Sink stimulation of leaf photosynthesis by the carbon costs of rhizobial and arbuscular mycorrhizal fungal symbioses

Key words: biochemical model of leaf photosynthesis; carbon sink strength; chlorophyll fluorescence; harvest index; leaf protein; leaf senescence; legumes; photosynthetic nutrient use efficiency; Pi recycling; source-sink regulation; ureides

One of the most fascinating processes in plant physiology and agronomy is the capability of legumes to associate symbiotically with rhizobial bacteria and arbuscular mycorrhizal (AM) fungi. The legumes supply photosynthates in exchange for nitrogen, derived from biological N2 fixation, and soil nutrients mainly phosphate, obtained from foraging of AM fungi from the soil. The rhizobial and arbuscular mycorrhizal symbioses each may use 4-16% of recently fixed photosynthates to maintain their activity, growth and reserves, but in turn, may supply 100% of the plant nutrient requirements. The C costs of the symbioses are often assumed to limit plant productivity due to photosynthate competition between the microsymbiont and the host. In addition, the C costs are often used as an entry point to understand the evolution of the symbioses.
It is intriguing that despite of the symbiotic C costs, plants associated with rhizobia and/or AM fungi often produce more biomass and grains than fertilized plants. Increases in plant growth are traditionally attributed to improved plant nutrition and enhanced photosynthesis. This thesis gives evidence that plants – and particularly legumes – are able to overcome any putative C limitation associated with rhizobial and AM fungal symbioses by increasing the rates of photosynthesis due to sink stimulation, over and above the expected nutritional benefits from the symbioses. Sink stimulation of photosynthesis is a consequence of increased C demand from photosynthesis, which increases the export of triose-P from chloroplasts, recycling more inorganic phosphates and activating more photosynthetic enzymes. In the thesis, I report a literature study, which provides a framework for the quantification of sink stimulation of photosynthesis. Apparently, sink stimulation of photosynthesis by symbioses just equals the C costs, which in the long term is still beneficial for plant growth. Sink stimulation of photosynthesis implies that plants and symbioses are not limited by photosynthates, which means that the cost : benefit theories for symbioses need to be re-conceptualized.
Photosynthesis is limited by three biochemical processes: rubisco activity, electron transport, and triose-P export (often referred as sink limitation). In Chapter 3, I apply a biochemical model expressing these three limitations in CO2 response curves of soybean (Glycine max [L.] Merrill) inoculated with rhizobial strains with putative different C costs (Bradyrhizobium japonicum CPAC 390 or CPAC 7) or fertilized with KNO3, to understand the effects of rhizobial symbioses on the photosynthetic capacity. Plants associated with putatively more expensive strains have higher photosynthetic capacity than those associated with less ‘expensive strains’. The effect of sink stimulation of photosynthesis is evident because plants with higher triose-P export rates consistently had higher rates of electron transport and rubisco activity. These results suggest that the C costs of rhizobial symbioses generate feedbacks between the rates of triose-P export with rubisco activity and electron transport rates.
I also describe three subsequent experiments with two different soybean varieties nodulated with two rhizobial strains or fertilized with two doses of KNO3 fertilizer. Plants associated with rhizobial symbioses always had higher rates of photosynthesis and accumulated less starch in the leaves than N-fertilized plants throughout the whole cycle. Furthermore, nodulated plants maintained higher chlorophyll concentrations for a longer period than N-fertilized plants. Both photosynthesis and N2 fixation were synchronized over the plant cycle. One of the conclusions of Chapter 4 is that C costs of rhizobial symbioses lead to sink stimulation of photosynthesis, which in turn, delays leaf senescence. These mechanisms together are likely to contribute for increase in plant productivity.
Overall, the thesis indicates that the C costs of symbioses are not disadvantageous, as usually thought. Higher activity of rhizobial and AM fungal symbioses results in sink stimulation of photosynthesis, which leads to higher plant growth over time. Sink stimulation of photosynthesis implies that the microsymbionts and plants are not limited by photosynthate. Increased rates of photosynthesis in initial stages of plant development delay the rates of leaf senescence in the later stages of plant development. The C costs of symbioses bring advantages to the plant’s adaptation under elevated CO2 concentration, because they remove the sink limitation of photosynthesis. It means that effectiveness of the symbioses (the capacity to supply nutrients) is more important than the C costs or the efficiency with which photosynthates are used.