Perennial lifestyle--an adaptation to nutrient limitation?

Trees account for a quarter of the ≈ 400 000 vascular plant species and are among the largest and longest-lived organisms on Earth, growing up to 114 m tall and living in excess of 4000 years (Schulman 1958, Raven and Crane 2007). Since early in human evolution, trees have provided habitat, food, fuel, fibres and building materials. In the past 2000 years, lower-impact uses of trees and forests have given way to large-scale replacement of forests with agricultural landscapes. Forests and tree plantations are increasingly considered for their central role as providers of habitat and regulators of global biogeochemical, temperature and water cycles. This special issue draws together knowledge of nutrient relations of trees, forests and plantations. A unique feature of all plants is their capability to produce biomass from carbon dioxide, light energy, water and nutrients. Whilst carbon dioxide and light are often present in excess, the availability of water and nutrients, in particular nitrogen and phosphorus in young and ancient soils, respectively (Wardle et al. 2004), are the most important factors limiting growth and development of plants. The latter is obvious from the fact that nearly all commercial fertilizers applied in bioproduction systems contain nitrogen and phosphorus as the most abundant constituents (Tilman et al. 2002, Gruber and Galloway 2008). However, other nutrients, including potassium and calcium, can also limit plant growth including wood formation of trees (this issue: Fromm 2010). In addition to efficient and balanced acquisition and use of nutrients for growth and development, the competitive success of plants depends on nutrient allocation between growth and defence measures (this issue: Simon et al. 2010). Many forest ecosystems have developed in environments with marginal soils characterized by growth-limiting availability of macronutrients such as nitrogen (N) and phosphorus (P) (Lovett et al. 2004, Chapman et al. 2006, Rennenberg et al. 2009, this issue: Raven and Andrews 2010); but despite such limitations, forests can have high productivity. Extreme adaptation to nutrient limitation has resulted, as evidenced by high nitrogen-use and nutrient-resorption efficiencies in mangrove forests (this issue: Reef et al. 2010). To optimize growth in soils with growth-limiting nutrient availability, trees have evolved special features at the cellular/molecular, whole-plant and ecosystem levels. At the molecular level, nutrient cycling processes require distinct seasonal expression patterns of nutrient transport proteins in different cellular compartments and organs (Dürr et al. 2010) as well as metabolic inter-conversion between storage and transport forms of nutrients (this issue: Wildhagen et al. 2010). The uncoupling of nutrient uptake from nutrient use for growth and development, but also the need to reduce ecosystem losses of growth-limiting nutrients may require regulatory mechanisms of nutrient acquisition different from demand-driven control at the whole plant level. Demand-driven control has been postulated from laboratory experiments for uptake of inorganic nitrogen and sulphur (Muller et al. 1996, Rennenberg et al. 2007), but has not yet been demonstrated for perennial plants under nutrient limitation in the field. At the whole-plant level, temporal uncoupling of nutrient uptake from the phases of predominant nutrient requirement for growth and development seems to be a particular feature of trees (this issue: Millard and Grelet 2010). Such uncoupling of uptake and use of nutrients makes growth and development of trees largely independent from immediate nutrient supply from soils and enables developmental processes even when soil temperatures or water relations are unfavourable for nutrient uptake. Uncoupling of uptake and use of nutrients is achieved by seasonal storage and mobilization processes (this issue: Millard and Grelet 2010, Wildhagen et al. 2010). At the ecosystem level, nutrient-limited forests exhibit closed nutrient cycles that reduce losses of growth-limiting nutrients to the hydrosphere and atmosphere to levels below the usually low input from ecosystem external sources (Rennenberg et al. 2009, 2010). Thereby, a slow, long-term increase in the availability of growth-limiting nutrients can be achieved and maintained, as evidenced from the accumulation of nutrients in standing biomass of forests with increasing age of the trees for a major part of their life cycle on nutrient-limited soils. However, over long geological time spans of thousands to millions of years and in the absence of soil renewal and rejuvenating disturbances, rates of nutrient cycling decline are accompanied by decreasing primary productivity (Pelzer et al. 2010). In many regions, ‘climax’ forests are not maintained indefinitely (Lambers et al. 2008, Pelzer et al. 2010), yet a key feature of these forest ecosystems is the tight cycling of nutrients. The immediate use of all chemical forms of a growth-limiting nutrient seems to be required to reduce overall nutrient losses from the ecosystem. Plant available N for non-N-fixing trees, for example, is predominantly produced during decay and depolymerization of root and leaf litter via fungal and bacterial activities. Immediate uptake by roots of the amino acids produced during these processes (Näsholm et al. 2009, this issue: Stoelken et al. 2010) reduces the loss of N from the ecosystem because the most important competitive process to uptake by roots, i.e. bacterial nitrification of amino acids, generates nitrate which is easily leached into the hydrosphere (Rennenberg et al. 2009). In addition, there is evidence that nutrients prone to loss into the hydrosphere are taken up by tree roots in excess of plant needs and stored in roots rather than being loaded into the xylem and transported to the shoot; this has been shown particularly for sulphate (Kreuzwieser et al. 1996, van der Zalm et al. 2005). Upon root turnover, stored nutrients are released and are subject to partitioning within the ecosystem which restricts losses of nutrients and largely maintains flexibility of nutrient use within different ecosystem processes. Efficient prevention of nutrient losses is essential under nutrient limitation to allow for high internal nutrient cycling and adaptation of nutrient distribution at the ecosystem level (Lovett et al. 2004, Chapman et al. 2006, Rennenberg et al. 2009, 2010). Among the environmental factors that interact with nutrient acquisition of trees, water availability, temperature and increasing atmospheric carbon dioxide concentrations are of particular significance (this issue: Kreuzwieser and Gessler 2010, Lukac et al. 2010, Millard and Grelet 2010), and at the ecosystem level, their relative importance is strongly modulated by species composition (this issue: Richards et al. 2010). The adaptive processes that control the interaction between nutrition and environmental factors require integration of nutritional requirements at the whole-plant level and, hence, regulatory mechanisms with above-ground processes such as photosynthesis and photorespiration (this issue: Herschbach et al. 2010, Lukac et al. 2010). These regulatory processes can differ between genotypes of the same species (this issue: Hawkins et al. 2010), necessitating already today the selection of genotypes that are best adapted to future environments. Besides these features that are specific to perennial plants, trees have additional adaptations similar to herbaceous plants, to make use of new resources and to improve the efficiency of nutrient acquisition. These adaptations include specializations such as symbiosis with mycorrhizal fungi, symbiotic nitrogen fixation, cluster roots and parasitism (this issue: Adams et al. 2010, Plassard and Dell 2010, Raven and Andrews 2010), whereas ectomycorrhizal symbioses are restricted to woody plant species (Smith and Read 2008). However, even diazotrophic N fixation may show peculiarities unique to woody plant ecosystems. In mixed eucalypt/acacia forests, for example, symbiotic N fixation in acacia roots is maintained only during initial forest development until a certain amount of N has accumulated in the ecosystem. Upon further forest growth, this costly symbiotic process is suppressed and may enable a switch of energy expenditure which results in enhanced productivity (Pfautsch et al. 2009, this issue: Adams et al. 2010). Considering the practical applications of tree nutrition, there is evidence that failing reforestation can, among other factors, be attributed to inadequate nutrient supply. Yet, rapid N accumulation can occur in N-fixing legume tree-dominated reforestations and cause increased nitrification and tighter P cycles compared with diverse species mixtures with a low presence of N-fixing trees (Siddique et al. 2008). The importance of resource-use efficiency in determining forest productivity has been demonstrated in monoculture plantations, but mixed tree species plantations are increasingly considered for reforestation because of their potential for greater stability and enhanced biodiversity, especially in regions of the subtropics and tropics where natural forests are composed of a highly diverse tree species mixture. Reasons for complementary nutrient use in mixtures compared with monocultures include diverse nutrient acquisition strategies and differing nutrient demand. In a mixed species rainforest plantation, complementary interaction occurred between species with respect to nutrient uptake, nutrient-use efficiency and nutrient cycling (Richards and Schmidt 2010). An analysis of N- and P-use efficiencies of tree species grown in mixtures compared with monoculture demonstrates that resource-use efficiency is generally greater for a given species in mixtures and the resulting systems are more productive than monocultures (this issue: Richards et al. 2010). Thus, there is mounting evidence that nutrient acquisition and use is enhanced in tree species mixtures compared with monocultures, and selection of complementary tree species is an avenue to improve reforestation and forestry practices. Although tree nutrition often focuses on nutrient limitations imposed by soil and environmental conditions, trees also occur in environments that exhibit high nutrient availability, either naturally, due to anthropogenic nutrient input, or because N-fixing trees are chosen as main species for reforestation (this issue: Reef et al. 2010, Rennenberg et al. 1998, 2010). Under such conditions, open rather than closed ecosystem nutrient cycles have been observed (Siddique et al. 2008, Kreutzer et al. 2009). In summary, perennial plants have evolved nutritional features that can be regarded an adaptation to nutrient limitation, but also make use of adaptive features that are widely distributed in the plant kingdom in annual and perennial plants. Thus, one could argue that it is not the perennial lifestyle per se that allows growth and development under nutrient limitation, but that the perennial lifestyle provides a set of competitive advantages under conditions of low nutrient supply which include long-term investment and exploration of a large soil volume. This special issue of Tree Physiology addresses a selection of tree-, plantation- and forest-based features of tree nutrition that span from the molecular to the ecosystem level. From these features, it is evident that sustainability and productivity of tree plantations and forests ultimately depend on ecosystem biogeochemistry and properties of tree species for efficient acquisition, use and cycling of nutrients.