Metabolic Adaptations of the Non‐Mycotrophic Proteaceae to Soils With Low Phosphorus Availability

Lambers, Hans; Clode, Peta L.; Hawkins, Heidi‐Jayne; Laliberté, Étienne; Oliveira, Rafael S.; Reddell, Paul; Shane, Michael W.; Stitt, Mark; Weston, Peter H.

doi:10.1002/9781118958841.ch11

Cited by 44 publications

(43 citation statements)

References 192 publications

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“…Species that are P sensitive show a low capacity to downregulate P uptake, along with a preferential allocation of P to mesophyll cells (Shane et al, 2004a,b;Hawkins et al, 2008;Hayes et al, 2018). This disproportionately increases mesophyll [P], explaining their sensitivity to P, even at relatively low P availability (Shane et al, 2004a,b;Hawkins et al, 2008;Lambers et al, 2015;Hayes et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Calcium‐enhanced phosphorus toxicity in calcifuge and soil‐indifferent Proteaceae along the Jurien Bay chronosequence

et al. 2018

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Summary Many Proteaceae are highly phosphorus (P)‐sensitive and occur exclusively on old nutrient‐impoverished acidic soils (calcifuge), whilst a few also occur on young calcareous soils (soil‐indifferent) that are higher in available calcium (Ca) and P. Calcium increases the severity of P‐toxicity symptoms, but its underlying mechanisms are unknown. We propose that Ca‐enhanced P toxicity explains the calcifuge habit of most Proteaceae. Four calcifuge and four soil‐indifferent Proteaceae from South‐Western Australia were grown in hydroponics, at a range of P and Ca concentrations. Calcium increased the severity of P‐toxicity symptoms in all species. Calcifuge Proteaceae were more sensitive to Ca‐enhanced P toxicity than soil‐indifferent ones. Calcifuges shared these traits: low leaf zinc concentration ([Zn]), low Zn allocation to leaves, low leaf [Zn]:[P], low root : shoot ratio, and high seed P content, compared with soil‐indifferent species. This is the first demonstration of Ca‐enhanced P toxicity across multiple species. Calcium‐enhanced P toxicity provides an explanation for the calcifuge habit of most Proteaceae and is critical for the management of this iconic Australian family. This study represents a major advance towards an understanding of the physiological mechanisms of P toxicity and its role in the distribution of Proteaceae.

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Section: Introductionmentioning

confidence: 99%

Calcium‐enhanced phosphorus toxicity in calcifuge and soil‐indifferent Proteaceae along the Jurien Bay chronosequence

et al. 2018

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“…In contrast to δ 13 C values, δ 15 N of leaf tissue showed a similar relationship for the two species in relation to slope (Figure 7b), despite a substantial (~5‰) offset. In addition to the well-known role that cluster roots play in P acquisition (Lambers, Clode et al, 2015;Lambers, Martinoia et al, 2015), they have been implicated in the modification of N cycling. Organic acids, such as those exuded by cluster roots, are known to increase the solubility of organic-N in the soil (Matsumoto, Ae, & Matsumoto, 2005) Reforestation methods vary between countries and among land managers and are dependent upon the ecological circumstances and stated goals of the reforestation programme (Lamb, Erskine, & Parrotta, 2005).…”

Section: Discussionmentioning

confidence: 99%

“…In stark contrast, F. brayleyana displays the largest range and significant skew in its height distribution ( Figure 2 May 2017). Cardwellia sublimis has proteoid cluster roots typical of the Proteaceae (Figure 3), a morphological adaptation often associated with phosphorus-impoverished soils (Lambers, Clode et al, 2015;Lambers, Martinoia, & Renton, 2015;Shane & Lambers, 2005). Cluster roots are ephemeral rootlet structures that release carboxylates to mobilize otherwise recalcitrant soil P (Shane & Lambers, 2005), allowing Proteaceae to exploit even the highly recalcitrant organic P form, phytate (Steidinger, Turner, Corrales, & Dalling, 2015).…”

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confidence: 99%

“…Cluster roots are ephemeral rootlet structures that release carboxylates to mobilize otherwise recalcitrant soil P (Shane & Lambers, 2005), allowing Proteaceae to exploit even the highly recalcitrant organic P form, phytate (Steidinger, Turner, Corrales, & Dalling, 2015). Proteaceae are commonly non-mycorrhizal (Lambers, Clode et al, 2015;Lambers, Martinoia et al, 2015), with studies in local natural systems showing 0% occurrence of arbuscular mycorrhizae (AM) in saplings of five species of Proteaceae including C. sublimis (Gehring & Connell, 2006). In contrast, F. brayleyana, a member of Rutaceae, does not exhibit cluster root formation, instead relying upon AM associations to facilitate nutrient exchange at the soil-plant interface (Gehring & Connell, 2006;Richardson, Barea, McNeill, & Prigent-Combaret, 2009).…”

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The role of topography and plant functional traits in determining tropical reforestation success

Cheesman

Preece

Oosterzee

et al. 2017

Journal of Applied Ecology

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Early establishment and sapling growth is a key phase in ensuring cost‐effective reforestation success in relation to biodiversity outcomes. Therefore, species selection must consider the interaction between plant functional traits and the often‐challenging and heterogeneous biophysical environment of degraded landscapes. In this study, we examine how microtopography (slope) results in spatial heterogeneity of soil nutrients, especially phosphorus (P) in a degraded tropical pasture landscape in Queensland, Australia. We then explore how this small‐scale heterogeneity influences the growth of two native tree species, Cardwellia (C.) sublimis (Proteaceae) and Flindersia (F.) brayleyana (Rutaceae), which differ in key nutrient‐acquisition strategies. The proteaceous C. sublimis was found to be buffered from possible P limitation in degraded soils due to its effective P acquisition by cluster roots. In contrast to C. sublimis, which showed no difference in growth after 5 years across a range of soil conditions, F. brayleyana was found to be highly responsive to soil conditions with increased growth in low‐slope, higher P availability areas. The ability of F. brayleyana to take advantage of high soil P levels, including the development of leaves with higher P concentrations, resulted in an apparent switch in competitive fitness between these two species across a landscape gradient. Synthesis and applications. In a detailed study of a landscape reforestation experiment in North Queensland, Australia, we demonstrate that site edaphic factors can vary within tens of metres due to topographic relief, and that species respond differently to these conditions. We therefore show the need to consider both the spatial heterogeneity of edaphic factors and the below‐ground functional traits of potential reforestation species when planning reforestation programmes.

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“…melletica) were considered as having the same leaf P-allocation pattern of the congeneric species. The Proteaceae species (Conospermum stoechadis) was also considered to preferentially allocate its P to mesophyll cells (Hawkins, Hettasch, Mesjasz-Przybylowicz, Przybylowicz, & Cramer, 2008;Hayes et al, 2018;Lambers et al, 2015;Shane, Mccully, & Lambers, 2004).…”

Section: Leaf Nutrient Analyses Leaf Cell-specific P Allocation Anmentioning

confidence: 99%

Trait convergence in photosynthetic nutrient‐use efficiency along a 2‐million year dune chronosequence in a global biodiversity hotspot

et al. 2019

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The Jurien Bay dune chronosequence in south‐western Australia’s biodiversity hotspot comprises sites differing in nutrient availability, with phosphorus (P) availability declining strongly with increasing soil age. We have explored the exceptionally high photosynthetic P‐use efficiency (PPUE) of Proteaceae in this region, triggering the question what the PPUE of co‐occurring species in other families might be along the Jurien Bay chronosequence. We explored how traits associated with PPUE, photosynthetic nitrogen (N)‐use efficiency (PNUE) and leaf respiration might converge along the chronosequence, and whether Proteaceae and non‐Proteaceae species differ in leaf traits associated with nutrient use. Seven to 10 species were sampled at three sites differing in nutrient availability (ranging from N‐ to P‐limited). Measurements of leaf light‐saturated photosynthesis and dark respiration were integrated with measurements of total N and P concentration in both mature and senesced leaves, and leaf mass per unit area (LMA). Contrary to what is known for other chronosequences, rates of photosynthesis and respiration did not decrease with increasing soil age and LMA along the Jurien Bay chronosequence. However, they increased when expressed per unit leaf P. Both N and P were used much more efficiently for photosynthesis on nutrient‐poor sites, in both Proteaceae and non‐Proteaceae species. Proteaceae had the fastest rate of photosynthesis per unit leaf P, followed by species that preferentially allocate P to mesophyll cells, rather than epidermal cells. Synthesis. Our results show that with declining soil P availability, photosynthetic P‐use efficiency of all investigated species from different families increased. Plants growing on the oldest, most nutrient‐impoverished soils exhibited similar rates of CO2 exchange as plants growing on more nutrient‐rich younger soils, and extraordinarily high photosynthetic P‐use efficiency. This indicates convergence in leaf traits related to photosynthetic nutrient use on severely P‐impoverished sites.

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Metabolic Adaptations of the Non‐Mycotrophic Proteaceae to Soils With Low Phosphorus Availability

Cited by 44 publications

References 192 publications

Calcium‐enhanced phosphorus toxicity in calcifuge and soil‐indifferent Proteaceae along the Jurien Bay chronosequence

Calcium‐enhanced phosphorus toxicity in calcifuge and soil‐indifferent Proteaceae along the Jurien Bay chronosequence

The role of topography and plant functional traits in determining tropical reforestation success

Trait convergence in photosynthetic nutrient‐use efficiency along a 2‐million year dune chronosequence in a global biodiversity hotspot

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