A TALE of Transposition: Tn 3 -Like Transposons Play a Major Role in the Spread of Pathogenicity Determinants of Xanthomonas citri and Other Xanthomonads

Abstract

Members of the genus Xanthomonas are among the most important phytopathogens. A key feature of Xanthomonas pathogenesis is the translocation of type III secretion system (T3SS) effector proteins (T3SEs) into the plant target cells via a T3SS. Several T3SEs and a murein lytic transglycosylase gene (mlt, required for citrus canker symptoms) are found associated with three transposition-related genes in Xanthomonas citri plasmid pXAC64. These are flanked by short inverted repeats (IRs). The region was identified as a transposon, TnXax1, with typical Tn3 family features, including a transposase and two recombination genes. Two 14-bp palindromic sequences within a 193-bp potential resolution site occur between the recombination genes. Additional derivatives carrying different T3SEs and other passenger genes occur in different Xanthomonas species. The T3SEs include transcription activator-like effectors (TALEs). Certain TALEs are flanked by the same IRs as found in TnXax1 to form mobile insertion cassettes (MICs), suggesting that they may be transmitted horizontally. A significant number of MICs carrying other passenger genes (including a number of TALE genes) were also identified, flanked by the same TnXax1 IRs and delimited by 5-bp target site duplications. We conclude that a large fraction of T3SEs, including individual TALEs and potential pathogenicity determinants, have spread by transposition and that TnXax1, which exhibits all of the essential characteristics of a functional transposon, may be involved in driving MIC transposition. We also propose that TALE genes may diversify by fork slippage during the replicative Tn3 family transposition. These mechanisms may play a crucial role in the emergence of Xanthomonas pathogenicity.

Ribosomal frameshifting and transcriptional slippage: From genetic steganography and cryptography to adventitious use

“…encoding transcription regulators or antibiotic resistance, can be within a 'transporter' IS element, and in other ways also relevant distinctions are becoming imprecise, e.g. among IS elements of Xanthomonas phytopathogens (199). The distinction between certain IS and the much larger ICE type elements is also becoming more 'fuzzy' in part because of the type of transposase used by several of the latter (183).…”

Using Ecology, Physiology, and Genomics to Understand Host Specificity in Xanthomonas

“…Several pathogenicity determinants such as TAL effector genes are often located in regions corresponding to mobile insertion cassettes (46), and knowledge about the structure, contents, and evolutionary history of those regions will greatly help in understanding the importance of recombination and HGT in host and tissue specialization. The recent sequencing and resequencing of several X. oryzae strains indeed revealed a dynamic genome structure and an important plasticity in TAL effector genes through HGT, duplication, and recombination (19).…”

Recombination‐prone bacterial strains form a reservoir from which epidemic clones emerge in agroecosystems

“…In phytopathogenic members of the genera Pseudomonas and Xanthomonas , such LHT‐associated genes are involved in host specificity; for instance, repertoires of these genes correlates with host range (Sarkar et al ., ; Lindeberg et al ., ; Hajri et al ., ; Mhedbi‐Hajri et al ., ; Hajri et al ., ; Mhedbi‐Hajri et al ., ; Schwartz et al ., ). LHT‐associated genes are often located on mobile genetic elements, such as plasmids or transposons, and can easily be lost or gained via HGT (Alfano and Collmer, ; Ferreira et al ., ; Huang et al ., ). If we wish to understand the evolutionary epidemiology of bacterial plant diseases, it will be crucial to characterize gene flows among nonpathogenic and pathogenic strains and examine the potential influence of nonpathogenic strains on the emergence of epidemic clones.…”