Phosphorus Nutrition of Proteaceae in Severely Phosphorus-Impoverished Soils: Are There Lessons To Be Learned for Future Crops?

Abstract

Australia harbors some of the most nutrient-impoverished soils on Earth. Southwestern Australian soils are especially phosphorus (P) impoverished, due to the age of this ancient landscape and it being unaffected by major geological disturbance for millions of years (Hopper, 2009; Lambers et al., 2010). We are only now beginning to understand how plants acquire and use P in such highly infertile landscapes. At the same time, we are running out of nonrenewable, global phosphate resources in an era when we need more P fertilizers to produce more food and fiber to sustain a growing global population (Vance et al., 2003; Cordell et al., 2009; Gilbert, 2009). Can we learn valuable lessons for crop selection, breeding, and engineering from a flora that has evolved to function in soils with an extremely low availability of P (Lambers et al., 2006, 2008b, 2010)? Or are the traits in this flora highly suitable for the most P-impoverished soils but disadvantageous on the more fertile soils in which our crops currently grow? These questions can only be answered by learning more about the mechanisms that underpin the high plant P-efficiency traits that enable survival in P-impoverished landscapes as found in southwestern Australia. This Update explores traits in Proteaceae from soils with extremely low P availability and assesses whether these traits would be desirable for crops. The ability to form root clusters and mycorrhizal associations are two adaptive traits that improve the ability of plants to acquire soil P (Lambers et al., 2008b; Smith et al., 2011). The root systems of species that develop cluster roots have a unique capacity for altered branch-root development (Shane and Lambers, 2005). Vast numbers of branch roots (“rootlets”) are initiated, which are compacted into specific regions along the axes of growing roots (Lambers et al., 2006). Species with root clusters (Shane and Lambers, 2005; Lambers et al., 2006) are relatively more abundant than mycorrhizal species on the most P-impoverished soils within old landscapes (Lambers et al., 2008b, 2010; Brundrett, 2009). Even though the majority of crop and forest species are mycorrhizal, some do form cluster roots, such as Macadamia integrifolia (macadamia nut), Aspalathus linearis (rooibos tea), Casuarina cunninghamiana (sheoak), Gevuina avellana, and Lupinus albus (white lupin); most of these species are nonmycorrhizal, but Casuarina species have both cluster roots and mycorrhizas (Halloy et al., 1996; Lambers and Shane, 2007). In addition to P acquisition, we compare P use in plants that are common in old landscapes, particularly members of the Proteaceae, with that in plants from other regions of the world. We focus on Proteaceae because this is a plant family that is well represented in landscapes with a low P availability (Pate et al., 2001); consequently, much research attention has been devoted to their P nutrition (Lambers et al., 2010). We discuss the P-use efficiency of photosynthesis and growth, P-remobilization efficiency and proficiency, and P allocation to seeds. More sustainable, P-efficient cropping systems are urgently needed, and knowledge about native plant physiology in ancient landscapes may guide us toward their development, either through directing the breeding or engineering of existing major crop species or through aiding the development as crops of species that originate from these P-impoverished landscapes (Ryan et al., 2009; Pang et al., 2010a, 2010b; Suriyagoda et al., 2010; Bell et al., 2011). Root clusters combine specialized structure and physiology (Johnson et al., 1994; Shane et al., 2004b) to maximize P acquisition from soils of low P availability, especially when P is present in insoluble complexes (e.g. rock phosphate and iron phosphate; Shane and Lambers, 2005; Lambers et al., 2006). They occur in monocots (e.g. “dauciform” roots in Cyperaceae; Lamont, 1982; Shane et al., 2005; Playsted et al., 2006) as well as dicots (e.g. “proteoid” roots in numerous families, including Proteaceae; Purnell, 1960; Gardner et al., 1983; Lamont, 2003; Lambers et al., 2006). Root clusters effectively “mine” soil P (Fig. 1A), as opposed to the “scavenging” strategy of mycorrhizas, and hence species that produce cluster roots dominate on the most P-depauperate soils (Lambers et al., 2008b, 2010). Simple and compound types of proteoid root clusters of Proteaceae. Both types have large numbers of ephemeral rootlets arising from a persistent mother root. A to C, Roots of G. avellana (in Parque Katalapi, Chile). A, Soil profile beneath G. avellana showing numerous white clumps of simple proteoid roots at the trench face. B, Young proteoid root with a high density of growing rootlet tips and normal-shaped apices. C, Mature proteoid rootlets, after the soil has been washed off in water, showing “claviform” apices. D, Roots of Banksia repens, native to southwestern Australia, hydroponically grown at a very low [P] (1 μm or less), with compound proteo