Bacterial spot of tomato and pepper: diverse Xanthomonas species with a wide variety of virulence factors posing a worldwide challenge

Abstract

Taxonomic status: Bacteria; Phylum Proteobacteria; Class Gammaproteobacteria; Order Xanthomonadales; Family Xanthomonadaceae; Genus Xanthomonas; Species Xanthomonas euvesicatoria, Xanthomonas vesicatoria, Xanthomonas perforans and Xanthomonas gardneri.

Microbiological properties: Gram-negative, rod-shaped bacterium, aerobic, motile, single polar flagellum.

Host range: Causes bacterial spot disease on plants belonging to the Solanaceae family, primarily tomato (Solanum lycopersicum), pepper (Capsicum annuum) and chilli peppers (Capsicum frutescens).

Disease symptoms: Necrotic lesions on all above-ground plant parts.

Distribution: Worldwide distribution of X. euvesicatoria and X. vesicatoria on tomato and pepper; X. perforans and X. gardneri increasingly being isolated from the USA, Canada, South America, Africa and Europe. A wide diversity within the bacterial spot disease complex, with an ability to cause disease at different temperatures, makes this pathogen group a worldwide threat to tomato and pepper production. Recent advances in genome analyses have revealed the evolution of the pathogen with a plethora of novel virulence factors. Current management strategies rely on the use of various chemical control strategies and sanitary measures to minimize pathogen spread through contaminated seed. Chemical control strategies have been a challenge because of resistance by the pathogen. Breeding programmes have been successful in developing commercial lines with hypersensitive and quantitative resistance. However, durability of resistance has been elusive. Recently, a transgenic approach has resulted in the development of tomato genotypes with significant levels of resistance and improved yield that hold promise. In this article, we discuss the current taxonomic status, distribution of the four species, knowledge of virulence factors, detection methods and strategies for disease control with possible directions for future research.

Keywords: Xanthomonas; bacterial spot; pepper; tomato.

Figure 1

Current worldwide distribution of Xanthomonas causing bacterial spot of tomato and pepper.

Figure 2

Colonization of bacterial spot Xanthomonas perforans in the tomato phyllosphere. On immigration to the leaf surface, X. perforans colonizes around the stomata (indicated by arrow) and in the grooves of the epidermal cells as seen in this confocal laser scanning micrograph. Five‐week‐old tomato plants were dip inoculated with 10⁶ colony‐forming units (cfu)/mL of green fluorescent protein (GFP)‐labelled X. perforans. The images were captured on day 3 post‐inoculation. (A) GFP channel. (B) Bright field. White bar, 25 μm.

Figure 3

Colonization of bacterial spot Xanthomonas perforans in the tomato phyllosphere. Bacterium enters though stomata (A), followed by growth in the substomatal chamber (B) (indicated by arrow). Bacterium multiplies in the intercellular spaces (C and D). Representative photomicrographs showing green fluorescent protein (GFP)‐labelled virulent X. perforans aggregates that are part of the lesion along a Z stack of 20 μm overlaid with Nomarski differential interference contrast images (40× magnification). Z values represent the distance in micrometres from the abaxial (lower) leaf surface. White bar, 25 μm.

Figure 4

Bacterial spot disease symptoms on the leaves (A) and fruits (B) of pepper and tomato. On the leaves, dark brown to black lesions with a necrotic blighted appearance are seen. Classic shot‐hole lesions are observed on tomato leaves infected with Xanthomonas perforans (shown as enlarged image). Scabby and raised lesions are seen on the fruit.

Figure 5

Foliar applications of bacteriophage have provided effective control of bacterial spot disease on tomato and pepper. The figure shows bacteriophage of X. vesicatoria attached to dividing cell of Xanthomonas. Photograph courtesy of Dr Botond Balogh, Nichino America, Inc.