Over 3 billion years ago, photosynthesis first evolved in ancient bacteria on a water-covered Earth. Over millions of years, these bacteria evolved into plants, adapting to environmental changes. About 30 million years ago, a more efficient form of photosynthesis called C4 emerged. While plants like rice continued using the older C3 method, others, such as corn and sorghum, adopted the more efficient C4 process.
Over 8,000 C4 plant species thrive in hot, dry environments and are among the most productive crops globally. However, most plants still use the older C3 photosynthesis method.
In collaboration with the University of Cambridge, scientists at Salk Institute have discovered a critical step that enabled C4 plants, like sorghum, to evolve their highly efficient photosynthesis. This breakthrough could improve the productivity and resilience of C3 crops like rice, wheat, and soybeans, making them better suited to our warming climate.
Professor Joseph Ecker, the senior author of the study, Salk International Council Chair in Genetics, and Howard Hughes Medical Institute investigator said, “Asking what makes C3 and C4 plants different is not just important from the basic biological perspective of wanting to know why something evolved and how it functions on the molecular level. Answering this question is a huge step toward understanding how to make the most robust and productive crops possible in the face of climate change and a growing global population.”
Around 95% of plants use C3 photosynthesis, where mesophyll cells convert light, water, and carbon dioxide into sugars. However, C3 photosynthesis has two major drawbacks: 1) Oxygen is sometimes used instead of carbon dioxide, wasting energy, and 2) Pores on leaves open too frequently, leading to water loss and increased vulnerability to drought and heat.
C4 photosynthesis solves these issues by using bundle sheath cells to help with photosynthesis, reducing oxygen mistakes, and keeping pores closed more often to conserve water. This makes C4 plants 50% more efficient than C3 plants.
The question is how C3 plants evolved into C4 plants on a molecular level and whether scientists could encourage C3 crops to adopt C4 photosynthesis.
Salk scientists used advanced single-cell genomics technology to answer these questions and compare C3 rice with C4 sorghum. Unlike previous methods, which couldn’t accurately distinguish between neighboring cell types like mesophyll and bundle sheath cells, single-cell genomics allowed researchers to analyze the genetic and structural changes in each plant cell type.
Prof. Ecker said, “We were surprised and excited to find that the difference between C3 and C4 plants is not the removal or addition of specific genes. Rather, the difference is on a regulatory level, which could make it easier for us to turn on more efficient C4 photosynthesis in C3 crops in the long run.”
All cells in an organism have the same genes, but their identity and function depend on which genes are expressed, a process influenced by transcription factors. These proteins bind to regulatory elements near genes, turning them “on” or “off.”
In their study of rice (C3) and sorghum (C4), the Salk scientists discovered that a transcription factor family called DOFs activates genes that create bundle sheath cells in both species.
They also found that in C4 sorghum, DOFs are bound to a regulatory element that activates bundle sheath identity genes and photosynthesis genes. This suggested that C4 plants had evolved by attaching ancestral bundle sheath regulatory elements to photosynthesis genes, allowing DOFs to activate both sets of genes simultaneously.
This insight reveals that both C3 and C4 plants have the required genes and transcription factors for C4 photosynthesis, offering hope for scientists aiming to encourage C3 plants to adopt this more efficient process.
Joseph Swift, co-first author of the study and a postdoctoral researcher in Ecker’s lab, said, “Now we’ve got this blueprint for how different plants utilize the sun’s energy to survive in different environments. The ultimate goal is to try to switch C4 photosynthesis on and, in turn, create more productive and resilient crops for the future.”
The team’s next goal is to determine if rice can be engineered to use C4 photosynthesis instead of C3, a long-term objective with significant technical challenges. This effort is part of the global “C4 Rice Project.” The findings will immediately contribute to the Salk Harnessing Plants Initiative, which aims to create crops optimized to combat and withstand climate change.
The team’s single-cell genomics data has been shared as a resource for scientists worldwide, sparking excitement as it answers a long-standing evolutionary mystery.
Journal Reference:
- Swift, J., Luginbuehl, L.H., Hua, L. et al. Exaptation of ancestral cell-identity networks enables C4 photosynthesis. Nature (2024). DOI: 10.1038/s41586-024-08204-3