C3 and C4 plant systems respond differently to the concurrent challenges of mercuric oxide nanoparticles and future climate CO₂

Future climate CO₂ (eCO₂) and contamination with nano-sized heavy metals (HM-NPs) represent concurrent challenges threatening plants. The interaction between eCO₂ and HM-NPs is rarely investigated, and no study has addressed their synchronous impact on the metabolism of the multifunctional stress-related metabolites, such as sugars and amino acids. Moreover, the characteristic responses of C3 and C4 plant systems to the concurrent impact of eCO₂ and HM-NPs are poorly understood. Herein, we have assessed the impact of eCO₂ (620 ppm) and/or HgO-NPs (100 mg/Kg soil) on growth, physiology and metabolism of sugars and amino acids, particularly proline, in C3 (wheat) and C4 (maize) plant systems. Under Hg-free conditions, eCO₂ treatment markedly improved the growth and photosynthesis and induced sugars levels and metabolism (glucose, fructose, sucrose, starch, sucrose P synthase and starch synthase) in wheat (C3) only. In contrast, HgO-NPs induced the uptake, accumulation and translocation of Hg in wheat and to less extend in maize plants. Particularly in wheat, this induced significant decreases in growth and photosynthesis and increases in photorespiration, dark respiration and levels of tricarboxylic acid cycle organic acids. Interestingly, the co-application of eCO₂ reduced the accumulation of Hg and recovered the HgO-NPs-induced effects on growth and metabolism in both plants. At stress defense level, HgO-NPs induced the accumulation of sucrose and proline, more in maize, via upregulation of sucrose P synthase, ornithine amino transferase, ∆¹-pyrroline-5-carboxylate (P5C) synthetase and P5C reductase. The co-existence of eCO₂ favored reduced sucrose biosynthesis and induced proline catabolism, which provide high energy to resume plant growth. Overall, despite the difference in their response to eCO₂ under normal conditions, eCO₂ induced similar metabolic events in C3 and C4 plants under stressful conditions, which trigger stress recovery.