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Leaf rust, also known as brown rust, is caused by the fungus Puccinia triticina Eriks., that can result in a significant threat to the grain yield and quality of wheat. Elevated disease severity, known as increased biotic stress pressure, correlates with increased accumulation of reactive oxygen species (ROS), where plants activate defence mechanisms against oxidative damage to regulate toxic levels of ROS. To improve our understanding of the physiological mechanism of wheat resistance to leaf rust, we set up the experiment with wheat seedlings of six genotypes differing in leaf rust resistance to elucidate interactions of this pathogen with carbohydrate and antioxidant metabolism of wheat genotypes. Obtained results showed that genotype with the highest severity of leaf rust symptoms decreased cytoplasmic invertase (cytInv) very early, 8 hours after inoculation (hai) with leaf rust. The downregulation of cytInv in susceptible plants may facilitate the maintenance of elevated apoplastic sucrose availability serving as nutrients for pathogen growth thus allowing spreading of symptoms more rapidly. The significant role in wheat seedling resistance to leaf rust can be attributed to vacuolar invertase (vacInv) that was supported by the fact that moderately resistant genotypes to leaf rust significantly increased vacInv when symptoms were fully developed. Also, vacInv were previously reported to assist in pathogen defence and scavenging of ROS. Simultaneously, glucose-6-phosphate dehydrogenase (G6PDH) and UDP-glucose pyrophosphorylase (UGPase) in moderately resistant genotypes decreased and further might restrict normal growth and development of pathogen due to reduced sugar content. The main contributors of leaf rust resistance in antioxidative metabolism were ascorbate peroxidase (APX) and catalase (CAT) activity resulting in less oxidative damage in the early stage of leaf rust development and thus maintaining a higher antioxidant capacity resulting in lower oxidative damage. Thereby, carbohydrate and antioxidant mechanisms acted mutually in defence of wheat seedlings during leaf rust stress. In addition to well-known antioxidative defence systems, carbohydrate metabolism can now be recognized as a crucial mechanism in coordinating plant developmental responses under leaf rust occurrence in wheat.