Photosynthetic Modulation in Response to Plant Activity and Environment

Summary

Modulation of foliar photosynthesis rate during short-term changes in abiotic environment as well as longer-term acclimation of photosynthetic capacity in response to abiotic factors or other organisms are summarized. Acclimation is informed by the balance between the rate at which photosynthate is produced and moved into the phloem and out of the leaf (source activity) and the rate at which photosynthate is removed from the phloem and utilized or stored in sinks (sink activity). We first review various experimental manipulative approaches utilized to perturb source to sink ratio within a plant and evaluate the impact of such perturbations on photosynthesis. In general, alterations that markedly increase the whole plant ratio of source to sink activity results in photosynthetic downregulation, whereas decreases in source to sink ratio often lead to photosynthetic upregulation. We then examine the impact of various environmental factors on plant activity and development, photosynthesis, dissipation of excess energy by the xanthophylls zeaxanthin and antheraxanthin, source-sink balance, photosynthate transport, and foliar carbohydrate levels. Environmental factors considered include fire, light, temperature, salinity, availability of water and essential nutrients, pollution, and herbicides. The response of foliar photosynthesis varies depending on species (growth habit) and the environmental condition(s) to which the plant is exposed. In some circumstances, photosynthesis is upregulated in concert with enhanced foliar mesophyll, vascular infrastructure, and photosynthate transport and utilization. In yet others, photosynthesis is downregulated in concert with decreased growth and photosynthate transport as well as increased accumulation of carbohydrates and employment of sustained zeaxanthin-associated energy dissipation as a form of photoinhibition. As source to sink ratio increases, surplus photosynthate may be used to produce compatible solutes, phenolics (including anthocyanins as well as other flavonoids), structural components of cells and the cuticle, and volatile organic compounds released into the atmosphere. In addition to serving as enhanced sinks for photosynthate, all of these products can also serve in defense against abiotic and biotic stresses. Biotic factors impacting photosynthesis include competition, herbivory, pathogens (bacteria, fungi, and viruses), xylem- and phloem-tapping parasitic plants, and symbiotic and mutualistic fungi and bacteria. Many biotic factors can also trigger either upregulation or downregulation of photosynthesis, depending on the nature of the interaction. For instance, in some cases herbivory can result in a decreased ratio of plant source to sink activity and photosynthetic upregulation, while in other cases an increased ratio of source to sink activity and photosynthetic downregulation is seen. Competition for water by xylem-tapping insects or parasitic plants can lead to photosynthetic downregulation, while phloem-tapping insects and parasitic plants, as additional sinks for photosynthate, can induce photosynthetic upregulation. Some pathogens block photosynthate export from leaves, leading to foliar carbohydrate accumulation and feedback inhibition of photosynthesis, whereas other pathogens induce production of additional tissue that acts as a sink for photosynthates and stimulates photosynthetic upregulation. Symbiotic fungi and bacteria (e.g., mycorrhizal fungi, nitrogen-fixing bacteria, endophytes) and mutualistic soil microbes generally promote plant growth and act as additional sinks themselves, thereby stimulating photosynthetic upregulation. Across the spectrum of abiotic and biotic influences, foliar photosynthesis responds to the demand for its products through acclimation either within the constraints of the existing foliar infrastructure in mature leaves or through production of new leaves compatible with the altered level of need. These connections are placed into the context of global climate change and its impact on plant abiotic and biotic interactions.