Systematic hyper-variation and evolution at a lipopolysaccharide locus in the population of Xanthomonas species that infect rice and sugarcane

Advent of high throughput sequencing and population genomics is enabling researchers to investigate selection pressure at hyper-variable genomic loci encoding pathogen-associated molecular patter (PAMP) molecules like lipopolysaccharide (LPS) in an unprecedented manner. Xanthomonas is a model group of phytopathogenic bacteria that infects host in tissue-specific manner. Our in-depth investigation revealed that the successful emergence of lineages infecting major cereals and grasses like rice, sugarcane, and wheat was mediated by acquisition and later replacement of an ancestral type (BXO8) of LPS cassette by distinct one. In the population of the rice xylem pathogen, X. oryzae pv. oryzae (Xoo), the BXO8 is replaced by a distinct BXO1 type of cassette. Alternatively, in diverse Xanthomonas species that infect sugarcane, the BXO8 ancestral cassette has been replaced by yet another kind of Xvv type of LPS cassette, suggesting convergent evolution at an LPS locus mediated by horizontal gene transfer (HGT) events. Aside from xylem, two closely related lineages of X. oryzae that infect parenchyma tissue of rice and Leersia hexandra grass have acquired an LPS cassette from Xanthomonas pathogens that infect citrus, walnut, and strawberry parenchyma, indicating yet another instance of parallel evolution facilitated by HGT. Our targeted and mega-population-based genome dynamic studies revealed potential role of acquisition of specific types of LPS cassettes in the emergence and evolution of tissue specificity in Xanthomonas. Additional cellular, molecular, genetic, and plant studies will help us figure out how a distinct type of LPS help Xanthomonas pathovars and lineages adapt to parenchyma and xylem tissues.