EFFECT OF PSEUDOMONAS SYRINGAE PV. TAGETIS INFECTION ON SUNFLOWER LEAF PHOTOSYNTHESIS AND ASCORBIC ACID RELATIONS

Authors: Robinson, Michael; Lydon, John; Murphy, Charles; Rowland, Randy; Smith, Ramona

Submitted to: International Journal of Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/16/2003
Publication Date: 3/1/2004
Citation: Robinson, J.M., Lydon, J., Murphy, C.A., Rowland, R., Smith, R. 2004. Effect of pseudomonas syringae pv. tagetis infection on sunflower leaf photosynthesis and ascorbic acid relations. International Journal of Plant Science. 165:263-271.

Interpretive Summary: Understanding the mechanisms associated with the synthesis of ascorbic acid (vitamin C) is important because vitamin C is an antioxidant that assists crop plants in withstanding oxidative stress caused by stressors such as elevated ozone and drought. Current evidence indicates that ascorbic acid is synthesized in leaf mitochondria, but ascorbic acid is an extremely important antioxidant in the chloroplast which is highly oxygenic in high light. Ascorbic acid levels are higher in the leaf chloroplasts than in any other organelle. Thus a current question that requires an answer concerns the identification of what leaf chloroplasts contribute to the synthesis of ascorbic acid in leaf cells. A new tool has been developed which assists in examination of the chloroplasts' role in ascorbate synthesis. A bacterial plant pathogen, P.syringae pv tagetis, which synthesizes a phytotoxin which inhibits the synthesis of chloroplast RNA polymerase, and which results an interference in chloroplast development to the extent that chloroplast are chlorophylless and have poorly developed internal membranes. At the same time the leaf cells of infected plants are able to develop normal mitochondria. Without chlorophyll, chloroplasts in the infected tissue are not photosynthetically competent, and the infected leaf tissue often has as little as 15-28% of normal ascorbic acid levels found in normal leaves. It is concluded that the bacterial toxin may inhibit one or more enzymes associated with the synthesis of acorbic acid, and this is the first report that a bacterial toxin can interfere with the synthesis of ascorbic acid in plants. This work is important to both plant physiologists, plant pathologist, and plant breeders, because it indicates that photosynthesis may play a role in ascorbic acid synthesis, that pathogens can cause reduction of antioxidants in crop plants, and that plant breeders whose mission is to improve on vitamin C content in plants should understand the the role of photosynthetic metabolism in supporting ascorbic acid synthesis.

Technical Abstract: Current evidence in several laboratories indicates that in plant leaf cells, ascorbic acid (vitamin C) is synthesized mainly in mitochondria, but not in chloroplasts. The question arises that since chloroplasts often have the highest ascorbic acid levels of any organelles in leaf cells, then is there a role of chloroplasts in ascorbic acid synthesis? We approached this question by infecting sunflower plants with a bacterial pathogen, Pseudomonas syringae, that interferes with leaf chloroplast development, but does not influence the development other cell organelles such as mitochondria. Electron microscopy of toxin infected sunflower plant leaves revealed that leaf cells possess chloroplasts containing disorganized thylakoids without grana, but in contrast there were distinct and well formed mitochondria, nucleii, and other organelles. The infected tissue had many and well formed mitochondria and compared with control plants leaves, had as much as 15 to 28% less total ascorbate (ascorbate + dehydroascorbate) than control leaves. However, the leaf cells of the infected plants also displayed the ability to maintain at least 80% of the total ascorbic acid in the reduced form indicating that the ascorbate-glutathione cycle enzymes in the cytosol, mitochondria and other leaf cell organelles were functional. Without chlorophyll, chloroplasts in the infected tissue are not photosynthetically competent, and the infected tissue often has as little as 15-28% of normal ascorbic acid levels. The results are interpreted to suggest that functional chloroplast and/or photosynthetic carbon metabolism contribute to the synthesis of ascorbic acid in plant leaf cells.