Plant community-, environment- and soil-mediated relationships
between elevation and above- and belowground plant pathogens
Together, our results provide broad evidence that above- and belowground
pathogens had distinct geographical vertical pattern which were shaped
by different mechanisms. For foliar fungal pathogens, we found empirical
evidence that plant community characteristics (i.e. community proneness
index and evenness), rather than soil properties, were the main drivers
of community pathogen load in our field survey. However, results did not
support any direct or indirect relationship between elevation and foliar
fungal disease.
These results highlight the importance of host identity to determine
community-level diseases. In the field survey, shifts in plant community
proneness to diseases ultimately led to difference in community pathogen
load, a finding that is consistent with other studies from both plant
diseases (Mitchell et al., 2002; Liu et al., 2017) and alsoRibeiroia ondatrae caused amphibian diseases (Johnson et al.,
2013). However, although only a small part of the 73 plant species’
distributions overlaps with each other and generates considerable
variance in the composition of host communities for pathogens along the
elevation gradient, the degree of communities prone to disease did not
synchronously change. Therefore, plant community mediated effect was not
found in our study.
In general, our results indicated that abiotic factors mediated the
association between elevation and soil fungal pathogen richness, while
elevation showed no significant direct or indirect association with
foliar fungal diseases and soil fungal pathogen relative abundance.
Indeed, different measurements for pathogens (i.e. OTU richness versus
relative abundance) may explain the inconsistent responses of pathogens
to abiotic and biotic factors. For instance, positive plant richness-
pathogen diversity relationship and negative diversity- disease
relationship can be observed in natural plant communities, given that
increasing plant species diversity provides more diverse hosts while
simultaneously inducing dilution effects (Rottstock et al., 2014).
However, there is insufficient evidence to determine the relative
strength of which pathogen richness responds to the abiotic and biotic
environment. In addition, the different patterns of above- and
belowground plant pathogens along elevational gradients can be partly
explained by their differences in life history characteristics. Rusts
(e.g. Phragmidium , Puccinia and Uromyces ) are the
dominant foliar fungal pathogens in our study site (Liu et al., 2019);
these fungi belong to a group of obligate biotrophic pathogens that can
only extract nutrients from living plant cells (Duplessis et al., 2021)
and have relatively narrow host ranges (one or just a few
phylogenetically close plant species; Zhang, 2009). In contrast, soil
plant pathogens are commonly necrotrophic with a relatively broad host
range (Delgado-Baquerizo et al., 2020). Therefore, we expect that
negative biodiversity-disease relationships might occur more commonly
for foliar pathogens; foliar diseases are strongly dependent on their
hosts, so they can be easily captured by host composition rather than
environmental factors (e.g. temperature). For soil biota, we found
empirical evidence that increasing elevation was associated with
reductions in soil fungal pathogen richness via changes in soil
properties (Soil PCA1 ). Our meta-analysis providing further
evidence of a general negative association between soil fungal pathogen
richness and elevation among studies. However, elevation had no
significant association with soil fungal pathogen relative abundance.
Unlike the severity of foliar fungal disease or fungal pathogen relative
abundance, soil fungal pathogen richness depends on the relative rate of
fungal colonization and extinction of fungal taxa. On the one hand,
temperature may promote soil fungal pathogen richness through the
following three mechanisms: First, temperature is a key limiting factor
for plant biomass and richness (Chu et al., 2019). Broad evidence from
plants suggests that the species richness of lower trophic levels can
determine the diversity of higher trophic levels, including fungal
pathogens (Kamiya et al., 2014; Rottstock et al., 2014; Liu et al.,
2016). Moreover, increased plant biomass provides greater host
availability and more diverse habitats for pathogens. These
plant-mediated paths can shape a potential negative relationship between
elevation and soil fungal pathogen richness. Second, temperature can
promote coevolution between hosts and pathogens, given the stronger
inter-trophic interactions in warm areas (Roslin et al., 2017; Liu,
Chen, et al., 2020); this is thought to be a main factor shaping
pathogen richness. Third, temperature can determine the distribution of
soil pathogens via environment filtering (Tedersoo et al., 2014); the
fitness of pathogens is largely affected by temperature and humidity
through impacts on survival, growth, dispersal and reproduction, both at
local and global scales (Tedersoo et al., 2014; Liu et al., 2019;
Delgado-Baquerizo et al., 2020).
On the other hand, soil properties may be a regulator of plant
pathogens. Firstly, soil nutrients may benefit pathogens in both agro-
and natural ecosystems by increasing tissue nitrogen concentration
(Huber and Watson, 1974; Veresoglou et al., 2013; Liu et al., 2017).
Secondly, soil properties can alter the competition dynamics and shape
plant community composition (e.g. inducing the light asymmetry under
nitrogen addition; Xiao et al., 2021), which possibly indirectly
influence soil plant pathogens by preferring species with better growth
ability (Cappelli et al., 2020). The soil fungal pathogen relative
abundance showed no significant variation along the elevation gradient,
despite considerable changes in temperature and soil properties. We
attribute this to the small proportion of soil fungal pathogens relative
to total soil fungi (i.e. percentage of soil fungal pathogens copy
number; on average of 7.72% in our study), which may potentially limit
the ability of soil pathogens to respond to biotic and abiotic
variables.