Abstract
  1. Ectomycorrhizal (ECM) roots are evolutionary strategies of plants for effective nutrient uptake under varying abiotic conditions. Formation and morphological differentiations of ECM roots are important strategies in foraging environments. However, little is known on how such strategies mediate the nutrients of the below- and aboveground tissues and the balances among nutrient elements across environmental gradients.
  2. We studied the function of ECM symbiosis in Abies faxonianaacross its distributional range in Southwest China. The effects of differential ECM strategies, i.e. the contact exploration type, the short-distance exploration type, and the medium-distance exploration type, and root tips functional traits, etc., on root and foliar N and P and N:P ratio were examined across natural environmental gradients.
  3. The ECM symbionts preferentially facilitated P uptake in A. faxoniana under both N and P limitations. The uptakes of N and P were primarily promoted by the effectiveness of ECM roots, e.g. ECM root tips per unit biomass, superficial area of ECM root tips, the ratio of living and dead root tips, but negatively related to the ECM proliferations and morphological differentiations. Generally, plant N and P nutrients were always promoted by the contact exploration type, while negatively affected by the short-distance exploration type inA. faxoniana . Root and foliar N and P nutrients were expected to be affected by the medium-distance exploration type in dynamics. Especially, root P limitation could be relieved when the frequency of medium-distance exploration type up to c .15%, whilst root N limitation was strengthen when the frequency of medium-distance exploration type over 20%.
  4. We suggest that both below- and above-ground nutritional traits of host tree species could be strongly affected by ECM symbiosis in natural environments. The ECM strategies responding to environmental conditions significantly affect the plant nutrient uptakes and trade-offs. ECM soil exploration types are the great supplementary mechanisms for plant nutrient uptake.
Keywords: Abies faxoniana ; ectomycorrhizal morphology; ectomycorrhizal strategy; plant N, plant P; plant N:P ratio; soil exploration types
1 INTRODUCTION
Over 80% of tree species in forest ecosystems could form ectomycorrhizal (ECM) symbionts. ECM fungi are irreplaceable to the health and growth of forest trees by enhancing soil nutrients uptake, particularly N and P elements (Smith & Read, 2008; Barrett et al., 2011). It is certain that functional genes related to N and P exist in ECM fungi (Perez et al. , 2011; Cappellazzo et al. , 2008; Nehls et al. , 1999). ECM roots absorb and transport soil nutrients for host plants through root tips, being important adaptations to assistant to nutrient uptake (Figure 1), and emanating hyphae which are the important functional ECM traits. Varying emanates of ECM could be classified as different soil exploration types. Agerer (2001) defined the soil exploration types into five groups: contact exploration type (smooth mantle and only a few emanating hyphae), short-distance exploration type (ECM root with a voluminous envelope of emanating hyphae but no rhizomorphs), medium-distance exploration type (ECM root with rhizomorphs), long-distance exploration type (ECM root with long rhizomorphs), and pick-a-back exploration (ECM formed by members of the Gomphidiaceae ). Different soil exploration types absorb soil water and nutrients at a different distance from the root tips (e.g. contact exploration with length of emanating elements 0 mm, short distance exploration type with length of emanating elements < 1 mm, and medium distance exploration type with length of emanating elements < 1 cm) (Tedersoo et al. , 2012; Pritsch & Garbaye, 2011); these features have important implications to plant nutrient absorption. The differentiation of ECM hyphae is an important feature of ECM, which could form different ECM morphologies (Agerer, 1987-2006; Agerer, 1991). ECM root tips, length of emanating hyphae or rhizomorphs, and morphological differentiation always responded to resources limitation, soil acidity, and climatic changes (Graefe et al ., 2010; Ostonen et al ., 2009; Toljander et al ., 2006; Rosinger et al ., 2018). Furthermore, changes of ECM root traits resulted in the variation of the nutrient uptake efficiency or ability in the host tree (Chen et al . 2016; Chen et al . 2018). The morphology, hyphae characteristics, and soil exploration types of ECMs are important foraging strategies for host plants to respond to environmental changes.
Nitrogen (N) and/or phosphorus (P) limitations are common in terrestrial ecosystems. Both N and P are important nutrient elements for plant growth and health. The ratio of N to P of plant tissue is generally used to indicate the nutrients limitation in plant growth and community health (Olde Venterink et al. , 2003; Güsewell & Koerselman, 2002). Generally, plant N:P ratio is a relatively stable trait. It was suggested that the values of N:P ratio < 14 or > 16, respectively, indicated N limitation or P limitation in plants (Güsewell & Koerselman, 2002; Tessier & Raynal, 2003). The value of plant N:P ratio is a helpful tool to diagnose the nutrient limitation condition or nutrient allocation partiality in individual (Koerselman & Meuleman, 1996). However, to some degree, P could be the ultimate limiting element in ecosystems, as evidenced by the fact that N nutrient uptake could be promoted when adding P (Vitousek et al ., 2010). N and P uptakes of tree species are strongly affected by climate, soil environmental conditions and nutrient acquisition capacity of the species (Güsewell, 2004; He et al. , 2008), as illustrated in Figure 1. Positive effects of rainfall but negative effects of air temperature on foliar N and P have been reported (Reich & Oleksyn, 2004; Han et al. , 2005). Climate eventually influences plant N:P ratios and productivity. He et al . (2008) believes that soil resources instead of climate play greater impacts on plant N and P, such that availability of soil N and P largely limits the nutrient uptake of plant species. Importantly, N and P nutrition in tree species largely depend on their nutrient capture ability of soil resources (Brandeset al. , 1998; Bardgett et al. , 2014).
The uptake efficiency of N and P is dependent of the root systems with strategies adapting to environmental conditions (Chien et al. , 2011; Hodge, 2004; Jackson & Caldwell, 1996). Of which, the ECM symbionts play an important role when tree species undergo environmental stresses (Alonso et al. , 2003; Ahonen-Jonnarth et al. , 2000) or nutrient deficiency (Almeida et al. , 2019; Hajong,et al. , 2013). The symbionts usually promote plant nutrients absorption by altering hyphae length, or modifying the morphology of root tips or microbial communities, etc., when plants are under stresses (Lõhmus et al. , 2006; Ostonen et al. , 2009; Boomsma & Vyn, 2008). Under natural environmental conditions, uptakes of N and P by roots are promoted by ECM foraging strategies, such as increases in ECM root tips and changes in hyphae length or morphology, etc. (Ostonenet al. , 2007; Ostonen et al. , 2011). The important foraging strategies discovered so far include the secretion of enzymes decomposing N or P complex by ECM root tips, and facilitation of nutrient acquisition far from the root distal by extending hyphae or rhizomorphs (Nehls & Plassard, 2018; Courty et al. , 2010; Pritsch & Garbaye, 2011). ECM plants are characteristically of low foliar nutrients and high leaf mass per unit area (especiallyPinaceae and Fagaceae ) (Koele et al. , 2012; Read, 1991; Cornelissenm et al., 2001). The intimate connections of foliar N nutrition and ECM symbiosis are widely reported (Koele et al ., 2012; Hobbie & Hobbie, 2006; Hobbie et al. , 2005). For instance, isotope tracing experiments proved the transfers of N element among plant tissues and mycorrhizal fungi (Steven et al ., 2004; Hobbie & Högberg, 2012). Still, few studies reported the associations of ECM traits and foliar nutrients. There are observations of the associations of root and leaf nutrient traits (Craine & Lee, 2003; Tjoelker et al. , 2005) and reports of the positive correlations of N or P between roots and leaves (Liu et al. , 2010; Güsewell, 2004.). It is clearly known conceptually that mycorrhizal root systems assimilate N and P and then transfer them to shoots (Michelsen et al. , 1996; Smith & Read, 2008; Plassard & Dell, 2010) (Figure 1). Previous researches have revealed the relationship of foliar N with mycorrhizal fungi, asserting that mycorrhizal associations influence the foliar N transfer (Hobbie & Hobbie, 2006; Craine et al ., 2009). Controlled experiments demonstrated that the mycorrhizal symbionts affected the allocation of N and P nutrients among roots, stems, and leaves (Chen et al. , 2010; Johnson, 2010; Landis & Fraser, 2008; Wang et al ., 2006; Brandes et al. , 1998). Explicit knowledge concerning the distinctive impacts of ECM strategies on the root and leaf nutrients was required to be explored across the natural environment (Figure1). Combining the plant elemental stoichiometry with the ECM strategies can improve our understanding of the implications of ECM in the nutrition trade-offs, hence the health of plants. How ECM strategies mediate the below- and aboveground nutrients balance in plants in response to environmental changes is yet to be further explored.
Abies faxoniana is an ancient species in the genus Abiesthat experienced the glacial and interglacial periods (Florin, 1963). It is a typical ECM tree species and naturally distributed from 2700 to 3900 m asl. in subalpine area of Sichuan province, Southwest China. A. faxoniana forest is the primary vegetation type in that subalpine ecosystem. In this study, we investigated the effects of ECM strategies on the N and P nutrients between below- and aboveground tissues in plants under different environmental gradients. The root and foliar N and P contents, ECM traits representing nutrients uptake pathway (soil exploration types, ECM morphological diversity) and efficiency (fine root biomass, the ratio of living and dead root tips, the colonization ratio of the ECM root, ECM root tips per unit root biomass, the superficial area of ECM roots) were measured along the natural environmental gradients. Our objective was to determine how the ECM strategies in A. faxoniana regulated the nutrient preference of N and P nutrition and the nutrient uptake of the below- and aboveground. We hypothesized that (i) ECM strategies conduct the partiality of N and/or P nutrition of the below- and aboveground in A. faxoniana across the nature environmental gradients, and (ii) ECM soil exploration types distinctively regulate the nutrient uptakes in host tree.