To C4 or not to C4 if you’re a tree? Some possible answers

C₄ photosynthesis is a technique used by some plant species to maximise the efficiency with which they fix carbon dioxide from the atmosphere. It is associated with both anatomical and biochemical traits that improve the efficiency of carbon dioxide-fixation. How these anatomical and biochemical traits arise and develop is currently a topic of much interest, because of the possibility that we may be able to use them to improve the productivity of major non-C₄ food crops. Rather remarkably, C₄ photosynthesis has evolved almost 70 times independently in a diverse variety of plants. Despite being widely-distributed in plants, C₄ photosynthesis is only known to be present in a single group of trees, specifically some members of the genus Euphorbia. The fact that so few C₄ trees exist compared to other kinds of plant has attracted comment in the past and remains an unresolved conundrum. In their recent Open Access article in Journal of Experimental Botany Sophie Young and colleagues discuss why C₄ photosynthesis is so rare in trees and come to the conclusion that multiple factors are likely involved in this.

As Young and colleagues point out early in their article, C₄ trees do exist (albeit rarely) and so there seems to be no universal incompatibility between C₄ photosynthesis and being a tree. Their rarity may therefore derive from a more complex series of factors that seldom unite, which may occassionally result in C₄ photosynthesis being of sufficient benefit to a tree. A major point in untangling this is understanding how C₄ photosynthesis actually came to be in members of the Euphorbia genus. C₄ Euphorbia species all occur in Hawaii, and Young and colleagues point out that current evidence indicates that these derive from a C₄ ancestor that was not a tree. In other words, C₄ Euphorbia species likely arose through C₄ plants becoming trees, rather than trees acquiring C₄ photosynthesis traits. However, the fact that this has been apparently such a rare occurrence suggests that this must be a difficult road to take.

One possible reason why C₄ photosynthesis is seldom found in trees may be due to the challenges trees face, particularly tall, canopy-forming trees. Young and colleagues highlight that studies have found leaves in the canopy of tall tree species to have high variability in cell water potentials and as a possible consequence, variable pressure differences between different cells or tissues. As C₄ photosynthesis relies on a specialised flow of metabolites between leaf cells through plasmodesmata, the authors speculate that this may be incompatible with tall canopy-forming tree forms. This would certainly fit with the current form of C₄ Euphorbia species, which are not tall, canopy-forming trees. Related to this is that trees tend to exhibit specific arrangements of plasmodesmata to support long-distance flow of materials between source and sink via the phloem,  which the authors speculate may partially cancel out the effects of arrangements of plasmodesmata used to direct flow of metabolites in C₄ plant species.

The authors point out that species of the Euphorbia genus are very morphologically diverse and have an apparently high degree of adaptive plasticity and short generation times. They point out that these features may have facilitated the relatively rapid emergence of tree characteristics from a C₄ ancestor in Euphorbia more easily than in other genuses. These factors may also have allowed C₄ Euphorbia to acquire some degree of shade tolerance that allows them to grow sometimes in the shadow of canopy-forming tree species in Hawaii, sidestepping the phenotypic variability constraints usually imposed by C₄ photosynthesis.

So it seems that several factors may come together to ensure that C₄ trees are a rare occurrence, and those that do occur seem to be quite constrained  by these factors in the form they take. As Young and colleagues conclude: ‘routes to the evolution of a C4 tree are potentially tortuous, which may together explain the global rarity of C4 tree species.’ Whether or not there are more unidentified C₄ tree species out there remains unclear but for now, as Young and colleagues discuss, the circumstances seem to be pretty unique for them to emerge.