François P. Teste

Proteaceae from severely phosphorus‐impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus‐use‐efficiency

Proteaceae species in south-western Australia occur on severely phosphorus (P)-impoverished soils. They have very low leaf P concentrations, but relatively fast rates of photosynthesis, thus exhibiting extremely high photosynthetic phosphorus-use-efficiency (PPUE). Although the mechanisms underpinning their high PPUE remain unknown, one possibility is that these species may be able to replace phospholipids with nonphospholipids during leaf development, without compromising photosynthesis. For six Proteaceae species, we measured soil and leaf P concentrations and rates of photosynthesis of both young expanding and mature leaves. We also assessed the investment in galactolipids, sulfolipids and phospholipids in young and mature leaves, and compared these results with those on Arabidopsis thaliana, grown under both P-sufficient and P-deficient conditions. In all Proteaceae species, phospholipid levels strongly decreased during leaf development, whereas those of galactolipids and sulfolipids strongly increased. Photosynthetic rates increased from young to mature leaves. This shows that these species extensively replace phospholipids with nonphospholipids during leaf development, without compromising photosynthesis. A considerably less pronounced shift was observed in A. thaliana. Our results clearly show that a low investment in phospholipids, relative to nonphospholipids, offers a partial explanation for a high photosynthetic rate per unit leaf P in Proteaceae adapted to P-impoverished soils.

Plant-soil feedback and the maintenance of diversity in Mediterranean-climate shrublands.

Soil biota and plant diversity Soil biota, including symbionts such as mycorrhizal fungi and nitrogen-fixing bacteria, as well as fungal and bacterial pathogens, affect terrestrial plant diversity and growth patterns (see the Perspective by van der Putten). Teste et al. monitored growth and survival in Australian shrubland plant species paired with soil biota from plants of the same species and from other plants that use different nutrient acquisition strategies. Plant-soil feedbacks appear to drive local plant diversity through interactions between the different types of plants and their associated soil biota. Bennett et al. studied plant-soil feedbacks in soil and seeds from 550 populations of 55 species of North American trees. Feedbacks ranged from positive to negative, depending on the type of mycorrhizal association, and were related to how densely the same species occurred in natural populations. Science, this issue p. 134, p. 173; see also p. 181 Feedback between plants and soil biota influences diversity in Australian shrublands. Soil biota influence plant performance through plant-soil feedback, but it is unclear whether the strength of such feedback depends on plant traits and whether plant-soil feedback drives local plant diversity. We grew 16 co-occurring plant species with contrasting nutrient-acquisition strategies from hyperdiverse Australian shrublands and exposed them to soil biota from under their own or other plant species. Plant responses to soil biota varied according to their nutrient-acquisition strategy, including positive feedback for ectomycorrhizal plants and negative feedback for nitrogen-fixing and nonmycorrhizal plants. Simulations revealed that such strategy-dependent feedback is sufficient to maintain the high taxonomic and functional diversity characterizing these Mediterranean-climate shrublands. Our study identifies nutrient-acquisition strategy as a key trait explaining how different plant responses to soil biota promote local plant diversity.

Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species

Abstract Proteaceae species in south-western Australia occur on phosphorus- (P) impoverished soils. Their leaves contain very low P levels, but have relatively high rates of photosynthesis. We measured ribosomal RNA (rRNA) abundance, soluble protein, activities of several enzymes and glucose 6-phosphate (Glc6P) levels in expanding and mature leaves of six Proteaceae species in their natural habitat. The results were compared with those for Arabidopsis thaliana. Compared with A. thaliana, immature leaves of Proteaceae species contained very low levels of rRNA, especially plastidic rRNA. Proteaceae species showed slow development of the photosynthetic apparatus (‘delayed greening’), with young leaves having very low levels of chlorophyll and Calvin–Benson cycle enzymes. In mature leaves, soluble protein and Calvin–Benson cycle enzyme activities were low, but Glc6P levels were similar to those in A. thaliana. We propose that low ribosome abundance contributes to the high P efficiency of these Proteaceae species in three ways: (1) less P is invested in ribosomes; (2) the rate of growth and, hence, demand for P is low; and (3) the especially low plastidic ribosome abundance in young leaves delays formation of the photosynthetic machinery, spreading investment of P in rRNA. Although Calvin–Benson cycle enzyme activities are low, Glc6P levels are maintained, allowing their effective use.

Phosphorus nutrition of phosphorus-sensitive Australian native plants: threats to plant communities in a global biodiversity hotspot

South-western Australia harbours a biodiversity hotspot on severely phosphorus-impoverished soils. Threats include eutrophication due to phosphorus enrichment, due to increased fire frequency and spraying with phosphite to reduce the impacts of the introduced pathogen Phytophthora cinnamomi. We propose a strategy to work towards alternatives to phosphite for pathogen management.

Interactions between arbuscular mycorrhizal and non‐mycorrhizal plants: do non‐mycorrhizal species at both extremes of nutrient availability play the same game?

The vast majority of vascular plants are capable of forming an arbuscular mycorrhizal symbiosis, and only 18% cannot (Brundrett 2009). It is widely accepted that all ancestors of vascular plant species were arbuscular mycorrhizal (Pirozynski & Malloch 1975; Wang et al. 2010). Nonmycorrhizal species presumably lost or suppressed their ability to establish an arbuscular mycorrhizal symbiosis because its benefits did not outweigh its costs, but the mechanism explaining a high cost to benefit relationship may have been very different in distant plant lineages, as explored below. Non-mycorrhizal plant families include, broadly speaking, two groups, occupying strongly contrasting habitats (Fig. 1). One group comprises those that typically occur in disturbed habitats, where competition with other plants is low and soil phosphorus (P) availability is high; for example, Amaranthaceae, Brassicaceae, Caryophyllaceae, Chenopodiaceae, Polygonaceae and Urticaceae (Harley & Harley 1987; Tester, Smith & Smith 1987; Francis & Read 1994; Olsson & Tyler 2004). We refer to this group as the Brassicaceae type; these species lack specialized roots to access poorly available P (Figs 1 & 2). The benefits of a mycorrhizal habit in the nutrient-rich habitat of these species are presumably very low, thus providing a selective force against mycorrhization. The other group comprises families that dominate on soil where the P availability is very low; these species have a range of root specializations that allow them to mine soil P, for example, proteoid or cluster roots (Watt & Evans 1999; Shane & Lambers 2005), dauciform roots (Playsted et al. 2006; Shane et al. 2006) and possibly others, for example, capillaroid and sand-binding roots that have not received as much attention (Lambers et al. 2006, 2013a). These nonmycorrhizal families with (putative) specialized P-mining roots include Cyperaceae, Haemodoraceae, Proteaceae and Restionaceae (Newman & Reddell 1987; Tester et al. 1987; Brundrett & Abbott 1991). We refer to this group as the Proteaceae type (Figs 1 & 2). The benefits of a P-scavenging arbuscular mycorrhizal habit in the nutrient-impoverished habitat of these species are presumably much less than those of the P-mining strategy, thus providing a selective force against mycorrhization. As with most broad generalizations in biology, there are exceptions, and mycorrhizal species do occur in typical non-mycorrhizal families (Boulet & Lambers 2005; Lagrange et al. 2011). Similarly, non-mycorrhizal species, for example, Daviesia and Kennedia (Fabaceae; Brundrett & Abbott 1991) or even genera, for example, Lupinus (Fabaceae), occur in typical mycorrhizal families (Lambers, Clements & Nelson 2013b). Notwithstanding these exceptions, the broad groups of non-mycorrhizal species represent an ecologically meaningful division; they show that non-mycorrhizal species are found at both ends of a spectrum of soil fertility (Fig. 1).

Complementary plant nutrient‐acquisition strategies promote growth of neighbour species

Summary1. Greater understanding of positive interspecific interactions in nutrient-poor soils is a prior-ity, particularly in phosphorus (P)-limited ecosystems where plants with contrasting nutrient-acquiring strategies co-occur. It is also relevant to agro-ecosystems, since global P stocks arebeing depleted. In this study, we assess positive interactions between sympatric plants withcontrasting nutrient-acquiring strategies from highly P-impoverished soils from the biodiversityhotspot of south-western Australia.2. Four plant species (Banksia menziesii, Eucalyptus marginata, Verticordia nitens and Melaleucapreissiana) that are non-mycorrhizal (cluster-rooted), ectomycorrhizal (EM), arbuscular (AM) ordual AM/EM, respectively, were grown together in a specially designed ‘common garden’ micro-cosm with nutrient-poor or fertilized soil, with or without root intermingling and fungal hyphaecontact. We measured growth, mycorrhizal colonization, root intermingling and nutrient uptaketo determine positive or negative growth patterns amongst the various plant assemblies.3. Growth of the AM/EM host was best when interacting with both the EM host and a non-mycorrhizal nutrient-mining plant with cluster roots (Banksia) in microcosms where root inter-mingling was not possible. Growth promotion was only seen in pots with nutrient-poor soils,where the better growth of Melaleuca coincided with higher shoot P, manganese, calcium, ironand boron content, whereas an increase in soil nutrient status through fertilizer additionresulted in a decrease in nutrient-sharing between co-occurring species. Furthermore, the dualAM/EM Melaleuca exhibited enhanced EM colonization and favoured EM over AM fungiwhen grown beside Eucalyptus and Banksia. We surmise that mycorrhizal networks wereinstrumental in the variation in both mycorrhizal type and colonization levels.4. We conclude that complementarity of plant nutrient-acquisition strategies can promotegrowth of neighbour species. The results show a synergistic effect between EM hyphal scaveng-ing and mobilization of limiting nutrients by cluster roots. The positive and negative interac-tions enable coexistence to go far beyond the traditional view that plants interact mainlythrough resource depletion. This study improves our understanding of how root interactionscould shape plant communities and promote species diversity and packing in nutrient-impover-ished habitats.Key-words: biodiversity hotspot, cluster roots, manganese, microcosm, mycorrhizal networks,nutrient-poor soils, phosphorus, Proteaceae, root competitionIntroduction

Soil properties influencing compactability of forest soils in British Columbia

The widespread use of heavy machinery during harvesting and site preparation in timber plantations in British Columbia (BC) has led to concerns that compaction causes a reduction in long-term soil productivity. Impacts of properties such as total C, water content, and texture on compactability of forest soils in BC were assessed. Two compactability indices were used: maximum bulk density (MBD) and susceptibility to compaction (SC) determined by the standard Proctor test. Soil samples were collected from 16 sites throughout BC covering a wide range of biogeoclimatic zones. Soils varied in texture (12 to 87% sand, 9 to 76% silt, and 2 to 53% clay) and organic matter content (18 to 76 g kg-1 total C). A strong negative correlation was observed between MBD and gravimetric water content at which MBD was achieved (WMBD) and between MBD and total C. Similarly, WMBD and total C had strong effects on SC. The estimation of either MBD or SC values was not substantially improved by including texture parameters to the...

Seed release in serotinous lodgepole pine forests after mountain pine beetle outbreak

There are concerns that large-scale stand mortality due to mountain pine beetle (MPB) could greatly reduce natural regeneration of serotinous Rocky Mountain (RM) lodgepole pine (Pinus contorta var. latifolia) because the closed cones are held in place without the fire cue for cone opening. We selected 20 stands (five stands each of live [control], 3 years since MPB [3-yr-MPB], 6 years since MPB [6-yr-MPB], and 9 years since MPB [9-yr-MPB] mortality) in north central British Columbia, Canada. The goal was to determine partial loss of serotiny due to fall of crown-stored cones via breakage of branches and in situ opening of canopy cones throughout the 2008 and 2009 growing seasons. We also quantified seed release by the opening of forest-floor cones, loss of seed from rodent predation, and cone burial. Trees killed by MPB three years earlier dropped approximately 3.5 times more cones via branch breakage compared to live stands. After six years, MPB-killed stands had released 45% of their canopy seed bank through cone opening, cone fall due to breakage, and squirrel predation. Further losses of canopy seed banks are expected with time since we found 9-yr-MPB stands had 38% more open canopy cones. This was countered by the development of a modest forest-floor seed bank (6% of the original canopy seed bank) from burial of cones; this seed bank may be ecologically important if a fire or anthropogenic disturbance reexposes these cones. If adequate levels of regeneration are to occur, disturbances to create seedbeds must occur shortly after tree mortality, before the seed banks are lost. Our findings also suggest that the sustained seed rain (over at least nine years) after MPB outbreak may be beneficial for population growth of ground-foraging vertebrates. Our study adds insight to the seed ecology of serotinous pines under a potentially continental-wide insect outbreak, threatening vast forests adapted to regeneration after fire. Key words: biotic disturbance; cone burial; cone opening; Dendroctonus ponderosae; ground-foraging vertebrates; mountain pine beetle; natural regeneration; Pinus contorta var. latifolia; Rocky Mountain lodgepole pine; seed banks; serotiny (canopy seed storage); Tamiasciurus hudsonicus.

The rise and fall of arbuscular mycorrhizal fungal diversity during ecosystem retrogression

Ecosystem retrogression following long‐term pedogenesis is attributed to phosphorus (P) limitation of primary productivity. Arbuscular mycorrhizal fungi (AMF) enhance P acquisition for most terrestrial plants, but it has been suggested that this strategy becomes less effective in strongly weathered soils with extremely low P availability. Using next generation sequencing of the large subunit ribosomal RNA gene in roots and soil, we compared the composition and diversity of AMF communities in three contrasting stages of a retrogressive >2‐million‐year dune chronosequence in a global biodiversity hotspot. This chronosequence shows a ~60‐fold decline in total soil P concentration, with the oldest stage representing some of the most severely P‐impoverished soils found in any terrestrial ecosystem. The richness of AMF operational taxonomic units was low on young (1000s of years), moderately P‐rich soils, greatest on relatively old (~120 000 years) low‐P soils, and low again on the oldest (>2 000 000 years) soils that were lowest in P availability. A similar decline in AMF phylogenetic diversity on the oldest soils occurred, despite invariant host plant diversity and only small declines in host cover along the chronosequence. Differences in AMF community composition were greatest between the youngest and the two oldest soils, and this was best explained by differences in soil P concentrations. Our results point to a threshold in soil P availability during ecosystem regression below which AMF diversity declines, suggesting environmental filtering of AMF insufficiently adapted to extremely low P availability.

Peeking into the black box: a trait‐based approach to predicting plant–soil feedback

Feedbacks between plants and soil communities may be elusive, yet they have far-reaching consequences for plant physiology, competition and community structure. Plant–soil feedbacks (PSFs) are plant-mediated changes to soil properties that ultimately influence the performance of the same or other plants (Van der Putten et al., 2013). These PSFs may be mediated by root-associated organisms (hereafter, root-mediated feedbacks) or saprotrophic organisms and associated litter characteristics (hereafter, litter-mediated feedbacks). However, we know little about the potential mechanistic linkages and relative strengths between these distinct, but connected, processes as root- and litter-mediated feedbacks have generally been studied independently from each other. This is despite the fact that root-associated organisms and saprotrophs can interact through various mechanisms, either directly or as mediated by the plant (e.g. Wardle, 2006). By using a trait-based approach,Ke et al. (in this issue of New Phytologist, pp. 329–341) make an important contribution by integrating root- and litter-mediated PSFs in a nitrogen (N)-based, stage-structured plant population and microbial community model. Their approach allows us to start peeking into the ‘black box’ thereby promoting a better understanding of how PSFs operate interactively. Ke et al. considered various plant traits (e.g. decomposability), but also incorporated trait variation in the physiology, demography and composition of the soil microbial community, and tested their separate and interactive effects on PSF strength in a comprehensive simulation framework. Finally, they used empirical evidence from the literature to support their model predictions.