Complexity of Brassica oleracea-Alternaria brassicicola Susceptible Interaction Reveals Downregulation of Photosynthesis at Ultrastructural, Transcriptional, and Physiological Levels.

Violetta Katarzyna Macioszek,Agnieszka Zmienko,Andrzej Skoczowski,Magdalena Gapińska,Jakub Oliwa,Mirosław Sobczak,Andrzej Kiejstut Kononowicz

doi:10.3390/cells9102329

Abstract

Black spot disease, caused by Alternaria brassicicola in Brassica species, is one of the most devastating diseases all over the world, especially since there is no known fully resistant Brassica cultivar. In this study, the visualization of black spot disease development on Brassica oleracea var. capitata f. alba (white cabbage) leaves and subsequent ultrastructural, molecular and physiological investigations were conducted. Inter- and intracellular hyphae growth within leaf tissues led to the loss of host cell integrity and various levels of organelle disintegration. Severe symptoms of chloroplast damage included the degeneration of chloroplast envelope and grana, and the loss of electron denseness by stroma at the advanced stage of infection. Transcriptional profiling of infected leaves revealed that photosynthesis was the most negatively regulated biological process. However, in infected leaves, chlorophyll and carotenoid content did not decrease until 48 hpi, and several chlorophyll a fluorescence parameters, such as photosystem II quantum yield (Fv/Fm), non-photochemical quenching (NPQ), or plant vitality parameter (Rdf) decreased significantly at 24 and 48 hpi compared to control leaves. Our results indicate that the initial stages of interaction between B. oleracea and A. brassicicola are not uniform within an inoculation site and show a complexity of host responses and fungal attempts to overcome host cell defense mechanisms. The downregulation of photosynthesis at the early stage of this susceptible interaction suggests that it may be a part of a host defense strategy, or, alternatively, that chloroplasts are targets for the unknown virulence factor(s) of A. brassicicola. However, the observed decrease of photosynthetic efficiency at the later stages of infection is a result of the fungus-induced necrotic lesion expansion.

Highlights

Brassica oleracea var. capitata from the Brassicaceae family is one of eight Brassica subspecies and an important vegetable in the human diet due to its nutritional values [1]
Infections caused by necrotrophic fungi in host plants during susceptible interactions are related to unrestricted cell death visible as spreading lesions, the appearance of which is strictly correlated to a fungal infection cycle and the production of a wide set of virulence factors [37,38]
We have focused on changes in the ultrastructure of chloroplasts in infected mesophyll cells, mostly due to the observed clear stages of their degradation (Figure 6) and the fact that analysis of our microarray data pointed out photosynthesis as the most negatively regulated process during infection of B. oleracea leaves with A. brassicicola (Table S3)

Summary

Introduction

Brassica oleracea var. capitata (head cabbage) from the Brassicaceae family is one of eight Brassica subspecies and an important vegetable in the human diet due to its nutritional values [1]. Capitata (head cabbage) from the Brassicaceae family is one of eight Brassica subspecies and an important vegetable in the human diet due to its nutritional values [1]. Many white, red, and Savoy cabbage cultivars are cultivated widely in Europe, Asia, and North America, and used as a staple diet item, an ingredient of many national cuisine vegetable dishes or an addition to salads. In Northern Europe and New Zealand, cabbage is often used as feed for sheep and cattle [1,2]. Cabbage is exposed to many bacterial and fungal diseases, which lower its yield all over the world. One of the most devastating fungus-induced diseases to all Brassicas is black spot disease, caused by Alternaria brassicicola. Cabbage cultivars show various levels of susceptibility to

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