REVIEW ARTICLE

Environment-Pathogen Interaction in Plant Diseases

Rajat Sharma1, Shalini Verma2 10.18805/ag.R-1859

A b s t r ac t
The environment is an important aspect of plant ecology. And global environmental change is of major concern that is caused by natural
and human activities which alter greenhouse gas concentrations in the atmosphere. An increase in the concentration of greenhouse
gases is foreseen to continue to raise the average global temperature. Elevated concentration of carbon dioxide with increased
temperature influences the plant-disease interactions. The environment influences the development as well as temporal and spatial
dissemination of plant diseases. The result of a change in environment can either be favorable, non-favorable or impartial, as these
changes can either lessen, expand or have no influence on diseases as each disease may be attributed differently to these variations
in accordance to an area or time of year. Variation in environmental conditions is said to be influencing plants in natural ecosystems all
around the world and change in climate directly impacts crops, along with their synergy in accordance with the microbial population.
The important elements governing magnification and spread of plant diseases are temperature, moisture, light, and carbon dioxide
concentration. Environment change causes a significant impact on germination, reproduction, sporulation, spore dispersal, along with
perforation by pathogens as a pernicious pathogen will not invade a vulnerable host if the environmental conditions are not facilitative
for the disease. The environment influences all life stages of host as well as that of a pathogen and as a result, induces an opposition
to various pathosystems. Resistance mechanisms of plants, including effector-triggered immunity (ETI), pattern-triggered immunity
(PTI) and defense network of hormones, are particularly influenced by environmental elements. Pathogenic virulence mechanisms
like fabrication of virulence proteins and toxins, and also spore germination and survival are governed by factors such as atmospheric
carbon dioxide, temperature, and humidity. A large number of in-vitro experiments to understand interactions between plants and
pathogens rely on predetermined pathosystems by making use of ascertained environmental conditions which take into consideration
relatively small part of vital plant–pathogen–environment interactions occurring in a natural ecosystem. Thus, there is a need to research
effectiveness of disease management strategies that is, to assess current management strategies to understand the multifaceted nature
of environment-pathogen interactions for the production of crops that are irrepressible to environmental change.
Keywords: Effector triggered immunity (ETI), Emergence diseases, Environment change, Microbe-or-pathogen-associated molecular
pattern (MAMP or PAMP), Pattern triggered immunity (PTI), Plant-pathogen–environment interactions.
Agricultural Reviews (2019)

Introduction 1-2
Department of Plant Pathology, Dr. Yashwant Singh Parmar

H uman undertakings are generally credited to enhance

the rate of global environmental changes that directly
impact the bionomics. Greenhouse gases involving, carbon
University of Horticulture and Forestry, Nauni Solan-173230 H.P.
India
Corresponding Author: Shalini Verma, Department of Plant
dioxide (CO2), Methane (CH4), water vapor (H2O), nitrous oxide Pathology, Dr. Yashwant Singh Parmar University of Horticulture
(N2O), Ozone (O3), and hydrofluorocarbons (HFCs) present in and Forestry, Nauni Solan-173230 H.P. India, Email: shaleiniverma@
the atmosphere trap solar radiation to increase the surface [Link]
temperature of the earth (Mahato, 2014). Pathogens that How to cite this article: Sharma, R. and Verma, S. (2019).
are known to infect plants are manifold, fluctuating from Environment-Pathogen Interaction in Plant Diseases. Agricultural
intracellular viruses and bacteria to extracellular, fungi, and Reviews, 40(3): 192-199.
nematodes. Based on the mode of nutrition, pathogens are Source of support: Nil
classified as biotrophs or necrotrophs. Biotrophs are the Conflict of interest: None
organisms which attain nutrients from living cells of the host, Submitted: 31-12-2018  Accepted: 04-07-2019  Published: 21/08/2019
whereas necrotrophs are known to kill host cells. Also, there
is an abundance of hemibiotrophs, which show an initial
biotrophic phase before finally killing the host. Change in plant pathology characterizes the interaction of both plants
environmental factors has an impact on the emergence of and pathogen with the environment.
plant diseases in accordance with water, air, and soil pollution The global environment is known to be influenced
caused by human activities (Regniere, 2012). According to by an abundance of factors and has a direct impact on all
Inter-governmental Panel on Climate Change (IPCC, 2007), three constraints of disease triangle, involving, pathogen,
the planet earth is confronting an environment change, host, and environment (Legreve and Duveiller, 2010). Due to
and atmospheric CO2 has increased by as much as 30% and environment change, pathogens are presented with short life
temperature by 0.3 to 0.6°C. Plants and pathogens are not cycles; as a result, the reproduction rate is increased, and the
known to interact in isolation. The ‘disease triangle’ concept in dispersion structure responds quickly. (Coakley et al., 1999).

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 Environment-Pathogen Interaction in Plant Diseases

Elevated temperature and CO2 concentration have an of plant organs, leaf thickness, also the diameter of stems
influence on plant-disease interaction as it enhances the (Bowes, 1993 and Pritchard et al., 1999); as a result, host
chances of diseases such as blast (Magnaporthe grisea) and resistance is elevated (Coakley et al., 1999).
sheath blight (Rhizoctonia solani) of rice (Kobayashi et al., • Consequently, higher leaf area index favors the occurrence
2006). Crop growth and productivity can be affected due of Stemphylium blight, powdery mildew, rust, and
to high temperature and atmospheric CO2 concentration Alternaria blight. Higher levels of CO2 concentrations
in accordance with the availability of water (Rosenzweig result in the production of more fungal spores. As a result
and Tubiello, 2007, Ghini et al., 2008, and Chakraborty and of elevated atmospheric CO2 concentration opening
Newton, 2011). For disease to transpire, susceptible plant of stomata is also reduced leaf chemistry is modified,
host, virulent pathogen, and a favorable environmental resulting in less disease incidence (Mcelrone et al., 2005).
conditions are needed, as the absence of favorable conditions For example, in soybean, the enhanced concentration
or any of three factors will result in dereliction for the disease of O3 and CO2 modified the incidence of three soybean
to develop (Stevens, 1960). The impact of environmental diseases, which are downy mildew (Peronospora
constraints (e.g., high temperature) on pathogens and plants Manchuria), brown spots (Septoria glycines) and sudden
can have a positive, neutral, or negative impact on plant death syndrome (Eastburn et al., 2010).
disease development. Both pathogens and plants have a • Barley plants with increased CO2 concentration accumulate
prerequisite environmental condition for their magnification silica and produce papillae at the site of appressorial
and reproduction. The more the environmental conditions penetration by Erysiphe graminis (Hibberd et al., 1996).
vary from this ‘disease optimum’, the lesser disease symptoms • Elevated atmospheric CO2 concentrations are known
will present themselves on the plant. to increase the photosynthetic rate and crop yield of C3
Host-pathogen-environment interactions: plants. However, it also enhances disease severity in rice
and wheat (620 and 780 ppm, respectively), (Kobayashi
The interaction between host, pathogen, and environment is
et al., 2006 and Vary et al., 2015).
nonspatial, ranging in order of interactions which completely
facilitate the disease to those in which a susceptible plant • C4 plants (e.g., corn and sugarcane), however, do not
is not infected at all. Environmental variables are known to profit from this enhance in atmospheric CO2 as a result
have a significant impact on a host plant’s substantial state, of their inherent CO2 concentration mechanisms (Long
such as, its expansion, resistance mechanisms in accordance et al., 2006).
to biotic/abiotic stress response, along with a pathogen’s • In case of fungal pathogen Fusarium graminearum,
survival, germination, and production of virulence proteins. enhanced CO2 levels increased the vulnerability of wheat
These ever-changing environmental criterions can result in varieties in accordance with the virulence of the fungal
a host plant being fully vulnerable to being fully resistant, isolate (Vary et al., 2015). Whereas, in case of interactions
whereas the pathogen, on the other hand, ranges from being between soybean and Peronospora manshurica, CO2
severely virulent to being weakly pathogenic. concentrations of 550 ppm decreased the incidence of
the disease by more than 50% (Eastburn et al., 2010).
Impact of atmospheric carbon dioxide concentration on
plant diseases Impact of temperature on plant diseases
• Elevated atmospheric CO2 concentration enhances • The temperature, in general, is known to influence the
photosynthesis, water use efficiency and lessens the amount/number of spores which are formed in a unit
damage incurred from ozone (von Tiedmann and plant area and the number of spores delivered in a
Firsching, 2000), also plant height and yield of crop given period of time. Due to variations in temperature
increases significantly at higher concentrations of CO2 and moisture, environment change may modify the
(Eastburn et al., 2011). development rate of spores, pathogenicity of pathogens,
• Increased concentration of atmospheric CO2 levels results and the resistance of the host plant (Charkraborty and
in an increase in overall leaf area, numbers of leaves, size Datta, 2003).

A summary of the influence of elevated CO2 on some host crop and pathogen interaction and pathogen fitness.
Author/Reference Crop /Host Disease/Pathogen Climate Change Change in Severity
Manning and Tiedemann, 1995 Barley Smut – Ustilago hordei Elevated CO2 Increase
Hibberd et al., 1996 Barley Powdery mildew – Blumeria Elevated CO2 Decrease
graminis
Hibberd et al., 1996 Barley Barley yellow dwarf virus Elevated CO2 Decrease
Milus et al., 2006 Wheat Stripe rust – Puccinia striiformis Elevated CO2 Decrease
Melloy et al., 2010 Wheat Crown rot –Fusarium pseudo- Elevated CO2 Increase
graminearum
(Debela and Tola, 2018)\

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 Environment-Pathogen Interaction in Plant Diseases

A summary of the influence of elevated temperature on some host and pathogen interaction and pathogen fitness.
Author/Reference Crop/Host Disease/Pathogen Climate Change Change in Disease Severity
Boland et al., 2004 Wheat Dwarf bunt- Tilletia controversa Elevated temperatures Increase
Milus et al., 2006 Wheat Wheat Stripe rust – Puccinia striiformis Higher Temperature Increase
Jesus Junior, 2007 Citrus Anthracnose Colletotrichum acutatum Elevated Temperatures Increase
Jesus Junior, 2007 Citrus Guignardia citricarpa, Elevated Temperatures Increase
Hannukkala et al., 2007 Potato Late blight – Phytophthora infestans Elevated temperatures Increase
causing earlier seasons
Ghini et al., 2008 Coffee Meloidogyne incognita Elevated temperatures Increase
(Debela and Tola, 2018)

• Enhanced global temperature results in a variation of plant diseases in many complementary ways.
the spatial distribution in which a crop is vulnerable to a • Moisture is a prerequisite factor for:
particular pathogen. This is true for pathogens that are • Initiation of fungal, bacterial, nematode and certain viral
in possession of specialized structures to be used under pathogens.
unfavorable conditions (Ritchie et al., 2013). • The development of fungal spores.
• A particular optimum temperature is needed by both • Perforation of the host by the germ tube.
plants and pathogens to advance. Temperature is • The dispersal of pathogens either on the same plant or
known to influence various events in a disease cycle from one plant to another one.
such as germination, dispersal, survival, penetration, With elevated temperature, high rainfall events, and
advancement, and also reproduction rate for various enhanced atmospheric humidity occur. As a result, crops
pathogens. produce healthful and larger canopies which retain moisture
• High temperature and elevated CO2 concentration favor as leaf wetness for a longer periods of time and as a result,
and initializes disease advancement, as well as survival conditions conducive for diseases such as powdery mildews
and multiplication of fungal spores of various pathogens and late blights occur (Coakley et al., 1999). Majority of the
(Agrios, 2005). At increased temperatures, pathogens get plant diseases are facilitated by environmental conditions
activated to cause an infection. Incidence of late blight of rainfall, elevated air humidity and increased availability
of potato and tomato, caused by Phytophthora infestans, of moisture in the soil. In general, the pathogenicity of
is increased under high availability of moisture and at pathogens that contaminate aerial tissues is highly facilitated
a temperature range lying between 7.2°C and 26.8°C. by rain and high atmospheric humidity. For example, the
The occurrence of pathogen Phytophthora cinnamomi virulence of Sclerotinia sclerotiorum enhances as atmospheric
on Eucalyptus sp. is highly elevated when the soil humidity is increased, with maximum development of disease
temperature is between 12-30°C (Podger et al., 1990). in lettuce plants as the RH crosses the mark of 80 per cent
• Sunlight influences pathogens as it leads to the hoarding (Clarkson et al., 2014).
up of phytoalexins in tissues of the host. Crop plants like Development of a disease can be assessed with an
wheat and oats are more vulnerable to rust pathogens important factor termed as leaf wetness. For instance, virulent
when CO2 and temperature get elevated (Coakley et al., pathogens such as Magnaporthe oryzae (rice blast fungus)
1999).
and Puccinia striiformis (stripe rust fungus) require at least 5
• For trilateral interactions, including a pathogen-relaying
hours of leaf wetness for disease and symptom development
vector, temperature affects disease occurrence by
(Magarey et al., 2005). Moreover, the chance for dew collection
influencing the vector. It is important for viruses, the
and as a result, pathogen infection is elevated at enhanced
predominantly of which are relayed by insects (Whitfield
temperatures. Pathogens such as Fusarium sp. and Aspergillus
et al., 2015). Also, the occurrence of viral and other
sp. under the influence of high humidity produce mycotoxins.
vector-borne diseases also gets modified. The higher
For instance, under high humidity, wheat plants infected by
temperature in winter increases the survivability of
F. graminearum (head blight fungus), produce mycotoxin
aphids; as a result, the incidence of Barley yellow dwarf
deoxynivalenol (Beyer et al., 2005 and Cowger et al., 2009).
virus (BYDV) increases and also increases the incidence
Increased water availability is favorable for foliar diseases
of viruses of potato (Thomas, 1989). For example,
Banana bunchy top virus (BBTV) that is further relayed and also for certain soil-borne pathogens such Pythium,
by Pentalonia nigronervosa has least death rate at 25°C Phytophthora, Sclerotium rolfsii and Rhizoctonia solani.
with maximum expansion (Robson et al., 2007) that is Infection initiated by Phytophthora capsici, development of
exactly the same temperature at which transmission of pathogen, and symptom development is greatest at almost
BBTV is most effective. 100% RH (Granke and Hausbeck, 2010). Reduced moisture
in soil is known to reduce the occurrence of infection of
Impact of Moisture Availability on plant diseases: Ralstonia solanacearum in tomato plants (Islam and Toyota,
• Moisture affects the commencement and expansion of 2004).

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 Environment-Pathogen Interaction in Plant Diseases

Influence of Climate Change on Vector-Borne Diseases: (Panchal and Melotto, 2017), as part of the plant defense
Both host plant and insect vector populations are influenced against bacterial entry into the leaf apoplast.
by environmental change and disperse the plant viruses • Panchal et al., (2016) showed that high humidity
(Jones, 2009). The likelihood of vector-borne disease in conditions blocked PTI-induced stomatal closure in
accordance to local and regional level is restricted by the both arabidopsis and bean plants. Likewise, PTI signaling
environmental needs of disease vectors (Malmstrom et al., can be altered by temperature changes (Vedukola
2011). Phenology of the host is also affected by environmental et al., 2019). In arabidopsis, short warm-temperature
change, thereby influencing its virus vulnerability. Global treatments (28°C for 15 minutes) induced higher PTI-
warming is known to impact the primary infection of the associated MAPK (mitogen-activated protein kinase)
host, the dispersal of the infection within the host and/or phosphorylation and PTI marker gene expression after
the horizontal relay of the virus to new hosts by the vector. PAMP exposure, suggesting that PTI may be enhanced
Variation in environment results in manifold effects on vectors at warm temperatures (Cheng et al., 2013).
like alteration of vector phenology, vector’s over-wintering, Environmental impact on Effector-triggered immunity (ETI)
stability, and its migration. The enhanced CO2 concentrations ETI is an important form of genetically controlled resistance
have indirect influence by changing the size and composition implied against plant pathogens. During ETI, a virulence-
of insects prey populations. Any variation either in host plant promoting pathogen effector or its activity inside plant cells is
or insect vector population due to environment change could sensed by a plant resistance (R) protein, most of which are NLR
spread plant viruses (Canto et al., 2008). (nucleotide-binding domain and leucine-rich repeat) proteins
Combined effect of environmental factors: (Jones et al., 2016). This recognition triggers a signaling
cascade that usually culminates in a hypersensitive response
For various fungal pathogens, the interaction of high
(HR), a type of programmed cell death thought to contain
temperatures and elevated humidity results in the
the pathogen at the site of infection (Mukhtar et al., 2016 and
development of optimum conditions for disease incidence
Thakur et al., 2019). In many pathosystems, high temperatures
(Clarkson et al., 2014). In arabidopsis, turnip mosaic virus
compromise ETI. For example, the tobacco N protein for the
(TuMV) when exposed to heat and drought infection results
resistance against tobacco mosaic virus (TMV) (Witham et al.,
in a maximum reduction in the growth of a plant as compared
1996), do not mount an effective ETI at temperatures higher
to each individual factor when brought into focus (Prasch and than 30°C. The suppressive effect of high temperature on ETI
Sonnewald, 2013). In case of disease caused by Botrytis cinerea is also evident in certain ‘autoimmune’ mutant plants in which
in grapes, relative humidity when reaches an approximation ETI and spontaneous cell death are constitutively activated.
of 100% and temperature range is between 20-25°C, and
these conditions are prerequisite for the development of Concept of emerging diseases
disease (Ciliberti et al., 2015). An emerging disease is defined as an indigenous expression
or group of expressions which are newly recognized or have
Environmental impact on PAMP-triggered immunity (PTI)
recently appeared in an area which increases rapidly in
• PTI is known to prevent proliferation of a large number of occurrence and severity (Daszak et al., 2003). It is represented
non-pathogenic microbial populations. Virulent bacterial by an initial development of an infection in a crop which
pathogens cause the leaf apoplast to be water-soaked as can result in disease epidemics. The continuous evolution
part of the infection cycle (Xin et al., 2016 and Schwartz of emerging pathogens particularly leads to the occurrence
et al., 2017). of new, virulent strains for plants. New crop varieties are
• Making leaves water-soaked in the apoplast under introduced in varying countries and are grown in large
high humidity lets PTI-inducing non-pathogenic monoculture plots. Also, the varieties and cultivars are
Pseudomonas bacteria to develop in host plants such as chosen basically on the basis of their productivity, without
Arabidopsis, bean, and tobacco plants. PTI is a mechanism taking into account their vulnerability to pathogens. These
in which conserved molecules of microbes (pathogen-or facilitative conditions stand to reason why the incidence of
microbe-associated molecular patterns, PAMP or MAMP, new diseases occur and thrive (Oliver and Solomon, 2008).
respectively) are recognized by plant plasma-membrane-
localized pattern recognition receptors (PRR). MAM Pathogen dispersion
recognition causes a signaling cascade that includes In accordance to various countries or areas, the occurrence of
protein phosphorylation, reactive oxygen species (ROS) emerging diseases elevates rapidly in a short period of time
production, Ca2+ concentration increases, and gene with greater emergence rates in certain countries than others,
activation that lead to halt of microbial growth (Couto and which might be as a result of an accumulation of favorable
Zipfel, 2016). Whereas under elevated humidity, stomata conditions (Daszak et al., 1999). Emerging pathogens are
open while ABA accumulation decreases (Okamoto et known to have an ability to infect a large number of host
al., 2009). PTI activation triggers the closure of stomata plants. For example, human pathogens have been known to
after the recognition of MAMPs by stomatal guard cells affect plants. Enterobacter cloacae is an example of a human

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 Environment-Pathogen Interaction in Plant Diseases

pathogen infecting plant hosts but is also a plant pathogen To respond, plants regulate defense molecules. For instance,
infecting onion (Allium cepa L.) in the USA (Bishop and Davis, in the interaction between avocado fruit and the fungus
1990). Colletotrichum gloesposporioides where the flavonoid
Xylella fastidiosa generally infects grape (Vitis vinifera epicatechin is modulated by the avocado fruit to protect
L.) but is known to be the causal organism of mulberry itself from the laccase protein produced by C. gloeosporioides.
leaf scorch in California (Hernandez-Martinez et al., 2007).
UV-B, O3, and CO2 involvement with Emergence
Raffaelea lauricola sp. nov. infects redbay (Persea borbonia).
Diseases:
The fungus and its transmitting vector, Xyleborus glabratus,
have their origin as Japan and Taiwan. The disease has also Ultraviolet B (UV-B), ozone (O3), and carbon dioxide (CO2)
occurred in the Southeastern USA since 2003 (Rabaglia et are environmental factors that have been designated in
al., 2006) but presently, the pathogen has been reported accordance to environmental change and the emergence
in Florida resulting in avocado wilt (Ploetz et al., 2012). of pathogens.
Candidatus Phytoplasma phoenicium sp. nov. bacterium causes Certain species show variable sensitivity to UV-B radiation;
witches´ broom in almond with its first time report in Lebanon while some may be negatively influenced, others may be
in the 1990s (Choueiri et al., 2001). Further, symptoms of tolerant. Paul, (2000) suggested that elevated UV-B after
almond witches´ broom were reported in Iran, along with inoculation lessened disease in wheat, as the influence
some genetic variability among the strains (Zirak et al., 2009). of direct UV-B damaged the pathogen. Similarly, bacteria
Tomato leaf curl New Delhi virus (ToLCNDV) was initially and fungi are generally more sensitive to damage by UV-B
reported on tomatoes in 1995 in India (Anonymous, 2016) radiation (Caldwell et al., 2007). As a result, researchers have
followed by other countries in Asia. After Spain, it was drawn a conclusion that environment change, with enhanced
reported from Tunisia in January 2015, causing a high rate solar UV-B, could expose plants to opportunistic pathogens
of infection on cucumber and melon. Puccinia graminis f. sp. as mentioned in the previous section.
tritici is known to be available in Uganda, Kenya, Ethiopia, Ozone (O3) influences pathogens and host plants
Sudan, Yemen, Iran, Tanzania, Eritrea, Rwanda, Egypt, South differently. Environment change has been associated neither
Africa, Zimbabwe, and Mozambique. It infects wheat. to emerging pathogen nor to changes in plant pathogenicity
However, a new virulent strain was observed in wheat fields in gene mutations. We currently have restricted information
Uganda in 1999, it was entitled Ug99. This new race surpassed regarding pathogen’s adaptability to climate change
the resistance provided by the gene Sr31. Relay, as in case of (Desprez- Loustau et al., 2007).
other rusts, is carried out by wind or by people carrying the Emergent Disease Dispersal:
fungus (Singh et al., 2011).
As soon as new pathogens emerge, an important threat is
Possible causes of Emerging Pathogens: their dispersal into new spatial distribution. The dispersal
• The microbe might have been endemic in the particular of plant pathogens takes place via momentary and long-
crop locality but discovered on a new host recently. distance dispersion pathways. Short-distance dispersal
• After flourishing as an endemic organism, it became includes human practices (grafting and pruning) and vectors
pathogenic, as a result of an enhancement in its virulence, (e.g., insects or humans) (Ashraf et al., 2014).
or due to increased susceptibility of host. Mitigation Strategies
• The pathogen’s introduction to a new locale along with
Various countries are developing strategies to reduce threats
unexposed hosts might be new.
by initiating regulatory measures to prevent, control, or
• Insect vectors feed upon new plants nurturing the
eradicate diseases caused by potential pathogens.
pathogen and relay the pathogen to other hosts.
Phytosanitary regulations are designed in order to
The occurrence of diseases is an outcome of manifold
prevent and eradicate pests affecting plants. For example,
factors such as interactions amongst other pathogens, host- quarantines to prevent or delay the movement of pests from
pathogen interaction, plant-vector-pathogen interaction, and areas where they are not known to exist, also, quarantines
variable environmental conditions. Environmental factors allow delayed introduction of pathogens into new areas until
could result in variation in the nature of microorganisms, risk evaluation has been carried out.
converting them into opportunistic pathogens. When
plants grow weak or are under stress due to climatic factors, C o n c lu s i o n
pathogens can easily colonize hosts, thereby causing host
• There is a need to evaluate current management
mortality (Moricca et al., 2016). Modifications in the plant- strategies and suggesting alternatives in order to get
pathogen interaction process and spatial distribution are prepared against the challenge of environment change so
also important criterions in the incidence of emerging as to allow the mitigation practices to be highly effective
pathogens. Pathogens use specialized secretion systems to and resilient to change.
make infectious proteins or produce specialized structures • Research needs to be carried out to study the influence
or produce toxins to penetrate plant cells. of environmental change on crop as well as disease

196 Agricultural Reviews, Volume 40 Issue 3 (July-September 2019)

 Environment-Pathogen Interaction in Plant Diseases

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