Regulation of carbohydrate partitioning during the interaction of potato virus Y with tobacco

Abstract

To test whether carbohydrates may play a signalling function during plant pathogenesis, we investigated the interaction between tobacco and potato virus Y (PVY(N)). Four days after PVY(N) infection, leaves started to accumulate soluble sugars and leaf photosynthesis decreased. The accumulation of soluble sugars was accompanied by an induction of cell wall invertase and a gradual decrease in the sucrose-to-hexose ratio. In parallel to changes in carbohydrate metabolism and photosynthesis, transcripts encoding PR-proteins accumulated. Based on this coincidence, it was hypothesized that elevated hexose levels may enhance the expression of defence-related functions and might possibly explain the phenomenon of high sugar resistance in plants. This notion has been supported by the fact that cell wall invertase-expressing transgenic tobacco plants were found to be resistant against PVY(N) (Herbers et al., 1996b). To exclude the possibility that salicylate, which accumulates in plants expressing invertase, may be responsible for the observed resistance, these transgenic plants were crossed with salicylate hydroxylase-expressing plants (nahG). The progeny were selected for high levels of sugar and low levels of salicylate. Necrotic lesions also developed, typically formed on the leaves of plants expressing invertase, and transcripts encoding PR-Q accumulated in the absence of salicylate. On the other hand, accumulation of PR-1b transcripts decreased, indicating that sugars are not sufficient for PR-1b induction. Infection experiments using these plants as hosts revealed resistance towards PVY(N). Thus, the mechanism of apoplastic invertase induced virus resistance is salicylate independent and most likely sugar mediated.

RNA Interference-Mediated Repression of Cell Wall Invertase Impairs Defense in Source Leaves of Tobacco

“…Transcripts of the acidic, salicylate-inducible protein PR-1b (Herbers et al, 1996(Herbers et al, , 2000 accumulated at the infection site in the wild type from an early stage of infection on, whereas the expression of PR-1b was weaker and only slightly induced in cwINV-deficient plants (Fig. 4A).…”

“…In source leaves, constitutive expression of cwINV leads to the accumulation of carbohydrates and a metabolic source-to-sink shift. These plants also show increased gene expression of PR proteins and enhanced resistance against viral infection (Herbers et al, 1996(Herbers et al, , 2000.…”

“…Similar observations were made in barley (Hordeum vulgare) leaves during an interaction with powdery mildew (Blumeria graminis; Swarbrick et al, 2006) and in various other plant-pathogen interactions (for review, see Roitsch et al, 2003). A specific role of cwINV during plant defense has been suggested (Ehness et al, 1997), based on observations that cwINV activity is often induced during various plant-pathogen interactions (for review, see Roitsch et al, 2003) and the finding that overexpression of a yeast (Saccharomyces cerevisiae) invertase in the apoplast increases plant resistance against viruses (Herbers et al, 1996(Herbers et al, , 2000. It is also reported that pathogens can stimulate host cwINV activity (Swarbrick et al, 2006).…”

“…Several lines of evidence suggest that plants establish high hexose levels in response to invading pathogens, which in turn support defense responses of the host (e.g. Herbers et al, 1996Herbers et al, , 2000Roitsch et al, 2003;Biemelt and Sonnewald, 2006;Swarbrick et al, 2006;Berger et al, 2007;Seo et al, 2007). On the other hand, those hexoses could be a nutrient source for pathogens.…”

Inducible expression of magnesium protoporphyrin chelatase subunit I (CHLI)-amiRNA provides insights into cucumber mosaic virus Y satellite RNA-induced chlorosis symptoms

“…The disturbance of chloroplast functions may be responsible for the production of chlorosis that is associated with virus infection [19]. Several plant-virus interaction studies have revealed that virus infection inhibits host photosynthesis, which is usually accompanied by viral symptoms [7,9,10,16,29]. Virus infection commonly causes chlorosis resulting into impaired chlorophyll biosynthesis and reduced photosynthetic activities that lead to a decrease in biomass production and significant loss in crop yield [44].…”