The evolution of oligotrophy: implications for the breeding of crop plants for low input agricultural systems

Abstract

SummaryOligotrophy, the obligate or facultative capacity to live in low‐nutrient habitats, has played a major role in the evolution of photosynthetic organisms. Energy/carbon deficiency: evolution of photosynthesis about 3.5 Gyr (billion years) ago, then use of H2O as electron donor, and accumulation of O2 from about 2.3 Gyr ago. Deficiency in combined N: evolution of biological N2 fixation about 2.0‐2.3 Gyr ago. Deficiency in soluble relative to particulate organic C: evolution of phagotrophy in eukaryotes, opening the way to endosymbiotic origin of photosynthesis in eukaryotes. Deficiency of P and Fe resulting from oxygenation: evolution of mechanisms increasing access to P and Fe. Deficiency of H2O for land plants gaining C from the atmosphere: evolution of homoiohydry following origin of significant land flora from 0.5 Gyr ago. Deficiency of CO2 resulting from increased weathering by land plants: evolution of large leaves. Increased competition for resources among land plants: evolution of mechanisms economizing in use of soil‐derived resources, and increasing ability to acquire resources. Economising on resource use in photosynthetic organisms is subject to a number of constraints. There are very limited possibilities for reducing the use of N in proteins with a given catalytic function, but greater possibilities using substitution of an analogous protein with that function. The same applies to Fe. Possibilities for economising on the use of P are very limited if the growth rate is to be maintained: the marine cyanobacterium Prochlorococcus is a good example of restricted P requirement. H2O use can be constrained by C4 and, especially, CAM photosynthesis.A possible role of the study of oligotrophy in the context of sustainable, low‐input agriculture includes modified agricultural practice to minimise losses of resources. Information on oligotrophy and its evolution can also be used to inform the alteration of crop plants by genetic modification related to resource acquisition (e.g. associative, or nodule‐based, symbiotic diazotrophy) and the economy of resource use (e.g. partial or complete conversion of a C3 crop to a C4 crop which could economise in the use of N and/or H2O). The attempts to convert C3 to C4 plants have not thus far been fully successful, and the advantages of conversion to C4 are being increasingly offset by the effect of increasing atmospheric CO2 on C3 plants. However, more success has been achieved with selection of the most appropriate diazotrophic symbionts for crop plants in particular environments.