Structural specificity in plant-filamentous pathogen interactions

Abstract

Plant diseases bear names such as leaf blights, root rots, sheath blights, tuber scabs, and stem cankers, indicating that symptoms occur preferentially on specific parts of host plants. Accordingly, many plant pathogens are specialized to infect and cause disease in specific tissues and organs. Conversely, others are able to infect a range of tissues, albeit often disease symptoms fluctuate in different organs infected by the same pathogen. The structural specificity of a pathogen defines the degree to which it is reliant on a given tissue, organ, or host developmental stage. It is influenced by both the microbe and the host but the processes shaping it are not well established. Here we review the current status on structural specificity of plant-filamentous pathogen interactions and highlight important research questions. Notably, this review addresses how constitutive defence and induced immunity as well as virulence processes vary across plant organs, tissues, and even cells. A better understanding of the mechanisms underlying structural specificity will aid targeted approaches for plant health, for instance by considering the variation in the nature and the amplitude of defence responses across distinct plant organs and tissues when performing selective breeding.

Keywords: developmental stages; filamentous pathogens; organ; plant disease; structural specificity; tissue.

FIGURE 1

Examples of structural specificity among plant–microbe interactions. (a), (b), and (c) Considered a structural generalist, Phytophthora capsici can infect all organs of pepper (Capsicum annuum), including fruits (a), roots (b), and leaves (c), where resistance to each disease syndrome appears to be differentially inherited. Pathogens considered as structural generalists can sometimes infect all organs while being limited to certain tissues within these organs. Interestingly, this limitation sometimes changes in hemibiotrophic pathogens, depending on whether the pathogen is in its biotrophic or necrotrophic phase. For example, vascular pathogens such as Fusarium oxysporum will remain strictly limited to xylem tissues and surrounding cells as long as the plant is alive (d). Once the infected plant is killed, the fungus then invades parenchymatous tissues and sporulates on the plant surface. Other pathogens, often considered as extreme structural specialists, can infect most tissues asymptomatically, but will exhibit symptoms (or sporulate) only in highly specific tissues, such as anthers in the case of Microbotryum species and other anther smut fungi (e). Powdery mildews, such as Golovinomyces cichoracearum, are among the most extreme structural specialists, most species being confined to the epidermal cells of aerial plant parts (f). Rust fungi are also known as structural specialists, being only able to infect aerial organs. Interestingly, even though they can invade the whole mesophyll, many heteroecious rusts will produce pycnia specifically on the adaxial sides of leaves (black arrow) while aecia will be found on the abaxial side of leaves (blue arrow) (g). Structural specificity is not restricted to filamentous pathogens. Well‐known examples also exist among filamentous mutualists such as mycorrhizal fungi (e.g., Laccaria bicolor), which are restricted to root tissues up to the endodermis (h). Photograph credits: (a) Gerald J. Holmes, California Polytechnic State University; (b) Nancy Fisher Gregory, University of Delaware; (c) Christine Smart, Cornell University; (d) Guo et al. (2014) ; (e):Donald E. Groth, Louisiana State University, AgCenter; (f) Richard Bélanger and The American Phytopathological Society, (Wurms et al., 1999 ); (g) George L. Barron, University of Guelph Atrium Collection, https://atrium.lib.uoguelph.ca/xmlui/handle/10214/7059; (h) Clémence Bonnot and Francis Martin, INRA

FIGURE 2

Resistance and susceptibility in a plant–pathogen interaction depend on the abundance levels of both R and Avr factors, which can vary between organs. Blue elements: Hyaloperonospora parasitica–Arabidopsis thaliana interaction. For a given R‐gene expression level, A. thaliana roots are susceptible whereas leaves are resistant to H. parasitica (Hermanns et al., 2003). This contrasted phenotype may rely on distinct Avr gene expression in leaves and roots from the pathogen. Yellow elements: Phytophthora infestans–Solanum tuberosum interaction. In this context, a given level of expression of the R‐gene (e.g., from one copy of the gene RB) might be sufficient to trigger a hypersensitive reaction in leaves, where the cognate Avr is highly expressed. However, it might prove insufficient in tubers where the Avr could be weakly expressed, a situation where a higher level of expression of RB (e.g., from multiple copies of it as a transgene) could thus complement this difference to achieve the same outcome (resistance; Gao and Bradeen, 2016). Note: Abundance can fluctuate for various reasons, whether expression levels or the existence of distinct delivery mechanisms and/or infection structures

FIGURE 3

Various levels of structural specificity in a plant–filamentous pathogen interaction. The first level of structural specificity is at the organ level. Organs are often divided as being above or below ground, and encompass well‐known structures (leaves, stems, flowers, and fruits vs. roots and tubers). Specificity can be also restricted to tissues (e.g., vascular tissues, dermal tissues) or cell types (e.g., sieve elements, guard cells). Various components of each of the plant defence layers appear to segregate and act differently: (1) preformed defences (e.g., cuticle in leaf vs. exo/endodermis in roots), (2) PRR‐mediated immunity (PMI), and (3) NLR‐mediated immunity (NMI; both PMI and NMI showing specialist and generalist receptors). Filamentous pathogen processes also exhibit structural specificity: (A) morphological and developmental adaptation, (B) nutrient availability/acquisition, and (C) effector waves. The black arrow depicts the putative influence of organ‐specific nutrients on the morphological and developmental adaptation of pathogens