Temporal and Spatial Variability of Fungal Structures and Host Responses in an Incompatible Rust–Wheat Interaction

Abstract

Information about temporal and spatial variability of fungal structures and host responses is scarce in comparison to the vast amount of genetic, biochemical, and physiological studies of host–pathogen interactions. In this study, we used avirulent wild type and virulent mutant isolates of Puccinia striiformis to characterize the interactions in wheat carrying yellow rust Yr2 resistance. Both conventional and advanced microscopic techniques were used for a detailed study of morphology and growth of fungal colonies and associated host cell responses. The growth of the wild type isolates was highly restricted due to hypersensitive response (HR, plant cell death) indicated by autofluorescence and change in the shape of the affected plant cells. The host response appeared post-haustorial, but large variation in the time and stage of arrest was observed for individual fungal colonies, probably due to a delay between detection and response. Some colonies were stopped right after the formation of the primary infection hyphae whereas others formed highly branched mycelia. HR was first observed in host cells in direct contact with fungal structures, after which the defense responses spread to adjacent host cells, and eventually led to encasement of the fungal colony. Several cells with HR contained haustoria, which were small and underdeveloped, but some cells contained normal sized haustoria without signs of hypersensitivity. The growth of the virulent mutants in the resistant plants was similar to the growth in plants without Yr2 resistance, which is a strong indication that the incompatible phenotype was associated with Yr2. The interaction between P. striiformis and wheat with Yr2 resistance was highly variable in time and space, which demonstrate that histological studies are important for a deeper understanding of host–pathogen interactions and plant defense mechanisms in general.

Spatiotemporal changes in fungal growth and host responses of six yellow rust resistant near‐isogenic lines of wheat

“…For future studies, the number of colonies associated with one or both categories of HCD can be used to differentiate fungal growth with respect to time and Pst isolate. The pattern of distorted host cells with autofluorescence in close proximity of fungal colonies were also reported in Yr2 resistance (Sørensen et al , ). The microphenotype of extensive cell death and distortion may result in the manifestation of large chlorotic areas on AvocetYr1 leaves compared to the leaves of AvocetYr5.…”

“…These previous studies highlighted different histological parameters but none of them investigated the spatiotemporal changes in fungal growth and extent of HR. More recently, the histological characterization of Yr2 revealed large variation in colony size, colony morphology and associated HR (Sørensen et al , ). The above studies provide motivation for histological characterization of widely used yellow rust resistance genes in agriculture.…”

“…death of infected and adjacent cells. Host cell autofluorescence is an indication of HR, often morphologically associated with distortion and disruption of cellular components (Mur et al , ; Sørensen et al , ). ETI‐associated HR is an effective defence strategy for the host plant, particularly against biotrophic pathogens (Glazebrook, ), but effector recognition and the HR may vary significantly with respect to time and space (Wang et al , ).…”

“…The yellow rust–wheat interaction phenotype can be characterized through both macroscopic and microscopic assessment (Jagger et al , ; Sørensen et al , ). Macroscopically, the phenotype of the interaction involving an R gene with major effect is scored by infection types (IT), e.g.…”

Histochemical and Phenotypic Studies Revealed the Diverse Nature of Wheat-Yellow Rust Interaction

“…Yield losses as high as 75% have been reported in highly susceptible cultivars. Severe yield losses are caused by the development of new races and the unpredictable nature of this fungus (Wellings, 2011;Sorensen et al, 2017;Aboukhaddour et al, 2020). The wheat stripe rust disease has been reported as an increasing problem (Walter et al, 2016;Hovmoller et al, 2016) due to various reasons, such as its migratory nature, higher mutation rate from avirulence to virulence, adaptation to different climatic conditions (Thach et al, 2016) and the capacity to form new variants via sexual cycle to overcome resistance.…”