Photosynthesis and carbohydrate metabolism in tobacco leaves during an incompatible interaction with Phytophthora nicotianae

• Published in: Plant, cell and environment cell and environment, 2005-11, Vol.28 (11), p.1421-1435
• Main Authors: Scharte, J, Schon, H, Weis, E
• Format: Article
• Language: English
• Subjects: apoptosis; Biological and medical sciences; callose; carbohydrate metabolism; chlorophyll‐a fluorescence imaging; disease resistance; electron transport chain; Fundamental and applied biological sciences. Psychology; fungal diseases of plants; host-pathogen relationships; hypersensitive response; leaves; Metabolism; Nicotiana; Nicotiana tabacum; oxidative pentose phosphate pathway (OPPP); pentose phosphate cycle; photorespiration; photosynthesis; Photosynthesis, respiration. Anabolism, catabolism; Phytophthora nicotianae; plant biochemistry; plant defence; plant pathogenic fungi; plant physiology; Plant physiology and development; primary metabolism; reactive oxygen species; resistance mechanisms; stomatal movement; sucrose; tobacco
• ISSN: 0140-7791; 1365-3040
• DOI: 10.1111/j.1365-3040.2005.01380.x

The metabolic and cellular changes in source leaves of Nicotiana tabacum L. cv SNN during an incompatible interaction with Phytophthora nicotianae van Breda de Haan were investigated and compared with defence reactions. Hypersensitive cell death was preceded by a rapid and highly localized shift to non-assimilatoric metabolism. During the first 6 h post infection (hpi), reactive oxygen species (ROS) accumulated. Callose was deposited at the interface of adjacent mesophyll cells (>=1 hpi), the export of sucrose collapsed and its content in the apoplast increased. Stomata closed and photosynthetic flux was reallocated from CO2 assimilation in favour of photorespiration. This was accompanied by an increase in respiration, glucose-6-phosphate dehydrogenase (G6PDH) activity, apoplastic invertase and hexose content. Later (>6 hpi) the photosynthetic electron transport chain was interrupted and photosynthesis completely collapsed. This was accompanied by a further increase in apoplastic invertase and carbohydrates, respiration and oxidative pentose phosphate pathway (OPPP) and followed by further burst in ROS release. Hypersensitive cell death did not appear until photosynthesis completely declined. Photosynthesis was visualized by chlorophyll-a fluorescence imaging on a macro- and microscopic scale. Decline in photosynthesis and defence reactions were highly localized processes, which occur in single mesophyll cells. We propose that in photoautotrophic leaves, photosynthesis and assimilatory metabolism must be switched off to initiate respiration and other processes required for defence. An early blockage of intercellular sugar transportation, due to callose deposition, in conjunction with enhanced apoplastic invertase activity could facilitate this metabolic shift.