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Genomic divergence between Dickeya zeae strain EC2 isolated from rice and previously identified strains, suggests a different rice foot rot strain.

ABSTRACT: Rice foot rot caused by Dickeya zeae is an important bacterial disease of rice worldwide. In this study, we identified a new strain EC2 from rice in Guangdong province, China. This strain differed from the previously identified strain from rice in its biochemical characteristics, pathogenicity, and genomic constituents. To explore genomic discrepancies between EC2 and previously identified strains from rice, a complete genome sequence of EC2 was obtained and used for comparative genomic analyses. The complete genome sequence of EC2 is 4,575,125 bp in length. EC2 was phylogenetically closest to previously identified Dickeya strains from rice, but not within their subgroup. In terms of secretion systems, genomic comparisons revealed that EC2 harbored only type I (T1SS), type? (T2SS), and type VI (T6SS) secretion systems. The flagella cluster of this strain possessed specific genomic characteristics like other D. zeae strains from Guangdong and from rice; within this locus, the genetic diversity among strains from rice was much lower than that of within strains from non-rice hosts. Unlike other strains from rice, EC2 lost the zeamine cluster, but retained the clustered regularly interspaced short palindromic repeats-1 (CRISPR-1) array. Compared to the other D. zeae strains containing both exopolysaccharide (EPS) and capsular polysaccharide (CPS) clusters, EC2 harbored only the CPS cluster, while the other strains from rice carried only the EPS cluster. Furthermore, we found strain MS1 from banana, carrying both EPS and CPS clusters, produced significantly more EPS than the strains from rice, and exhibited different biofilm-associated phenotypes. Comparative genomics analyses suggest EC2 likely evolved through a pathway different from the other D. zeae strains from rice, producing a new type of rice foot rot pathogen. These findings emphasize the emergence of a new type of D. zeae strain causing rice foot rot, an essential step in the early prevention of this rice bacterial disease.

SUBMITTER: Zhang J

PROVIDER: S-EPMC7575072 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Genomic divergence between Dickeya zeae strain EC2 isolated from rice and previously identified strains, suggests a different rice foot rot strain.

Zhang Jingxin J Arif Mohammad M Shen Huifang H Hu John J Sun Dayuan D Pu Xiaoming X Yang Qiyun Q Lin Birun B

PloS one 20201020 10

Rice foot rot caused by Dickeya zeae is an important bacterial disease of rice worldwide. In this study, we identified a new strain EC2 from rice in Guangdong province, China. This strain differed from the previously identified strain from rice in its biochemical characteristics, pathogenicity, and genomic constituents. To explore genomic discrepancies between EC2 and previously identified strains from rice, a complete genome sequence of EC2 was obtained and used for comparative genomic analyses ...[more]

PMID: 33079956

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Project description:BackgroundDickeya zeae is a bacterial species that infects monocotyledons and dicotyledons. Two antibiotic-like phytotoxins named zeamine and zeamine II were reported to play an important role in rice seed germination, and two genes associated with zeamines production, i.e., zmsA and zmsK, have been thoroughly characterized. However, other virulence factors and its molecular mechanisms of host specificity and pathogenesis are hardly known.ResultsThe complete genome of D. zeae strain EC1 isolated from diseased rice plants was sequenced, annotated, and compared with the genomes of other Dickeya spp.. The pathogen contains a chromosome of 4,532,364 bp with 4,154 predicted protein-coding genes. Comparative genomics analysis indicates that D. zeae EC1 is most co-linear with D. chrysanthemi Ech1591, most conserved with D. zeae Ech586 and least similar to D. paradisiaca Ech703. Substantial genomic rearrangement was revealed by comparing EC1 with Ech586 and Ech703. Most virulence genes were well-conserved in Dickeya strains except Ech703. Significantly, the zms gene cluster involved in biosynthesis of zeamines, which were shown previously as key virulence determinants, is present in D. zeae strains isolated from rice, and some D. solani strains, but absent in other Dickeya species and the D. zeae strains isolated from other plants or sources. In addition, a DNA fragment containing 9 genes associated with fatty acid biosynthesis was found inserted in the fli gene cluster encoding flagellar biosynthesis of strain EC1 and other two rice isolates but not in other strains. This gene cluster shares a high protein similarity to the fatty acid genes from Pantoea ananatis.ConlusionOur findings delineate the genetic background of D. zeae EC1, which infects both dicotyledons and monocotyledons, and suggest that D. zeae strains isolated from rice could be grouped into a distinct pathovar, i.e., D. zeae subsp. oryzae. In addition, the results of this study also unveiled that the zms gene cluster presented in the genomes of D. zeae rice isolates and D. solani strains, and the fatty acid genes inserted in the fli gene cluster of strain EC1 were likely derived from horizontal gene transfer during later stage of bacterial evolution.

Project description:Bacterial soft rot of banana, caused by Dickeya zeae, is spreading rapidly in important banana growing areas in China and seriously threatens banana production. In this study, we sequenced the high-quality complete genomes of three typical banana strains, MS1 (size: 4,831,702-bp; genome coverages: 538x), MS_2014 (size: 4,740,000-bp; genome coverages: 586x) and MS_2018 (size: 4,787,201-bp; genome coverages: 583x), isolated in 2009, 2014, and 2018, respectively. To determine their genomic and phenotypic diversity with respect to their hosts of origin, they were compared with other D. zeae strains, including another representative banana strain MS2 from China. The sequenced strains were similar in utilization of carbon source and chemical substrates, and general genomic features of GC content, and tRNA and rRNA regions. They were also conserved in most virulence determinants, including gene-encoding secretion systems, plant cell wall degrading enzymes, and exopolysaccharides. We further explored their genomic diversity in the predicted genomic islands (GIs). These GIs were rich in integrases and transposases, where some genomic dissimilarity was observed in the flagellar gene cluster and several secondary metabolite gene clusters. Different constituents of core biosynthetic modules were found within the bacteriocin and aryl polyene (APE) pigment gene clusters, and the strains from banana showed different phenotypes with respect to antibiosis effects and colony pigmentation. Additionally, clustered regularly interspaced short palindromic repeat (CRISPR) and prophage elements, such as type I-F and III-A CRISPR arrays and an intact prophage of MS1-P5, contributed to bacterial diversity. Phylogenetic tree analysis and genome-genome nucleotide comparison confirmed the genomic divergence among the strains isolated from banana. Considering these characteristics, MS2 and MS_2014 probably diverged later than MS1, while MS_2018 was different and more similar to foreign strains isolated from other hosts in several characteristics. Strain MS_2018 caused severe symptoms on banana varieties previously considered moderately resistant or moderately susceptible, including varieties of Cavendish (Musa AAA) and Plantain (Musa ABB). Our study of genomic and phenotypic diversity raises public attention to the risk of spreading new pathogenic variants within banana growing regions and supports development of predictive strategies for disease control.

Dataset Information

Genomic divergence between Dickeya zeae strain EC2 isolated from rice and previously identified strains, suggests a different rice foot rot strain.

Publications

Genomic divergence between Dickeya zeae strain EC2 isolated from rice and previously identified strains, suggests a different rice foot rot strain.

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