Carbohydrate Metabolism in Higher Plant Tissues Infected With Obligate Parasites

Abstract

Several reports (7, 8, 22) have described apparently fundamental changes in the rates and nature of respiratory pathways during infection of higher plant tissues by obligate parasites, particularly rust fungi. Although disease can cause increases of 400 % in rates with a marked lowering of C6/C1 ratios, there is considerable uncertainty about the carbohydrate changes which accompany the respiratory alteration. Allen (1) first reported increases in sucrose and hexoses in wheat infected by powdery mildew. Gerwitz and Durbin (10) have described increases in both reducing and non-reducing carbohydrates in wheat infected by rust fungi while otbers (5,15, 16) have reported marked decreases in both types of compounds. Shaw and Samborski (22) found increases at 3 and 7 days after infection of wheat with rust fungi, but at 5 and 10 days the diseased tissue contained less sucrose and hexose than healthy controls. Inman (13) has pointed out that the amount of infection and the stage of parasite development are two factors which are important in such studies. With heavy infection of the bean rust fungus, the levels of reducing and non-reducing carbohydrates increased by 50 and 300 %, respectively, just prior to sporulation. Subsequently, and within 72 hours, the levels fell to 50 % of control tissue. With progressively fewer infections per unit of leaf area the changes were neither as great nor as abrupt in time. In cases of light infection the concentrations of soluble carbohydrate did not fall below the levels in control plants. It is of interest that, despite the consistently low C6/C1 ratios in conjunction with high rates of respiration, only the usual hexoses and sucrose have been positively identified in detectable amounts in diseased tissue. Failure to observe changes in concentrations in carbohydrates, especially pentoses or heptuloses, postulated to arise by reactions of an oxidative pentose pathway, is not completely unexpected because of possible kinetic difficulties (i.e. small pool sizes). It is also possible that intermediates of glucose catabolism via shunt metabolism may be sequestered as phosphate derivatives and thus not readily identified by usual chromatographic analysis. Similar failure to detect changes in sugars have been reported for tissues in which low C6/C1 ratios have been induced by other means (2, 20). In instances of disease-induced changes in C6/C1 ratios, there is circumstantial evidence that an oxidative pentose pathway is involved. It has been shown that low C,/C1 ratios occurred in the infected areas of diseased tissues, not in adjacent uninvaded tissue. The germinating spores of the parasite show low C6/C1 ratios and all of the enzymes of the oxidative pentose pathway are present with the possible exccption of transaldolase (23). There are two reports of alterations in carbohydrates that appear to be related to respiratory changes due to infection by obligate parasites. Jain and Pelletier (14) reported increased labelling in sedoheptulose when plants with low levels of infection metabolized C1409 in the light. Wang (26) reported similar results and found that this change occurred in uninfected host cells of diseased leaves. In view of the association of respiratory changes with invaded tissue and the complicating role of light in these experiments, the increased synthesis of sedoheptulose by a pentose pathway in diseased tissue is not established. Furthermore, it is to be noted that in both papers the evidence presented for the occurrence of sedoheptulose apparently is based chiefly on the similarities of Rf values of a radioactive spot with known compounds, usually in one dimensional chromatograms. Other workers have not mentioned the presence of sedoheptulose in rusted tissue (10, 15, 22) and separation of sedoheptulose from fructose sometimes is difficult (3). A similar criticism can be advanced for Wang's admittedly tentative identification of inannose (26), also not indicated to be present in other studies, as a major component of diseased tissue. 'Received Jan. 30, 1962. 2 Published with the approval of the Director as Paper No. 1188, Journal Series, Nebraska Agricultural Experiment Station. Supported by funds from USPH, grant E-2000 and the Research Council, University of Nebraska. 3 Present address, Shade Tree Laboratory, University of Massachusetts. Field Station. Waltham. Mass.