Facilitative and competitive interactions between mycorrhizal and nonmycorrhizal plants in an extremely phosphorus-impoverished environment: role of ectomycorrhizal fungi and native oomycete pathogens in shaping species coexistence.

Nonmycorrhizal cluster root-forming species enhance the phosphorus (P) acquisition of mycorrhizal neighbours in P-impoverished megadiverse systems. However, whether mycorrhizal plants facilitate the defence of nonmycorrhizal plants against soil-borne pathogens, in return and via their symbiosis, remains unknown. We characterised growth and defence-related compounds in Banksia menziesii (nonmycorrhizal) and Eucalyptus todtiana (ectomycorrhizal, ECM) seedlings grown either in monoculture or mixture in a multifactorial glasshouse experiment involving ECM fungi and native oomycete pathogens. Roots of B. menziesii had higher levels of phytohormones (salicylic and jasmonic acids, jasmonoyl-isoleucine and 12-oxo-phytodienoic acid) than E. todtiana which further activated a salicylic acid-mediated defence response in roots of B. menziesii, but only in the presence of ECM fungi. We also found that B. menziesii induced a shift in the defence strategy of E. todtiana, from defence-related secondary metabolites (phenolic and flavonoid) towards induced phytohormone response pathways. We conclude that ECM fungi play a vital role in the interactions between mycorrhizal and nonmycorrhizal plants in a severely P-impoverished environment, by introducing a competitive component within the facilitation interaction between the two plant species with contrasting nutrient-acquisition strategies. This study sheds light on the interplay between beneficial and detrimental soil microbes that shape plant-plant interaction in severely nutrient-impoverished ecosystems.

Life at the conservative end of the leaf economics spectrum: intergeneric variation in the allocation of phosphorus to biochemical fractions in species of Banksia (Proteaceae) and Hakea (Proteaceae).

In severely phosphorus (P)-impoverished environments, plants have evolved to use P very efficiently. Yet, it is unclear how P allocation in leaves contributes to their photosynthetic P-use efficiency (PPUE) and position along the leaf economics spectrum (LES). We address this question in 10 species of Banksia and Hakea, two highly P-efficient Proteaceae genera. We characterised traits in leaves of Banksia and Hakea associated with the LES: leaf mass per area, light-saturated photosynthetic rates, P and nitrogen concentrations, and PPUE. We also determined leaf P partitioning to five biochemical fractions (lipid, nucleic acid, metabolite, inorganic and residual P) and their possible association with the LES. For both genera, PPUE was negatively correlated with fractional allocation of P to lipids, but positively correlated with that to metabolites. For Banksia only, PPUE was negatively correlated with residual P, highlighting a strategy contrasting to that of Hakea. Phosphorus-allocation patterns significantly explained PPUE but were not linked to the resource acquisition vs resource conservation gradient defined by the LES. We conclude that distinct P-allocation patterns enable species from different genera to achieve high PPUE and discuss the implications of different P investments. We surmise that different LES axes representing different ecological strategies coexist in extremely P-impoverished environments.

Growing in phosphorus-impoverished habitats in south-western Australia: How general are phosphorus-acquisition and -allocation strategies among Proteaceae, Fabaceae and Myrtaceae species?

Numerous phosphorus (P)-acquisition and -utilisation strategies have evolved in plants growing in severely P-impoverished environments. Although these strategies have been well characterised for certain taxa, like Proteaceae, P-poor habitats are characterised by a high biodiversity, and we know little about how species in other families cope with P scarcity. We compared the P-acquisition and leaf P-allocation strategies of Fabaceae and Myrtaceae with those of Proteaceae growing in the same severely P-impoverished habitat. Myrtaceae and Fabaceae exhibited multiple P-acquisition strategies: P-mining by carboxylates or phosphatases, P uptake facilitated by carboxylate-releasing neighbours, and dependence on the elevated soil P availability after fire. Surprisingly, not all species showed high photosynthetic P-use efficiency (PPUE). Highly P-efficient species showed positive correlations between PPUE and the proportion of metabolite P (enzyme substrates), and negative correlations between PPUE and phospholipids (cellular membranes) and nucleic acid P (mostly ribosomal RNA), while we found no correlations in less P-efficient species. Overall, we found that Myrtaceae and Fabaceae used a wider range of strategies than Proteaceae to cope with P scarcity, at both the rhizosphere and leaf level. This knowledge is pivotal to better understand the mechanisms underlying plant survival in severely nutrient-impoverished biodiverse ecosystems.

Growth-defence trade-off in rice: fast-growing and acquisitive genotypes have lower expression of genes involved in immunity.

Plant ecologists and molecular biologists have long considered the hypothesis of a trade-off between plant growth and defence separately. In particular, how genes thought to control the growth-defence trade-off at the molecular level relate to trait-based frameworks in functional ecology, such as the slow-fast plant economics spectrum, is unknown. We grew 49 phenotypically diverse rice genotypes in pots under optimal conditions and measured growth-related functional traits and the constitutive expression of 11 genes involved in plant defence. We also quantified the concentration of silicon (Si) in leaves to estimate silica-based defences. Rice genotypes were aligned along a slow-fast continuum, with slow-growing, late-flowering genotypes versus fast-growing, early-flowering genotypes. Leaf dry matter content and leaf Si concentrations were not aligned with this axis and negatively correlated with each other. Live-fast genotypes exhibited greater expression of OsNPR1, a regulator of the salicylic acid pathway that promotes plant defence while suppressing plant growth. These genotypes also exhibited greater expression of SPL7 and GH3.2, which are also involved in both stress resistance and growth. Our results do not support the hypothesis of a growth-defence trade-off when leaf Si and leaf dry matter content are considered, but they do when hormonal pathway genes are considered. We demonstrate the benefits of combining ecological and molecular approaches to elucidate the growth-defence trade-off, opening new avenues for plant breeding and crop science.

A shift from phenol to silica-based leaf defences during long-term soil and ecosystem development.

The resource availability hypothesis predicts that plants adapted to infertile soils have high levels of anti-herbivore leaf defences. This hypothesis has been mostly explored for secondary metabolites such as phenolics, whereas it remains underexplored for silica-based defences. We determined leaf concentrations of total phenols and silicon (Si) in plants growing along the 2-million-year Jurien Bay chronosequence, exhibiting an extreme gradient of soil fertility. We found that nitrogen (N) limitation on young soils led to a greater expression of phenol-based defences, whereas old, phosphorus (P)-impoverished soils favoured silica-based defences. Both defence types were negatively correlated at the community and individual species level. Our results suggest a trade-off among these two leaf defence strategies based on the strength and type of nutrient limitation, thereby opening up new perspectives for the resource availability hypothesis and plant defence research. This study also highlights the importance of silica-based defences under low P supply.

Comparative analysis of borate fusion versus sodium carbonate extraction for quantification of silicon contents in plants.

Studies of plant-silicon (Si) interaction benefit from safe, affordable and accurate methods to measure acid-insoluble silica (phytoliths) for a large number of plant samples. This study aimed to evaluate the comparability between two chemical methods to dissolve leaf silica, borate fusion and 1% sodium carbonate (Na2CO3) extraction, in combination of two detection methods (ICP, molybdenum-blue colorimetry).We compared the results obtained by these methods, using dried leaf samples of five tropical tree species that differ widely in Si concentrations (4 to 100 mg g DW-1). Leaf Si concentration values determined after the two extraction methods were highly correlated (y = 0.79x, R2 = 0.998). However, compared to the extraction with borate fusion, the 1% Na2CO3 method resulted in lower Si concentration per unit dry mass by 16% to 32% (mean of 24.2%). We also found that molybdenum-blue colorimetry method may interfere with certain extraction methods. A simple equation can be used to correct for systematic underestimation of Si contents determined after extraction with 1% Na2CO3, which is the least expensive and safest among commonly used methods for extraction of Si from land plants.

Why do plants silicify?

Despite seminal papers that stress the significance of silicon (Si) in plant biology and ecology, most studies focus on manipulations of Si supply and mitigation of stresses. The ecological significance of Si varies with different levels of biological organization, and remains hard to capture. We show that the costs of Si accumulation are greater than is currently acknowledged, and discuss potential links between Si and fitness components (growth, survival, reproduction), environment, and ecosystem functioning. We suggest that Si is more important in trait-based ecology than is currently recognized. Si potentially plays a significant role in many aspects of plant ecology, but knowledge gaps prevent us from understanding its possible contribution to the success of some clades and the expansion of specific biomes.

Nitrogen availability and plant-plant interactions drive leaf silicon concentration in wheat genotypes.

Estimating plasticity of leaf silicon (Si) in response to abiotic and biotic factors underpins our comprehension of plant defences and stress resistance in natural and agroecosystems. However, how nitrogen (N) addition and intraspecific plant-plant interactions affect Si concentration remains unclear.We grew 19 durum wheat genotypes (Triticum turgidum ssp. durum) in pots, either alone or in intra- or intergenotypic cultures of two individuals, and with or without N. Above-ground biomass, plant height and leaf [Si] were quantified at the beginning of the flowering stage.Nitrogen addition decreased leaf [Si] for most genotypes, proportionally to the biomass increase. Si plasticity to plant-plant interactions varied significantly among genotypes, with both increases and decreases in leaf [Si] when mixed with a neighbour, regardless of the mixture type (intra-/intergenotype). Besides, increased leaf [Si] in response to plant-plant interactions was associated with increased plant height.Our results suggest the occurrence of both facilitation and competition for Si uptake from the rhizosphere in wheat mixtures. Future research should identify which leaf and root traits characterise facilitating neighbours for Si acquisition. We also show that Si could be involved in height gain in response to intraspecific competition, possibly for increasing light capture. This important finding opens up new research directions on Si and plant-plant interactions in both natural ecosystems and agroecosystems. More generally, our results stress the need to explore leaf Si plasticity in responses to both abiotic and biotic factors to understand plant stress resistance. Read the free Plain Language Summary for this article on the Journal blog.

Silicon mobilisation by root-released carboxylates.

Plants have evolved numerous strategies to acquire poorly available nutrients from soil, including the release of carboxylates from their roots. Silicon (Si) release from mineral dissolution increases in the presence of chelating substances, and recent evidence shows that leaf [Si] increases markedly in old phosphorus (P)-depleted soils, where many species exhibit carboxylate-releasing strategies, compared with younger P-richer soils. Here, we propose that root-released carboxylates, and more generally rhizosphere processes, play an overlooked role in plant Si accumulation by increasing soil Si mobilisation from minerals. We suggest that Si mobilisation is costly in terms of carbon but becomes cheaper if those costs are already met to acquire poorly available P. Uptake of the mobilised Si by roots will then depend on whether they express Si transporters.