In the Spotlight: The unexpected protagonists that shape plant survival

Linked article: this spotlight refers to Shi et al. (2024). To view this article, please visit https://doi.org/10.1111/ppl.14463.

Plants are masters of adaptation, constantly adapting their metabolism to thrive in changing environments. A new study by Shi et al. (2024) reveals how two unassuming metals, magnesium (Mg²⁺) and manganese (Mn²⁺), act as molecular switches, influencing the most important enzyme on Earth, Rubisco. When Mg²⁺ is present, Rubisco fuels photosynthesis, but when Mn²⁺ takes over, plants redirect carbon into alternative pathways that help them cope with stress. This ancient survival trick, dating back over two billion years, still shapes plant metabolism today. Understanding how plants control these metals could unlock new strategies for engineering climate-resilient crops and securing our food supply in an unpredictable world. Sometimes, the smallest elements hold the biggest secrets (Figure 1).

Imagine a world where plants, the silent architects of our ecosystem, are secretly fine-tuning their metabolism, adapting to environmental changes with the help of unexpected allies: metals. Magnesium (Mg²⁺) and manganese (Mn²⁺) might not sound like protagonists in a high-stakes survival story, but they are. When Mg²⁺ is bound to Rubisco, the enzyme responsible for photosynthesis, plants efficiently fix carbon and fuel sugar production. But when Mn²⁺ steps in, it's like flipping a metabolic switch. Rubisco shifts gears, prioritizing pathways that help plants handle stress. It's a biochemical balancing act, with plants strategically deciding when to accelerate photosynthesis and when to detour toward survival mode. A recent study by Shi et al. published in Physiologia Plantarum reveals how plants use these metals as molecular levers to switch between different metabolic strategies, optimizing their energy use in response to fluctuating conditions (Shi et al., 2024). And if we understand this biochemical balance, we might unlock new ways to engineer crops that thrive in an unpredictable climate.

How do we know all this? Shi et al. didn't just assume plants were playing this metal-swapping game, they put it to the test. Using Arabidopsis thaliana, a model plant species, the researchers ran biochemical assays, tracking how Rubisco behaves when different metals are in charge. The results? When Mg²⁺ was present, Rubisco stuck to its classic role, capturing CO₂ and fueling photosynthesis. But when Mn²⁺ took over, the enzyme pivoted toward oxygenation, increasing photorespiration and rerouting carbon into malate and pyruvate. To confirm these findings outside the lab, the team used gas exchange measurements and chlorophyll fluorescence imaging, monitoring how living plants dynamically adjusted their metabolism based on metal availability. The main takeaway here is that plants aren't just passive players in their environment—they are making strategic biochemical choices in real-time.

But wait, where did this trick come from? It turns out swapping metals isn't just a modern-day survival hack—it's an ancient one. Over two billion years ago, during the Great Oxidation Event, Earth's oxygen levels skyrocketed, forcing early photosynthetic organisms to evolve new ways to cope. Mn²⁺ played a starring role in this adaptation, becoming essential in Photosystem II, where plants split water molecules to release oxygen (Fischer et al., 2016; Lingappa et al., 2019). Fast forward to today, and Mn²⁺ is still pulling strings behind the scenes, helping plants adapt to fluctuating CO₂ levels, nutrient imbalances, and environmental stress. And it is not just Rubisco feeling the effects. Shi et al. found that Mn²⁺ also alters the function of the plastidic malic enzyme, a key player in carbon and nitrogen metabolism. To see this in action, the researchers used stable isotope labelling to trace carbon movement in plants exposed to different Mn²⁺: Mg²⁺ ratios. When Mn²⁺ was abundant, plants ramped up malate production, a process crucial for nitrogen assimilation and stress resistance. But when Mg²⁺ levels were higher, plants redirected carbon toward pyruvate and energy production. This flexibility allows plants to adjust their metabolism like a thermostat, optimizing for growth when conditions are good and switching to survival mode when resources are scarce.

So, why should we care about a tiny metal shuffle happening inside plants? Because understanding this biochemical flexibility could change the way we approach agriculture. Imagine engineering crops that can actively adjust their metal usage to thrive in tough conditions. By fine-tuning Mg²⁺ and Mn²⁺ availability, scientists could develop plants that flourish in nutrient-poor soils, resist extreme weather, and maintain high yields despite environmental stress.

The next step? Exploring how this metal-switching mechanism operates across different plant species and ecosystems. Could tropical crops make better use of Mn²⁺ in nutrient-deficient soils? Could this knowledge lead to crops that use nitrogen more efficiently, reducing fertilizer dependency? As researchers dig deeper, they may uncover even more hidden metabolic pathways shaped by these tiny but mighty elements. The smallest players in plant metabolism might just hold the biggest secrets for the future of agriculture and sustainability.

FUNDING INFORMATION

This work was supported by the University of Florida CALS Dean's Award to N.P.