Abstract
Hemibiotrophic plant pathogens first establish a biotrophic interaction with the host plant and later switch to a destructive necrotrophic lifestyle. Studies of biotrophic pathogens have shown that they actively suppress plant defenses after an initial microbe-associated molecular pattern-triggered activation. In contrast, studies of the hemibiotrophs suggest that they do not suppress plant defenses during the biotrophic phase, indicating that while there are similarities between the biotrophic phase of hemibiotrophs and biotrophic pathogens, the two lifestyles are not analogous. We performed transcriptomic, histological, and biochemical studies of the early events during the infection of maize (Zea mays) with Colletotrichum graminicola, a model pathosystem for the study of hemibiotrophy. Time-course experiments revealed that mRNAs of several defense-related genes, reactive oxygen species, and antimicrobial compounds all begin to accumulate early in the infection process and continue to accumulate during the biotrophic stage. We also discovered the production of maize-derived vesicular bodies containing hydrogen peroxide targeting the fungal hyphae. We describe the fungal respiratory burst during host infection, paralleled by superoxide ion production in specific fungal cells during the transition from biotrophy to a necrotrophic lifestyle. We also identified several novel putative fungal effectors and studied their expression during anthracnose development in maize. Our results demonstrate a strong induction of defense mechanisms occurring in maize cells during C. graminicola infection, even during the biotrophic development of the pathogen. We hypothesize that the switch to necrotrophic growth enables the fungus to evade the effects of the plant immune system and allows for full fungal pathogenicity.
Highlights
Hemibiotrophic plant pathogens first establish a biotrophic interaction with the host plant and later switch to a destructive necrotrophic lifestyle
We observed the formation of primary hyphae within the infected cells, which is consistent with the establishment of the biotrophic stage
From 36 to 60 hpi, we continue to see the development of primary hyphae, which spread to adjacent cells (Fig. 1, A and B)
Summary
Hemibiotrophic plant pathogens first establish a biotrophic interaction with the host plant and later switch to a destructive necrotrophic lifestyle. Anthracnose Development and Defense Mechanisms in Maize regularly shaped hyphae, called secondary hyphae, that extensively colonize the intercellular and intracellular spaces of the tissue, causing the death of host cells prior to colonization (O’Connell et al, 1985; Bergstrom and Nicholson, 1999; Wharton et al, 2001; Mims and Vaillancourt, 2002) This process of disease development, called hemibiotrophy or facultative biotrophy, raises questions about the importance of lifestyle differences among fungi. A transcriptional profiling of maize genes during U. maydis infection and tumor development revealed a complex cell reprogramming due to specific transcriptional and metabolic changes induced by the pathogen (Doehlemann et al, 2008) Those changes include a transient induction of defense mechanisms in maize that, with the onset of biotrophy at 24 h post infection (hpi), are suppressed. This conclusion still remains to be fully confirmed for this pathosystem
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