Protein Poly(ADP-ribosyl)ation Regulates Arabidopsis Immune Gene Expression and Defense Responses

Abstract

Perception of microbe-associated molecular patterns (MAMPs) elicits transcriptional reprogramming in hosts and activates defense to pathogen attacks. The molecular mechanisms underlying plant pattern-triggered immunity remain elusive. A genetic screen identified Arabidopsis poly(ADP-ribose) glycohydrolase 1 (atparg1) mutant with elevated immune gene expression upon multiple MAMP and pathogen treatments. Poly(ADP-ribose) glycohydrolase (PARG) is predicted to remove poly(ADP-ribose) polymers on acceptor proteins modified by poly(ADP-ribose) polymerases (PARPs) with three PARPs and two PARGs in Arabidopsis genome. AtPARP1 and AtPARP2 possess poly(ADP-ribose) polymerase activity, and the activity of AtPARP2 was enhanced by MAMP treatment. AtPARG1, but not AtPARG2, carries glycohydrolase activity in vivo and in vitro. Importantly, mutation (G450R) in atparg1 blocks its activity and the corresponding residue is highly conserved and essential for human HsPARG activity. Consistently, mutant atparp1atparp2 plants exhibited compromised immune gene activation and enhanced susceptibility to pathogen infections. Our study indicates that protein poly(ADP-ribosyl)ation plays critical roles in plant immune gene expression and defense to pathogen attacks.

From Chaos to Harmony: Responses and Signaling upon Microbial Pattern Recognition

“…The Mediator complex is also implicated in plant defense, yet its precise connection with PTI signaling is not established (82). Using a forward genetic screen based on flg22-induced gene transcriptional change, protein poly(ADP-ribosyl)ation (PARylation), which is reversibly regulated by poly(ADP-ribose) polymerases (PARPs) and poly(ADP-ribose) glycohydrolases (PARGs), was indicated to play a role in regulating MAMP-responsive gene expression (41). flg22 treatment induces the PARylation of the forkhead-associated domain protein DAWDLE, a substrate of Arabidopsis PARP2, to regulate some of late PTI responses (42).…”

Phosphorylation of Trihelix Transcriptional Repressor ASR3 by MAP KINASE4 Negatively Regulates Arabidopsis Immunity

“…FRK1 is a specific and early immune-responsive gene activated by multiple MAMPs (Asai et al, 2002;He et al, 2006). A series of mutants with altered FRK1 promoter activity upon flg22 treatment or inoculation with nonpathogenic Pseudomonas syringae pv tomato (Pst) DC3000 type III secretion mutant hrcC were identified and named as Arabidopsis genes governing immune gene expression (aggies) (Li et al, 2014a;Feng et al, 2015). During the map-based cloning of the aggie1 mutant, a collection of homozygous Salk T-DNA insertion mutants for individual genes located in a 110-kb region on Chromosome 2 was analyzed for disease resistance to the virulent bacterium Pst DC3000 infection and flg22-induced FRK1 expression.…”

Protein ADP-Ribosylation Takes Control in Plant–Bacterium Interactions

“…AtPARP1 bears the highest homology to HsPARP-1, which is the most active, ubiquitous, and abundant member of PARPs in humans. However, Arabidopsis AtPARP2 is enzymatically more active than AtPARP1 in both in vitro and in vivo assays and plays a predominant role in DNA damage responses and plant immunity [14,15]. AtPARP3 is primarily expressed in seeds [15].…”

“…Compared to only one PARG gene in humans and mice, Arabidopsis contains two PARGs ( AtPARG1 and AtPARG2 ) (Fig 1B). AtPARG1 shows strong PAR glycohydrolase activity, and AtPARG2, which carries a polymorphism in the PARG signature motif, is likely enzymatically inactive [15,18]. The ARH hydrolase has not been found in plants.…”

“…Recent studies suggest the essential role of protein PARylation in plant immunity [14,15,19,20]. A transcriptomic analysis of plant ETI responses identified AtPARG2 as one of the highly induced genes in multiple plant–bacterium interactions [20].…”