A review of the known unknowns in the early stages of septoria tritici blotch disease of wheat

Abstract

Septoria tritici blotch (STB) disease of wheat is caused by the fungal pathogen Zymoseptoria tritici. It is the most important foliar disease of wheat in western Europe and affects wheat cultivation worldwide. The combination of intensive fungicide usage, a polycyclic asexual life cycle and an active sexual cycle has led to the emergence of fungal strains resistant/tolerant to all the major classes of fungicides used in its control. The hallmark of this disease is a long, symptomless latent phase that precedes the onset of visible symptoms. Understanding the processes that occur during the symptomless phase of infection is paramount in developing alternative strategies for disease control; however, large gaps in our knowledge of the disease remain. The known unknowns of the latent stage of infection can be summarized in three questions. Does the fungus initiate or manipulate host defences to trigger programmed cell death in order to facilitate nutrient acquisition or is the host acting exclusively? Does the fungus feed during both the latent phase and the necrotrophic phase like a true hemibiotroph? Does the long latent phase serve a beneficial function for the fungus or is it simply an artefact of evolution? This review aims to distil observations made during studies that have directly or indirectly contributed to answering these questions and points towards their most likely answers.

Asynchronous development of Zymoseptoria tritici infection in wheat

“…During plant infection, Z. tritici goes through a series of developmental stages ( Rudd et al, 2015 ). These steps are generally thought to be sequential, with germination of the spores on the leaf surface (0 -1 days post infection, =dpi), subsequent hyphal penetration of stomata (1-3 dpi), followed by mesophyll colonization (3-11 dpi) and pycnidia development in neighboring stomatal cavities (11 dpi +; Brennan et al, 2019 ). In particular, later during the infection, developmental stages, such as fruiting body formation and spore maturation) appear to follow each other in time, yet vary between different isolates of Z. tritici ( Haueisen et al, 2019 ; see Fig.…”

Insights into the resistance of a synthetically-derived wheat to Septoria tritici blotch disease: less is more

“…Paramount to identifying novel sources of genetic resistance is the need to fully understand the life cycle of the pathogen and its interaction with the host. Approximately 3 h after contact with the leaf surface, Z. tritici spores germinate and the fungus penetrates the leaf through the stomata anywhere between 12 h and 10 days post infection (DPI) [ 14 , 15 ]. The fungus grows in the sub-stomatal cavity and spreads through the apoplast to neighbouring substomatal spaces [ 16 ], before host cells begin to die and the fungus starts to feed necrotrophically [ 14 , 17 ].…”

“…In fact, it has been suggested that the latent phase may be an artefact of evolution, as Z. tritici appears to have more genetic similarity with endophytes than other pathogens [ 18 ]. There is little evidence of nutrient acquisition from the host during the latent phase [ 14 , 19 ], confuting suggestions that the fungus is feeding biotrophically. However, the latent phase does appear to impact the asexual fecundity of the pathogen; shortening the latent phase by silencing the plant homeodomain protein TaR1 allows the disease to progress to necrotrophy earlier, but reduces asexual sporulation of the fungus [ 20 ], whereas absence of some of the Z. tritici accessory chromosomes also brings forward the switch to necrotrophy but leads to an increase in numbers of pycnidia [ 21 ].…”

“…Given that the latent phase affects asexual spore production and abundance, and that up to 70% of the Z. tritici population in the field at the end of a growing season results from asexual reproduction [ 3 ], the interaction between host and pathogen during the latent phase is undoubtedly an important consideration for elucidating STB resistance mechanisms. However, a multitude of factors influence the duration of the latent phase, including host genotype, varietal growth stage when infected, environmental conditions, inoculum isolate and inoculum density [ 14 , 22 ].…”

The ZtvelB Gene Is Required for Vegetative Growth and Sporulation in the Wheat Pathogen Zymoseptoria tritici

“…Zymoseptoria tritici spreads to susceptible host plants by asexual pycnidiospores and sexual ascospores which, following germination, infect the wheat leaf via the stomata (reviewed in Brennan et al, 2019). The lifestyle of the fungus is characterised by a symptomless latent period which typically lasts 10–14 days post-infection (dpi) (Eyal et al, 1987).…”