Abstract
- 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.
- 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.
- 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%.
- 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.