with snoRNA-derived sRNAs (Taft et 399

al., 2009; Gonzalez et al., 2010) raises many questions about its involvement in noncoding RNA 400

maturation. 401

402

403

Author contributions 404

MB, SSB, LS ZSK, AJ, JD, participated in preparing a draft of this manuscript. JD prepared the figure. 405

ZSK, AJ, JD participated in writing and editing the final manuscript. 406

407

Figure legends 408

Figure 1. Diverse functions of ARGONAUTE1 in Arabidopsis thaliana. In addition to its cytoplasmic 409

role in mRNA target cleavage and translation inhibition, AGO1 is associated with chromatin and plays 410

an important role in the regulation of transcription, cotranscriptional miRNA biogenesis, and DNA 411

repair. It is highly probable that AGO1 is also involved in chromatin remodeling and cotranscriptional 412

splicing regulation as well as RNA maturation in the nucleolus. 413

414

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ADVANCES

• Discovery of functional AGO1 in the nucleus has led to re-evaluation of its role in plant cells.

• AGO1 is loaded with miRNAs in the nucleus, and AGO1:miRNA complexes are exported from the nucleus to the cytoplasm to act in various pathways.

• AGO1:miRNA complexes bind to chromatin and positively affect gene transcription.

• AGO1 negatively affects the transcription of select MIR genes.

• AGO1 binds uviRNAs and participates in the repair of UV-induced DNA damage as part of the AGO1:uvi-RNA:DDB2 complex.



OUTSTANDING QUESTIONS

What is the mechanism underlying the selectivity of nuclear-cytoplasmic shuttling?

What are the factors controlling whether the AGO1:miRNA complex is retained in the nucleus? Why is this complex retained in the nucleus?

What elements lead to the stimulation or downregulation of transcription by AGO1?

Does AGO1 influence miRNA levels via cotranscriptional precursor cleavage or abortive transcription?

Does AGO1 bind stress-induced sRNAs (other than uviRNAs) and play a physiological role in the stress response?

Is AGO1 recruited to chromatin by specific histone modifications? Is chromatin remodeling complex recruitment a consequence of AGO1 binding to chromatin?

Does AGO1 affect RNAPII processivity and alternative splicing?

Is AGO1 involved in RNA maturation in the nucleolus?



Nucleus

Cytoplasm

AAAAAA

Translation inhibitionmRNA cleavage

Nucleo-cytoplasmaticshuttling

HSP90

Co-transcriptionalmiRNA biogenesis

Microprocessor DDB2

DNA repair

SWI/SNF

Transcription

Chromatin remodelingNucleolus

Co-transcriptionalmRNA splicing

Spliceosome

RNA maturation

AGO1

Figure 1. Diverse functions of Argonaute1 in Arabidopsis thaliana. In addition to itscytoplasmic role in mRNA target cleavage and translation inhibition, AGO1 is associatedwith chromatin and plays an important role in the regulation of transcription,cotranscriptional miRNA biogenesis, and DNA repair. It is highly probable that AGO1 isalso involved in chromatin remodeling and cotranscriptional splicing regulation as well asRNA maturation in the nucleolus.



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Documents

Nuclear functions of AGO1 · 2019/1/3 · uclear functions of plant AGO proteins 72 were first described for AGO4 (Zilberman et al., 2003) and AGO6 (Zheng et al., 2007; McCue et