Verticillium longisporum, the invisible threat to oilseed rape and other brassicaceous plant hosts

Abstract

Introduction: The causal agents of Verticillium wilts are globally distributed pathogens that cause significant crop losses every year. Most Verticillium wilts are caused by V. dahliae, which is pathogenic on a broad range of plant hosts, whereas other pathogenic Verticillium species have more restricted host ranges. In contrast, V. longisporum appears to prefer brassicaceous plants and poses an increasing problem to oilseed rape production.

Taxonomy: Kingdom Fungi; Phylum Ascomycota; Class Sordariomycetes; Subclass Hypocreomycetida; Family Plectosphaerellaceae; genus Verticillium.

Disease symptoms: Dark unilateral stripes appear on the stems of apparently healthy looking oilseed rape plants at the end of the growing season. Microsclerotia are subsequently formed in the stem cortex beneath the epidermis.

Genome: Verticillium longisporum is the only non-haploid species in the Verticillium genus, as it is an amphidiploid hybrid that carries almost twice as much genetic material as the other Verticillium species as a result of interspecific hybridization.

Disease management: There is no effective fungicide treatment to control Verticillium diseases, and resistance breeding is the preferred strategy for disease management. However, only a few Verticillium wilt resistance genes have been identified, and monogenic resistance against V. longisporum has not yet been found. Quantitative resistance exists mainly in the Brassica C-genome of parental cabbage lines and may be introgressed in oilseed rape breeding lines.

Common name: Oilseed rape colonized by V. longisporum does not develop wilting symptoms, and therefore the common name of Verticillium wilt is unsuitable for this crop. Therefore, we propose 'Verticillium stem striping' as the common name for Verticillium infections of oilseed rape.

Keywords: Arabidopsis; Brassica; amphidiploid; disease management; host range; pathogenicity; vascular wilt.

Figure 1

Microscopic appearance of Verticillium longisporum in vitro. (A) Verticillate conidiophores (bar, 20 µm). (B) Conidia (bar, 10 µm). (C) Young microsclerotia (bar, 25 µm).

Figure 2

The genetic constitution of the three lineages of Verticillium longisporum. (A) Phylogenetic relationship between the parents of V. longisporum (adjusted from Inderbitzin and Subbarao, 2014). (B) The three hybridization events that resulted in the hybrid species V. longisporum. A1 and D1 progenitors are unknown and provisionally named haploid Verticillium species, whereas progenitors D2 and D3 are both V. dahliae lineages. A1 is a parent of all three V. longisporum lineages, as it hybridized with D1, D2 and D3, resulting in the three V. longisporum lineages A1/D1, A1/D2 and A1/D3, respectively.

Figure 3

Disease cycle of Verticillium longisporum on oilseed rape. 1. Microsclerotia are persistent resting structures that reside in the soil and bridge the gap between hosts. 2. Triggered by root exudates, microsclerotia start to germinate and hyphae grow towards the root of the plant. 3. The fungus enters the root through wounds, or by direct penetration of epidermal cells of lateral roots or root hairs. In the root, hyphae grow intercellularly and intracellularly towards the central cylinder and enter the xylem. 4. No disease symptoms are observed during the major part of the growing season. 5. Dark unilateral striping develops on the stem of oilseed rape during the ripening of the crop. Ultimately, black microsclerotia are formed in the stem cortex. 6. Microsclerotia are released into the soil on decomposition of plant debris.

Figure 4

Typical disease symptoms caused by Verticillium longisporum on oilseed rape. Dark unilateral striping appears on the stems of apparently healthy looking plants at the end of the growing season (A), indicating the necrosis of cortical tissue. The necrosis develops further in a later stage of the disease, which may lead to stem cracks (B). Finally, microsclerotia are formed in the stem cortex beneath the epidermis (C).