Silicon enrichment alters functional traits in legumes depending on plant genotype and symbiosis with nitrogen‐fixing bacteria

Abstract

Silicon (Si) uptake and deposition (silicification) in tissues is known to alleviate stresses and generally improve plant health. This is mostly studied in Si‐high accumulators, such as grasses, with comparatively less known about its effects on other plant functional groups, such as legumes. There is speculation that Si may positively impact the symbiosis between legumes and the nitrogen‐fixing bacteria (rhizobia) they associate with, but this is poorly understood. This study examined the effects of Si enrichment on legume species associated with rhizobia and the potential underlying mechanism of Si impacts. We conducted a glasshouse experiment with lucerne Medicago sativa and barrel medic M. truncatula associated with a model rhizobial strain. Six genotypes (three per species) were either supplemented with Si (+Si) or untreated (−Si). We quantified 16 functional traits which could be classified as plant growth, physiology, elemental chemistry, nodule activity and nitrogen fixation. The two legume species responded to Si distinctively. For example, Si supplementation increased shoot biomass by more than 10% in lucerne but growth was unaffected in barrel medic. Conversely, nitrogen‐fixing enzyme (nitrogenase) activity was promoted by more than 85% in +Si barrel medic plants but not in lucerne. Moreover, Si supplementation of lucerne increased the concentrations of Si in leaves by more than 36% but not in root nodules. Increased foliar concentrations of Si in lucerne were positively associated with increased shoot and root biomass in Sequel and Trifecta genotypes, respectively. Conversely, Si supplementation of barrel medic increased the concentration of Si in root nodules by 29% but not that in foliar tissues. Nitrogenase activity and where silicification occurred, differed between genotypes in barrel medic; nitrogenase activity was correlated with concentrations of Si in root nodules rather than that in foliar tissues in one genotype (Sephi) but the reverse was true in another (Hannaford). This study demonstrates that two closely related legume species can respond to Si in distinct ways, depending on plant genotype and symbiosis. These results present the overlooked function of Si in legume–rhizobia interactions, which could potentially enhance productivity of this important group of plants. A free Plain Language Summary can be found within the Supporting Information of this article.

Benefits of silicon-enhanced root nodulation in a model legume are contingent upon rhizobial efficacy

“…Seeds of this genotype were obtained from the Australian Pasture Genebank, Adelaide, Australia. Seeds were surface-sterilised in 70% ethanol (v/v), 40% sodium hypochlorite (v/v) and then washed in a sterile MQ-water following methods from Putra et al (2021) and Terpolilli et al (2008). Afterwards, seeds were singly inoculated either with Ensifer meliloti (previously known as Sinorhizobium meliloti) Sm1021 or E. meliloti Sm1022 strains.…”

“…Both strains were originally provided by the Rhizobium Stock Centre, Murdoch University, Australia and subsequently sub-cultured on yeast mannitol agar (YMA) according to Howieson and Dilworth (2016). Growing conditions and inoculations of rhizobia (OD 595nm = 0.1 or 10 8 CFUs ml −1 ) were similarly adopted from (Putra et al 2021) prior to sowing seeds.…”

“…However, the underlying mechanisms underpinning these benefits remain unclear. It was recently reported that Si supply promoted nitrogenase activity in the model legume M. truncatula, which was positively associated with silicification in either the foliage or the root nodule, depending on host genotype (Putra et al 2021). Furthermore, some studies hypothesised that Si may promote root nodulation by increasing symbiotic chemical signals, such as flavonoids (Nelwamondo and Dakora 1999;Johnson et al 2017).…”

“…A previous study by Putra et al (2021) indicated the significant differences in plant growth and nodule function might be related to the level of symbiotic efficacy of the rhizobial strain depending on the Medicago plant species (M. sativa vs M. truncatula) and their genotypes. Therefore, to examine this hypothesis, we specifically used the model legume M. truncatula genotype A17 in association with either rhizobial strain Sm1021 ('low-efficiency') or Sm1022 ('high-efficiency'), grown under N-limited conditions.…”

“…We measured plant growth, root nodulation and changes in metabolites within nodules (flavonoids) and plant shoots (free amino acids, soluble protein, and elemental C, N and Si) in response to Si supply and rhizobial association. Additionally, we determined if rhizobial efficacy affected the outcomes because the relationship between Si and rhizobia could potentially depend on the efficiency of the strain as discussed in Putra et al (2021). For example, Si might have more beneficial effects in plants with low-efficiency strains because these are more likely to be under (symbiotic) stress.…”