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Grey mould of strawberry, a devastating disease caused by the ubiquitous necrotrophic fungal pathogen Botrytis cinerea

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p>The fungal pathogen Botrytis cinerea causes grey mould, a commercially damaging disease of strawberry. This pathogen affects fruit in the field, storage, transport and market. The presence of grey mould is the most common reason for fruit rejection by growers, shippers and consumers, leading to significant economic losses. Here, we review the biology and epidemiology of the pathogen, mechanisms of infection and the genetics of host plant resistance. The development of grey mould is affected by environmental and genetic factors; however, little is known about how B. cinerea and strawberry interact at the molecular level. Despite intensive efforts, breeding strawberry for resistance to grey mould has not been successful, and the mechanisms underlying tolerance to B. cinerea are poorly understood and under-investigated. Current control strategies against grey mould include pre- and postharvest fungicides, yet they are generally ineffective and expensive. In this review, we examine available research on horticultural management, chemical and biological control of the pathogen in the field and postharvest storage, and discuss their relevance for integrative disease management. Additionally, we identify and propose approaches for increasing resistance to B. cinerea in strawberry by tapping into natural genetic variation and manipulating host factors via genetic engineering and genome editing.</p
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MOLECUL AR PL ANT PATHOLOGY
PUBLISHED BY BRITISH SOCIE TY FO R PLANT PATHOLOGY AN D JOHN
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MOLECULAR PLANT PATHOLOGY (2019) DOI: 10 .1111/m pp.12 79 4
1
Review
Grey mould of strawberry, a devastating disease caused by the
ubiquitous necrotrophic fungal pathogen
Botrytis cinerea
STEFAN PETRASCH1, STEVEN J. KNAPP1, JAN A. L. VAN KAN2 AND BARBARA BLANCO-ULATE 1,*
1 Department of Plant Sciences,University of California, Davis, Davis, CA USA
2 Laboratory of Phytopathology,Wageningen University, Wageningen, Netherlands
SUMMARY
The fungal pathogen
Botrytis
cinerea
causes grey mould, a com-
mercially damaging disease of strawberry. This pathogen affects
fruit in the field, storage, transport and market. The presence of
grey mould is the most common reason for fruit rejection by
growers, shippers and consumers, leading to significant eco-
nomic losses. Here, we review the biology and epidemiology of
the pathogen, mechanisms of infection and the genetics of host
plant resistance. The development of grey mould is affected by
environmental and genetic factors; however, little is known
about how
B. cinerea
and strawberry interact at the molecular
level. Despite intensive efforts, breeding strawberry for resist-
ance to grey mould has not been successful, and the mechanisms
underlying tolerance to
B. cinerea
are poorly understood and
under-investigated. Current control strategies against grey
mould include pre- and postharvest fungicides, yet they are gen-
erally ineffective and expensive. In this review, we examine avail-
able research on horticultural management, chemical and
biological control of the pathogen in the field and postharvest
storage, and discuss their relevance for integrative disease man-
agement. Additionally, we identify and propose approaches for
increasing resistance to
B. cinerea
in strawberry by tapping into
natural genetic variation and manipulating host factors via
genetic engineering and genome editing.
Keywords: disease management, fruit ripening, fruit-
pathogen interaction, plant breeding, plant defence, primary
infection, secondary infection.
INTRODUCTION
Strawberry (
Fragaria
×
ananassa
) is an important soft fruit crop
that is grown worldwide on more than 370 000 hectares (FAO
STAT, 2014) and, for the United States alone, the total value of
the annual strawberry production exceeds US$2.3 billion (USDA,
2016). Strawberries are beneficial to the human diet as a source
of macro- and micronutrients, vitamins and health promoting
antioxidants (Basu
et al.
, 2014; Giampieri
et al.
, 2015; Wang and
Lin, 2000).
Strawberry is a perennial herbaceous plant with short
stems (crowns) and densely spaced leaves. Strawberry pro-
duces complex accessory and aggregate fruit composed of
achenes and a receptacle (Darrow, 1966). Achenes are small
single-seeded fruit, whereas the receptacle is considered to be
anatomically equivalent to floral meristem tissue (Hollender
et al.
, 2012).
F
. ×
ananassa
is an allo-octoploid (2n = 8x = 56)
that originated as a synthetic hybrid between the octoploid
species
Fragaria chiloensis
and
Fragaria virginiana
(Bringhurst,
1990; Edger
et al.
2019; Darrow, 1966; Rousseau-Gueutin
et
al.
, 2008).
Strawberry is affected by several pathogens including fungi,
bacteria, viruses and nematodes. The most economically impact-
ful pathogens of strawberry are fungi, which can infect all parts of
the plant and cause severe damage or death (Garrido
et al.
, 2011).
Amongst the fungal pathogens, the ascomycete
Botrytis cinerea
is considered the primary pathogen of harvested strawberries in
the world leading to impactful economical losses to the straw-
berry industry.
B. cinerea
causes grey mould in fruit and senescing
organs but can also affect vegetative tissues (Fig. 1). Under wet
conditions, more than 80% of strawberry flowers and fruits can
be lost if plants are not sprayed with fungicides (Ries, 1995).
THE PATHOGEN
BOTRYTIS CINEREA
B. cinerea
has no apparent host specificity and can infect more
than 1000 plant species (Elad
et al.
, 2016). The pathogen is
found worldwide and causes disease in many fruit, flower
and leafy vegetable crops (Boff, 2001; Carisse, 2016; Elad
et
al.
, 2007).
B. cinerea
is classified as a necrotroph, meaning
that it prefers to infect and grow on damaged or senescing
*
Correspondence
: Email: bblanco@ucdavis.edu
bs_bs_banner
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2 S. PETRASCH
et al
.
tissues, eventually causing tissue death. The inoculum (e.g.
conidia) of the fungus is highly abundant and ubiquitous and
usually comes from infected plant tissues (Jarvis, 1962).
B.
cinerea
mainly enters the host via wounds or natural openings
(Holz
et al.
, 2007). Infections of non-senescing or unripe plant
organs usually lead to limited damage and quiescent infections
(Dewey and Grant-Downton, 2016; Jarvis, 1962). Different
types of quiescence have been described: (i) delay of conidia
germination or growth arrest after germination (Jarvis, 1994),
(ii) endophytic symptomless growth in the apoplast (Barnes
and Shaw, 2003; Sowley
et al.
, 2010), (iii) colonization of ab-
scising flower organs (e.g. petals) followed by growth into
ovaries or receptacles where growth arrests (Bristow
et al.
,
1986). Independent of the type of infection, the pathogen gen-
erally enters a short asymptomatic, biotrophic phase at the
beginning of the disease cycle (Veloso and van Kan, 2018). An
aggressive necrotrophic phase commonly succeeds the quies-
cent or asymptomatic phase once plant organs start to senesce
or ripen, during which
B. cinerea
causes rapid decay of the
infected tissues (Elad
et al.
, 2007).
B. cinerea
’s infection mechanisms have been studied in model
organisms and further characterized thanks to the availability of
high-quality reference genome sequences (Amselem
et al.
, 2011;
Van Kan
et al.
, 2017; Staats and van Kan, 2012). The fungus is
known to actively promote plant susceptibility by employing a
variety of virulence factors (Choquer
et al.
, 2007; Nakajima and
Akutsu, 2014; Petrasch
et al.
, 2019). In early stages,
B. cinerea
deploys sRNAs and effector proteins to suppress premature host
cell death and immune responses, which enables the fungus to
establish inside the host and accumulate biomass prior to the
necrotrophic phase (Veloso and van Kan, 2018). It was demon-
strated that
B. cinerea
Dicer-like proteins DCL1 and DCL2 produce
sRNAs that are secreted from fungal hyphae and translocated to
the plant cell where they interfere with the host RNAi mecha-
nisms to silence host immune response genes in
Arabidopsis
and
tomato leaves (Wang
et al.
, 2017b; Weiberg
et al.
, 2013).
Some secreted virulence factors can lead to host cell death,
like effector proteins, toxins and enzymes involved in reactive
oxygen species (ROS) production (Schumacher, 2016).
B. cinerea
can also secrete oxalic acid that lowers the pH of the host tissues
Fig. 1 Symptoms of
Botrytis cinerea
infections in strawberry. Panel A shows a senesced flower with
B. cinerea
mycelium grow th. Panel B shows an advanced
floral infection. Panels C and D show infections of fruit at different stages. An infected petal can be seen as the source of fruit infection in Panel D. Browning of
leaves due to
B. cinerea
infections is shown in Panels E and F.
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Botrytis cinerea – strawberry fruit pathosystem 3
and stimulates the production and activity of fungal enzymes like
pectinases, laccases and proteases (Fernández-Acero
et al.
, 2010;
Manteau
et al.
, 2003; Prusky and Lichter, 2007; Sharon
et al.
,
2007). Furthermore, oxalic acid accumulation leads to Ca2+ che-
lation, which in turn weakens the pectin structures of plant cell
walls and inhibits the deposition of callose (Chakraborty
et al.
,
2013). Other virulence factors are cell wall degrading enzymes
(CWDEs) that enable
B. cinerea
to cause plant cell lysis and
loosen walls to facilitate tissue penetration (Blanco-Ulate
et al.
,
2016a). The fungus is known to produce plant hormones or hor-
mone analogues that may disturb the host’s cellular metabolism
and immune responses. The relevance of these mechanisms for
the capacity of
B. cinerea
to infect strawberry remains unknown.
STRAWB ERRY-
BOTRYTIS CINEREA
PATHOSYSTEM
Grey mould in strawberries can result from
B. cinerea
infections
of open flowers (primary infections) or by penetration of fruit
receptacle tissues (secondary infections) (Bristow
et al.
, 1986).
In primary infections,
B. cinerea
infects flower organs during
or right after flowering, allowing hyphae to grow into the re-
ceptacle (Fig. 2). The sources of primary inoculum range from
overwintering sclerotia to conidia or mycelium from infected
neighbouring plants (Jarvis, 1962). Infected senescent petals,
stamens and calyxes can facilitate primary infections in fruit
(Powelson, 1960). Histological studies have shown that even
though styles are frequently infected, fungal growth appears to
be strongly inhibited and never reaches the receptacle. In con-
trast, fungal growth in colonized stamens can reach the recepta-
cle in some cultivars (Bristow
et al.
, 1986).
Following infection of the unripe receptacle by
B. cinerea
,
fungal growth is usually arrested and a symptomless quiescent
phase occurs. The mechanisms that lead to quiescent infections
are not yet fully understood. Proanthocyanins (PAs) appear to
induce
B. cinerea
quiescence in unripe fruit by restricting the
activity of fungal enzymes like polygalacturonases (PGs) that
are necessary for aggressive infection of hosts (50% inhibition
in unripe fruit compared to 8% inhibition in ripe fruit). Even
though PA content in fruit remains constant during ripening, in-
creasing polymerization of PAs leads to lower inhibitory activity
in ripe fruit (Jersch
et al.
, 1989). Similarly, anthocyanins might
delay
B. cinerea
infections or cause quiescence (van Baarlen
et
al.
2007). For instance, strawberries illuminated with white fluo-
rescent light showed increased anthocyanin content and delayed
Fig. 2
Botrytis cinerea
disease cycle in strawberry. Sources of
B. cinerea
inoculum include infected leaves and sclerotia. Primary infections of flowers and
secondar y infections of fruit are depicted.
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4 S. PETRASCH
et al
.
development of grey mould (Saks
et al.
, 1996). Reduced fruit
decay has also been observed in raspberries with high pigmen-
tation (Harshman
et al.
, 2014) and in transgenic tomatoes that
accumulate anthocyanins (Bassolino
et al.
, 2013; Zhang
et al.
,
2013). Other small phenolics, especially catechins, may have a
role in quiescence. High levels of catechins inhibit fungal growth,
and a decrease in catechins is correlated with a reduction of
other antifungal compounds such as lipoxygenases (Prusky and
Lichter, 2007). Interestingly, young and ripe fruit have low cat-
echin concentration, suggesting that initial infections of young
receptacles are possible because they do not yet accumulate
enough catechins to stop colonization (Puhl and Treutter, 2008).
B. cinerea
quiescence is complex and involves additional factors
besides the accumulation of phenolic compounds. It has been
proposed that quiescence in unripe fruit is initiated by: (i) lack
of nutrients such as sugars (e.g. mono- and disaccharides) from
the host, (ii) presence of preformed antifungal compounds, (iii)
unsuitable environment for fungal virulence factors (Prusky and
Lichter, 2007). In unripe strawberries, factors from all three cate-
gories are present, including lack of available sugars (Knee
et al.
,
1977), preformed antifungal compounds (Hébert
et al.
2002;
Terry
et al.
, 2004), and high activity of PG-inhibiting proteins
(PGIPs) (Mehli
et al.
, 2005). Induction of the necrotrophic phase
in ripe strawberries could be triggered by changes in biochemi-
cal composition of the host tissues associated with the ripening
process, such as increased sugar content, volatile production and
alteration of plant defences (Neri
et al.
, 2015; Prusky and Lichter,
2007). These modifications promote not only fungal growth but
also host susceptibility, e.g. via the release of oxalic acid and
efflux of toxins (Prusky and Lichter, 2007).
During secondary infections, the fungus initiates the necro-
trophic phase without quiescence (Holz
et al.
, 2007). The
sources of conidia for secondary infections can also be diverse,
from senescent leaves to infected fruit (Fig. 2). Conidia from
B. cinerea
-infected flower parts are major sources of secondary
inoculum (Bristow
et al.
, 1986). It has been estimated that more
than 64% of the strawberry infections result from organic frag-
ments that are in contact with the fruit, such as petals and
stamens (Fig. 1D; Jarvis, 1962). Contrary to other fruit (e.g. rasp-
berries), senescent flower parts often adhere to strawberries
long enough to retain water films for at least 8 h, which is the
time needed for
B. cinerea
conidia germination (Jarvis, 1962).
Secondary infections can also result from nesting, which cor-
responds to direct penetration of mycelia growing on neighbour-
ing plant organs such as infected leaves and fruit (Fig. 1F; Braun
and Sutton, 1988). Generally, secondary infections proceed rap-
idly and
B. cinerea
can complete its germination and infection as
fast as 16 h post-inoculation (hpi) with a rapid increase in fungal
biomass at 48 hpi (Fig. 3; Mehli
et al.
, 2005). Early responses
of strawberries to infection include higher expression of the de-
fence genes
FaPGIP
and
FaChi 2-1
(Class II Chitinase), whereas
lower expression of the reference gene DNA Binding Protein –
FaDBP
indicates extensive cell death induced by
B. cinerea
at late
stages of infection (Mehli
et al.
, 2005)
.
RELEVANCE OF RIPENING PROCESSES
TO
BOTRYTIS CINEREA
INFECTIONS OF
STRAWBERRIES
Fruit ripening influences the susceptibility of strawberry fruit to
B.
cinerea
(Fig. 4). Strawberries are mostly resistant to infection in
their unripe stage, where they restrict fungal growth by causing
quiescence. However, in the ripe stage, strawberries are highly
susceptible and decay rapidly. Fruit susceptibility to fung al disease
increases as ripening progresses; hence,
B. cinerea
appears to
promote susceptibility in unripe fruit by activating specific ripen-
ing-related processes (Blanco-Ulate
et al.
, 2016b). In tomato fruit,
master transcriptional regulators of ripening have been shown
to have different roles in disease susceptibility. For example, the
activity of the tomato transcription factor NON-RIPENING (NOR)
favours
B. cinerea
infection (Cantu
et al.
, 2009). Strawberries are
non-climacteric fruit with a ripening programme different from
that of climacteric tomatoes. Thus, a deeper understanding of
strawberry ripening regulation and how
B. cinerea
may modulate
particular ripening events are pivotal to characterize the dynam-
ics of the strawberry-
B. cinerea
pathosystem.
Recent transcriptomic studies of developing strawberries
point out that ripening events start between the ‘large green’
and ‘white’ stages, and involve changes in cell wall composi-
tion, sugar metabolism, hormone biosynthesis and responses,
pigmentation and antioxidant levels (Guo
et al.
, 2018; Sanchez-
Sevilla
et al.
, 2017; Wang
et al.
, 2017a). Moreover, a general
decrease of oxidative phosphorylation processes has been ob-
served during strawberry ripening (Sanchez-Sevilla
et al.
, 2017;
Wang
et al.
, 2017a). Normal strawberry ripening involves a vari-
ety of biochemical and physiological processes, some of which
are discussed below in the context of
B. cinerea
interactions.
Fig. 3 Progression of
Botrytis cinerea
infection in ripe strawberries.
Inoculation was performed by wounding the fruit and adding a
B.
cinerea
conidia suspension on the surface of the wound. Fruit are shown
immediately after inoculation, and at 24 h to 96 h post-inoculation (hpi).
Wounded controls are included.
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Botrytis cinerea – strawberry fruit pathosystem 5
Cell wall modifications
Ripening is associated with the disassembly of the fruit cell walls,
which leads to tissue softening. Cell wall degradation benefits
B. cinerea
as it reduces mechanical barriers to infection and
spread, increases the possibilities of bruising (e.g. leading to
more wounds for pathogen entry) and provides the fungus with
access to simple sugars as a carbon source (Blanco-Ulate
et al.
,
2016b; Blanco-Ulate
et al.
, 2016a; Brummel and Harpster, 2001).
In strawberry, cell wall solubilization occurs early in fruit
development when the walls start to swell (Knee
et al.
, 1977).
Cell wall solubilization correlates with an increase in fruit sugar
content, resulting from polysaccharide breakdown. A decrease
of acid-soluble pectins and the alcohol-insoluble fraction of cell
walls occur during ripening, whereas the water-soluble content
increases (i.e. enriched in non-covalent bound pectins). The
degree of pectin solubilization and depolymerization is highly-
related to strawberry fruit firmness (Rosli
et al.
, 2004). Silencing
of an endogenous pectin lyase (PL) gene in strawberry resulted
in fruit with higher external and internal firmness, mostly due
to low pectin solubilization, stiffer cell walls, and increased
cell to cell adhesion (Jimenez-Bermudez
et al.
, 2002; Santiago-
Domenech
et al.
, 2008). Besides PL, other enzymes that may
have affected strawberr y firmness include PGs, β-galactosidases,
endoglucanases, α-arabinofuranosidases and β-xylosidases
(Figueroa
et al.
, 2010).
In addition to the fruit endogenous cell wall disassembly,
B. cinerea
secretes an extensive array of CWDEs that target
most polysaccharides in the fruit cell walls, particularly pectins
(Blanco-Ulate
et al.
, 2016a). These CWDEs include fungal PGs,
such as
Bcpg2
, a gene that is mainly active in the early penetra-
tion stage (Mehli
et al.
, 2005). The expression of
B. cinerea
PGs
is dependent on the host species, the plant tissue, temperature
and the stage of infection (Blanco-Ulate
et al
. 2014; ten Have
et al.
, 2001).
Cuticle changes
Another barrier for
B. cinerea
infection is the fruit cuticle. During
fruit expansion and ripening the cuticle gets thinner, which
makes strawberries more susceptible to initial penetration by
germinating conidia.
B. cinerea
can penetrate the plant cuticle by
secretion of cutinases (van Kan, 2006). Additionally, cuticle prop-
erties can result in higher incidence of cracks and other damages
through which
B. cinerea
can enter the fruit without the need of
cutinases (Holz
et al.
, 2007). Studies on strawberry cuticles are
scarce and only exist for leaf tissues (Kim
et al.
, 2009). In tomato
fruit, thicker and stiffer cuticles lead to higher resistance to initial
Fig. 4 Ripening processes influence
Botrytis cinerea
infections of strawberries. Unripe fruit present unsuitable conditions for
B. cinerea
infection, while ripe
fruit provide a favourable environment for pathogen growth. Pathogenicity factors are activated by
B. cinerea
during strawberry ripening and lead to increased
susceptibility. ABA, abscisic acid; JA, jasmonic acid; PGIPs, PG-inhibiting proteins; ROS, reactive oxygen species.
MOLECULAR PL ANT PATHOLOGY (2019) © 2019 THE AUTHO RS. MOLECULAR PLANT PATHOLOGY PUBLISHED BY
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6 S. PETRASCH
et al
.
B. cinerea
infections. Moreover, it is known that the chemical
composition of the cuticle changes during tomato ripening, and
this is likely to be the case in strawberry (Isaacson
et al.
, 2009;
Kosma
et al.
, 2010).
Sugar accumulation
During ripening, the content of sugar in strawberries increases
and therefore can serve as nutrients for
B. cinerea
. In unripe
strawberries, the main sugars are glucose and fructose with
low concentrations of sucrose. Sucrose levels increase rapidly
during de-greening and red colouring (Jia
et al.
, 2011). In to-
mato, it has been shown that the
Cnr
mutant, which does not
accumulate high levels of sugars is still highly susceptible to
B. cinerea
infection (Blanco-Ulate
et al.
, 2016b). This observa-
tion suggests that even though sugars may serve as a suscep-
tibility factor, high sugar concentrations are not essential for
B. cinerea
infection. However, sugar content could still influ-
ence susceptibility to
B. cinerea
as specific sugars may serve
as ripening initiation signals. For instance, sucrose regulates
abscisic acid (ABA) levels in strawberries, which are necessary
for normal ripening and could influence fruit susceptibility as
described below (Blanco-Ulate
et al.
, 2016b; Jia
et al.
, 2011;
Li
et al.
, 2011). Like other ripening-related events,
B. cinerea
can alter neutral sugar and sugar acid levels in the infected
host tissues, mainly by degradation and depolymerization of
cell walls. This was reported for infections in tobacco and
Arabidopsis
leaves, where the fungus degrades pectins to
release the monosaccharide galacturonic acid (Zhang and van
Kan, 2013).
Plant hormone biosynthesis and signalling
ABA is the main hormone regulating and inducing ripening in
strawberries (Jia
et al.
, 2016; Li
et al.
, 2011). ABA biosynthesis
during fruit ripening is triggered by a decrease in pH, turgor
changes, sugar accumulation, and the switch of sugars from
mainly glucose and fructose to sucrose (Jia
et al.
, 2011; Li
et al.
, 2011). Effects of ABA on strawberry susceptibility to
fungal disease have not been extensively studied, but down-
regulation of the ABA biosynthetic gene β-glucosidase
FaBG3
has been reported to result in fruit with limited ripening and
higher
B. cinerea
resistance (Li
et al.
2013). In tomato, ABA
accumulation is related to higher pathogen susceptibility,
probably via activation of senescence (Blanco-Ulate
et al.
,
2013; Harrison
et al.
, 2011; Lee
et al.
, 2011). During strawberry
ripening, the increase of ABA is correlated with a decrease
of auxin, which induces early fruit growth and expansion
but is known to inhibit ripening processes (Jia
et al.
, 2011).
The role of auxin in fruit susceptibility seems to depend on
the plant species, as indole acetic acid (IAA) treatment in
Arabidopsis
leads to susceptibility, whereas IAA-treated
tomato leaves and eggplant fruit show lower infection sever-
ity (Savatin
et al.
, 2011; Sharon
et al.
, 2007). Ethylene has
a secondary organ-specific role in strawberry ripening, par-
ticularly in achenes and green and white receptacles (Knee
et al.
, 1977; Merchante
et al.
, 2013). Ethylene increases the
susceptibility of tomato to
B. cinerea
by inducing ripening;
however, its functions during strawberry infections are yet to
be fully characterized. ABA, IAA and ethylene accumulation
are altered by polyamine levels, which are positively corre-
lated with fruit susceptibility to
B. cinerea
during strawberry
ripening (Guo
et al.
, 2018). Other hormones, such as brassi-
nosteroids (BRs) and jasmonic acid (JA) are present at lower
levels during strawberry ripening. BR positively regulates
vitamin C levels, sugar and anthocyanin biosynthesis during
ripening, while negatively regulating acidity and concentra-
tion of other phenolic compounds (Ayub
et al.
, 2018). JA acts
synergistically with ethylene by activating its biosynthesis in
strawberries (Mukkun and Singh, 2009). Endogenous JA lev-
els are modulated by methyl jasmonate (MeJA) and the JA
carboxyl methyltransferase that lead to high levels in white
fruit and a decline during ripening, antagonistically to ABA
(Garrido-Bigotes
et al.
, 2018; Preuß
et al.
, 2014). In straw-
berry, JA appears to be involved in defence responses against
B. cinerea
. For example, strawberries treated with MeJA had
a delayed and much slower progression of
B. cinerea
infec-
tions (Saavedra
et al.
, 2017; Zhang
et al.
, 2006).
HIJACKING OF RIPENING REGULATION BY
BOTRYTIS CINEREA
As indicated previously,
B. cinerea
releases enzymes and
metabolites that act as virulence factors but may also induce
plant responses that are beneficial for fungal infection (van Kan,
2006). A relevant example of the manipulation of physiological
processes in the host by
B. cinerea
is the interference with spe-
cific developmental processes. In tomato plants,
B. cinerea
infec-
tions modified host gene expression to increase susceptibility,
such as the induction of senescence in leaves (Swartzberg
et al.
,
2008). Moreover, infected unripe tomato fruit show premature
expression of genes involved in ethylene synthesis during tomato
ripening (Blanco-Ulate
et al.
, 2013; Cantu
et al.
, 2009). These
findings suggest that
B. cinerea
could initiate ethylene produc-
tion and thereby stimulate early ripening. As strawberries are
non-climacteric fruit, ethylene production of
B. cinerea
may not
have substantial effects on strawberry ripening; however, the
fungus was also shown to induce genes involved in the biosyn-
thesis of other plant hormones such as ABA . Moreover,
B. cinerea
can synthesize and secrete ABA that functions as a virulence fac-
tor (Siewers
et al.
2004, 2006). Besides hormones, increased oxi-
dative reactions caused by the pathogen may influence ripening
progression (Bianco
et al.
, 2009; Wang
et al.
, 2017a).
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Botrytis cinerea – strawberry fruit pathosystem 7
MECHANISMS OF DEFENCE AND AVOIDANCE
AGAINST
BOTRYTIS CINEREA
Defence mechanisms can be divided into preformed and in-
duced defences. In strawberries, preformed defence com-
pounds are especially abundant in the unripe stage, as
reviewed in the section on quiescence of
B. cinerea
. Even
though plants accumulate defence compounds,
B. cinerea
has mechanisms to cope with these metabolites by efflux and
detoxification of inhibitory substances. ATP-binding cassette
(ABC) transporters are used by
B. cinerea
to facilitate the ef-
flux of antifungal compounds, such as stilbenes (Schoonbeek
et al.
, 2002; Schoonbeek
et al.
, 2001).
B. cinerea
is capable of
detoxifying inhibitory substances, like epicatechin by secretion
of laccases (Amil-Ruiz
et al.
, 2011; Staples and Mayer, 1995).
Active
B. cinerea
infections can result in a reduction of spe-
cific secondary metabolites. It has been reported that levels
of flavan-3-ol, benzoic acid and phenylpropanoids drop in
B.
cinerea
-infected strawberries (Nagpala
et al.
, 2016).
Strawberries respond to
B. cinerea
infection by trigger-
ing defences. In some cases, preformed and induced defences
can overlap such as in the case of PGIPs. An endogenous PGIP
appears to be constitutively expressed in fruit from various
strawberry cultivars (Mehli
et al.
, 2004). However, this PGIP and
six additional ones show higher expression levels upon infec-
tion with
B. cinerea
(Schaart
et al.
, 2005). Overexpression of
FaPGIP1a
and
FaPGIP2a
in cisgenic plants conferred enhanced
resistance to grey mould (Schaart, 2004). Other enzymes induced
by
B. cinerea
infections are chitinases. Expression of the chiti-
nases
FaChi2-1
and
FaChi2-2
peaked 16 hpi in
B. cinerea-
infected
strawberries (Mehli
et al.
, 2005). Furthermore, heterologous
expression of
Phaseolus vulgaris
chitinase cH5B in strawberry
resulted in higher resistance to infection (Vellicce
et al.
2006).
Another study demonstrated that application of heat-inactivated
cells of the yeast
Aureobasidium pullulans
promoted tolerance to
B. cinerea
in strawberries (Adikaram
et al.
, 2002). This primed
resistance is probably due to the fruit’s perception of chitin from
the yeast leading to induction of chitinases or other plant immune
responses. Moreover, fruit defence responses may be primed
using mechanical stimulation as it was reported for strawberry
leaves (Tomas-Grau
et al.
, 2017 ).
Induced defences include accumulation of secondary metab-
olites and ROS. For instance, strawberries accumulate proantho-
cyanins around infection zones possibly to restrict fungal growth
(Feucht
et al.
, 1992; Jersch
et al.
, 1989). The surroundings of
infection sites generally display higher ROS production (Tomas-
Grau
et al.
, 2017). ROS can serve as an effective defence against
pathogens but also can lead to cell death, which is considered
beneficial for necrotrophic fungi (Prusky and Lichter, 2007).
B. cinerea
itself produces ROS to induce host cell death, deplete
plant antioxidants and increase lipid peroxidation (van Kan,
2006). It is therefore interesting that, in unripe tomato fruit ROS
production leads to resistance against
B. cinerea
, whereas in ripe
fruit it seems to promote susceptibility (Cantu
et al.
, 2008, 2009).
Future research will likely shed more light on the role of ROS in
induced defences of strawberry fruit.
Basal immunity is activated upon fungal infection.
Degradation of fruit cell wall pectins can produce demethyl-
ated oligogalacturonides that trigger basal immune responses
(Amil-Ruiz
et al.
, 2011). Expression of the
F. x ananassa
pectin
methylesterase 1
FaPE1
in
Fragaria vesca
resulted in reduced
methyl-esterification of oligogalacturonides in fruit. This
reduced esterification activated basal defences via the salicylic
acid (SA) signalling pathway that led to a higher resistance to
B. cinerea
(Osorio
et al.
, 2011). Involvement of SA signalling in
responses against
B. cinerea
was previously suggested when
strawberry plants and fruit treated with SA showed decreased
postharvest decay (Babalar
et al.
, 2007).
B. cinerea
can suppress
the expression of plant defence responses by hijacking the host
sRNA regulatory pathways (Weiberg
et al.
, 2013). In strawberry
fruits,
B. cinerea
infections c an alter the expression of microRNAs
involved in the regulation of defence genes, including the plant
intracellular Ras group-related LRR protein 9-like gene (Liang
et al.
2018). Interestingly,
B. cinerea
can also take up plant
sRNAs during its interaction with the host. For instance, trans-
genic plants expressing sRNA that targets
B. cinerea
DCL1 and
DCL2 show significantly reduced fungal growth in strawberries
(Wang
et al.
, 2016). The suppression of fungal growth via host
sRNA is not well understood, and it is yet to be demonstrated
that this mechanism of defence naturally occurs in plants.
VARIATION OF QUANTITATIVE RESISTANCE
TO
BOTRYTIS CINEREA
IN STRAWBERRY
The diverse arsenal of infection mechanisms employed by
B. ci-
nerea
explains its extremely wide-host range. It is therefore not
surprising that entirely resistant strawberry genotypes do not
exist (Bestfleisch
et al.
, 2015; Bristow
et al.
, 1986). Several au-
thors have analysed field resistance of strawberries to
B. cinerea
by quantifying disease development without artificial inocula-
tion. A multi-year study of three strawberry cultivars found a
significant effect of year, cultivar and cultivar by year interaction
on the incidence of
B. cinerea
infections (Rhainds
et al.
, 2014,
2002). Moreover, there was a positive correlation between row
density and disease. Other studies investigated field resistance in
annual winter production systems and found that variation of
B.
cinerea
incidence between years was larger than genotype dif-
ferences within years (Chandler
et al.
, 2004; Seijo
et al.
, 2008).
Even though field resistance assessments investigate conditions
similar to commercial production, considerable variability be-
tween environmental conditions and years can interfere with the
detection of genotype differences.
MOLECULAR PL ANT PATHOLOGY (2019) © 2019 THE AUTHO RS. MOLECULAR PLANT PATHOLOGY PUBLISHED BY
BRITISH SOCIET Y FOR PLANT PATHOLOGY AND JOHN WILEY & SONS LTD
8 S. PETRASCH
et al
.
Due to the confounding effects of different non-genetic vari-
ables in field studies, assessment of postharvest resistance to
B. cinerea
infections has been pursued to determine genotype
differences between strawberry cultivars or species. A large
study of grey mould development during postharvest storage of
non-inoculated fruit reported variation in disease incidence and
speed of progression amongst cultivars, but no complete resis-
tance was observed (Lewers
et al.
, 2012). Another approach to
reducing environmental effects in disease tests is to inoculate
fruit with
B. cinerea
conidia suspensions. Bestfleisch
et al.
(2015)
tested quantitative resistance in 107 accessions of wild and cul-
tivated strawberry. In this study, two wild ecotypes of
F. virgin-
iana
showed high resistance to
B. cinerea
infections and slow
disease progression. Such high tolerance in wild species was also
reported in
B. cinerea
-inoculated leaves and fruit of
F. chiloensis
accessions from Chile (González
et al.
, 2009). In these wild ac-
cessions,
B. cinerea
grew much slower. Comparative studies of
disease progression indicated that fruit from the cultivar Chandler
developed lesions at 24 hpi, while fruit from an
F. chiloensis
eco-
type developed symptoms at 72 hpi (González
et al.
, 2013). Fruit
were entirely covered with mould at 6 days post-infection (dpi)
for the cultivar Chandler and at 9 dpi for the
F. chiloensis
ecotype.
Considering that some accessions, particularly wild ecotypes,
show reduced grey mould incidence and progression, there
might be genetic sources of resistance against
B. cinerea
that
could be used to increase resistance in strawberry. However,
information about resistance mechanisms is mostly based on
assumptions or empirical data. Differences in ripening patterns
have been suggested as a potential explanation for resistance.
For instance, some strawberries ripen from inside to outside,
leaving the skin, which is the entry point of infections, unripe and
thus resistant for a longer time (Jersch
et al.
, 1989). Some more
tolerant cultivars remain white or unripe around the calyx (white
shoulders), which is where many
B. cinerea
infections tend to
initiate. Another mechanism of resistance could be the presence
of fungal inhibitors or the induction of PR proteins.
FcPR5
and
FcPR10
are highly induced in resistant
F. chiloensis
accessions
when compared to commercial
F. x ananassa
cultivars (González
et al.
, 2013). Based on sequence homology,
FcPR5
probably pos-
sesses antifungal activity, and
FcPR10
is likely a ribonuclease.
These findings reflect that even though efforts have been made
to explore resistance mechanisms of strawberry to
B. cinerea,
very little is known. Therefore, more research is necessary to
better understand the biology of strawberry interactions with
B.
cinerea
infections using diverse germplasm accessions.
CURRENT AND NEW MANAGEMENT
APPROACHES FOR
BOTRYTIS CINEREA
IN
STRAWBERRY PRODUCTION
Many disease management strategies have been implemented
for the control of
B. cinerea
in strawberry as further described
below. However, even combined approaches are only capable of
reducing disease incidence and severity but cannot completely
prevent or eliminate grey mould in strawberries (Feliziani and
Romanazzi, 2016).
Agronomic and horticultural practices
Historically,
B. cinerea
infections in strawberry production have
been managed by agronomic and horticultural practices, such as
removal of senescent plant material to avoid inoculum buildup
(Daugaard, 1999). Preventing contact of fruit with soil (e.g. cover-
ing the planting beds with polyethylene foils) is another common
practice to avoid
B. cinerea
infections, as most of the inoculum
is present on the ground and soil moisture promotes conidia ger-
mination (Daugaard, 1999). Selecting the right irrigation system
could help reduce grey mould incidence; mainly, the use of drip
irrigation and micro-sprinklers results in limited inoculum spread
and reduction of water films on the fruit (Dara
et al.
, 2016; Terry
et al.
, 2007). As canopy characteristics influence microclimates
(e.g. humidity, airflow, contact between plants), nitrogen fer-
tilization can lead to dense canopies and favour grey mould
(Daugaard, 1999). Similarly, shorter plant spacings promote
higher incidence of
B. cinerea
in the field (Legard
et al.
, 2005).
Additionally, plastic tunnels can avoid airborne inoculum and
B.
cinerea
incidence is lower in non-fungicide treated tunnels than
in fungicide treated fields (Xiao
et al.
, 2001), but tunnels favour
powdery mildew and complicate harvest. In summary, cultural
practices are essential to limit preharvest
B. cinerea
infections of
strawberries, especially in organic agriculture.
Fungicides
In modern production, pesticide applications are the most com-
mon management practice for
B. cinerea
control (see Table 1).
In the previous two decades, the main pesticides used in straw-
berry production against
B. cinerea
belonged to the Fungicide
Resistance Action Committee (FRAC) Groups 1 and 2, as well
as captan (Sutton, 1990; Wedge
et al.
, 2007, 2013). However,
due to increasing fungicide resistance and new legal restrictions,
producers have been forced to diversify their fungicide regimen
(Vellicce
et al.
, 2006; Wedge
et al.
, 2013). The frequency and
timing of fungicide applications are crucial for
B. cinerea
control.
One application of fenhexamid (FRAC 17) at anthesis can be as
efficient as multiple weekly applications (Mertely
et al.
, 2002).
Additionally, alternation and combination of different fungicides
with different modes of action are recommended (Wedge
et al.
,
2007).
Resistance of
B. cinerea
to fungicides is a real challenge in
horticulture and fungicide resistance profiles can shift consid-
erably even within a single season (Cosseboom
et al.
, 2019;
Konstantinou
et al.
, 2015; Leroch
et al.
, 2013; Wedge
et al.
,
2007). A screen of 13
B. cinerea
isolates in Louisiana (USA)
© 2019 THE AUTHORS. MOLECULAR PL ANT PATHOLOGY PUBL ISHED BY BRI TISH SOCIETY F OR PLANT PATHOLOGY AND JOHN
WILEY & SONS LTD MOLECULAR PLAN T PATHOLOGY (2019)
Botrytis cinerea – strawberry fruit pathosystem 9
showed that all were partial to full resistance to FRAC 1 fungi-
cides, and several of the isolates also had different levels of resis-
tance to FRAC 2 fungicides (Wedge
et al.
, 2013). A larger survey
of 1890
B. cinerea
isolates (189 fields in 10 states of the USA)
revealed that 7 isolates from different locations were resistant to
all single-action site FRAC fungicides groups that are registered
for
B. cinerea
control (Fernández-Ortuño
et al.
, 2015).
B. cinerea
resistance to fungicides is usually associated with overexpression
of efflux transporters or with modification of fungicide targets.
These resistance mechanisms are acquired via mutations and
recombination that occur frequently in
B. cinerea
due to heter-
okaryosis, sexual reproduction and the presence of abundant
transposable elements in its genome (Konstantinou
et al.
, 2015).
Efflux of fungicides or accumulation of altered fungicide targets
has also been shown to lead to multi-resistances (Konstantinou
et al.
, 2015; Rupp
et al.
, 2017). The presence of resistant isolates
against the most common multi-action site fungicides reinforces
the need for innovative management practices. A new genera-
tion of RNA-based fungicides has been proposed, which relies
on the application of sRNA or dsRNAs that target
B. cinerea
vir-
ulence genes to reduce fungal infections in strawberries (Wang
et al.
, 2016). However, these RNA-based fungicides remain far
from commercialization, which is why fungicide resistance man-
agement such as mixture and rotation of different fungicides or
testing local isolates for resistance is necessary (Hahn, 2014).
Biological control
To date,
B. cinerea
biocontrol products are mostly
Bacillus sub-
tilis
-based, but their use in commercial strawberry production is
limited because of their insufficient applicability in the field or
supply chain (Pertot
et al.
, 2017). Nevertheless, there is social
and scientific interest in using biocontrol against
B. cinerea
as
an alternative to chemical pesticides. Isolates of
Colletotrichum
gloeosporioides, Epicoccum purpurascens, Gliocladum roseum,
Penicillium sp., Trichoderma sp.
have displayed high efficiency in
controlling
B. cinerea
and were reported to reduce grey mould
incidence on strawberry stamens by 79%–93% and on fruit by
48%–76% (Peng and Sutton, 1991). Interestingly, in some exper-
iments, the efficiency of biocontrol by these organisms exceeded
the efficacy of control via the fungicide captan. Similar results
were obtained for other microbes, such as the yeasts
A. pul-
lulans
(Adikaram
et al.
, 2002) and
Candida intermedia
(Huang
et al.
, 2011), the filamentous ascomycete
Ulocladium atrum
(Boff, 2001; Boff
et al.
, 2002a, 2002b), or the bacterium
Bacillus
amyloliquefaciens
(Sylla
et al.
, 2015).
Biocontrol via microbes can work via different modes of
action, including competition for nutrients, secretion of anti-
biotic compounds and induction of host defence mechanisms
like the up-regulation of chitinase and peroxidase activity
(Adikaram
et al.
, 2002; Ippolito
et al.
, 2000; Lima
et al.
, 1997;
McCormack
et al.
, 1994). Because biocontrol of
B. cinerea
Table 1 Registered fungicides for control of
Botrytis cinerea
in strawberry production.
FRAC code FRAC group Target site Target action Risk of resistance Example
FRAC 1 Benzimidazoles β-tubulin assembly in
mitosis
Cytoskeleton High Benomyl
FRAC 2 Dicarboximides MAP/histidine kinase in
osmotic signal
transduction (os-1,
Daf1)
Signal transduction Medium to high Iprodione
FRAC 7 Succinate dehydro-genase
inhibitors
Succinate
dehydrogenase
Respiration Medium to high Boscalid
FRAC 9 Anilinopyrimidines Methionine synthesis Amino acid and protein
synthesis
Medium Cyp rodinil
FR AC 11 Quinone outside inhibitors Cytochrome BC1 at Qo
Site
Respiration High Azoxystrobin
FR AC 12 Phenylpyrroles MAP/histidine kinase in
osmotic signal
transduction (os-2,
HOG1)
Signal transduction Low to medium Fludioxonil
FR AC 17 Sterol biosynthesis
inhibitors class III
3-Keto reductase in C4
de-methylation
Inhibition of sterol
biosynthesis in
membrane
Low to medium Fenhexamid
FRAC M03 Dithiocarbamates and
relatives
Multi-site mode of action Low Thiram
FRAC M0 4 Phthalimides Multi-Site Mode of Action Low Captan
MOLECULAR PL ANT PATHOLOGY (2019) © 2019 THE AUTHO RS. MOLECULAR PLANT PATHOLOGY PUBLISHED BY
BRITISH SOCIET Y FOR PLANT PATHOLOGY AND JOHN WILEY & SONS LTD
10 S. PETRASCH
et al
.
relies on a variety of mechanisms, the most significant effects
are observed when different organisms are applied in combi-
nation (Sylla
et al.
, 2015; Xu and Jeger, 2013). As alternative
to applying living microbes, use of extracts or volatiles derived
from biocontrol microbes has been suggested (Huang
et al.
,
2011). Use of non-synthetic antifungal substances, like phe-
nol-rich olive oil mill wastewater, has also been reported to
control
B. cinerea
growth
in vitro
and on strawberries (Vagelas
et al.
, 2009). However, these approaches are not implemented
on a commercial scale due to high costs compared to the con-
ventional
B. cinerea
control
Postharvest treatments
It is common practice to handpick strawberries and place them
into clamshells in the field, in order to reduce wounding and
bruising of the fruit. Rapid and constant cooling of strawber-
ries at temperatures below 2.5 ºC is another critical strategy to
reduce or inhibit reactivation of
B. cinerea
quiescent infections
(Nunes
et al.
, 1995). Often, strawberries are also stored in modi-
fied atmospheres, which are generally low in oxygen and high in
carbon dioxide to slow down metabolic processes, senescence
and fungal decay (Feliziani and Romanazzi, 2016). Relative hu-
midity during storage is usually kept around 85%–90% to pre-
vent dehydration of fruit, but limit fungal growth (Almeida
et al.
,
2015).
Novel postharvest treatments of strawberries have been sug-
gested to prevent
B. cinerea
infections during storage. Examples
are edible fruit coatings of chitosan, silk fibroin or methylcel-
lulose that prevent water loss and can include antifungal com-
pounds (Marelli
et al.
, 2016; Nadim
et al.
, 2015; Romanazzi
et al.
, 2017). MeJA treatment to induce fruit defence mechanisms
(Zhang
et al.
, 2006), ultraviolet and visual light treatment (Saks
et al.
, 1996), enrichment of storage atmosphere with chlorine or
ozone (Avis
et al.
, 2006; Nadas
et al.
, 2003), and soft mechanical
stimulation (Tomas-Grau
et al.
, 2017) have also been tested as
alternative treatments. Most of these approaches are still in an
experimental stage or not yet adaptable to commercial settings.
LOOKING INTO THE FUTURE: IMPROVING
STRAWBERRY RESISTANCE TO
BOTRYTIS
CINEREA
Several aspects of the genetics of resistance to
B. cinerea
are
unclear in strawberry. Significant phenotypic variation of inci-
dence or severity of grey mould has been reported; however,
F
. x
ananassa
genotypes appear to be universally susceptible
and complete resistance has not been observed (Bestfleisch
et al.
, 2015). Substantial genotypic variation has not been
documented and the heritability of resistance to
B. cinerea
is
unknown. Mild phenotypic differences in fruit resistance levels
reported in various postharvest studies (Bestfleisch
et al.
, 2015;
Lewers
et al.
, 2012) indicate that genetic variation for resistance
may be limited and that its heritability is low. A contributing fac-
tor is the intrinsic characteristics of the pathogen, its broad host
range, diverse ways of infection and necrotrophic lifestyle, which
explain the abse nce of a gene-for-gene resist ance of strawberry to
B. cinerea
(Amil-Ruiz
et al.
, 2011). Therefore, breeding for escape
and tolerance, which includes physiological and biochemi-
cal traits, is a more practical option (Elad and Evensen, 1995).
While limited in scale and scope, earlier studies strongly sug-
gest that the incidence and progression of
B. cinerea
infections
differ between cultivars with soft fruit and those with firm fruit
(Barritt, 1980; Gooding, 1976). Hence, previously reported dif-
ferences amongst cultivars could be the result of the pleiotropic
effects of selection for increased fruit firmness and shelf life and
the associated developmental and ripening changes, as opposed
to direct genetic gains in innate resistance to the pathogen.
As discussed, fruit firmness is an important trait associated
with resistance to
B. cinerea
(Hancock
et al.
, 2008; Terry
et al.
,
2004). The strawberry germplasm displays natural variation for
fruit firmness and developing cultivars with firmer fruit is an
important aim in breeding programmes (Hummer
et al.
2011;
Salentijn
et al.
, 2003). Changes in flower morphology could also
enhance tolerance to
B. cinerea
. In strawberry, most
B. cinerea
infections in fruit appear to originate from primary infections of
flowers or secondary infections caused by direct contact with
infected flower parts (Bristow
et al.
, 1986; Jarvis, 1962; Powelson,
1960). It was reported that removal of stamen and petals result in
lower grey mould incidence (Jersch
et al.
, 1989; Powelson, 1960).
Faster abscission of flower parts, especially petals, has the po-
tential to aid the escape of strawberries from
B. cinerea
infec-
tions (Elad and Evensen, 1995). Similarly, plants with pistillate
flowers (i.e. flowers with pistils but no stamen) have a lower grey
mould incidence in fruit (Bristow
et al.
, 1986; Elad and Evensen,
1995).
B. cinerea
growth inhibition in stamens is reported to vary
within the strawberry germplasm, potentially due to differences
in their biochemical composition (Bristow
et al.
, 1986). Similarly,
antifungal compounds in fruit can prevent or limit
B. cinerea
infections. Several reports indicate that anthocyanin accumula-
tion contributes to tolerance of strawberries to
B. cinerea
(Jersch
et al.
, 1989; Saks
et al.
, 1996). Anthocyanins do not just improve
tolerance to grey mould but also provide health benefits (Terry
et al.
, 2004). Breeding for higher anthocyanin content in straw-
berries is possible and facilitated by existing variation in the ger-
mplasm (Fredericks
et al.
, 2013; Jing, 2012). Inducing anthocyanin
accumulation in flowers could also help to limit flower infections.
As breeding for higher
B. cinerea
tolerance will be tedious
and likely will not result in complete resistance, complemen-
tary approaches should be considered. Currently, no genetically
modified strawberry cultivars are commercially grown; however,
© 2019 THE AUTHORS. MOLECULAR PL ANT PATHOLOGY PUBL ISHED BY BRI TISH SOCIETY F OR PLANT PATHOLOGY AND JOHN
WILEY & SONS LTD MOLECULAR PLAN T PATHOLOGY (2019)
Botrytis cinerea – strawberry fruit pathosystem 11
several reports show great potential to improve tolerance to grey
mould via trans- or cis-genesis. For example, the expression of
chitinases or PGIPs from other organisms in strawberries can
prevent or slow down fungal infections (Powell
et al.
, 2000).
Another potential transgenic approach is to increase fruit firm-
ness by altering the expression or activity of pectin degrading
enzymes, such as PL or PG (Jimenez-Bermudez
et al.
, 2002). The
existing natural variation of PL expression levels and activity
in the cultivated strawberry germplasm could be used for cis-
genic approaches. Increasing phenolic levels in strawberries by
genetic modifications can also be explored as the transcription
factor MYB10 was identified as a regulator of anthocyanin levels
in strawberries (Lin-Wang
et al.
, 2010; Lin-Wang
et al.
2014);
Medina-Puche
et al.
, 2014). Transgenic plants (both
F. x anan-
assa
and
F. v esca
) with ectopic overexpression of MYB10 show el-
evated anthocyanin levels throughout the entire plant (Lin-Wang
et al.
, 2010); however, the resistance of these plants against
B.
cinerea
have not been tested. In summary, these novel breeding
approaches should be supported by integrative management
strategies including horticultural and agronomic practices,
and potentially biocontrol, to achieve maximum control of the
disease.
CONCLUSION
Many details about grey mould of strawberries are still poorly
understood. Future research is necessary to characterize the ge-
netic pathways and biochemical components that are involved
in strawberry-
B. cinerea
interactions. Molecular analyses of the
infection process and the physiological causes for the failure of
host defences should provide a basis to develop robust solutions
against the disease, or at least provide information for control
strategies that are likely to fail and therefore be discouraged.
Furthermore, current disease management needs to be re-eval-
uated to cope with increasing restrictions and lack of efficacy of
fungicides. Investigations on biocontrol approaches and pre- and
postharvest treatments are necessary to manage grey mould.
On the other hand, breeding for escape and tolerance against
B. cinerea
can be a feasible approach for commercial varieties.
Research on genetic modifications of strawberry that restrict
B.
cinerea
infections could also be used for guiding conventional
breeding efforts or developing new varieties once the market is
ready for their acceptance.
ACKNOWLEDGEMENTS
We would like to acknowledge Casper van den Abeele and Pedro
Bello for contributions with the images in Figures 1 and 3. We
thank Jaclyn A. Adaskaveg and Nancy Nou Her for their review
of the manuscript’s narrative.
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... The necrotrophic fungus B. cinerea is considered the most important post-harvest pathogen of strawberries, causing significant losses for the industry and producers, since annual economic losses worldwide tend to exceed US$ 10 billion [4,5]. In this context, B. cinerea was classified as the second most important phytopathogenic fungus in the world, based on its effects on many plant species, causing the as known as "gray mold" or "gray rot" [6]. ...
... B. cinerea produces pectinases (polygalacturonase), cellulase and xylanase enzymes, responsible for cell wall degradation, however, fortunately, this species does not produce toxins, given its role in the production of special wines [4,8]. ...
... Disease cycle caused by Botrytis cinerea in strawberries. Source: Extracted from Petrasch et al.[4]. ...
Article
This work aimed to carry out a literature review of the deterioration of strawberries by gray mold, covering the main responsible fungus, Botrytis cinerea, in addition to causes, failures, and recently studied strategies for postharvest control. It was observed that the main post-harvest control strategies with promising results were the application of essential oils, antifungal lamps, active packaging/films, emerging techniques (O3 and high-CO2), and antifungal compounds synthesized by bacteria. However, some strategies may have some disadvantages, such as essential oils, which can impart undesirable odors and flavors to fresh fruits, while the use of emerging technologies requires greater financial investment. In this sense, applications that allow the use of commercially available lamps and the production of active coating/films, have more potential to be applied, considering the effectiveness of inhibiting the growth of Botrytis cinerea and the cost of implantation.
... The fruit are highly appreciated for their flavor and nutritional values (Ulrich et al., 1997;Wang and Lin, 2000;Giampieri et al., 2015). However, strawberry cultivation is often hampered by the occurrence of numerous pests and diseases, including the necrotrophic fungus Botrytis cinerea, resulting in gray mold of fruit and leaves and, as such, causing huge production and economic losses (Petrasch et al., 2019). B. cinerea is mainly controlled by fungicides. ...
... The induced defense response of strawberry leaves and fruit against B. cinerea has been well-documented (Jersch et al., 1988;Nagpala et al., 2016;Bui et al., 2019;Haile et al., 2019;Hu et al., 2019;Petrasch et al., 2019). However, while it is clear that constitutive resistance mechanisms also play a role in the resistance of strawberry against B. cinerea, a comprehensive view on the underlying mechanisms is lacking. ...
... Gray mold caused by B. cinerea leads to substantial economic losses worldwide . B. cinerea can infect multiple parts of the strawberry plant including fruit, flowers and leaves (Petrasch et al., 2019). Currently, fungicides are used to control B. cinerea on strawberries, which has resulted in the increased development of fungicide-resistant strains (Leroch et al., , 2013Veloukas et al., 2011;Bestfleisch et al., 2013). ...
Article
Full-text available
The necrotrophic fungus Botrytis cinerea is a major threat to strawberry cultivation worldwide. By screening different Fragaria vesca genotypes for susceptibility to B. cinerea, we identified two genotypes with different resistance levels, a susceptible genotype F. vesca ssp. vesca Tenno 3 (T3) and a moderately resistant genotype F. vesca ssp. vesca Kreuzkogel 1 (K1). These two genotypes were used to identify the molecular basis for the increased resistance of K1 compared to T3. Fungal DNA quantification and microscopic observation of fungal growth in woodland strawberry leaves confirmed that the growth of B. cinerea was restricted during early stages of infection in K1 compared to T3. Gene expression analysis in both genotypes upon B. cinerea inoculation suggested that the restricted growth of B. cinerea was rather due to the constitutive resistance mechanisms of K1 instead of the induction of defense responses. Furthermore, we observed that the amount of total phenolics, total flavonoids, glucose, galactose, citric acid and ascorbic acid correlated positively with higher resistance, while H2O2 and sucrose correlated negatively. Therefore, we propose that K1 leaves are more resistant against B. cinerea compared to T3 leaves, prior to B. cinerea inoculation, due to a lower amount of innate H2O2, which is attributed to a higher level of antioxidants and antioxidant enzymes in K1. To conclude, this study provides important insights into the resistance mechanisms against B. cinerea, which highly depend on the innate antioxidative profile and specialized metabolites of woodland strawberry leaves.
... Strawberry (Fragaria × ananassa Duch.) is extensively cultivated worldwide because of its nutritional value, owing to the vitamins, minerals, antioxidants, macronutrients, and micronutrients it contains (Petrasch et al. 2019). Mexico is one of the main strawberry producing and exporting countries. ...
... Therefore, it is essential to identify the microorganisms responsible and determine the potential risks associated with them (Melo et al. 2020). Botrytis, Colletotrichum, and Rhizopus are among the genera that cause the most significant losses to strawberries (Dean et al. 2012;Arceo-Martínez et al. 2019;Petrasch et al. 2019). For papaya, the most important genera are Colletotrichum, Alternaria, Rhizopus, and Aspergillus (Dean et al. 2012;Suárez-Quiroz et al. 2013). ...
... Botrytis cinerea can infect more than 200 plant species, including strawberries. It is considered one of the primary fungal pathogens of this crop globally, resulting in significant economic losses because it affects vegetative tissues, senescent organs, and fruits (Dean et al. 2012;Petrasch et al. 2019). Similarly, several authors have reported that, in recent years, C. nymphaeae, a species belonging to the Colletotrichum acutatum complex, is one of the fungal species most associated with anthracnose symptoms in various crops, such as strawberries (Nan-Yi et al. 2019). ...
... In the case of raspberries, B. cinerea infects stems, petals, buds, and fruits, generating a berry-brown color and a soft texture once collected, while the fruit remains on the plant looks dry and covered with a powder-gray-produced by conidia (Carisse et al., 2018). Moreover, B. cinerea is considered the major fungal pathogen present in strawberries, affecting both fruits and vegetative tissues in humidity conditions greater than 80% (Petrasch et al., 2019). Both primary (open flowers) and secondary (receptacle tissue) infections can occur in strawberries (Petrasch et al., 2019). ...
... Moreover, B. cinerea is considered the major fungal pathogen present in strawberries, affecting both fruits and vegetative tissues in humidity conditions greater than 80% (Petrasch et al., 2019). Both primary (open flowers) and secondary (receptacle tissue) infections can occur in strawberries (Petrasch et al., 2019). Strawberries can also be infected with Rhizopus spp., which presents pectic enzymes generating an aqueous decomposition of the fruit by rupture of pectin along with the appearance of a white mycelium (Tournas and Katsoudas, 2005). ...
Article
Full-text available
The world's population is growing, which requires more resources, including food. Some necessary foods, such as berries, are very perishable fresh products that suffer contamination by pathogens, generating great economic losses. Various physical and chemical strategies have been used to mitigate these losses over the years, including the use of pesticides. However, the negative impact on the environment and human health of these chemical products has aroused interest in the development of other control methods. Biocontrol is one of these innovative strategies, in which various biological control agents can be used, including bacteria probiotics. Probiotics act as antagonists of fungal pathogens by competition for space and nutrients, production of secondary metabolites, such as volatile organic compounds (VOCs), lytic enzymes, and activation of plant defenses. On the other hand, there are materials in which protection against pathogens has been seen, such as edible coatings, since they have components, such as chitosan, with antimicrobial properties. In addition, probiotics can be used in conjunction with other elements such as edible coatings, resulting from a new control strategy against post-harvest diseases. This review compiles studies that use probiotics and/or edible coatings as a method of reducing post-harvest diseases, specifically, in berries.
... Plant hormones such as salicylic acid (SA), jasmonic acid (JA), ethylene (ET), and abscisic acid (ABA) also contribute to the plant resistance to B. cinerea (AbuQamar et al., 2017). However, to date, little information has been obtained about the effects of B. cinerea infection on these processes in strawberry (Fragaria × ananassa) (Underwood, 2012;González et al., 2013;Li et al., 2013;Petrasch et al., 2019;Lu et al., 2020), a popular small fruit crop with short production cycles, extremely high nutrition, and good flavor. ...
... Botrytis cinerea preferentially infects strawberry flowers and fruits, leading to flower blight and fruit rot, which are the two most important causes of yield and economic losses. Studies have demonstrated that B. cinerea inoculum primarily enters the strawberry flower organs; the infected petals, stamens, and calyxes and then facilitate primary infection in fruits (Petrasch et al., 2019). The previous studies have focused primarily on the interaction of on B. cinerea with strawberry fruit (Liang et al., 2018;Xiong et al., 2018;Haile et al., 2019) while paying little attention to its interaction with the flower. ...
Article
Full-text available
Gray mold caused by Botrytis cinerea, which is considered to be the second most destructive necrotrophic fungus, leads to major economic losses in strawberry (Fragaria × ananassa) production. B. cinerea preferentially infects strawberry flowers and fruits, leading to flower blight and fruit rot. Compared with those of the fruit, the mechanisms of flower defense against B. cinerea remain largely unexplored. Therefore, in this study, we aimed to unveil the resistance mechanisms of strawberry flower through dynamic and comparative transcriptome analysis with resistant and susceptible strawberry cultivars. Our experimental data suggest that resistance to B. cinerea in the strawberry flower is probably regulated at the transcriptome level during the early stages of infection and strawberry flower has highly complex and dynamic regulatory networks controlling a multi-layered defense response to B. cinerea. First of all, the higher expression of disease-resistance genes but lower expression of cell wall degrading enzymes and peroxidases leads to higher resistance to B. cinerea in the resistant cultivar. Interestingly, CPKs, RBOHDs, CNGCs, and CMLs comprised a calcium signaling pathway especially play a crucial role in enhancing resistance by increasing their expression. Besides, six types of phytohormones forming a complex regulatory network mediated flower resistance, especially JA and auxin. Finally, the genes involved in the phenylpropanoid and amino acids biosynthesis pathways were gene sets specially expressed or different expression genes, both of them contribute to the flower resistance to B. cinerea. These data provide the foundation for a better understanding of strawberry gray mold, along with detailed genetic information and resistant materials to enable genetic improvement of strawberry plant resistance to gray mold.
... The ascomycete Botrytis cinerea is considered the most important postharvest pathogen in strawberry. It produces gray mold on fruit and senescing organs but also affects vegetative tissues [2]. Other relevant pathogens of the crop are those transmitted by the soil, such as the oomycete Phytophthora cactorum and the mitosporic fungus Verticillium dahliae. ...
Article
Full-text available
Gray mold (Botrytis cinerea Pers.), crown and fruit rot (Phytophthora cactorum (Lebert and Cohn) J.Schröt), and verticillium wilt (Verticillium dahliae Kleb.) are among the main diseases that affect the strawberry crop. In the study presented herein, the bark extract of Uncaria tomentosa (Willd. ex Schult.) DC, popularly known as “cat’s claw”, has been evaluated for its capability to act as a sustainable control method. The bioactive compounds present in the aqueous ammonia extract were characterized by gas chromatography–mass spectroscopy, and the antimicrobial activity of the extract—alone and in combination with chitosan oligomers (COS)—was assessed in vitro and as a coating for postharvest treatment during storage. Octyl isobutyrate (30.7%), 19α methyl-2-oxoformosanan-16-carboxylate (9.3%), tetrahydro-2-methyl-thiophene (4.7%), and α-methyl manofuranoside (4.4%) were identified as the main phytoconstituents. The results of in vitro growth inhibition tests showed that, upon conjugation of the bark extract with COS, complete inhibition was reached at concentrations in the 39–93.75 μg∙mL−1 range, depending on the pathogen. Concerning the effect of the treatment as a coating to prolong the storage life and control decay during post-harvest storage, high protection was observed at a concentration of 1000 μg∙mL−1. Because of this effectiveness, higher than that attained with conventional synthetic fungicides, the bark extracts of cat’s claw may hold promise for strawberry crop protection.
... The phytopathogens and herbivores attack at different sites and cause either localized or systematic infection (Gimenez et al. 2018). The infection may result in vascular wilt, canker, root rot, root knot, spots on leaf, nutrition deprivation, overproduction of reactive oxygen species (ROS), and/or even cell death (Rossi et al. 2017;Gimenez et al. 2018;Saddique et al. 2018;Petrasch et al. 2019). ...
Article
Botrytis is an important genus of plant pathogens causing pre- and post- harvest disease on diverse crops worldwide. This study evaluated Botrytis isolates collected from strawberry, blueberry, and table grape berries in California. Isolates were evaluated for resistance to eight different fungicides, and 60 amplicon markers were sequenced (neutral, species-identification, and fungicide-resistance associated) distributed across 15 of the 18 B. cinerea chromosomes. Fungicide resistance was common among the populations, with resistance to pyraclostrobin and boscalid being most frequent. Isolates from blueberry had resistance to the least number of fungicides, while isolates from strawberry had the highest number. Host and fungicide resistance-specific population structure explained, 12% and 7 to 26%, respectively of the population variability observed. Fungicide resistance was the major driver for population structure with select fungicides explaining up to 26% and resistance to multiple fungicides (MFR) explaining 17% of the variability observed. Shared and unique significant SNPs associated with host and fungicide resistance (fluopyram, thiabendazole, pyraclostrobin, and fenhexamid) associated population structure were identified. While overlap between host and fungicide-resistance SNPs were detected, unique SNPs suggest that both host and fungicide resistance play an important role in Botrytis population structure.
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Fungi are an important group of microorganisms that can spoilage food during storage and transportation, thereby affecting the quality and shelf life of these products. Although synthetic antifungal agents efficiently control the fungal spoilage of food, the continuous use of these substances can cause several problems. The use of ribonucleic acid interference (RNAi) as a fungicide has emerged as an alternative approach with less negative environmental impact. Spray-induced gene silencing (SIGS) is an innovative approach to silence target genes in fungi using RNAi. This review presents state-of-the-art information on the use of SIGS to control fungi during food storage.
Article
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Worldwide, 20–25% of all harvested fruit and vegetables are lost annually in the field and throughout the postharvest supply chain due to rotting by fungal pathogens. Most postharvest pathogens exhibit necrotrophic or saprotrophic lifestyles, resulting in decomposition of the host tissues and loss of marketable commodities. Necrotrophic fungi can readily infect ripe fruit leading to the rapid establishment of disease symptoms. However, these pathogens generally fail to infect unripe fruit or remain quiescent until host conditions stimulate a successful infection. Previous research on infections of fruit has mainly been focused on the host’s genetic and physicochemical factors that inhibit or promote disease. Here, we investigated if fruit pathogens can modify their own infection strategies in response to the ripening stage of the host. To test this hypothesis, we profiled global gene expression of three fungal pathogens that display necrotrophic behavior—Botrytis cinerea, Fusarium acuminatum, and Rhizopus stolonifer—during interactions with unripe and ripe tomato fruit. We assembled and functionally annotated the transcriptomes of F. acuminatum and R. stolonifer as no genomic resources were available. Then, we conducted differential gene expression analysis to compare each pathogen during inoculations versus in vitro conditions. Through characterizing patterns of overrepresented pathogenicity and virulence functions (e.g., phytotoxin production, cell wall degradation, and proteolysis) among the differentially expressed genes, we were able to determine shared strategies among the three fungi during infections of compatible (ripe) and incompatible (unripe) fruit tissues. Though each pathogen’s strategy differed in the details, interactions with unripe fruit were commonly characterized by an emphasis on the degradation of cell wall components, particularly pectin, while colonization of ripe fruit featured more heavily redox processes, proteolysis, metabolism of simple sugars, and chitin biosynthesis. Furthermore, we determined that the three fungi were unable to infect fruit from the non-ripening (nor) tomato mutant, confirming that to cause disease, these pathogens require the host tissues to undergo specific ripening processes. By enabling a better understanding of fungal necrotrophic infection strategies, we move closer to generating accurate models of fruit diseases and the development of early detection tools and effective management strategies.
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Cultivated strawberry emerged from the hybridization of two wild octoploid species, both descendants from the merger of four diploid progenitor species into a single nucleus more than 1 million years ago. Here we report a near-complete chromosome-scale assembly for cultivated octoploid strawberry (Fragaria × ananassa) and uncovered the origin and evolutionary processes that shaped this complex allopolyploid. We identified the extant relatives of each diploid progenitor species and provide support for the North American origin of octoploid strawberry. We examined the dynamics among the four subgenomes in octoploid strawberry and uncovered the presence of a single dominant subgenome with significantly greater gene content, gene expression abundance, and biased exchanges between homoeologous chromosomes, as compared with the other subgenomes. Pathway analysis showed that certain metabolomic and disease-resistance traits are largely controlled by the dominant subgenome. These findings and the reference genome should serve as a powerful platform for future evolutionary studies and enable molecular breeding in strawberry.
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Sensitivity of Botrytis cinerea to seven fungicide chemical classes was determined for 888 isolates collected in 2016 from 47 California strawberry fields. Isolates were collected early season (minimum fungicide exposure) and late season (maximum fungicide exposure) from the same planting block in each field. Resistance was determined using a mycelial growth assay, and variable frequencies of resistance were observed to each fungicide at both sampling times (early season %, late season %): boscalid (12, 35), cyprodinil (12, 46), fenhexamid (53, 91), fludioxonil (1, 4), fluopyram (2, 7), iprodione (25, 8), isofetamid (0, 1), penthiopyrad (8, 25), pyraclostrobin (77, 98), and thiophanate-methyl (81, 96). Analysis of number of chemical class resistances (CCRs) revealed an increasing shift in CCR from the early to late season. Phenotypes of 40 isolates that were resistant or sensitive to different chemical classes were associated with presence or absence of mutations in target genes. Fungicide-resistance phenotypes determined in the mycelial growth assay closely matched (93.8%) the genotype observed. Previously described resistance-conferring mutations were found for each gene. A survey of fungicide use from 32 of the sampled fields revealed an average of 15 applications of gray mold-labeled fungicides per season at an average interval of 12 days. The most frequently applied fungicides (average number of applications during the 2016 season) were captan (7.3), pyraclostrobin (2.5), cyprodinil (2.3), fludioxonil (2.3), boscalid (1.8), and fenhexamid (1.4). Multifungicide resistance is widespread in California. Resistance management tactics that reduce selection pressure by limiting fungicide use, rotating among Fungicide Resistance Action Committee codes, and mixing/rotating site-specific fungicides with multisite fungicides need to be improved and implemented.
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MicroRNAs are endogenous small non-coding RNAs that negatively regulate mRNAs, mainly at the post-transcriptional level, and play an important role in resistance response of plants. To date, there are few reports on resistance response of strawberry miRNAs to pathogens. In this study, using high-throughput sequencing, 134 conserved and 35 novel miRNAs were identified in six libraries within the treatment of Botrytis cinerea. A total 497 potential target genes were predicted using Fragaria vesca genome. Most of the differential expressed miRNAs in strawberry fruits were up-regulated in early libraries and down-regulated in late libraries. PIRL, the target gene of miR5290a, showed the opposite expressed trend compared with miR5290 from T1 to T3 libraries, and functional analysis of the PIRL gene shows that it has obvious resistance to B. cinerea in the strawberry fruits with overexpressed PIRL gene. We speculate that miR5290a negatively regulates its target gene PIRL to increase resistance to pathogen infection, and further analysis of PIRL function is meaningful for studying the plant-pathogen relationship and improving strawberry fruit quality and yield.
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Polyamines (PAs) participate in many plant growth and developmental processes, including fruit ripening. However, it is not clear whether PAs play a role in the ripening of strawberry (Fragaria ananassa), a model non-climacteric plant. Here, we found that the content of the PA spermine (Spm) increased more sharply after the onset of fruit coloration than did that of the PAs putrescine (Put) or spermidine (Spd). Spm dominance in ripe fruit resulted from abundant transcripts of a strawberry S-adenosyl-L-methionine decarboxylase gene (FaSAMDC), which encodes an enzyme that generates a residue needed for PA biosynthesis. Exogenous Spm and Spd promoted fruit coloration, while exogenous Put and a SAMDC inhibitor inhibited coloration. Based on transcriptome data, up- and downregulation of FaSAMDC expression promoted and inhibited ripening, respectively, which coincided with changes in several physiological parameters and their corresponding gene transcripts, including firmness, anthocyanin content, sugar content, polyamine content, auxin (IAA) content, abscisic acid (ABA) content, and ethylene emission. Using isothermal titration calorimetry, we found that FaSAMDC also had a high enzymatic activity with a Kd of 1.7 × 10-3 M. In conclusion, PAs, especially Spm, regulate strawberry fruit ripening in an ABA-dominated, IAA-participating and ethylene-coordinated manner, and FaSAMDC plays an important role in ripening.