From C3 to C3-C4 and C4 photosynthesis

  • Motivation: Most of life’s major innovations evolved just once and those origins are so deep in our evolutionary history that how they evolved will probably always remain a matter of speculation. However, C4 is an exception to this pattern: the C4 pathway is a major evolutionary innovation; it has evolved not just once, but dozens of times; and the most recent origins of C4 are so close to present that we can still study the C3-C4 intermediate states.

  • Background: On the one hand, a number of lines of evidence suggest that C3-C4 photosynthesis represents an intermediate stage in evolutionary transitions from C3 to C4 photosynthesis. On the other hand, no ecological conditions have yet been identified under which C3-C4 photosynthesis provides C3-C4 plants with unique physiological advantages over C3 and C4 plants. At the heart of this puzzle is the question: what are the relative advantages and disadvantages of C3, C3-C4, and C4 photosynthesis?

  • Approach: While the C3-C4 syndrome has been studied for decades by plant physiologists, the key measurements have almost always been: (a) made on plants that were grown under controlled conditions and measured in the laboratory, and (b) interpreted qualitatively rather than quantitatively. In this paper, we describe a general model of C3, C3-C4, and C4 photosynthesis that is designed to facilitate quantitative analysis of physiological measurements, and we demonstrate how it can be used to interpret measurements from the lab and the field.

  • 1. Diamond Y Spring Preserve

    This story is set in the Diamond Y Spring Preserve, a unique ecosystem in Pecos County, Texas that has been protected from oil and gas development by the Nature Conservancy.

  • 2. Water in the desert

    The Diamond Y Spring Preserve is one of the largest ciénegas, or desert wetlands, that remains in North America. In this type of system, groundwater flows from the spring, and then evaporates into the desert climate.

  • 3. A unique plant community

    The conditions at this site support a unique plant community where there is competitive coexistence between plants using C3, C3-C4 intermediate, and C4 photosynthesis.

  • 4. Evolutionarily stable strategy

    The persistence of C3-C4 intermediate plants in this community suggests that the ecological conditions here allow C3-C4 photosynthesis to represent an evolutionarily stable strategy (ESS).

  • 5. Aboveground environment

    To explore this idea, we examined the microclimate at the Diamond Y Spring Preserve by deploying a suite of environmental sensors during the peak of the summer growing season.

  • 6. Belowground environment

    At the same time, we examined the properties of the belowground environment. Here, Eric Slessarev is excavating a C3-C4 plant that sends roots laterally over the surface of the inundated, salt-rich soil.

  • 7. Photosynthetic performance

    We then examined how the photosynthetic performance of C3, C3-C4 intermediate, and C4 species varied and how the physiological variation was related to environmental variation. Here, Claire Kouba is measuring gas-exchange with a LI-6400 system.

  • 8. A surprising discovery

    While the C3 and C4 plants we examined all exhibited typical patterns of photosynthetic performance, the C3-C4 species exhibited a lower CO2 compensation point in the field than we had previously observed in the lab.

  • 9. How does C3-C4 photosynthesis work?

    To understand the basis of this, we first turned to the classic model of C3-C4 photosynthesis developed by Susanne von Caemmerer. However, this model could not explain all of the observed properties of the CO2 compensation point.

  • 10. We needed a new model

    We then extended our new description of the C3 electron transport system to the C3-C4 and C4 pathways, and found that this framework could explain the observed properties of the CO2 compensation point across all of the different pathways.

  • 11. We figured it out!

    The new model is described here: J. E. Johnson, C. B. Field, and J. A. Berry. 2021. The limiting factors and regulatory processes that control the environmental responses of C3, C3-C4 intermediate, and C4 photosynthesis. Oecologia 197: 841-866.

The full story, and its significance

  • Full story: The details of this study can be found in the following reference:

  • Significance: The new model explains two of the unique and puzzling physiological characteristics of C3-C4 plants: the light dependence of the CO2 compensation point, and population-level variation in the CO2 compensation point. It also introduces an intriguing new hypothesis for the evolutionary origins of the C4 pathway: that it may have evolved to smooth out energy supply and demand, rather than to concentrate CO2. This framework has a wide range of potential applications to physiological, ecological, and evolutionary questions.