mRNA deadenylation by PARN is essential for embryogenesis in higher plants

Abstract

Deadenylation of mRNA is often the first and rate-limiting step in mRNA decay. PARN, a poly(A)-specific 3' --> 5' ribonuclease which is conserved in many eukaryotes, has been proposed to be primarily responsible for such a reaction, yet the importance of the PARN function at the whole-organism level has not been demonstrated in any species. Here, we show that mRNA deadenylation by PARN is essential for viability in higher plants (Arabidopsis thaliana). Yet, this essential requirement for the PARN function is not universal across the phylogenetic spectrum, because PARN is dispensable in Fungi (Schizosaccharomyces pombe), and can be at least severely downregulated without any obvious consequences in Metazoa (Caenorhabditis elegans). Development of the Arabidopsis embryos lacking PARN (AtPARN), as well as of those expressing an enzymatically inactive protein, was markedly retarded, and ultimately culminated in an arrest at the bent-cotyledon stage. Importantly, only some, rather than all, embryo-specific transcripts were hyperadenylated in the mutant embryos, suggesting that preferential deadenylation of a specific select subset of mRNAs, rather than a general deadenylation of the whole mRNA population, by AtPARN is indispensable for embryogenesis in Arabidopsis. These findings indicate a unique, nonredundant role of AtPARN among the multiple plant deadenylases.

A poly(A)-specific ribonuclease directly regulates the poly(A) status of mitochondrial mRNA in Arabidopsis

“…As reported previously, mutations disrupting AHG2 are embryonic lethal [19][20][21] , and ahg2-1 causes hypersensitivity to the phytohormones ABA and SA 21 , demonstrating that the defect in Relative amounts of mt-DNA to genomic DNA, mt-DNA to mitochondrial protein and mitochondrial mRNA to mt-DNA. Total DNA prepared from 2-week-old plants was used for qPCR analysis of mitochondrial-encoded cox2 and nad4, and of nuclear-encoded AGS1, and the relative amount of mt-DNA to nc-DNA was deduced.…”

“…Arabidopsis possesses one gene encoding a functional PARN, named AHG2 (also known as AtPARN) [19][20][21] . Plants harbouring a weak mutant allele of this gene display a dwarf phenotype and respond abnormally to the stress-related phytohormones abscisic acid (ABA) and salicylic acid (SA) 21,22 .…”

“…Plants harbouring a weak mutant allele of this gene display a dwarf phenotype and respond abnormally to the stress-related phytohormones abscisic acid (ABA) and salicylic acid (SA) 21,22 . Null mutants are not viable [19][20][21] , suggesting that AHG2 has an important and unique function in Arabidopsis. Here we show that AHG2, in cooperation with a bacterial-type PAP named AGS1, regulates mitochondrial mRNA by affecting the poly(A) tract, which acts as a degradation tag.…”

The Arabidopsis homologs of CCR4-associated factor 1 show mRNA deadenylation activity and play a role in plant defence responses

“…This is likely because of a redundancy in mRNA deadenylation systems in Arabidopsis. AtPARN, homolog of the important deadenylase PARN in mammalian cells, has deadenylation activity on some embryo-specific transcripts [8]. Furthermore, the genome of Arabidopsis also encodes a putative homolog of yeast PAN2 protein.…”

“…Three enzyme complexes, CCR4-NOT [4], PAN2-PAN3 [5,6] and PARN [7][8][9], have been identified as mRNA deadenylases in eukaryotic cells. CCR4-associat-npg ed factor 1 (CAF1) is a subunit of the CCR4-NOT complex, which is an evolutionarily conserved protein complex.…”