Genomic Analysis of Xanthomonas translucens Pathogenic on Wheat and Barley Reveals Cross-Kingdom Gene Transfer Events and Diverse Protein Delivery Systems

Abstract

In comparison to dicot-infecting bacteria, only limited numbers of genome sequences are available for monocot-infecting and in particular cereal-infecting bacteria. Herein we report the characterisation and genome sequence of Xanthomonas translucens isolate DAR61454 pathogenic on wheat and barley. Based on phylogenetic analysis of the ATP synthase beta subunit (atpD) gene, DAR61454 is most closely related to other X. translucens strains and the sugarcane- and banana- infecting Xanthomonas strains, but shares a type III secretion system (T3SS) with X. translucens pv. graminis and more distantly related xanthomonads. Assays with an adenylate cyclase reporter protein demonstrate that DAR61454's T3SS is functional in delivering proteins to wheat cells. X. translucens DAR61454 also encodes two type VI secretion systems with one most closely related to those found in some strains of the rice infecting strain X. oryzae pv. oryzae but not other xanthomonads. Comparative analysis of 18 different Xanthomonas isolates revealed 84 proteins unique to cereal (i.e. rice) infecting isolates and the wheat/barley infecting DAR61454. Genes encoding 60 of these proteins are found in gene clusters in the X. translucens DAR61454 genome, suggesting cereal-specific pathogenicity islands. However, none of the cereal pathogen specific proteins were homologous to known Xanthomonas spp. effectors. Comparative analysis outside of the bacterial kingdom revealed a nucleoside triphosphate pyrophosphohydrolase encoding gene in DAR61454 also present in other bacteria as well as a number of pathogenic Fusarium species, suggesting that this gene may have been transmitted horizontally from bacteria to the Fusarium lineage of pathogenic fungi. This example further highlights the importance of horizontal gene acquisition from bacteria in the evolution of fungi.

Brachypodium as an emerging model for cereal–pathogen interactions

“…Xanthomonas translucens is a pathogen of wheat and/or barley (Adhikari et al, 2011) causing bacterial leaf streak (BLS), or 'black chaff', which is a significant wheat disease globally with up to 40 % yield losses (Forster and Schaad, 1988). Current understanding of cereal-bacterial pathogen interactions is limited (Gardiner et al 2014) and a brachypodium-X. translucens model system may help to improve such understanding.…”

“…Recently, the genome of a wheat and barley-infecting X. translucens isolate 'DAR61454' has been sequenced (Gardiner et al, 2014). We have observed that DAR61454 is pathogenic on a range of brachypodium ecotypes, including major community ecotypes Bd21-3 and Bd21 (Fig.…”

“…2B). DAR61454 possesses a Type III secretion system and is capable of delivering heterologous proteins into wheat cells (Gardiner et al, 2014). This delivery system may prove to be useful for the characterization of cereal pathogen effectors.…”

Systems and synthetic biology perspective of the versatile plant-pathogenic and polysaccharide-producing bacterium Xanthomonas campestris

“…Other genome-scale reconstructions are available for maize [239] and barley [240], a host of X. translucens pv. translucens [241,242], and it is likely that more plant models will become available with the increasing number of genomes being sequenced. On the pathogen side, besides the Xcc models mentioned above, there are genome-scale metabolic reconstructions for other plant pathogenic bacteria [243][244][245].…”

Mapeamento de QTL (Quantitative Trait Loci) associados à resposta do maracujá-doce à bacteriose usando a abordagem de modelos mistos

“…O trabalho clássico de Singh (1986) e outros mais recentes (ARSHIYA et al, 2014;GARDINER et al, 2014;MISHRA et al, 2013;TARDIANI et al, 2014) Mishra et al (2013) identificaram 10 genes (Xa1, Xa3, Xa4, Xa5, Xa7, Xa8, Xa10, Xa11, Xa13, Xa21) …”