Commonalities and differences of T3SSs in rhizobia and plant pathogenic bacteria

Abstract

Plant pathogenic bacteria and rhizobia infect higher plants albeit the interactions with their hosts are principally distinct and lead to completely different phenotypic outcomes, either pathogenic or mutualistic, respectively. Bacterial protein delivery to plant host plays an essential role in determining the phenotypic outcome of plant-bacteria interactions. The involvement of type III secretion systems (T3SSs) in mediating animal- and plant-pathogen interactions was discovered in the mid-80's and is now recognized as a multiprotein nanomachine dedicated to trans-kingdom movement of effector proteins. The discovery of T3SS in bacteria with symbiotic lifestyles broadened its role beyond virulence. In most T3SS-positive bacterial pathogens, virulence is largely dependent on functional T3SSs, while in rhizobia the system is dispensable for nodulation and can affect positively or negatively the mutualistic associations with their hosts. This review focuses on recent comparative genome analyses in plant pathogens and rhizobia that uncovered similarities and variations among T3SSs in their genetic organization, regulatory networks and type III secreted proteins and discusses the evolutionary adaptations of T3SSs and type III secreted proteins that might account for the distinguishable phenotypes and host range characteristics of plant pathogens and symbionts.

Keywords: atypical T3SSs; nodulation; pili; plant pathogenic bacteria; plant-associated bacteria; rhizobia; translocator; type III secretion.

Figure 1

Neighbor-joining phylogenies of SctU proteins from representative phytopathogenic and plant-associated bacteria. The red asterisk denotes atypical hrp/hrc gene clusters, as discussed in the text. The bacteria belonging to hrp/hrc3 group also harbor a hrp/hrc1 gene cluster which is not represented in the tree, in all cases (see Table 1). The evolutionary distances were estimated using the p-distance method and are in the units of the number of amino acid differences per site. Numbers to the left of the branches are bootstrap values for 1000 replications. Bootstrap values greater than 50% are shown, and the scale bar represents the number of substitutions per site. Branch lengths are proportional to the amount of evolutionary change. Evolutionary analyses were conducted in MEGA6 (Tamura et al., 2013).

Figure 2

Neighbor-joining phylogenies of SctU proteins from rhizobia. The evolutionary distances were estimated using the p-distance method and are in the units of the number of amino acid differences per site. Numbers to the left of the branches are bootstrap values for 1000 replications. Bootstrap values greater than 50% are shown, and the scale bar represents the number of substitutions per site. Branch lengths are proportional to the amount of evolutionary change. Evolutionary analyses were conducted in MEGA6 (Tamura et al., 2013).

Figure 3

Genetic organization of functional rhizobial T3SS gene clusters. Genes are represented by colored arrows showing the sense of transcription. Conserved rhc genes are shown as red arrows and the capital letters above the arrows are abbreviations of the T3SS families according to the sct nomenclature. Red dotted arrows show rhizobial-specific T3SS genes. Gene names below the arrows generally correspond to nomenclature from the literature. nod boxes are indicated by red arrowheads and tts boxes by black arrowheads. Yellow arrows show type III effector genes (T3E) with homologs in other rhizobia and/or pathogenic bacteria, while blue arrows indicate T3E genes unique in the corresponding strain/species and the green ones show the genes coding for the transcriptional regulator of rhizobial T3SSs. Open arrows indicate unknown or possibly unrelated T3SS genes. Black dashed arrows show transposases/integrases and blue asterisks show regions rich in mobile elements. The locus tags of each tts cluster are as follows: S. fredii NGR234a: NGR_a00520-NGR_a00800; S. fredii USDA257: USDA257_p02960-USDA257_p02630; M. loti: mlr6327-mlr8765; B. japonicum: bll1796-bll1844; B. elkanii: GenBank accession number FM162234; R. etli: RHE_PD00051-RHE_PD00067; C. taiwanensis: RALTA_B1250-RALTA_B1267. The tts cluster of S. fredii HH103 is not presented since it is identical to the S. fredii USDA257.

Figure 4

Non-canonical T3SS gene clusters in phytopathogenic bacteria and rhizobial species. Genes are represented according to the key of Figure 1. The locus tags for inv/mxi/spa-type T3SS are as follows: E. amylovora CFBP1430: EAMY_0771-EAMY_0792 (T3SS-II) and EAMY_1573-EAMY_1593 (T3SS-III); Pantoea stewartii stewartii DC283: CKS_4544-CKS_4519; Xanthomonas albilineans GPE PC73: XALc_1472-XALc_1511. The locus tags for hrp/hrc3 in Psp 1448A are: PSPPH_2515-PSPPH_2540. The locus tags of each tts cluster are as follows: S. fredii NGR234a: NGR_b22750-NGR_b23010; S. fredii USDA257: USDA257_c21410-USDA257_c21670; S. fredii HH103_pSfHH103e: SFHH103_04955-SFHH103_04964; S. meliloti GR4_pRmeGR4c: C770_GR4pC1282-C770_GR4pC1261; S. meliloti GR4_pRmeGR4b: C770_GR4pB203-C770_GR4pB213, C770_GR4pB244-C770_GR4pB246, C770_GR4pB251-C770_GR4pB253; A. radiobacter K84: Arad_8755-Arad_8778; A. rhizogenes A4: arA4DRAFT_00042330-arA4DRAFT_00042490. The tts cluster of R. leguminosarum bv. phaseoli 4292 (Rleg18DRAFT_6856-Rleg18DRAFT_6875) is not presented since it is identical in gene content and organization to that of R. etli strains (Figure 3).