The Type III Secretion System of Xanthomonas fuscans subsp. fuscans Is Involved in the Phyllosphere Colonization Process and in Transmission to Seeds of Susceptible Beans

Abstract

Understanding the survival, multiplication, and transmission to seeds of plant pathogenic bacteria is central to study their pathogenesis. We hypothesized that the type III secretion system (T3SS), encoded by hrp genes, could have a role in host colonization by plant pathogenic bacteria. The seed-borne pathogen Xanthomonas fuscans subsp. fuscans causes common bacterial blight of bean (Phaseolus vulgaris). Directed mutagenesis in strain CFBP4834-R of X. fuscans subsp. fuscans and bacterial population density monitoring on bean leaves showed that strains with mutations in the hrp regulatory genes, hrpG and hrpX, were impaired in their phyllospheric growth, as in the null interaction with Escherichia coli C600 and bean. In the compatible interaction, CFBP4834-R reached high phyllospheric population densities and was transmitted to seeds at high frequencies with high densities. Strains with mutations in structural hrp genes maintained the same constant epiphytic population densities (1 ؋ 10 5 CFU g ؊1 of fresh weight) as in the incompatible interaction with Xanthomonas campestris pv. campestris ATCC 33913 and the bean. Low frequencies of transmission to seeds and low bacterial concentrations were recorded for CFBP4834-R hrp mutants and for ATCC 33913, whereas E. coli C600 was not transmitted. Moreover, unlike the wild-type strain, strains with mutations in hrp genes were not transmitted to seeds by vascular pathway. Transmission to seeds by floral structures remained possible for both. This study revealed the involvement of the X. fuscans subsp. fuscans T3SS in phyllospheric multiplication and systemic colonization of bean, leading to transmission to seeds. Our findings suggest a major contribution of hrp regulatory genes in host colonization processes.

Transmission of Plant-Pathogenic Bacteria by Nonhost Seeds without Induction of an Associated Defense Reaction at Emergence

“…phaseoli var. fuscans are strongly impaired in their ability to transmit to seeds, but transmission through the floral pathway is not completely abolished for these strains (12). None of the five adhesins identified in the X. citri pv.…”

“…The floral transmission of bacteria to seeds is a permissive pathway compared to transmission through the vascular system (12). Floral transmission allows the contamination of seeds by a cohort of diverse bacteria, including biocontrol agents (17,52).…”

Emergence Shapes the Structure of the Seed Microbiota

“…While the internal transmission by the host xylem is probably restricted to pathogens or endophytes, many plant-associated microorganisms are potentially transmitted to the seed by the floral pathway. Indeed, the floral pathway allows the transmission of biocontrol microorganisms (7) and phytopathogenic bacteria in nonhost seeds (8,9). Finally, the external pathway is probably the most permissive way of microorganism transmission from plant to seed, although very few data are currently available in the literature (10).…”

Insights into the Extracytoplasmic Stress Response of Xanthomonas campestris pv. campestris : Role and Regulation of σ E -Dependent Activity

“…Mutation of genes encoding structural components and regulatory genes of the T3SS of Xanthomonas fuscans subsp. fuscans altered the ability of the bacterium to transmit to bean seeds through both vascular and floral pathways (21). The importance of rpoE in resisting external stresses suggests that E may be involved in survival in the environment, which constitutes a prerequisite to plant infection and disease development (35).…”