Diversity and functional importance of phytoplasma membrane proteins

Abstract

0.5–1.3 Mbp) that are phylogenetically classified in the classMollicutes. Phytoplasmas inhabit the phloem sieveelements of plants and cause numerous plant diseases.They are also intracellular parasites of phloem-feedinginsects and are transmitted between plants by insects [1].Like other organisms in the Mollicutes such as mycoplas-mas, phytoplasmas lack a cell wall; therefore, theirmembrane proteins are in direct contact with thecytoplasm of plant or insect host cells and might haveimportant roles in host–bacterium interactions. However,little is known about phytoplasma membrane proteinsbecause of the difficulty of culturing phytoplasmasin vitro. Previous studies have proposed that a subset ofmembrane proteins, usually referred to as immunodomi-nant membrane proteins (IDPs), constitute a majorportion of the total cellular membrane proteins in mostphytoplasmas [2]. Here, we discuss the diversity andimportance of IDPs.Three non-homologous types of IDPRecently, genes that encode IDPs have been isolated fromseveral groups of phytoplasmas [2,3] and these studiesrevealed that the IDPs are classified into three distincttypes: (i) immunodominant membrane protein (Imp); (ii)immunodominant membrane protein A (IdpA); and (iii)antigenic membrane protein (Amp). The phylogeneticrelationships of phytoplasmas [4] and the gene organiz-ation and transmembrane structures of these three typesof IDP are summarized in Figure 1. These IDPs show noamino acid similarity, are located on different parts of thegenome (Figure 1a) and their predicted transmembranestructures differ greatly (Figure 1b). Interestingly, thegene encoding imp was observed in the genomes of theWestern X-disease phytoplasma (WX) [5] and onionyellows phytoplasma (OY) (S. Kakizawa et al., unpub-lished) in addition to their original IDP genes. Therefore,one of three non-homologous types of IDP can have anidentical role in different phytoplasmas, constituting themajor portion of the plasma membrane proteins.In some host–bacteria associations, there are reports ofmembrane-protein gene exchange with silent gene copies(e.g. the pilE gene of Neisseria meningitidis [6] or genesfor the P35 family of Mycoplasma penetrans [7]). Onecould speculate that the existence of three IDP types hasresulted from gene exchange. The gene encoding imp ishighly conserved across phytoplasma species and it islikely that this form of IDP was present in the ancestralphytoplasma and that the IDPs of several phytoplasmassuch as WX and OY have undergone changes. An analysisof differences in the expression level and condition ofdifferent types of IDP would shed light on the function ofnon-homologous IDPs.The variability and importance of IDPsThe IDPs within a type can be highly variable and thesequence variability of IDP genes between phytoplasmasis lower than their upstream or downstream genes or non-coding regions [2]. In most cases, coding regions rarelyshow lower identities than non-coding regions because offunctional constraints; thus, these observations suggestthat IDPs have been subjected to strong divergentselective pressure. Moreover, it has been reported thatthe sequence identities of imp in several phytoplasmaswere not correlated with that of 16S rDNA, whichsuggests that the variability of IDPs reflects some factorsother than evolutionary time [3].Possible function of IDP and future perspectivesWhat are the functions of IDPs and why are they sovariable? Although these questions remain unclear, thevariabilityofIDPsshouldbestronglycorrelatedwiththeirfunction because not all membrane proteins of phytoplas-mas have been subjected to strong divergent selectivepressure [8]. Several studies have reported that host–bacterium interactions promote the variability of bacterialmembrane proteins [9]. Based on these examples, onecould extrapolate to the phytoplasmas and suggestdivergent selective pressures such as adaptation to avoidthe insect vector immune system (similar to severalmembrane proteins of animal pathogens [6,7,9])orattachment to host proteins, which is an important stepin establishing infection for several pathogens [10,11].Inthe example of the membrane protein OspC of Borreliaburgdorferi (the causative agent of Lyme disease) [12], theattachment protein, which has an important role ininfection, must co-evolve with the host and might alsoneed to change itself positively to adapt to a new hostspecies. Insights into the diversity and function of IDPsshould be an important focus for future research. Isolationof the host proteins that interact with IDPs will elucidate