<p>Silicon (Si) is widely recognized as an important regulator of the global carbon (C) cycle via its effect on diatom productivity in oceans and the weathering of silicate minerals on continents. Si is also a beneficial plant nutrient, improving resistance to herbivory and pathogens and mitigating the negative effects of several abiotic stresses, including nutrient limitation. However, changes in Si sources and cycling during long-term development of terrestrial ecosystems remain poorly understood. We studied Si in soils and plants along two 2-Ma coastal dune chronosequences in southwestern Australia (Jurien Bay and Guilderton). Soil development along these chronosequences includes carbonate leaching in Holocene soils, formation of secondary Si-bearing minerals in Mid-Pleistocene soils, followed by their loss via dissolution, to yield quartz-rich soils of Early-Pleistocene age. The chronosequences also exhibit an extreme gradient of soil fertility in terms of rock-derived nutrients, and shifts from nitrogen (N) to phosphorus (P) limitation of plant productivity as soils age. Along each chronosequence, we quantified the pools of reactive Si-bearing phases and plant-available Si in the soils, and physically extracted soil phytoliths (amorphous silica formed in plant tissues). We also quantified Si, macronutrients and total phenols in the most abundant plants growing along the best-studied of the two chronosequences (Jurien Bay). We found that plant-available Si was lowest in young and carbonate-rich soils, because carbonates weathering reduces the weathering of silicate minerals by consuming protons, and Si is strongly sorbed by secondary minerals in alkaline soils. Plant-available Si increased in intermediate-age soils during the formation of secondary minerals (kaolinite), and finally decreased in old, quartz-rich soils, due to continuous desilication. As pedogenic Si pools became depleted with increasing soil age, Si availability was increasingly determined by soil phytoliths. At Jurien Bay, foliar Si increased continuously as soils aged, in contrast with foliar macronutrients that declined markedly in strongly weathered soils. Finally, foliar phenol concentrations declined with increasing soil age and were negatively correlated with foliar Si at the community and individual species level, suggesting a tradeoff between these two leaf defense strategies. Our results highlight a nonlinear response of plant-available Si to long-term pedogenesis, with an increase during carbonate loss and a decrease in the silicates weathering domain. They also demonstrate that the retention of Si by plants during ecosystem retrogression sustains its terrestrial cycling by leveraging the high reactivity of soil phytoliths compared with soil-derived aluminosilicates. Moreover, the continuous increase of plant Si concentrations as rock-derived nutrients are depleted suggests important plant benefits associated with Si in P-impoverished environments. This is in line with the resource availability hypothesis, which predicts that plants adapted to infertile soils have high levels of anti-herbivore leaf defenses. In particular, old and P-depleted soils increased the relative expression of Si-based defenses, while young soils where plant productivity is limited by N promoted leaf phenol accumulation. Overall, our results demonstrate that long-term ecosystem and soil development strongly influence soil-plant Si dynamics, with cascading effects on plant ecology and global Si and C biogeochemistry.</p>
