Comparative genomic analysis uncovered phylogenetic diversity, evolution of virulence factors, and horizontal gene transfer events in tomato bacterial spot Xanthomonas euvesicatoria

Chien-Jui Huang; Ting-Li Wu; Yu-Lin Wu; Ruei-Shiuan Wang; Yao-Cheng Lin

doi:10.3389/fmicb.2024.1487917

Comparative genomic analysis uncovered phylogenetic diversity, evolution of virulence factors, and horizontal gene transfer events in tomato bacterial spot Xanthomonas euvesicatoria

Front Microbiol. 2024 Nov 5:15:1487917. doi: 10.3389/fmicb.2024.1487917. eCollection 2024.

Authors

Chien-Jui Huang¹, Ting-Li Wu^{2

3}, Yu-Lin Wu^{2

3}, Ruei-Shiuan Wang^{2

3}, Yao-Cheng Lin^{2

3}

Affiliations

¹ Department of Plant Medicine, National Chiayi University, Chiayi, Taiwan.
² Biotechnology Center in Southern Taiwan, Academia Sinica, Tainan, Taiwan.
³ Agriltural Biotechnology Research Center, Academia Sinica, Taipei, Taiwan.

Abstract

Introduction: Bacterial spot, caused by diverse xanthomonads classified into four lineages within three species, poses a significant threat to global pepper and tomato production. In Taiwan, tomato bacterial spot xanthomonads phylogenetically related to an atypical Xanthomonas euvesicatoria pv. perforans (Xep) strain NI1 from Nigeria were found.

Methods: To investigate the genetic structure of Taiwanese Xep strains and determine the phylogenetic position of the atypical strains, we completed high-quality, gap-free, circularized genomes of seven Taiwanese Xep strains and performed comparative genomic analyses with genomes of X. euvesicatoria pathovars. Average nucleotide identity, core genome analysis, and phylogenomic analysis were conducted.

Results: Three sequenced strains were identified as typical Xep, while four clustered with the atypical strain NI1, forming a distinct genomovar within X. euvesicatoria, proposed as X. euvesicatoria genomovar taiwanensis (Xet). This new lineage likely originated in Taiwan and spread to Nigeria through global seed trade. At the genomovar level, chromosomes remained conserved among Taiwanese strains, while plasmids likely contributed to bacterial virulence, avirulence, and field fitness. Gap-free genomes revealed associations between the evolution of type III effectors, horizontal gene transfer events, plasmid diversity, and recombination.

Discussion: This study highlights the critical roles of horizontal gene transfer and plasmids in shaping the genetic makeup, evolution, and environmental adaptation of plant pathogenic xanthomonads. The identification of a new genomovar, X. euvesicatoria genomovar taiwanensis, provides insights into the diversity and global spread of bacterial spot pathogens through seed trade.

Keywords: Xanthomonas euvesicatoria; bacterial spot; comparative genomics; microbial diversity; microbial evolution; virulence factors.

Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This research was funded by the Ministry of Science and Technology (MOST, grant nos. 110-2313-B-415-007, 111-2313-B-415-002, and 112-2313-B-415-006) to C-JH; and the Innovative Translational Agricultural Research Program (AS-KPQ-110-ITAR-03, AS-KPQ-111-ITAR-11107, AS-ITAR-111-L11102), Agricultural Biotechnology for Sustainability (AS-KPQ-111-ITAR-11207 and AS-ITAR-113030), and Academia Sinica Institutional funding to Y-CL. These funding bodies played no role in the design of the study, collection, analysis or interpretation of data, or in writing the manuscript.