Genomic Comparisons and Phenotypic Diversity of Dickeya zeae Strains Causing Bacterial Soft Rot of Banana in China.

Jingxin Zhang,Huifang Shen,Xiaoming Pu,Birun Lin,Dayuan Sun,John Hu,Mohammad Arif,Qiyun Yang

doi:10.3389/fpls.2022.822829

Abstract

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.

Highlights

Banana (Musa spp.) is an important fruit in tropical and subtropical regions and an essential food crop in some developing countries
Different with the high homogeneity shared by D. solani strains (Golanowska et al, 2018; Motyka-Pomagruk et al, 2020), we previously find high genomic heterogeneity occurred among different D. zeae strains isolated from different hosts
Dickeya zeae Strains From Banana Might Have Diverged Earlier From Ancestral Strains Than Strains From Other Hosts in China In Guangdong Province, China, bacterial soft rot of banana caused by D. zeae was first described in 2009 by our group (Lin et al, 2010)

Summary

Introduction

Banana (Musa spp.) is an important fruit in tropical and subtropical regions and an essential food crop in some developing countries. In 2009, we first reported bacterial soft rot of banana caused by Dickeya sp. Dickeya spp. are Gram-negative and necrotrophic bacteria in family Pectobacteriaceae, and the causative agents of bacterial soft rot in a wide range of hosts. This banana disease spread rapidly to most banana-growing regions, including Guangdong, Guangxi, Yunnan, Fujian, and Hainan Provinces in China, causing significant losses to the susceptible variety Musa ABB Pisang Awak (Zhang et al, 2014; Fan et al, 2016; Du et al, 2019). Dickeya paradisiaca was previously discovered infecting banana (Dickey and Victoria, 1980; Samson et al, 2005), and we first reported D. zeae as the causative agent in China (Zhang et al, 2014)

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Conclusion