A partial loss-of-function mutation in an Arabidopsis RNA polymerase III subunit leads to pleiotropic defects

Johnson, Kaeli C. M.; Yu, Yu; Gao, Lei; Eng, Ryan Christopher; Wasteneys, Geoffrey O.; Li, Xin

doi:10.1093/jxb/erw020

Cited by 17 publications

(14 citation statements)

References 52 publications

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“…The subtle phenotypes associated with the muse7 single mutants suggest that MUSE7 does not play a dramatic general role in immunity. Similar observations were made for several other muse mutants (Johnson et al ., , ). The increased level of SNC1 protein in muse7‐2 snc1 relative to snc1 did not correlate with elevated SNC1 transcription (Figure ).…”

Section: Discussionmentioning

confidence: 99%

“…Among the 10 published MUSE proteins, seven have been shown to play essential roles in NLR protein turnover (Huang et al ., ,b, ; Xu et al ., ; Copeland et al ., ). The other three include MUSE4/NRPC7, an RNA polymerase III subunit for which a partial loss‐of‐function mutation results in pleiotropic defects (Johnson et al ., ); MUSE5/AtPAM16, a component of the protein import motor in the mitochondrial inner membrane that negatively affects ROS production and immunity (Huang et al ., ); and MUSE9/SPLAYED, a SWI/SNF chromatin remodeler that affects SNC1 gene expression (Johnson et al ., ). Together, these reports demonstrate the efficacy of the MUSE screen in identifying new components that are involved in plant immunity.…”

Section: Introductionmentioning

confidence: 99%

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The putative kinase substrate MUSE7 negatively impacts the accumulation of NLR proteins

Johnson

Zhao

et al. 2017

The Plant Journal

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Stringent modulation of immune signaling in plants is necessary to enable a rapid response to pathogen attack without spurious defense activation. To identify genes involved in plant immunity, a forward genetic screen for enhancers of the autoimmune snc1 (suppressor of npr1, constitutive 1) mutant was conducted. The snc1 mutant contains a gain-of-function mutation in a gene encoding a NOD-like receptor (NLR) protein. The isolated muse7 (mutant, snc1-enhancing, 7) mutant was shown to confer a reversion to autoimmune phenotypes in the wild-type-like mos4 (modifier of snc1, 4) snc1 background. Positional cloning revealed that MUSE7 encodes an evolutionarily conserved putative kinase substrate of unknown function. The muse7 single mutants display enhanced resistance to the bacterial pathogen Pseudomonas syringae pv. tomato DC3000. While transcription of SNC1 is not enhanced, elevated SNC1 protein accumulation is associated with mutations in muse7. Accumulation of two additional NLR proteins, RPS2 (RESISTANCE TO PSEUDOMONAS SYRINGAE 2) and RPM1 (RESISTANCE TO PSEUDOMONAS SYRINGAE pv. MACULICOLA 1), was also observed in muse7 plants. Although proteasome-mediated degradation of NLR proteins is a well studied event in plant immunity, no interactions were detected between MUSE7 and selected components of this pathway. This study has demonstrated a role for MUSE7 in modulating plant immune responses through negatively affecting NLR accumulation, and will benefit future studies of MUSE7 homologs in other species.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The putative kinase substrate MUSE7 negatively impacts the accumulation of NLR proteins

Johnson

Zhao

et al. 2017

The Plant Journal

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“…This implies that the normal functioning of the subunit is altogether critical for plant development and survival. Recently, Johnson et al 60. demonstrated that a loss-of-function mutant of Arabidopsis RNAPIII subunit nrpc7-1 displayed multiple phenotypic defects including dwarf morphology, stunted siliques and serrated leaves60.…”

Section: Discussionmentioning

confidence: 99%

Virus-induced gene silencing of the RPC5-like subunit of RNA polymerase III caused pleiotropic effects in Nicotiana benthamiana

Nemchinov

Boutanaev

Postnikova

2016

Sci Rep

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In eukaryotic cells, RNA polymerase III is highly conserved and transcribes housekeeping genes such as ribosomal 5S rRNA, tRNA and other small RNAs. The RPC5-like subunit is one of the 17 subunits forming RNAPIII and its exact functional roles in the transcription are poorly understood. In this work, we report that virus-induced gene silencing of transcripts encoding a putative RPC5-like subunit of the RNA Polymerase III in a model species Nicotiana benthamiana had pleiotropic effects, including but not limited to severe dwarfing appearance, chlorosis, nearly complete reduction of internodes and abnormal leaf shape. Using transcriptomic analysis, we identified genes and pathways affected by RPC5 silencing and thus presumably related to the cellular roles of the subunit as well as to the downstream cascade of reactions in response to partial loss of RNA Polymerase III function. Our results suggest that silencing of the RPC5L in N. benthamiana disrupted not only functions commonly associated with the core RNA Polymerase III transcripts, but also more diverse cellular processes, including responses to stress. We believe this is the first demonstration that activity of the RPC5 subunit is critical for proper functionality of RNA Polymerase III and normal plant development.

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“…In zebra fish, a mutation resulting from a premature stop codon at Rpc9 locus impairs hematopoietic stem and progenitor cell maintenance (Wei et al, 2016). The nrpc7 mutation occurs in a gene encoding the Arabidopsis thaliana ortholog of the yeast RNAPIII subunit RPC25, which causes altered expression of a number of RNA molecules and a pleiotropic development abnormality in plant morphogenesis (Johnson et al, 2016). Meanwhile, several reports have demonstrated that the fine modulation of RNAPIII transcription mediated by key factors is also essential for normal organism development.…”

Section: Fl3 As a New Regulator In Rnapiii Transcription Machinerymentioning

confidence: 99%

The Maize Imprinted Gene Floury3 Encodes a PLATZ Protein Required for tRNA and 5S rRNA Transcription through Interaction with RNA Polymerase III

Wang

et al. 2017

Plant Cell

118

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Maize (Zea mays) floury3 (fl3) is a classic semidominant negative mutant that exhibits severe defects in the endosperm but fl3 plants otherwise appear normal. We cloned the fl3 gene and determined that it encodes a PLATZ (plant AT-rich sequence and zinc binding) protein. The mutation in fl3 resulted in an Asn-to-His replacement in the conserved PLATZ domain, creating a dominant allele. Fl3 is specifically expressed in starchy endosperm cells and regulated by genomic imprinting, which leads to the suppressed expression of fl3 when transmitted through the male, perhaps as a consequence the semidominant behavior. Yeast two-hybrid screening and bimolecular luciferase complementation experiments revealed that FL3 interacts with the RNA polymerase III subunit 53 (RPC53) and transcription factor class C 1 (TFC1), two critical factors of the RNA polymerase III (RNAPIII) transcription complex. In the fl3 endosperm, the levels of many tRNAs and 5S rRNA that are transcribed by RNAPIII are significantly reduced, suggesting that the incorrectly folded fl3 protein may impair the function of RNAPIII. The transcriptome is dramatically altered in fl3 mutants, in which the downregulated genes are primarily enriched in pathways related to translation, ribosome, misfolded protein responses, and nutrient reservoir activity. Collectively, these changes may lead to defects in endosperm development and storage reserve filling in fl3 seeds.

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A partial loss-of-function mutation in an Arabidopsis RNA polymerase III subunit leads to pleiotropic defects

Abstract: HighlightAnalysis of the first known viable RNA polymerase III subunit mutant in Arabidopsis reveals novel roles for this complex in maintaining RNA homeostasis, adjusting the expression of a diverse suite of genes, and indirectly modulating alternative splicing.

Cited by 17 publications

References 52 publications

The putative kinase substrate MUSE7 negatively impacts the accumulation of NLR proteins

The putative kinase substrate MUSE7 negatively impacts the accumulation of NLR proteins

Virus-induced gene silencing of the RPC5-like subunit of RNA polymerase III caused pleiotropic effects in Nicotiana benthamiana

The Maize Imprinted Gene Floury3 Encodes a PLATZ Protein Required for tRNA and 5S rRNA Transcription through Interaction with RNA Polymerase III

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