Target specificity among canonical nuclear poly(A) polymerases in plants modulates organ growth and pathogen response

Abstract

Polyadenylation of pre-mRNAs is critical for efficient nuclear export, stability, and translation of the mature mRNAs, and thus for gene expression. The bulk of pre-mRNAs are processed by canonical nuclear poly(A) polymerase (PAPS). Both vertebrate and higher-plant genomes encode more than one isoform of this enzyme, and these are coexpressed in different tissues. However, in neither case is it known whether the isoforms fulfill different functions or polyadenylate distinct subsets of pre-mRNAs. Here we show that the three canonical nuclear PAPS isoforms in Arabidopsis are functionally specialized owing to their evolutionarily divergent C-terminal domains. A strong loss-of-function mutation in PAPS1 causes a male gametophytic defect, whereas a weak allele leads to reduced leaf growth that results in part from a constitutive pathogen response. By contrast, plants lacking both PAPS2 and PAPS4 function are viable with wild-type leaf growth. Polyadenylation of SMALL AUXIN UP RNA (SAUR) mRNAs depends specifically on PAPS1 function. The resulting reduction in SAUR activity in paps1 mutants contributes to their reduced leaf growth, providing a causal link between polyadenylation of specific pre-mRNAs by a particular PAPS isoform and plant growth. This suggests the existence of an additional layer of regulation in plant and possibly vertebrate gene expression, whereby the relative activities of canonical nuclear PAPS isoforms control de novo synthesized poly(A) tail length and hence expression of specific subsets of mRNAs.

UBIQUITIN-SPECIFIC PROTEASE 14 interacts with ULTRAVIOLET-B INSENSITIVE 4 to regulate endoreduplication and cell and organ growth in Arabidopsis

“…We also found that da3-1 had small root meristems with a reduced cell number (Supplemental Figure 4), suggesting that DA3 influences cell proliferation in an organ-dependent manner. Similar contextdependent effects were also seen for da1-ko1 dar1-1 dar2-1 and paps1-1 mutants (Vi et al, 2013;Peng et al, 2015).…”

“…Several factors have been known to affect organ growth in an organ-dependent manner. For example, loss-of-function mutations in poly(A) polymerase PAPS1 caused large flowers and small leaves (Vi et al, 2013). The simultaneous disruption of DA1, DA1-related protein 1 (DAR1), and DAR2 resulted in large seeds and flowers, small leaves, and short roots (Peng et al, 2015).…”

The Polyadenylation Factor Subunit CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR30: A Key Factor of Programmed Cell Death and a Regulator of Immunity in Arabidopsis

“…Here, we showed that oxt6 and mips1 oxt6 mutants were more susceptible than wild-type control plants to the virulent bacterium Pst. Furthermore, it recently has been shown that the reduced activity of PAPS1, a poly(A) polymerase that is recruited to add the poly(A) tail after the cleavage of the nascent premRNA, leads to a constitutive pathogen response via an EDS1/PAD4-dependent mechanism Vi et al, 2013). Likewise, the Arabidopsis protein FPA, which functions independently of the CPSF complex to regulate alternative polyadenylation, has been shown to negatively modulate the flagellin response (Lyons et al, 2013).…”

Leaf development and morphogenesis

“…Furthermore, the E3 ubiquitin-ligase BIG BROTHER (BB) can repress plant organ growth, probably by marking cellular proteins for degradation (Disch et al, 2006). Recently, poly(A) polymerases (PAPS) have been shown to influence leaf size and shape, probably by affecting the expression of specific subsets of relevant genes (Vi et al, 2013). In Cardamine hirsuta, the ribosome-associated protein SIMPLE LEAF3 also affects leaf growth and leaflet development (Kougioumoutzi et al, 2013).…”