Ecological and Evolutionary Insights into Xanthomonas citri Pathovar Diversity

Abstract

Citrus canker, caused by Xanthomonas citri pv. citri, is a serious disease of citrus plants worldwide. Earlier phylogenetic studies using housekeeping genes revealed that X. citri pv. citri is related to many other pathovars, which can be collectively referred as Xanthomonas citri pathovars (XCPs). From the present study, we report the genome sequences of 18 XCPs and compared them with four XCPs available in the public domain. In a tree based on phylogenomic marker genes, all the XCPs form a monophyletic cluster, suggesting their origin from a common ancestor. Phylogenomic analysis using the type strain further established that all the XCPs belong to one species. Clonal analysis of the core genome revealed the presence of two major lineages within this monophyletic cluster consisting of some clonal variants. Incidentally, the majority of these XCPs were first noticed in India, corroborating their clonal relationship and their common origin. Comparative analysis revealed an open pan-genome and the role of interstrain genomic flux of these XCPs since their diversification from a common ancestor. Even though there are wide variations in type III gene effectomes, we identified three core effectors which can be valuable in resistance-breeding programs. Overall, genomic examination of ecological relatives allowed us to dissect the tremendous genomic potential of X. citri species to rapidly evolve into specialized strains infecting diverse crop plants.IMPORTANCE Host specialization is one of the characteristic features of highly evolved pathogens such as the Xanthomonas group of phytopathogenic bacteria. Since the hosts involve staple crops and economically important fruits such as citrus, detailed understanding of the diversity and evolution of such strains infecting diverse plants is important for quarantine purposes. In the present study, we carried out genomic investigation of members of a phylogenetically and ecologically defined group of Xanthomonas strains pathogenic to diverse plants, including citrus. This group includes the oldest Xanthomonas pathovars and also recently emerged pathovars in a particular country where they are endemic. Our high-throughput genomic study has provided novel insights into the evolution of a unique lineage consisting of serious pathogens and their ecological relatives, suggesting the nature, scope, and pattern of rapid and recent diversification. Further, from the level of species to that of clonal variants, the study revealed interesting genomic patterns in diversification of a Xanthomonas lineage and perhaps will inspire careful study of the host range of the included pathovars.

The Green Revolution shaped the population structure of the rice pathogen Xanthomonas oryzae pv. oryzae

“…4a), but because each recombination event introduces approximately six substitutions, recombination introduced substitution over mutation is 2.82 (95% CI: 2.81-2.83) times higher within recombinant fragments. These values were similar to those found in Indian Xoo populations [53] or what has been reported for other Xanthomonas species [59,60].…”

Phylogenomic Insights into Diversity and Evolution of Nonpathogenic Xanthomonas Strains Associated with Citrus

“…To look for lifestyle-specific genes among citrus associated strains of Xanthomonas, we carried out pan genome analysis, including 4 NPXc (LMG8989, LMG8992, LMG8993, and LMG9002) and 4 X. citri pv. citri strains (LMG9322, XACB100, XACJJ10, and XALG98) (8,32). Here, 2,344 and 7,736 genes constituted core genome and pan genome, respectively.…”

“…Xanthomonas pathogens of citrus and rice belong to X. citri and X. oryzae, respectively (7,8,33). In this context, it is interesting to find that nonpathogenic isolates from citrus are highly diverse, with each isolate belonging to a potentially novel species and altogether forming a species complex, the NPXc complex.…”

“…Owing to its economic importance as one of the top phytopathogenic bacteria, its evolution into successful species is of interest to researchers, policy makers, etc. Moreover, it is the most successful Xanthomonas species, harboring 22 pathovars known to be host specific to diverse plants (8).…”

Variation and inheritance of theXanthomonasgene cluster required for activation of XA21-mediated immunity

“…The topology of the resulting tree shares broad similarity with several 78other Xanthomonas phylogenetic trees in defining relationships between well-sampled species 79 (Midha & Patil, 2014, Rademaker et al, 2005, Hauben et al, 1997, Parkinson et al, 2007, 80 Parkinson et al, 2009, Ferreira-Tonin et al, 2012, Gardiner et al, 2014, Triplett et al, 2015, 81 Young, 2008. 82 rax gene cluster Notably, the raxX-raxSTAB gene cluster is absent from the group of strains classified as X. citri 104 pathovars (Rademaker group 9.5; (Rademaker et al, 2005, Bansal et al, 2017. These strains 105(some of which are denoted as X. axonopodis or X. campestris) cluster phylogenetically among 106 four of the raxX-raxSTAB gene cluster-positive groups: X. oryzae, X. vasicola, X. euvesicatoria 107 and X. axonopodis pv.…”