Evolution of Bacterial-Like Phosphoprotein Phosphatases in Photosynthetic Eukaryotes Features Ancestral Mitochondrial or Archaeal Origin and Possible Lateral Gene Transfer      

Abstract

Protein phosphorylation is a reversible regulatory process catalyzed by the opposing reactions of protein kinases and phosphatases, which are central to the proper functioning of the cell. Dysfunction of members in either the protein kinase or phosphatase family can have wide-ranging deleterious effects in both metazoans and plants alike. Previously, three bacterial-like phosphoprotein phosphatase classes were uncovered in eukaryotes and named according to the bacterial sequences with which they have the greatest similarity: Shewanella-like (SLP), Rhizobiales-like (RLPH), and ApaH-like (ALPH) phosphatases. Utilizing the wealth of data resulting from recently sequenced complete eukaryotic genomes, we conducted database searching by hidden Markov models, multiple sequence alignment, and phylogenetic tree inference with Bayesian and maximum likelihood methods to elucidate the pattern of evolution of eukaryotic bacterial-like phosphoprotein phosphatase sequences, which are predominantly distributed in photosynthetic eukaryotes. We uncovered a pattern of ancestral mitochondrial (SLP and RLPH) or archaeal (ALPH) gene entry into eukaryotes, supplemented by possible instances of lateral gene transfer between bacteria and eukaryotes. In addition to the previously known green algal and plant SLP1 and SLP2 protein forms, a more ancestral third form (SLP3) was found in green algae. Data from in silico subcellular localization predictions revealed class-specific differences in plants likely to result in distinct functions, and for SLP sequences, distinctive and possibly functionally significant differences between plants and nonphotosynthetic eukaryotes. Conserved carboxyl-terminal sequence motifs with class-specific patterns of residue substitutions, most prominent in photosynthetic organisms, raise the possibility of complex interactions with regulatory proteins.

Activation of Mitochondrial Protein Phosphatase SLP2 by MIA40 Regulates Seed Germination

“…In humans and Arabidopsis (Arabidopsis thaliana) the canonical eukaryotic PPP Ser/Thr protein phosphatase complement is encoded by 13 and 26 catalytic subunits respectively, most of which require interaction with regulatory proteins to direct their specificity within the cell (Moorhead et al, 2009;Heroes et al, 2013;Uhrig et al, 2013b). In Arabidopsis and all other plants, we have uncovered a unique subfamily of prokaryotic-like PPP-family phosphatases called the Shewanella-like protein (SLP) phosphatases (Andreeva and Kutuzov, 2004;Uhrig and Moorhead, 2011;Uhrig et al, 2013a), which was found to further divide into two distinct groups called SLP1 and SLP2, differing in both subcellular localization and spatial expression across the plant (Uhrig and Moorhead, 2011). Characterization of SLP phosphatases from Arabidopsis (At) showed that AtSLP1 is chloroplast targeted and expressed exclusively in photosynthetic tissues, while AtSLP2 is likely cytosolic and highly expressed in nonphotosynthetic tissues (Uhrig and Moorhead, 2011).…”

Protein phosphatase 2A regulatory subunits affecting plant innate immunity, energy metabolism, and flowering time – joint functions among B'η subfamily members

“…[1][2][3] The Arabidopsis PP2A regulatory subunits (B subunits) are classified into 3 non-related families; B/B55 (a and b), B' (a, b, g, d, e, z, h, u, and k), and B" (a, b, g, d, e, and TON2). 4,5 The B' family is divided into 3 subfamilies a, h, and k, where the h subfamily comprises the close homologs B'h, B'g, B'u, and B'z.…”

Enzymatic characteristics of an ApaH‐like phosphatase, PrpA, and a diadenosine tetraphosphate hydrolase, ApaH, from Myxococcus xanthus

“…The PPP superfamily contains conserved four-sequence motifs, GDXHG, GDXXDRG, GNHE and HGG, where X is any residue in the N-terminal subdomain of about 100 amino acids [8,17]. M. xanthus PrpA contains the three core signature motifs (GDXHG, GDXXDRG, and GNHE); however, M. xanthus ApaH possesses modified motifs 2 and 3, i.e., GDXXAKG and GNHD sequences, …”

“…One group of bacterial PPPs shares homology with diadenosine tetraphosphate (Ap 4 A) hydrolases (ApaHs), and is termed ApaHlike phosphatases [7][8][9]. The Ap 4 A is composed of two adenosine moieties joined in a 5-5 0 linkage by a chain of four phosphates that is ubiquitous in prokaryotic and eukaryotic cells [10].…”