The center of wheat domestication drives diversity of Clavibacter pathogens.

Microbial plant pathogens possess higher diversity in the center of domestication of their host plants than in the introduced geographic area of the corresponding crops. In this study, the center of wheat, barley, and oat domestication in the Iranian Plateau was surveyed to shed light on the population structure, taxonomic diversity, and biology of Clavibacter species associated with these crops. Comprehensive field surveys completed with pathological assays and molecular-phylogenetic analyses showed that phylogenetically diverse groups of Clavibacter strains were associated with bacterial mosaic symptoms on small grain cereals in this domestication center. Besides the two previously described species, Clavibacter tessellarius and Clavibacter zhangzhiyongii, three clades of atypical Clavibacter strains, phylogenetically distinct from all described Clavibacter species, were isolated from wheat, barley, and oat in this study. Thus, Clavibacter strains associated with small grain cereals in the center of domestication of these crops belong to at least five taxonomically distinct clades, whereas simultaneous occurrence of multitaxa Clavibacter strains on small grain cereals has never been reported outside the Iranian Plateau. All five phylogenetic Clavibacter clades were capable of inducing mosaic and chlorosis on their host of isolation. Whole genome sequence-based comparative investigations showed that most virulence-associated genomic contents of the five Clavibacter clades isolated in this study were somewhat similar. Data obtained in this study suggest a correlation between the center of wheat, barley, and oat domestication and the high taxonomic diversity of the accompanying Clavibacter pathogens. Additional phylogeographic investigations in the area would strengthen this co-evolutionary hypothesis.

Importance: Members of the gram-positive corynebacterial genus Clavibacter sp. (family Microbacteriaceae) are seed-borne plant pathogens causing economically important plant diseases on annual crops and vegetables. While comprehensive global-scale studies have been conducted to study the population structure of Clavibacter species infecting tomato, potato, and pepper, phylogenomics investigations have not yet been conducted to monitor the taxonomic diversity, pathogenicity, and origin of Clavibacter strains pathogenic to small grain cereals. Archaeobotanical investigations suggested that human agriculture was established ≈11,000 years ago in the foothills of the Zagros Mountains in Northwestern Iran, while wheat and barley were among the very first crops domesticated in these areas. Thus, the analyses of taxonomic diversity and population structure of Clavibacter strains in the Iranian Plateau would shed light on the correlation between the center of domestication of these crops and the center of diversity of accompanying bacterial pathogens. Our findings showed that most of the Clavibacter strains isolated from small grain cereals in Iran belonged to the two previously described species Clavibacter tessellarius and Clavibacter zhangzhiyongii, while several strains were grouped in three distinct clades, all representing hypothetical novel species in the genus.