Functions of the poly(ADP-ribose) polymerase superfamily in plants

Abstract

Poly(ADP-ribosyl)ation is the covalent attachment of ADP-ribose subunits from NAD(+) to target proteins and was first described in plants in the 1970s. This post-translational modification is mediated by poly(ADP-ribose) polymerases (PARPs) and removed by poly(ADP-ribose) glycohydrolases (PARGs). PARPs have important functions in many biological processes including DNA repair, epigenetic regulation and transcription. However, these roles are not always associated with enzymatic activity. The PARP superfamily has been well studied in animals, but remains under-investigated in plants. Although plants lack the variety of PARP superfamily members found in mammals, they do encode three different types of PARP superfamily proteins, including a group of PARP-like proteins, the SRO family, that are plant specific. In plants, members of the PARP family and/or poly(ADP-ribosyl)ation have been linked to DNA repair, mitosis, innate immunity and stress responses. In addition, members of the SRO family have been shown to be necessary for normal sporophytic development. In this review, we summarize the current state of plant research into poly(ADP-ribosyl)ation and the PARP superfamily in plants.

Fig. 1

Schematic representation of domains found in PARP superfamily proteins. Protein domains are illustrated by colored boxes and are defined according to Pfam 25.0 [34], unless otherwise noted. Proteins are shown to scale with their lengths in amino acids indicated. a Land plants contain proteins similar to HsPARP1. b Land plants contain proteins similar to HsPARP3. c Plants and other eukaryotes contain HsPARP8 orthologs. d The SRO family is land plant specific. BRCT BRCA-1 C-terminus domain (PF00533), FPE fungal PARP E2-associated domain [32], LLP domain of unknown function found in the PARP8 subfamily of the PARP superfamily (Citarelli, Lee and Lamb, unpublished data), PADR1 domain of unknown function found in PARPs (PF08063), PRD PARP regulatory domain, PARP PARP catalytic domain (PF00644), RST RCD-SRO-TAF4 domain (PF12174), SAP presumed nucleic acid binding domain (PF02037), UBCc ubiquitin E2 catalytic domain (PF00179), WGR domain defined by conserved tryptophan, glycine and arginine residues (PF05406), WWE presumed protein-protein interaction domain characterized by tryptophan and glutamic acid residues (PF02825), ZnF DNA binding zinc finger domain (PF00645). At Arabidopsis thaliana, Hs Homo sapiens, Mg Magnaporthe grisea, Pp Physcomitrella patens

Fig. 2

Multiple alignments of the PARP catalytic domains of land plant PARP proteins. These alignments only show the conserved PARP catalytic domain and the numbers indicate amino acids within these domains. Dots indicated gaps introduced to optimize the alignment. Identical amino acids are indicated by red shading and similar amino acids by orange shading. The amino acids present in the catalytic triad are boxed in blue and labeled C1, C2 and C3. The alignments were generated using the MUSCLE3.8.31 multiple alignment tool, using default settings [45]. Structures were obtained from the RCSB Protein Data Bank [117], unless otherwise noted. a Multiple alignment of HsPARP1 and its land plant orthologs. The structural elements present in HsPARP1 are shown at the bottom of the alignment. b Multiple alignment of HsPARP3 and its land plant orthologs. The structural elements present in HsPARP3 are shown at the bottom of the alignment. c Multiple alignment of HsPARP8, MgA4R2D2 and their green algal and moss orthologs. The structural elements present in HsPARP8 are shown below the alignment. d Multiple alignment of members of the SRO family. The predicted structural elements present in AtRCD1 are shown below the alignment. The structural prediction was done using Phyre [76]. Hs Homo sapiens, At Arabidopsis thaliana, Zm Zea mays, Sm Selaginella moellendorfii, Pp Physcomitrella patens, Os Oryza sativa, Mg Magnaporthe grisea, Ch Chlorella sp 142271, Cr Chlamydomonas reinhardtii, Vc Volvox carteri, Pt Populus trichocarpa

Fig. 3

PARP superfamily members are important for stress responses in Arabidopsis thaliana. a The activities of the bona fide PARPs, AtPARP1 and AtPARP2, must be balanced by PARGs and nudix hydrolases in order to maximize stress tolerance. The expression and/or activities of these proteins are induced under stress conditions, where they function to modify proteins that influence stress response. In order to avoid depletion of NAD⁺, PARG and nudix activities release AMP and R5P, which can be recycled. In the absence of PARP activity, accumulated NAD⁺ can be used to produce cADPR to activate ABA-responsive genes. b SRO family members modulate stress responses by repression of ROS and nitric acid. ABA absisic acid, AMP adenosine monophosphate, ATP adenosine triphosphate, cADPR cyclic nucleotide ADP-ribose, MAPK mitogen-activated protein kinase, NAD ⁺ nicotinamide adenine dinucleotide, NO nitric oxide, P5CDH Δ¹-pyrroline-5-carboxylate dehydrogenase, R5P ribose-5-phosphate, ROS reactive oxygen species, SIMR stress-induced morphogenetic response. References: [, –6, 22, 33, 38, 49, 64, 65, 70, 71, 98, 104, 109, 115, 123, 131, 133, 142, 147]