An introduced crop plant is driving diversification of the virulent plant pathogen Erwinia tracheiphila

Authors: SHAPIRO, LORI - Harvard Medical School; PAULSON, JOSEPH - Genentech; ARNOLD, BRIAN - Harvard School Of Public Health; Scully, Erin; ZHAXYBAYEVA, OLGA - Dartmouth College; PIERCE, NAOMI - Harvard University; KLEPAC-CERAJ, VANJA - Wellesley College; HOLTON, KRISTINA - Dana-Farber Cancer Institute

Submitted to: mBio
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/17/2018
Publication Date: 10/2/2018
Citation: Shapiro, L.R., Paulson, J.N., Arnold, B.J., Scully, E.D., Zhaxybayeva, O., Pierce, N., Klepac-Ceraj, V., Holton, K. 2018. An introduced crop plant is driving diversification of the virulent plant pathogen Erwinia tracheiphila. mBio. 9(5):e1307-18. https://doi.org/10.1128/mBio.01307-18.
DOI: https://doi.org/10.1128/mBio.01307-18

Interpretive Summary: Erwinia tracheiphila is a recently emerged plant pathogen that causes bacterial wilt disease in cucumber, muskmelon, squash, and pumpkins in North America. Despite the fact that this pathogen causes millions of dollars in agricultural losses each year, little is known about its genetic diversity, the identity of genes linked to host range and evasion of the host plant immune system, or the number of strains currently in circulation. In this study, the genomes of 84 different isolates collected across the United States from a variety of crop species displaying symptoms of wilt were sequenced and compared. This analysis led to the identification of three genetically distinct groups, which are referred to as Et-melo, Et-1, and Et-2. While isolates from groups Et-1 and Et-2 were found predominantly in the northeastern US and were capable of infecting cucumber, muskmelon, and squash, isolates from Et-melo were found throughout the US and were able to infect cucumber and muskmelon, but not squash. Differences in the number and types of genes linked to interactions with the plant and evasion of the host plant immune system, may explain the differences in range of plants infected among these three groups. In addition, cucumber was more susceptible to E. tracheiphila overall compared to muskmelon and squash. Not only were isolates from all three groups capable of infecting this plant, but symptoms appeared more rapidly and mortality rates were higher. Taken together, these findings suggest that cucumber is one of the more susceptible crops to this pathogen and that muskmelon and squash are susceptible to some of the circulating isolates. Additionally, these findings also suggest that isolates with expanded host ranges could emerge due to the acquisition of genes from other bacteria.

Technical Abstract: Worldwide, crop plant populations are becoming more genetically homogeneous over ever larger land areas. This lack of population diversity likely increases the susceptibility of these populations to invasion followed by rapid dissemination of virulent pathogens. Erwinia tracheiphila, the etiological agent of bacterial wilt of cucurbits, is one plant pathogen that has genomic characteristics indicative of a recent emergence into a susceptible crop plant population. To investigate why this virulent pathogen infects few species of closely related cucurbit crop plants, a geographically representative collection of 84 E. tracheiphila isolates was gathered and their genomes were sequenced. Phylogenomic analysis revealed that this collection of isolates is comprised of three distinct genetic clusters. The three clusters have low within-cluster genetic variation and distinct cluster-specific effector virulence gene repertoires. In the field and in a greenhouse setting, cucumber (Cucumis sativus), which was introduced to North America by early Spanish explorers, is the most susceptible host plant species, and is the only host plant susceptible to infection by isolates from all three clusters. Now planted in high acreage in its introduced range in Eastern North America, C. sativus may be acting as a highly susceptible reservoir host for E. tracheiphila, and potentially amplifying the E. tracheiphila epidemic. These findings have broad implications for agricultural sustainability by drawing attention to how agricultural intensification and worldwide crop plant movement may affect the emergence and epidemic persistence of virulent microbial pathogens.