Humidity and high temperature are important for predicting fungal disease outbreaks worldwide

Abstract

Climate change is expected to lead to adverse impacts on global agricultural production, as it influences plant disease occurrence and severity at spatial and temporal scales (Howden et al., 2007). Furthermore, climate change also affects plant growth by reduced water availability and other abiotic stress factors. Recent studies have shown that climatic variables (e.g. humidity, temperature) are important drivers explaining the global distribution of potentially pathogenic soil‐borne microorganisms (Větrovský et al., 2019; Delgado‐Baquerizo et al., 2020). These studies are fundamental for understanding the global incidence and potential impact of fungal plant pathogens on terrestrial ecosystems.

Full text

Letters
Humidity and high temperature
are important for predicting
fungal disease outbreaks
worldwide
Fungal pathogens cause major yield losses in many of the world’s
crops. It is important to understand which climatic factors drive
pathogen occurrence, also in view of climate change. Here, we use
a global electronic reporting system for outbreaks of emerging
diseases (ProMED) to assess the factors that predict fungal disease
outbreaks. Our results based on the ProMED database demon-
strate that high temperature is an important driver of pathogen
incidence. We further demonstrate that humidity is about twice as
important as high temperature in predicting fungal plant disease
outbreaks. We highlight here that in order to predict disease
incidence, amplicon-sequencing data should be complemented by
reports on actual disease outbreaks and the prevalence of specific
pathogen species should be confirmed by using species-specific
markers.
Climate change is expected to lead to adverse impacts on global
agricultural production, as it influences plant disease occurrence
and severity at spatial and temporal scales (Howden et al., 2007).
Furthermore, climate change also affects plant growth through
reduced water availability and other abiotic stress factors. Recent
studies have shown that climatic variables (e.g. humidity, temper-
ature) are important drivers explaining the global distribution of
potentially pathogenic soilborne microorganisms (Vetrovskyet al.,
2019; Delgado-Baquerizo et al., 2020). These studies are funda-
mental for understanding the global incidence and potential impact
of fungal plant pathogens on terrestrial ecosystems. However, it
remains poorly understood to what extent the prevalence of soil
pathogens and the factors affecting them translate into increased
incidence of disease outbreaks. To provide empirical evidence, we
analyzed actual disease incidence reported worldwide using the
ProMED database (www.promed-mail.org). ProMED is a global
electronic reporting system for outbreaks of emerging diseases from
the International Society for Infectious Diseases (www.isid.org),
which has already been used in the past to address the relative
contribution of different factors to emerging plant diseases
(Anderson et al., 2004). The ProMED database is based on
outbreak reports by authorities, stakeholders and individuals that
are submitted to a panel of moderators who review the quality of the
data and publish a post containing only reliable data (Yu & Madoff,
2004).
Within the ProMED database, we reviewed 264 posts on fungal
diseases covering the period 2014–2019 and all continents (see
Supporting Information Fig. S1). For every post, we retrieved the
archive number, date, disease, location, host, pathogen and driver
of emergence (see Dataset S1). Our results demonstrate that
climatic variables are important drivers of pathogen incidence and
highlight the prevailing role of humidity as a driving factor for
actual fungal plant disease outbreaks.
For all the posts reporting fungal outbreaks within the period
2014–2019, 36.4% indicated that an increase in relative humidity
could have provoked or facilitated the outbreak (Fig. 1). High
temperature (17.7%) and low temperature (9.9%) predicted
disease in fewer cases. Our results further indicate that pathogens
colonizing predominantly aboveground plant organs, including
the fungal genus Puccinia and most species within the genus
Fusarium, as well as the fungal-like (i.e. oomycete) genus
Phytophthora were most frequently reported as causative agents of
plant disease (Fig. 2). Fungi that predominantly occupy such
niches may be underrepresented if the focus is only on pathogenic
fungi inhabiting the soil.
Soilborne potential plant pathogens can be relatively abundant
in soils from natural ecosystems worldwide. A recent global study
revealed that, on average, 14.4% of all internal transcribed spacer
(ITS) sequences at a given sampling site are classified as potential
pathogenic phylotypes, with Alternaria,Fusarium,Venturia and
Phoma being most abundant (Delgado-Baquerizo et al., 2020).
According to the information reported in the ProMED database
(2014–2019), Fusarium (14.0%), Puccinia (12.9%) and
Phytophthora (12.9%)were the genera most frequently detected
Fig. 1 Percentage of outbreaks reported in the ProMED database (period
2014–2019; n=264) identifying a given factor among the main potential
drivers for disease outbreak start. Some studies reported a disease outbreak
but did not identify the cause of the disease (e.g. ‘Not specified’). For more
details, see Supporting Information Dataset S1.
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as the causative agents for plant disease outbreaks (Fig. 2). Of the
dominant pathogenic phylotypes reported in the database,
Fusarium was the only one being detected widely in soil. The
difference between the current study and the study by Delgado-
Baquerizo et al. (2020) can also be explained by the ecosystems
under study: for example, the ProMED database largely focuses on
agricultural systems, while Delgado-Baquerizo et al. (2020)
included many natural ecosystems in the analysis. Moreover, the
primer pair used in Delgado-Baquerizo et al. (2020) (targeting the
ITS gene) did not match to oomycetes such as Phytophthora and as
such these sequences were not detected. That makes direct
comparisons between both studies to be made with caution.
Studies that report on the distribution of pathogens in soils often
rely on relative abundance data obtained from next-generation
sequencing (NGS; Riddell et al., 2019; Ruiz Gomez et al., 2019;
Vetrovskyet al., 2019; Delgado-Baquerizo et al., 2020). Although
amplicon sequencing provides important information on the
distribution of microbial organisms, relative abundance outputs of
sequencing studies do not allow for quantifying the host’s actual
exposure (Knight et al., 2018) and the resulting disease severity.
Unfortunately, absolute abundances cannot be deduced from
compositional data using statistical methods, yet recent studies
have shown that absolute abundance of microbial taxa is biolog-
ically meaningful (Vandeputte et al., 2017). In addition, the
taxonomic resolution of ITS-based NGS data often remains at the
genus level, although the pathogenicity of a given taxon can vary
widely within the same genus for a range of species, including
beneficial, saprotrophic, necrotrophic and pathogenic species
(Walder et al., 2017). Therefore, a higher taxonomic resolution
such as that provided by exact sequence variants (ESVs) in
combination with longer sequenced reads and different target genes
could be useful in identifying pathogenicity hotspots (Knight et al.,
2018). Further tools, including quantitative species-specific PCR
and/or omics approaches, should be used to assess the abundance of
fungal pathogens, as has already been done for air- and residue-
borne fungi (Dannemiller et al., 2014).
According to Delgado-Baquerizo et al. (2020), climatic variables
disproportionately contribute to the relative abundance of fungal
pathogens in soil compared with elevation, latitude, longitude,
vegetation type or soil characteristics. In line with this, a recent
meta-analysis of 3084 soil samples revealed that 38.7% of the
variability in soil fungal composition could be explained by
variations in temperature (Vetrovskyet al., 2019). Our analysis
using the ProMED database confirms that climatic variables are
indeed the factors most likely to explain the emergence of disease.
However, when analyzing climatic variables in detail, data from the
ProMED database indicate that humidity, and not temperature, is
the leading factor (Fig. 1). In line with this, other authors have also
indicated that mean annual precipitation is the climatic factor best
predicting fungal global diversity (Tedersoo et al., 2014). Humid-
ity mostly increases the risk of aboveground infection by organisms
such as the highly noxious fungal genus Fusarium as well as the
oomycete genus Phytophthora. According to the information
retrieved from ProMED, 12.9% of the outbreaks reported in the
period 2014–2019 were caused by Phytophthora species (Fig. 2);
most of these outbreaks had an increase in humidity identified as a
likely driver of emergence.
We stress here the importance of including oomycetes (e.g.
Phytophthora) in future global surveys, as they include important
plant pathogens whose incidence is expected to increase as a result
Fig. 2 (a) Distribution of the main pathogens reported in the ProMED database during the period 2014–2019. Note that taxa names of different
reproductive stages of a fungus (e.g. teleomorph and anamorph) are merged and only reported once (e.g. Gibberella is reported as Fusarium). (b) Main
drivers of disease outbreaks (as % of posts identifying a given factor) for the four most relevant plant pathogens according to the information reported in
the ProMED database.
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of agricultural intensification and climate change (Corredor-
Moreno & Saunders, 2020). Moreover, the relative contribution of
fungal vs oomycete plant pathogens to plant disease outbreaks in a
climate change context is still poorly understood. Furthermore,
beside their effects on plants, fungal pathogens can act as keystone
taxa and have a big impact on the functioning and structure of
microbial communities (Banerjee et al., 2018).
In conclusion, our work demonstrates that climate variables
(relative humidity, high and low temperature) are key factors
explaining the occurrence of disease outbreaks. Thus, our analysis
of the ProMED database on emerging plant diseases together with
previous studies on the distribution of potential soil pathogens,
highlights the need for agricultural adaptation to climate change
(Anderson et al., 2020). Our analysis highlights that studies that
predict disease outbreaks using high-throughput sequencing
benefit from complementing such molecular data with actual
information on disease outbreaks and severity. Finally, a higher
resolution to species level as well as the elucidation of indirect effects
of climate change on pathogens, such as modified farming practices
(e.g. crop rotation, tillage, etc.), merit further research efforts.
Acknowledgements
This work was supported by a grant from the Swiss National
Science Foundation (grant no. 310030 188799). The authors
declare there are no competing interests
Author contributions
FR and SC reviewed and synthesized the entries in the ProMED
database. FR wrote the first version of the manuscript and managed
the subsequent versions. MGAvdH initiated the work and
contributed, together with FW, SFB and SV, to discussion and
revision of the manuscript.
ORCID
S. Franz Bender https://orcid.org/0000-0003-0895-2228
Marcel G. A. van der Heijden https://orcid.org/0000-0001-
7040-1924
Ferran Romero https://orcid.org/0000-0002-2986-4166
Susanne Vogelgsang https://orcid.org/0000-0002-7214-3575
Florian Walder https://orcid.org/0000-0001-7731-7469
Ferran Romero
1
*, Sabrina Cazzato
1
, Florian Walder
1
,
Susanne Vogelgsang
2
, S. Franz Bender
1,3
and Marcel
G. A. van der Heijden
1,3
*
1
Plant–Soil Interactions, Agroscope, Zurich, 8046 Switzerland;
2
Ecological Plant Protection in Arable Crops, Agroscope,
Zurich 8046, Switzerland;
3
Department of Plant and Microbial Biology, University of
Zurich, Zurich 8057, Switzerland
(*Authors for correspondence: email
ferran.romeroblanch@agroscope.admin.ch (FR);
marcel.vanderheijden@botinst.uzh.ch (MGAvdH))
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Supporting Information
Additional Supporting Information may be found online in the
Supporting Information section at the end of the article.
Dataset S1 Data extracted and synthesized from the ProMED
database and used in this letter. [Correction added after online
publication 12 April 2021: the Dataset has been revised.]
Fig. S1 Percentage of disease outbreaks reported in the ProMED
database (period 2014–2019; n=264) among geographical loca-
tions.
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Please note: Wiley Blackwell are not responsible for the content or
functionality of any Supporting Information supplied by the
authors. Any queries (other than missing material) should be
directed to the New Phytologist Central Office.
Key words: fungal disease, humidity, metabarcoding, oomycetes, temperature.
Received, 7 October 2020; accepted, 4 March 2021.
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