Patrick Enrico Hayes

The degree of plant silicification is classically proxied by organ-scale silicon concentration, [Si], which ignores where Si is allocated at the cellular scale. Bridging this scale gap is crucial to elucidate the physiological and ecological roles of silicification in high-Si taxa and its influence on biogeochemical cycles. We used high-resolution X-ray microtomography and cellular-scale element mapping to study silica allocation and silicification patterns in 15 species from the second most-abundant Si-accumulating family worldwide, namely Cyperaceae (sedges). Despite considerable variation in deposition sites and cellular [Si] between species and anatomical areas, we show that at least 78±17% of silica is localized in the epidermis, mostly as a silica layer in the outer tangential cell wall (OTW). Both the thickness and cellular-scale [Si] of this continuous layer, which is up to 18 µm thick, were highly correlated to organ-scale [Si] among species. Our findings demonstrate that bulk silica content is largely governed by deposition in the OTW in sedges, rather than by deposition in cell lumina. These findings open new perspectives for Si-related plant physiological and biogeochemical processes and pave the way for the use of X-ray microtomography not only to visualize, but also to quantify biogenic silica allocation in plants.

In recent years, the detection of numerous negative correlations between silicon (Si) and carbon (C)‐based compounds in plants has suggested trade‐offs between different stress resistance and/or mechanical support strategies. However, nearly all studies have involved whole‐leaf analysis, and it is unclear how the trade‐off operates mechanistically, at the cellular level. Here we combined leaf trait measurements and microscopic analyses (electron microscopy with elemental X‐ray mapping and X‐ray microtomography) of 17 species from a high‐Si family: Cyperaceae. Accumulation of Si was strongly negatively correlated with C‐based compounds, particularly tannins. Our microscopical investigations showed that the accumulation of phenolics and deposition of silica were mutually exclusive in the outer epidermal cell walls. This trade‐off was independent of that between the construction of tough, sclerenchyma‐rich leaves and growth potential (the leaf economics spectrum). We also identified a strong negative correlation between Si and accumulation of epicuticular waxes. Previous whole leaf analyses were, in effect, hiding the locations of the trade‐off between Si and C‐based compounds in plants. The epidermal location of this trade‐off and the specific involvement of tannins and waxes suggest the existence of different strategies to resist environmental stresses. Our study provides key insights into plant Si utilization and highlights the multidimensionality of plant stress resistance strategies.

Summary: 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.

Summary: 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.

Background and aims: Proteaceae are a prominent plant family in south-western Australia. Most Proteaceae are ‘calcifuge’, occurring exclusively on old phosphorus (P)-impoverished acidic soils, with a few ‘soil-indifferent’ species also found on young P-richer calcareous soils. Calcium (Ca)-enhanced P toxicity explains the calcifuge habit of Proteaceae. However, previous research has so far been focused exclusively on the roles of Ca and P in determining Proteaceae distribution, and consequently there is little knowledge on how other soil-based strategies influence this distribution. We aimed to study the effects of young calcareous soils on four soil-grown Proteaceae and assess differences between calcifuge and soil-indifferent Proteaceae to better understand their natural distribution. Methods: Two calcifuge and two soil-indifferent Proteaceae from south-western Australia were grown in six contrasting soils, including young calcareous, and old acidic soils. Results: When grown in calcareous soils all species showed root growth inhibition, micronutrient deficiency, Ca-enhanced P toxicity, and negative impacts on physiology. Calcifuge species were more sensitive to calcareous soils than soil-indifferent ones, although this varied between genera. Soil-indifferent species tended to produce more cluster roots, release more carboxylates per root mass, and allocate less Ca to their leaves, compared with calcifuges; they also had smaller seeds and were less sensitive to Ca-enhanced P toxicity. Conclusion: We surmise that a combination of these traits allows soil-indifferent species to tolerate calcareous soils. This study provides insight into how Proteaceae respond to young calcareous soils and how this influences their distribution.

Although significant intraspecific variation in photosynthetic phosphorus (P)-use efficiency (PPUE) has been shown in numerous species, we still know little about the biochemical basis for differences in PPUE among genotypes within a species. Here, we grew two high-PPUE and two low-PPUE chickpea (Cicer arietinum) genotypes with low P supply in a glasshouse to compare their photosynthesis-related traits, total foliar P concentration ([P]) and chemical P fractions (i.e. inorganic P (Pi), metabolite P, lipid P, nucleic acid P and residual P). Foliar cell-specific nutrient concentrations including P were characterized using elemental X-ray microanalysis. Genotypes with high PPUE showed lower total foliar [P] without slower photosynthetic rates. No consistent differences in cellular [P] between the epidermis and mesophyll cells occurred across the four genotypes. In contrast, high PPUE was associated with lower allocation to Pi and metabolite P, with PPUE being negatively correlated with the percentage of these two fractions. Furthermore, a lower allocation to Pi and metabolite P was correlated with a greater allocation to nucleic acid P, but not to lipid P. Collectively, our results suggest that a different allocation to foliar P fractions, rather than preferential P allocation to specific leaf tissues underlies the contrasting PPUE among chickpea genotypes.

Phosphorus (P) availability is often limiting for rice (Oryza sativa) production. Improving internal P-use efficiency (PUE) is crucial to sustainable food production, particularly in low-input systems. A critical aspect of PUE in plants, and one that remains poorly understood, is the investment of leaf P in different chemical P fractions (nucleic acid-P, lipid-P, inorganic-P, metabolite-P and residual-P). The overarching objective of this study was to understand how these key P fractions influence PUE. Three high-PUE and two low-PUE rice genotypes were grown in hydroponics with contrasting P supplies. We measured PUE, total P, P fractions, photosynthesis and biomass. Low investment in lipid-P was strongly associated with increased photosynthetic PUE (PPUE), achieved by reducing total leaf P concentration while maintaining rapid photosynthetic rates. All low-P plants exhibited a low investment in inorganic-P and lipid-P, but not nucleic acid-P. In addition, whole-plant PUE was strongly associated with reduced total P concentration, increased biomass and increased preferential allocation of resources to the youngest mature leaves. Lipid remodelling has been shown in rice before, but we show for the first time that reduced lipid-P investment improves PUE in rice without reducing photosynthesis. This presents a novel pathway for increasing PUE by targeting varieties with reduced lipid-P investment. This will benefit rice production in low-P soils and in areas where fertilizer use is limited, improving global food security by reducing P fertilizer demands and food production costs.

We introduce the AusTraits database - a compilation of values of plant traits for taxa in the Australian flora (hereafter AusTraits). AusTraits synthesises data on 448 traits across 28,640 taxa from field campaigns, published literature, taxonomic monographs, and individual taxon descriptions. Traits vary in scope from physiological measures of performance (e.g. photosynthetic gas exchange, water-use efficiency) to morphological attributes (e.g. leaf area, seed mass, plant height) which link to aspects of ecological variation. AusTraits contains curated and harmonised individual- and species-level measurements coupled to, where available, contextual information on site properties and experimental conditions. This article provides information on version 3.0.2 of AusTraits which contains data for 997,808 trait-by-taxon combinations. We envision AusTraits as an ongoing collaborative initiative for easily archiving and sharing trait data, which also provides a template for other national or regional initiatives globally to fill persistent gaps in trait knowledge.

The calcifuge habit of plants is commonly explained in terms of high soil pH and its effects on nutrient availability, particularly that of phosphorus (P). However, most Proteaceae that occur on nutrient‐impoverished soils in south‐western Australia are calcifuge, despite their ability to produce cluster‐roots, which effectively mobilize soil P and micronutrients. We hypothesize that the mechanism explaining the calcifuge habit in Proteaceae is their sensitivity to P and calcium (Ca), and that soil‐indifferent species are less sensitive to the interaction of these nutrients. In this study, we analyzed growth, gas‐exchange rate, and chlorophyll fluorescence of two soil‐indifferent and four calcifuge Hakea and Banksia (Proteaceae) species from south‐western Australia, across a range of P and Ca concentrations in hydroponic solution. We observed Ca‐enhanced P toxicity in all analyzed species, but to different extents depending on distribution type and genus. Increasing P supply enhanced plant growth, leaf biomass, and photosynthetic rates of soil‐indifferent species in a pattern largely independent of Ca supply. In contrast, positive physiological responses to increasing [P] in calcifuges were either absent or limited to low Ca supply, indicating that calcifuges were far more sensitive to Ca‐enhanced P toxicity. In calcifuge Hakeas, we attributed this to higher leaf [P], and in calcifuge Banksias to lower leaf zinc concentration. These differences help to explain these species' contrasting sensitivity to Ca‐enhanced P toxicity and account for the exclusion of most Proteaceae from calcareous habitats. We surmise that Ca‐enhanced P toxicity is a major factor explaining the calcifuge habit of Proteaceae, and, possibly, other P‐sensitive plants.

We introduce the AusTraits database - a compilation of measurements of plant traits for taxa in the Australian flora (hereafter AusTraits). AusTraits synthesises data on 375 traits across 29230 taxa from field campaigns, published literature, taxonomic monographs, and individual taxa descriptions. Traits vary in scope from physiological measures of performance (e.g. photosynthetic gas exchange, water-use efficiency) to morphological parameters (e.g. leaf area, seed mass, plant height) which link to aspects of ecological variation. AusTraits contains curated and harmonised individual-, species- and genus-level observations coupled to, where available, contextual information on site properties. This data descriptor provides information on version 2.1.0 of AusTraits which contains data for 937243 trait-by-taxa combinations. We envision AusTraits as an ongoing collaborative initiative for easily archiving and sharing trait data to increase our collective understanding of the Australian flora.