Plphys v179 4 1198

Update on Plant-Oomycete Interactions
Exchanges at the Plant-Oomycete Interface That

Influence Disease1[OPEN]
Howard S. Judelson,2,3 and Audrey M. V. Ah-Fong

Department of Microbiology and Plant Pathology, University of California, Riverside, California 92521
ORCID ID: 0000-0001-7865-6235 (H.S.J.).
Downloaded from https://academic.oup.com/plphys/article/179/4/1198/6116504 by guest on 02 November 2023

The microbial eukaryotes known as oomycetes trophic behaviors. Unlike many other oomycetes, Phy-
comprise more than 1,500 species, including many im- tophthora spp. are culturable and amenable to trans-
portant phytopathogens. Most exhibit filamentous formation; thus, they have been the subject of many
growth and feed osmotrophically. Oomycetes appear molecular studies.
fungus-like but are classified as stramenopiles along The largest genus of necrotrophic oomycetes, which
with brown algae and diatoms (Beakes et al., 2012). feed on nutrients from lysed cells, is Pythium. Most
Unlike most fungi, oomycetes are diploid, have cell members of this group are opportunistic root patho-
walls made primarily of cellulose and b-glucans instead gens with broad host ranges, such as Pythium ultimum,
of chitin, make aseptate hyphae, undergo oogamous which infects vegetables, grains, and trees (Kamoun
reproduction, and produce few secondary metabolites et al., 2015). Interestingly, some Pythium spp. also are
(Fawke et al., 2015). mycoparasites (Benhamou et al., 2012). Also appearing
Oomycetes exhibit diverse lifestyles across terrestrial to grow as a necrotroph is Aphanomyces euteiches, which
and aquatic niches. While best known as pathogens of causes root rot of legumes.
leaves, stems, roots, and fruit, some oomycetes are en- This review focuses on events at the plant-oomycete
dophytes, infect animals, or are saprophytes (Lamour interface, where exchanges of host and pathogen mol-
and Kamoun, 2009; Ploch and Thines, 2011; Aram and ecules play critical roles in determining the outcome of
Rizzo, 2018). Many are highly host adapted, uncultur- the association (Fig. 1). Oomycete pathogens sense,
able on artificial media, and grow only on living plants bind, and absorb nutrients from their hosts and also
as biotrophs. Examples include downy mildew patho- interact with other microbes in the phyllosphere and
gens such as Plasmopara viticola, which infects grapevine
(Vitis vinifera), and Albugo candida, which causes white
rust on crucifers (Kamoun et al., 2015). The obligate ADVANCES
pathogens typically cause minimal damage to the plant
but reduce yield and raise susceptibility to secondary • Differences between the biotrophic,
infection or abiotic stress. hemibiotrophic, and necrotrophic lifestyles of
Many oomycetes are hemibiotrophs, which start in- oomycetes have been attributed to variation in
fections like biotrophs but cause necrosis late in the
gene content and patterns of gene expression.
disease cycle. Most belong to the genus Phytophthora,
including Phytophthora cinnamomi, which infects hun- Such genes include those encoding metabolic
dreds of agricultural, forest, and ornamental hosts; enzymes, proteinaceous toxins, and defense-
Phytophthora infestans, which blights potato (Solanum suppressing effectors.
tuberosum) and tomato (Solanum lycopersicum); and • Haustoria represent a specialized interface for
Phytophthora sojae, which colonizes soybean (Glycine delivering effectors to plants.
max) and lupines. Some species, such as Ph. cinnamomi, • The extrahaustorial matrix seems to be made de
shift to necrotrophy early in infection, while others, novo through the polarized delivery of plant
such as Ph. infestans, make the transition much later, cargo, and differs from a typical plasma
reflecting differences in how the species balance the two membrane.
• Effectors have proved to be exquisite tools for
1
This work was supported by the National Science Foundation probing the plant immune response and
(grant no. IOS-1753749) and the National Institute of Food and Ag- understanding host-pathogen evolution.
riculture of the U.S. Department of Agriculture (grant no. 2016-67013- • Factors that regulate the production,
2481). germination, and homing responses of
2
Author for contact: [email protected].
3 oomycete spores are starting to be defined,
Senior author.
H.S.J. and A.M.V.A.-F. cowrote the article. including transcription factors and novel G-
[OPEN]
Articles can be viewed without a subscription. protein-related signaling pathways.
www.plantphysiol.org/cgi/doi/10.1104/pp.18.00979
1198 Plant PhysiologyÒ, April 2019, Vol. 179, pp. 1198–1211, www.plantphysiol.org Ó 2019 American Society of Plant Biologists. All Rights Reserved.
Judelson and Ah-Fong

Figure 1. Interactions at plant-oomycete interfaces. Illustrated at center left is a biotrophic infection, starting from a sporangium
and involving biflagellated zoospores, an appressorium formed from a germinated cyst, a primary infection vesicle (pv), an in-
tercellular mycelium, and a haustorium. The effects of plant signals such as isoflavones, sucrose (suc), and amino acids (aa) on
spore germination and/or homing are indicated. The bacterium at top right represents the effects of the microbiome on spores, as
discussed in Box 2. The oval organelle marked “sequestered nutrients” represents a starch granule; this only releases significant
carbohydrate to the pathogens during necrotrophy. The turquoise pentagon represents a nutrient such as sulfate that is located
primarily in a plant vacuole. Yellow stars represent apoplastic effectors such as protease inhibitors (ae) and cytoplasmic effectors
such as Crinklers (C) and RXLRs (R). The latter are shown inhibiting the delivery of defense materials, such as proteases and
callose, to the apoplast and EHMx by secretory or autophagosomal vesicles of a mesophyll cell. These defense responses also
occur in the epidermis. Shown at top right are the initial stages of infection initiated through a stomata (gray mycelium). Shown at
right is an opportunistic necrotroph (spotted mycelium) entering through a wound, feeding from a lysed cell, and exiting into soil.
Lysis of the host during infection by the necrotroph occurs due to the absence of defense-suppressing effectors, ROS generation,
and early expression of NLPs, as discussed in Box 3.
rhizosphere. Meanwhile, plants detect and deliver de- Host signals can be sensed by the asexual sporangia
fenses against infection. Plant-oomycete interfaces can since they are fully hydrated and metabolically active
be dynamic, varying with infection stage and as im- prior to germination, unlike most fungal spores, which
mune responses are deployed. Here, we discuss in- are desiccated. While sporangia require only free water
sights into these topics yielded by advances in cell to germinate, this can be hastened by plant signals.
biology, genome analysis, transcriptomics, and protein Studies have shown that Pl. viticola releases zoospores
structure analysis. faster on leaves than in a host-free system (Kiefer et al.,
2002) and that Pythium spp. germination is accelerated
by volatiles, sugars, and amino acids from seeds (Nelson,
1987). Root exudates, or sprouted potato tubers in the
PLANTS CAN ATTRACT UNWANTED GUESTS
case of Ph. infestans, also stimulate the germination of
Oomycetes employ several types of spores for sexual spores (oospores), which typically stay dormant
dissemination and host infection (Box 1). These in- in soil until a host is present (El-Hamalawi and Erwin,
clude both asexual and sexual spores (McCarren 1986; Pittis and Shattock, 1994). Studies with Ap. euteiches
et al., 2005; Granke et al., 2009). Colonization by indicated that its oospores respond more to host than
the majority of oomycetes begins when an asexual nonhost exudates (Shang et al., 2000). It is intriguing to
sporangium releases zoospores, which encyst and consider that in the future, it may be possible to use plant
form a germ tube (Fig. 1). As discussed below, many signal mimics to cause oospores to undergo suicide
aspects of spore behavior are influenced by plant germination before a crop is planted.
signals. The microbiome also affects spores and can Zoospores exhibit several homing responses, including
attenuate or worsen disease, as described in Box 2 chemotaxis, electrotaxis, host-triggered encystment, and
(Lioussanne et al., 2008; Windstam and Nelson, 2008; germ tube tropism (Deacon and Donaldson, 1993). These
Raaijmakers et al., 2010; Schlatter et al., 2017; Jack contribute to host specificity, especially with root patho-
and Nelson, 2018). gens. For instance, Ap. euteiches zoospores are attracted
Plant Physiol. Vol. 179, 2019 1199
Exchanges at the Plant-Oomycete Interface
BOX 1. A Diversity of Infectious Propagules

Many root pathogens such as Ph. sojae and most
Oomycetes produce several forms of
Pythium spp. produce sporangia that are
spores for survival, dissemination, and infection,
inseparable from the sporangiophore, and in such
with the multiplicity of types contributing to their
cases zoospores are liberated directly from lesions.
success as pathogens. The defining feature of the
This also occurs with Aphanomyces spp., but from
taxonomic group are oospores, which are thick-
sporangia that resemble normal hyphae. The
walled products of sexual reproduction that can
motility of zoospores expands the potential space
survive in plant debris or soil for years.
for infection, even though the maximum
Homothallism (self-fertility), heterothallism, and
swimming range may only be a few centimeters.

blended phenotypes are exhibited by different
Remarkably, zoospores of some species that fail to
species, even in the same genus. Interestingly,
infect a host can encyst and later produce a second
mating hormones made by Phytophthora spp. are
zoospore, thus providing two chances for
synthesized from phytol, an acyclic diterpene of
colonizing a plant. Despite its potential benefits,
plants, which indicates the close dependence of
the motile stage is absent from certain foliar
the genus on its hosts. Oospores germinate by
downy mildews, which instead extend germ tubes
producing hyphae that often form sporangia
from their asexual spores (conidia). Genes for
capable of discharging zoospores.
flagellar proteins are absent or degraded in such
Most oomycetes also produce zoospores species (Judelson et al., 2012).
from asexual sporangia, which cause the majority
Some Phytophthora and Pythium spp.
of infections within a growing season. Many foliar
also produce chlamydospores, which are thick-
pathogens such as Ph. infestans and Pl. viticola are
walled asexual cells. When conditions become
well-suited to wind dispersal since their sporangia
suited to growth, these can germinate and cause
detach easily from the sporangiophore, and are
infections vegetatively or through sporangia
lemon-shaped which retards their fall from air.
(McCarren et al., 2005). Otherwise, most
After landing on a moist surface such as a dew-
oomycetes do not initiate natural infections from
covered leaf, zoospores are released that later
mycelia except for most members of Pythium and
encyst and send out a germ tube, although these
a few species of Phytophthora (Aram and Rizzo,
sometimes extend directly from sporangia. Other
2018).
species such as Ph. capsici make sporangia that
require greater force to be dislodged, and thus are
spread more by rain, wind-driven rain, or flowing
water (Granke et al., 2009).
specifically to prunetin (Sekizaki et al., 1993), while Ph. before a plant is reached (Mostowfizadeh-Ghalamfarsa
sojae responds to daizein and genistein, which are pro- et al., 2018). Many spore-specific calcium channels and
duced by their respective hosts (Hosseini et al., 2014). calcium-regulated protein phosphatases and kinases
These isoflavones also influence encystment and germ have been identified, although none have been tested for
tube orientation (Morris et al., 1998). Recent data point to a function (Ah-Fong et al., 2017b).
role for G-proteins in these responses. Silencing of the Ph. Chemotaxis also occurs in foliar pathogens, where amino
sojae gene encoding its G-protein a-subunit interfered with acids such as Gln attract zoospores, a process that also
zoospore motility and chemotaxis (Hua et al., 2008), and appears to involve G-proteins (Latijnhouwers et al., 2004).
knockdowns of a G-protein a-subunit-interacting His triad Amino acid signaling may explain why zoospores of Ph.
protein inhibited chemotaxis (Zhang et al., 2016). In addi- infestans and many relatives concentrate near stomata (Dale
tion, encystment was stimulated and cyst germination was and Irwin, 1991). Few Pl. viticola zoospores were drawn to
impaired by knocking down the expression of a protein stomata closed by exogenous abscisic acid, suggesting that
that consists of a G-protein-coupled receptor domain the attractants are soluble or volatile substomatal chemicals.
coupled to a phosphatidylinositol phosphate kinase do- Such behavior is critical to Pl. viticola, which enters leaves
main (Yang et al., 2013). Oomycetes express several novel only through stomata (Kiefer et al., 2002).
G-protein-coupled receptor-like proteins with C-terminal
accessory domains (van den Hoogen et al., 2018).
Pharmacological studies have shown that calcium
OOMYCETES ENTER PLANTS THROUGH
influences most aspects of zoospore behavior. This ex-
MULTIPLE ROUTES
plains the biology behind the strategy of reducing root
diseases by adding gypsum (calcium sulfate) to soil, As water molds, most oomycetes prefer to grow in
which impairs zoosporogenesis or causes encystment moist environments such as the apoplast. Entry into
1200 Plant Physiol. Vol. 179, 2019
BOX 2. Other Microbes at the Interface: Friend

Or Foe?
A plant-oomycete interaction does not zoospores (Kong and Hong, 2016).

occur in a biological vacuum. It is long known that
Oomycetes can even attack other
bacteria and fungi in soil and the phyllosphere
oomycetes, with the best-described example
produce compounds that antagonize oomycetes,
being Py. oligandrum (Benhamou et al., 2012). This
such as lipopeptide surfactants that disrupt the
species parasitizes other oomycetes and fungi. An
zoospore plasma membrane (Raaijmakers et al.,
interesting question is how Py. oligandrum
2010; Schlatter et al., 2017). Microbes can also

distinguishes self from non-self during such
attenuate or promote maladies caused by
interactions. Py. oligandrum has also been
oomycetes in less direct ways. Bacteria recruited to
proposed to grow as an endophyte, and was
seedlings have been shown to reduce infection by
shown to reduce diseases in sugarbeet, cotton,
metabolizing fatty acids in plant exudates that
and other plants. This is believed to be due to the
would otherwise stimulate Py. ultimum sporangia
combined effects of mycoparasitism and the
to germinate, or by hampering the homing
priming of host defenses, since plants recognize
responses of Py. aphanidermatum zoospores
several Py. oligandrum proteins including its
(Windstam and Nelson, 2008; Jack and Nelson,
elicitins (Takenaka et al., 2011). Py. oligandrum has
2018). Interference with zoospore behavior was
also been shown to stimulate plant growth,
also reported for Glomus intraradices mycorrhizae
possibly because it makes the auxin precursor
on tomato, which reduced infection and produced
trypamine, and produces auxins when grown on
zoospore repellants such as isocitric acid
root exudates (Benhamou et al., 2012). Many
(Lioussanne et al., 2008). Some microbial
Albugo species are also reported to grow as
interactions may benefit the oomycete. Although
asymptomatic endophytes on crucifers, but
its significance requires further investigation,
whether these benefit the plant is unknown (Ploch
Phytophthora spp. produce the bacterial quorum-
and Thines, 2011).
sensing signal AI-2, which was proposed to recruit
bacteria that improve the infection potential of
the plant may occur when zoospores or germ tubes defense-suppressing effectors, and potential adhesion
pass through stomata or other natural openings, proteins (Kebdani et al., 2010).
transit through wounds, or grow between root ep- Mirroring the complexity of the plant cell wall, a typical
idermal cells. Examples include Pl. viticola, which oomycete expresses CWDEs belonging to as many as 28
enters through stomata, Ph. cinnamomi, which can glycosyl hydrolase groups (Blackman et al., 2015). A
move through peridermal gaps, and Ph. infestans, typical species of Phytophthora expresses about 200 genes
which often enters tubers through lenticels. Ph. encoding such proteins. Some of the (hemi)cellulases are
infestans, downy mildews, white rusts, and many predicted to bear glycophosphatidylinositol anchors and
Pythium spp. also penetrate tissue using appresso- probably serve to expand the oomycete wall, which
ria. These swellings form when cyst germ tubes contains mostly cellulose plus b-1,3- and b-1,6-glucans
contact hydrophobic surfaces such as the cuticle, (Mélida et al., 2013). Fewer types of CWDEs are expressed
especially if epidermal cell boundaries or their by biotrophs, as in the case of Albugo laibachii, which lacks
topographic mimics are sensed (Bircher and pectate lyase and pectin esterase (Kemen et al., 2011).
Hohl, 1997). Studies in Ph. infestans and relatives show that CWDEs are
Insight into the biology of oomycete appressoria has expressed in stages during sporulation, germination, and
lagged behind that of fungi. However, a study in Ph. in planta growth (Kebdani et al., 2010; Blackman et al.,
infestans using GFP-labeled F-actin identified an aster- 2015). A less ordered pattern of expression was reported
like structure where appressoria contact the leaf, which for Py. ultimum, which also expressed fewer CWDEs (Ah-
may focus cargo transport to the penetration peg (Kots Fong et al., 2017b). Other differences between Phytoph-
et al., 2017). Also, a basic leucine zipper domain tran- thora and Pythium spp. are highlighted in Box 3. The
scription factor and mitogen-activated protein ki- pattern of CWDE expression in Py. ultimum suggests that
nase were shown to regulate appressorium formation the enzymes of this necrotroph may be used primarily to
(Blanco and Judelson, 2005; Li et al., 2010). Genes burst host cells rather than to digest plant walls for car-
induced in the appressorium stage by Phytophthora bon. Indeed, cellulose is a poor carbon source for most
spp. include cell wall-degrading enzymes (CWDEs), oomycetes (Zerillo et al., 2013). Perhaps advanced
imaging techniques such as superresolution confocal mi- vesicles to discharge a glue-like thrombospondin repeat
croscopy with specific organic fluorophores could be protein toward the plant interface (Robold and
employed to obtain information about carbohydrate Hardham, 2005). A protein containing a Sushi do-
structure at penetration sites, the effects of CWDEs at main, which in animals mediates cell-cell adhesion,
different stages of infection, and polymer rearrangements reaches the plant surface from other zoospore vesicles
resulting from plant defenses. by kiss-and-run exocytosis (Zhang et al., 2013). Sticky
Most stages of infection require adherence of the substances also are released from germ tubes. The
pathogen to the host. Zoospores turn their ventral downy mildew Hyaloperonospora arabidopsidis was
grooves toward the host prior to encystment, allowing shown to secrete proteins and fibrillar b-1,3-glucans

BOX 3. Stealthy Phytophthora versus
aggressive Pythium
These two genera have distinct lifestyles For example, Py. ultimum expresses its secreted
despite being close neighbors in oomycete proteases and necrosis-inducing NLP proteins at
phylogenies. While most Pythium spp. are much higher levels than Ph. infestans (Fig. 2). In
aggressive cosmopolitan necrotrophs, contrast, inhibitors of host proteases are
Phytophthora spp. are hemibiotrophs and are expressed more by Ph. infestans. Catalase genes
often host-specific. Phytophthora spp. grow are expressed less by Py. ultimum, which suggests
primarily in the apoplast, which limits injuries to that eliminating peroxide delivered by the host to
host cells and minimizes the production of the pathogenic interface is not critical to its
damage-associated molecular patterns (DAMPs), lifestyle.
which would otherwise induce host defenses. Patterns of metabolic gene expression in
Host damage during the formation of haustoria, Ph. infestans and Py. ultimum also reflect their
which are not made by Pythium, is also minimal divergent lifestyles. A consequence of the stealthy
since the openings in the plant wall are only a few apoplastic mode of growth of Phytophthora is
microns in diameter. Imm une responses are also restricted access to nutrients. Thus, Ph. infestans
reduced since PRRs are excluded from the EHM. expresses at higher levels many genes needed to
Only towards the end of the disease cycle do synthesize metabolites that are at low
Phytophthora spp. exhibit signs of necrotrophy. In concentrations in the apoplast. Examples include
contrast, Pythium spp. seem to go full-speed genes that encode enzymes for making amino
ahead with a strategy of lysing host cells and acids such as arginine, nucleotides, and cofactors
extracting nutrients. such as coenzyme A (Fig. 2; Ah-Fong et al., 2017b
Some differences between the taxa are and H. Judelson and A. Ah-Fong, unpublished
due to variation in gene content. For example, results). In contrast, mRNA levels of genes
Pythium spp. lack the RXLR and CRN proteins that encoding enzymes that use nutrients that are
Phytophthora use to suppress host defenses. normally sequestered in plant cells but released
Moreover, only Pythium spp. encode the pore- during necrotrophy are much higher in Py.
forming toxins known as perforins. Other ultimum than Ph. infestans. Examples include
differences are reflected in the expression lipase, RNase, amylase for digesting starch, and
patterns of genes shared by Ph. infestans and Py. enzymes for assimilating sulfate.
ultimum, as seen during potato tuber colonization
(Ah-Fong et al., 2017b).

that bind its germ tubes to the substratum (Carzaniga that NLPs destabilize the host plasmalemma (Lenarčič
et al., 2001). This may help resist detachment by wind or et al., 2017). Oomycetes are immune to NLPs, since the
rain or protect against desiccation. Other potential ad- latter are specific for dicotyledonous sphingolipids. An
hesion proteins include mucin-like proteins (Larousse NLP from Phytophthora parasitica was shown to elicit
et al., 2014), jacalin-like and cellulose-binding elicitor defenses in crucifers, which suggests that some NLPs
(CBEL) lectins (Gaulin et al., 2002), and the ACWP affect plant cells both as pore-forming toxins and in-
family of acidic wall proteins (Resjö et al., 2017). Ab- ducers of PTI (Böhm et al., 2014).
normal appressoria resulted from the knockdown of Receptors for three oomycete PAMPs are known. The
ACWP genes, suggesting that they contribute to adhe- infestin elicitin of Ph. infestans and related proteins are
sion or wall integrity. Knockdowns of CBEL showed recognized in potato by elicitin response protein (ELR),
that it helped hyphae bind to cellulosic substances but a plasmalemma-associated factor that associates with
was not essential for pathogenicity (Gaulin et al., 2002). SUPPRESSOR OF BIR1-1 (SOBIR1), which is a leucine-

One of the few oomycete proteins known to concentrate rich repeat (LRR) receptor kinase (Domazakis et al.,
in haustoria, Hmp1, is membrane anchored and weakly 2018). This pairing is needed since ELR lacks an intra-
resembles lectins. Silencing Hmp1 in Ph. infestans im- cellular kinase domain. When infestin is detected, the
paired the formation of infection vesicles in epidermal ELR-SOBIR1 complex recruits the LRR receptor-like
cells and haustoria, suggesting that the protein helps kinase BRI1-ASSOCIATED KINASE-1, which is a
the pathogen bind to host interfaces (Avrova et al., known hub in defense responses. SOBIR1 also partici-
2008). pates in the reaction of Arabidopsis to NLPs, which are
recognized by the LRR receptor RLP23 (Albert et al.,
2015). Recently identified was Response to XEG1
PLANTS CAN DETECT OOMYCETES AND BRING
(RXEG1), an LLR protein that recognizes XEG1, a gly-
coside hydrolase 12 endoglucanase that is made by
DEFENSES TO THE INTERFACE
Phytophthora spp. RXEG1also forms a complex with
Plants have evolved sophisticated systems for BRI1-ASSOCIATED KINASE-1 and SOBIR1 to trans-
detecting microbes. One involves the binding of duce the defense signal (Wang et al., 2018). Interest-
pathogen-associated molecular patterns (PAMPs) to ingly, fungal glycoside hydrolase 12 proteins also have
plasmalemma-spanning pattern recognition receptors been shown to serve as PAMPS and act through the
(PRRs), which activates PAMP-triggered immunity same signaling hub (Gui et al., 2017).
(PTI; Saijo et al., 2018). The salicylic acid (SA) and jas- Once PTI is activated, defense molecules are de-
monic acid pathways both participate in PTI against livered to plant-oomycete interfaces, including
necrotrophic and (hemi)biotrophic oomycetes (Halim pathogenesis-related (PR) proteins, callose for thick-
et al., 2009). Disrupting jasmonate production in Ara- ening cell walls, and microbial toxins. Effector-
bidopsis (Arabidopsis thaliana) allowed Pythium irregu- triggered immunity reinforces and expands these
lare, which typically infects wounded or otherwise responses and often leads to hypersensitive cell death.
compromised hosts, to become a more severe pathogen Since PTI and effector-triggered immunity are not
(Staswick et al., 1998). oomycete specific, readers seeking more information
Constituents of the cell wall or plasma membrane are directed to other reviews (Kourelis and van der
were among the first oomycete PAMPs to be identified. Hoorn, 2018; Saijo et al., 2018). However, oomycetes
These include b-1,3- and b-1,6-glucans and arachidonic were used in many early studies of the cytoskeletal
acid (Fawke et al., 2015; Robinson and Bostock, 2015). dynamics that occur during infection, which showed
Medicago truncatula also responds to a chitosaccharide that plant actin microfilaments focused rapidly near
from Ap. euteiches; most other oomycete phytopatho- penetration sites (Takemoto et al., 2003). This causes
gens lack this PAMP, since they do not make chitin peroxisomes, nuclei, and the endomembrane transport
(Mélida et al., 2013; Nars et al., 2013). Proteinaceous network to move toward the infection, which may
PAMPs include a cell wall transglutaminase (Brunner help deliver defenses (Li and Staiger, 2018). Some
et al., 2002), the glycosyl hydrolase domain of the oli- (hemi)biotrophic oomycetes have evolved counter
gopeptide elicitor (OPEL) protein (Chang et al., 2015), defenses against these trafficking pathways and may
the cellulose-binding protein CBEL, the elicitin family have hijacked some to support haustoria.
of sterol-binding proteins (Takenaka et al., 2011; While the delivery of proteases, glucanases, and
Derevnina et al., 2016), and the XEG1 endoglucanase callose to oomycete-plant interfaces through canonical
(Wang et al., 2018). The latter are proposed to be used secretory and exocytosis pathways is long established,
for sterol acquisition by Phytophthora and Pythium spp., autophagic vesicles were shown recently to surround
which are sterol autotrophs. It is notable that Nep1-like Ph. infestans haustoria and also may convey defenses
proteins (NLPs) were classified recently as PAMPs by (Dagdas et al., 2018). It is unknown whether plants use
some researchers. Most NLPs in Phytophthora spp. are exosomes against oomycetes, for example by trans-
expressed late in infection and have been linked to porting inhibitory small RNAs, as shown recently with
necrotrophic growth (Feng et al., 2014). Analysis of fungi (Cai et al., 2018). Nevertheless, there are reports of
crystal structures identified similarity with pore- lettuce (Lactuca sativa) and potato being engineered to
forming cytotoxins of sea anemones, which suggests resist Bremia lactucae and Ph. infestans by host-induced
gene silencing using small RNAs targeting oomycete and knockdowns in tomato and N. benthamiana to de-
genes (Govindarajulu et al., 2015; Jahan et al., 2015). fend against Ph. infestans (Song et al., 2009; Kaschani
Reactive oxygen species (ROS) are delivered to plant- et al., 2010). Ph. infestans and relatives antagonize
oomycete interfaces through several pathways. ROS are these using effectors such as extracellular cystatin-like
derived from wall-bound peroxidases, respiratory protease inhibitor 1 (EPIC1). Studies of EPIC1 from Ph.
burst oxidase homologs in plasmalemma, and glycolate infestans and Phytophthora mirabilis (which infects Mir-
oxidase in peroxisomes, which move to infection sites abilis jalapa) and the host proteases were performed,
during cytoskeletal remodeling (Marino et al., 2012). guided by the crystal structure of a related protease-
ROS from tobacco (Nicotiana tabacum) roots have been inhibitor complex. Amino acid changes in EPIC1 were
implicated in blocking infection by Ph. parasitica zoo- implicated in helping the pathogens jump to new host
spores, which interestingly die through programmed species (Dong et al., 2014). Orthologs of EPIC1 genes
cell death (Galiana et al., 2005). Besides being antimi- occur in downy mildew, white rust, and Pythium spp.

crobial, ROS strengthens cell walls by initiating lignin genomes. Most oomycetes also can inhibit plant Ser
polymerization (Barros et al., 2015). Several other en- proteases, and one from Phytophthora palmivora was
zymes that fortify plant walls also are induced during shown to contribute to virulence against the rubber tree
PTI against oomycetes, including cinnamyl alcohol (Hevea brasiliensis; Ekchaweng et al., 2017).
dehydrogenase and callose synthase (Wang et al., 2013; Another example of host-pathogen coevolution in the
Hosseini et al., 2015). apoplast comes from studies of the endoglucanase
Toxic isoflavonoids, sesquiterpenes, polyacetylenes, XEG1 from Ph. sojae. Soybean produces an inhibitor of
and other molecules that are collectively named phy- this CWDE, which binds XEG1 and blocks its contri-
toalexins are believed to be delivered to the pathogen bution to virulence. To counteract the plant, Ph. sojae
by ATP-binding cassette (ABC) transporters. The ex- secretes an inactive enzyme as a decoy (Ma et al., 2017).
port of capsidiol during the elicitin-triggered defense With the defense protein unproductively bound to this
response of Nicotiana benthamiana against Ph. infestans trap, Ph. sojae can invade soybean more easily. Ortho-
involves ABCG1 and ABCG2, which are up-regulated logs of XEG1 and its decoy are conserved throughout
during PTI (Rin et al., 2017). Some phytoalexins, such as the Phytophthora genus.
a-tomatine of tomato, are preformed in plants, while Another apoplastic effector that counteracts host
others are induced by infection, such as capsidiol of defenses is the in planta-induced protein (IPI-O) of Ph.
Nicotiana spp. and pepper (Capsicum annuum), gly- infestans. IPI-O contains an Arg-Gly-Asp motif that is
ceollin of soybean, and camalexin of crucifers (Hahn believed to disrupt adhesion between the plant’s cell
et al., 1985; Bednarek et al., 2005). wall and plasmalemma by binding the lectin receptor
These defenses may combine to produce apoplastic kinase LecRK-I.9, thus promoting disease by reducing
(or intracellular) environments that are unfavorable to wall integrity (Bouwmeester et al., 2011). Intriguingly,
oomycetes. This may explain why necrotrophy begins IPI-O contains an RxLR motif (Arg-x-Leu-Arg) that is
earlier in some Phytophthora-plant pathosystems than shared by many oomycete effectors that enter plant
others, although the water soaking that is often associated cells to interfere with plant defenses. In planta expres-
with plant cell death may keep the pathogen hydrated. sion of IPI-O minus its signal peptide caused expanded
The low level of free water resulting from silicon polym- lesions, suggesting that IPI-O acts both at the host
erization in the apoplast also was invoked to explain why plasmalemma and intracellularly (Chen and Halterman,
soybean grown at high silicon concentrations was less 2017). The intracellular target, apparently, is resistance
susceptible to Ph. sojae (Rasoolizadeh et al., 2018). protein Rpi-blb1 (Champouret et al., 2009).
RxLRs along with CRN (Crinkler) proteins represent
the known cytoplasmic effectors of oomycetes. These
are absent from Pythium spp. (Box 3) but are encoded by
MANY OOMYCETES HAVE EVOLVED ELABORATE
COUNTER DEFENSES
large gene families in Phytophthora spp., downy mil-
dews, and white rusts, albeit with divergent signature
Oomycetes exhibit stealthy behaviors during bio- motifs in some species (Kemen et al., 2011). How these
trophic growth that minimize the immune response and proteins move into plants is not fully clarified, but RxLR
maintain host integrity, which helps these pathogens uptake may involve binding a receptor on lipid rafts, as
feed from living cells. This is not an issue for necrotrophs shown for a host-targeted protein from the animal
such as Pythium spp. (Box 3). The (hemi)biotrophs resist pathogenic oomycete Saprolegnia parasitica (Trusch
host defenses using cytoplasmic and apoplastic effector et al., 2018). RxLRs and CRNs are known to defeat
proteins that are secreted toward their interface with plant immune responses through many routes, which
plants. Oomycetes also produce enzymes that may de- include reprogramming host gene expression, altering
grade phytoalexins or immune-response hormones. The RNA metabolism, and binding to host proteins in-
existence of these enzymes and effectors highlights the volved in signaling (Wang and Wang, 2018). In this
power of selection in the pathogen and the importance of review, mention will be made only of RxLRs that act at
their plant targets to the host defense response. the oomycete-plant interface.
One example involves the plant apoplastic Cys pro- Many RxLRs affect the trafficking of defense molecules.
teases Rcr3 and C14, which were shown by mutation AVRblb2 accumulates in plants near haustoria and blocks
the secretion of C14 protease (Bozkurt et al., 2011). (Fig. 1). These specialized hyphae breach host cell walls
RxLR24 of Phytophthora brassicae interferes with the de- and become enveloped by a host membrane called the
livery of antimicrobial proteins such as PR-1 by attaching extrahaustorial membrane (EHM). Between the haus-
to a GTPase involved in exocytosis (Tomczynska et al., torium and EHM is a carbohydrate-rich amorphous
2018). Trafficking also is blocked by Avr1 of Ph. infestans, layer called the extrahaustorial matrix (EHMx), which
which binds exocyst protein SEC5 (Du et al., 2015), REX3 likely is of plant and pathogen origin (Caillaud et al.,
of Ph. palmivora, which interferes with brefeldin-sensitive 2014). Little is known about how haustoria form
secretion (Evangelisti et al., 2017), and PexRD54 of Ph. and function in oomycetes, including how the host
infestans, which depletes the Joka2 cargo protein from the machinery is coopted during their genesis and what
autophagosomal membrane-forming ATG8 complex limits their expansion; most haustoria are less than
(Dagdas et al., 2016). The latter is interesting since the 25 mm long.
pathogen may be hijacking autophagosomes to destroy Recent studies with Ph. infestans and H. arabidopsidis

defense molecules through selective autophagy. indicated that the EHM is assembled de novo, as sug-
Although their functions are unidentified, the RxLRs gested for fungi (Lu et al., 2012; Bozkurt et al., 2015).
Avh241 of Ph. sojae and HaRxL77 of H. arabidopsidis Secretory vesicles are abundant near developing haus-
localize to the plant plasmalemma and are hypothe- toria, along with trans-Golgi and late endosomal
sized to bind PRRs at the plant-oomycete interface markers such as Rab5 and Rab7 GTPases (Caillaud
(Caillaud et al., 2012; Yu et al., 2012). Causing auxin et al., 2014; Inada et al., 2016). Within the EHM are
levels to rise at the interface is Penetration Specific Ef- plasmalemma proteins such as the Pen1 syntaxin,
fector1 of Ph. parasitica, which is made in appressoria synaptotagmin, and remorin, which would be needed
and interferes with auxin carriers (Evangelisti et al., 2013). to deliver membrane material to growing haustoria.
This may elevate plant susceptibility since auxin inhibits Some plant proteins are excluded from the EHM, in-
SA signaling. cluding a calcium ATPase and at least some PRRs
Interestingly, some species of Pythium are known to (Lu et al., 2012). Reduced ATPase activity could favor
produce the auxin indole-3-acetic acid (Gravel et al., nutrient flow to the pathogen by reducing the plant’s
2007). While there is no proof that oomycetes make capacity to retrieve nutrients from the EHMx, while
other plant hormones, the sunflower (Helianthus PRR exclusion may minimize defense responses.
annuus) downy mildew Plasmopara halstedii apparently Haustoria accommodation also causes host cells to re-
encodes all enzymes for synthesizing cytokinin, which organize their contents, with changes including endo-
some bacteria make to direct host nutrients to infection plasmic reticulum aggregation, Golgi accumulation,
sites (Sharma et al., 2015). Pl. halstedii also seems capa- and nuclear migration toward the haustoria (Lu et al.,
ble of producing brassinolide from phytosterols, which 2012). The nuclear shift might be part of a defense re-
would negatively regulate the immune response. Many sponse or may be induced by the pathogen to facilitate
oomycetes also encode a predicted isochorismatase, the transport of CRN effectors, many of which act by
which may disrupt SA signaling by breaking down its reprogramming transcription (Song et al., 2015).
precursor. Interestingly, the enzyme in Ph. sojae local- Whether the reorganized endomembrane system de-
izes to haustoria (Liu et al., 2014). livers more transporters and/or nutrients to the EHM is
Unlike fungi, most oomycetes have a limited capacity an interesting question.
to degrade phytoalexins. Perhaps to compensate, There are dissimilarities between haustoria of dif-
oomycetes encode many more ABC transporters, which ferent species. While haustoria made by Phytophthora
may expel the toxins (Ah-Fong et al., 2017b). While many spp. are typically short and finger-like, those of downy
fungi can degrade a-tomatine, Phytophthora and Pythium mildews and white rusts are bulbous. Moreover, while
spp. that are pathogenic on tomato fail to degrade this Ph. infestans haustoria are anucleate and contain few
glycoalkaloid (Sandrock and Vanetten, 1998). Ph. sojae mitochondria and endoplasmic reticulum, those of H.
can break down some soybean phytoalexins but not the arabidopsidis have nuclei and many mitochondria and
most bioactive, glyceollin (Stossel, 1983). Whether Golgi bodies (Mims et al., 2004). While the FLS2 PRR
Pythium spp. have special mechanisms to counteract was excluded from the EHM with Ph. infestans, this
plant defenses is unknown. However, during tuber in- was not the case with H. arabidopsidis (Lu et al., 2012).
fection, mRNA levels of Py. ultimum ABC transporters Downy mildew haustoria also are more likely to
were about twice those of their counterparts in Ph. be surrounded by a callose collar than those of
infestans, suggesting that the transporters might help Phytophthora spp.
eliminate phytoalexins liberated from lysing cells (Ah- Several aspects of haustoria formation resemble plant
Fong et al., 2017b). Cytochrome P450 enzymes also were defense responses. Deposition of the b-glucans that
more highly expressed in Py. ultimum. form callose collars involves secretory vesicles, multi-
vesicular bodies, and Plasmodesmata-located-protein1
(PDLP1), which also is used to seal plasmodesmata
during infection by other pathogens (Caillaud et al.,
HAUSTORIA REPRESENT A SPECIALIZED INTERFACE
2014). Also possibly related to defense are haustorial
Biotrophic and hemibiotrophic oomycetes form inti- encasements, which are double-layered membranes
mate associations with their hosts using haustoria that often surround older haustoria (Lu et al., 2012).
These are common with H. arabidopsidis but are seen less reduced metabolic capabilities and, thus, a greater re-
with Ph. infestans. Encasements might restrict the liance on the host. While species of Phytophthora and
pathogen’s uptake of nutrients, impair effector trans- Pythium each encode approximately 850 enzyme ac-
location, or concentrate plant-derived antimicrobials. tivities based on Enzyme Commission numbers, H.
The EHM appears to have small invaginations, which arabidopsidis and Al. candida encode only about 740 and
also may promote its stability (Mims et al., 2004). The 650, respectively (Judelson, 2017). These obligate bio-
formation of these convolutions appears to involve trophs lack genes for nitrate assimilation and have
PDLP1, since they increased when PDLP1 was over- impaired abilities to incorporate inorganic sulfur due to
expressed (Caillaud et al., 2014). a lack of sulfite oxidase or reductase.
Although the contribution of oomycete haustoria to The metabolic deficiencies in the (hemi)biotrophs
nutrient uptake is unclear, as discussed in the next may help suppress immune responses, besides pro-
section, the role of this structure in transporting providing potential energy savings to the pathogen. The

teins to the EHMx is demonstrated. Effectors are dis- biotrophs are unable to make unsaturated fatty acids
charged from haustoria through at least two such as arachidonate, which are PAMPs in Phytophthora
mechanisms. Secretion of the EPIC1 protease inhibitor and Pythium spp. (Robinson and Bostock, 2015). The
was blocked by brefeldin A, indicating that it reaches haustoria-forming oomycetes lack molybdopterin-
the apoplast by the classic Golgi-mediated pathway utilizing pathways and consequently must acquire
(Wang et al., 2017). However, the delivery of RxLR thiamine from the host. This may be beneficial, since
Pi04314 was brefeldin A insensitive, suggesting that this vitamin can up-regulate plant defenses, as dem-
this cytoplasmic effector follows an alternative route onstrated in the Pl. viticola-grape system (Boubakri
even though it contains a classic signal peptide. Iso- et al., 2013).
chorismatases also are secreted but lack signal peptides, It is important to differentiate the theoretical metab-
suggesting that they use the unconventional secretion olism of oomycetes from what occurs in planta, since
pathway that has been documented in nonoomycetes not all nutrients are at each plant-oomycete interface.
(Liu et al., 2014). While biotrophs are restricted to apoplastic nutrients,
necrotrophs can access all compounds. Examples in-
clude starch and sulfate, which are sequestered within
starch granules and vacuoles, respectively. Data from a
NUTRIENT ACQUISITION AT THE
PLANT-OOMYCETE INTERFACE
study of Ph. infestans and Py. ultimum on potato tubers
(Ah-Fong et al., 2017b) showed that while both encode
Although not proven, oomycete haustoria often are a-amylase for starch utilization and adenylyl-sulfate
assumed to play a major role in nutrition. Nevertheless, kinase for incorporating sulfate, the Py. ultimum genes
they lack the neckband that encircles fungal haustoria, were expressed at greater than 10-fold higher levels
which is thought to help establish electrochemical gra- (Box 3). This is the logical outcome of substrate-level
dients for nutrient transport by sealing the EHMx induction. This situation changed during late infection
(Mims et al., 2004). Al. candida and H. arabidopsidis when tissue colonized by Ph. infestans became necrotic,
contain an electron-dense layer near their callose col- and mRNA levels for these enzymes equalized between
lars, which might function like a neckband, however the two pathogens. Similar patterns were observed for
(Soylu, 2004). In Ph. infestans, EHMx continuity with the enzymes that act on other nutrients sequestered during
apoplast was confirmed by studying the distribution of biotrophic growth, such as phytate and lipids. This in-
fluorescently tagged Avr3a (Whisson et al., 2007). Also dicates that the terminal lifestyle of Ph. infestans is
unlike fungi, no haustoria-specific transporters are necrotrophic and not just necrogenic, thus addressing a
identified in oomycetes. While Ph. infestans and Py. debate in Phytophthora-host interactions. One position
ultimum both express ;410 nutrient transporters, very has been that plant necrosis does not benefit the path-
few are specific to the haustoria-forming species (Ah- ogen and occurs simply because the pathogen no longer
Fong et al., 2017b). Most nutrients may be drawn from needs to suppress host defenses. The other viewpoint,
the apoplast, considering that analyses of images of which is supported by these results, is that necrosis is
potato leaves infected by Ph. infestans indicate that its induced to liberate additional nutrients.
haustoria represent only about 2% of the total pathogen
surface area (H. Judelson, unpublished data).
Regardless of where nutrients are acquired, plants
OOMYCETES HAVE AN EXIT STRATEGY
contain myriad compounds to support pathogen
growth. Metabolic models based on genome data in- The final chapter in disease involves the pathogen’s
dicate that most oomycetes can utilize the major plant egress from its host. Necrotrophs such as Pythium spp.
hexoses, disaccharides, organic acids, starch, and sugar can simply extend hyphae from macerated plant tissue
alcohols, although pentose utilization is restricted by into soil and transition to survival through saprophytic
the absence of arabinose isomerase (Rodenburg et al., growth; sporulation is optional. In contrast, most
2018). Most oomycetes also can use the major nitrogen (hemi)biotrophs must produce asexual spores. These
sources found in planta, including amino acids, am- are typically formed by root-rotting species at the
monium, and nitrate. However, the biotrophs have crown, surface-exposed roots, or subterranean spaces
(Ah-Fong et al., 2017a). NMRA also was proposed to

OUTSTANDING QUESTIONS control the transcription of late-induced effectors in
Phytophthora capsici (Pham et al., 2018). Spiking at the
• Are there effectors that cause nutrients to flow same time are mRNAs for genes used to assimilate ni-
to the oomycete-plant interface? trate, which is a nonpreferred nitrogen source com-
• Do oomycete haustoria play a major role in pared with amino acids (Abrahamian et al., 2016). Since
nutrient uptake, or is protein secretion their a study in Phytophthora cactorum found that adding
main function? amino acids or ammonium to media did not retard
sporulation, the process also may be prompted by an
• What cargo is carried by plant exosomes to the
accumulated metabolite (Elliott, 1989). The plant also
oomycete-host interface?
may affect sporulation, since its metabolic pathways are
• Why does the shift from biotrophy to linked to those of the pathogen during colonization. A

necrotrophy occur early during infection by dual-species systems approach to metabolism may help
some Phytophthora spp. and later in others? understand what influences sporulation, effector ex-
• Can genome-scale modeling of metabolism pression, phytohormone levels, and other aspects of
yield insight into the basis of obligate plant-oomycete interactions.
biotrophy?
• What are the molecular and environmental
(including in planta) factors that trigger CONCLUSION
sporulation?
• Considering that much of our knowledge of Oomycetes have developed diverse lifestyles over
oomycete-plant interactions comes from studies
their 400+ million years of evolution (Taylor et al.,
2006). The (hemi)biotrophs have learned to coopt their
of Phytophthora spp., what is needed to
hosts by suppressing defenses and coercing plants to
accelerate investigations of other oomycetes? form interfaces for effector and nutrient delivery. Such
lifestyles may have evolved by exploiting pathways
used by plants to harbor mutualists, since mutants of
adjoining roots. The task is more complicated for M. truncatula deficient in mycorrhizae formation were
foliage-infecting (hemi)biotrophs, which usually spor- shown to have reduced susceptibility to Ph. palmivora
ulate from sporangiophores that pass through stomata (Rey et al., 2015). Many oomycetes have become host-
(Farrell et al., 1969; Allègre et al., 2007). Most foliage- adapted to the extent that they depend on plant me-
infecting oomycetes sporulate at night. This maximizes tabolites for growth or reproduction. In contrast,
survival of the spores, which are prone to desiccation necrotrophs have less-specialized lifestyles, as they can
and lack UV-blocking pigments. Nocturnal sporulation grow as saprophytes or pathogens, overpowering their
is proposed to be regulated by cryptochromes in re- hosts and perhaps even profiting from the plant im-
sponse to blue light (Xiang and Judelson, 2014) and mune response. Most oomycetes also have retained a
requires modulating guard cell behavior, since stomata flagellated life stage, which expands their access to new
would normally be closed at night. Stomatal deregu- hosts, although this comes with a large genomic bur-
lation in the Pl. viticola-grape leaf interaction was pro- den. Meanwhile, plants have evolved complex multi-
posed to be determined by a secreted glycoprotein, layered defenses that balance survival against the
which caused stomata in colonized areas to remain growth penalty that comes from activating the immune
open during darkness, water stress, and abscisic acid response (Ning et al., 2017).
treatment (Allègre et al., 2007; Guillier et al., 2015). This Many of the defenses, counter defenses, spore be-
effect resembles that caused by the bacterial toxin cor- haviors, and interactions with other microbes that we
onatine (Melotto et al., 2006). have described have small individual effects on disease
Substantial genomic resources are devoted to spor- outcomes but are significant from an epidemiological
ulation. In Ph. infestans, this involves the up-regulation perspective. The infection potential of an oomycete
of more than 3,000 genes (;20% of the total), including spore on plant tissue is usually much less than 100%,
those encoding storage, effector, and adhesion proteins, similar to the situation in fungi (Mellersh and Heath,
and several hundred components of flagella (Judelson 2002; Kong and Hong, 2016). The progress of an epi-
et al., 2012; Ah-Fong et al., 2017a). Genes proven to demic will be influenced by factors that raise or lower
regulate sporulation include MADS box and Myb this infection potential or the time between penetration
transcription factors, a mitogen-activated protein ki- and sporulation (Willocquet et al., 2017). While many
nase, and a cell cycle phosphatase (Ah-Fong and plant scientists aim to develop strong resistance against
Judelson, 2011; Li et al., 2014; Xiang and Judelson, pathogens, natural defenses (as well as changes in
2014). However, the primary trigger for sporulation is pathogens that enhance fitness) need not have block-
unknown. Nutrient limitation is thought to play a role, buster effects to be retained during evolution.
which is concordant with the finding that the nitrogen Our knowledge of interactions involving Phytoph-
metabolite repression regulator NMRA is down- thora spp. has grown dramatically due to the avail-
regulated near the onset of sporulation in Ph. infestans ability of genome sequences and tools for functional
genomics, but research into other oomycetes has lag- Boubakri H, Chong J, Poutaraud A, Schmitt C, Bertsch C, Mliki A,
Masson JE, Soustre-Gacougnolle I (2013) Riboflavin (vitamin B-2) in-
ged. It is unfortunate that Pythium spp. have remained
duces defence responses and resistance to Plasmopara viticola in grape-
little studied despite their large agricultural impact, for vine. Eur J Plant Pathol 136: 837–855
example. Most Pythium spp. are easily cultured, so it Bouwmeester K, de Sain M, Weide R, Gouget A, Klamer S, Canut H,
should be possible for a new generation of researchers Govers F (2011) The lectin receptor kinase LecRK-I.9 is a novel Phy-
to improve our understanding of the genus. Studying tophthora resistance component and a potential host target for a RXLR
effector. PLoS Pathog 7: e1001327
the breadth of oomycetes is important since crop pro- Bozkurt TO, Schornack S, Win J, Shindo T, Ilyas M, Oliva R, Cano LM,
tection solutions developed for one group may not Jones AME, Huitema E, van der Hoorn RAL, et al (2011) Phytophthora
translate to others. infestans effector AVRblb2 prevents secretion of a plant immune prote-
ase at the haustorial interface. Proc Natl Acad Sci USA 108: 20832–20837
Received August 7, 2018; accepted November 19, 2018; published December 11,
Bozkurt TO, Belhaj K, Dagdas YF, Chaparro-Garcia A, Wu CH, Cano LM,
2018.
Kamoun S (2015) Rerouting of plant late endocytic trafficking toward a

pathogen interface. Traffic 16: 204–226
Brunner F, Rosahl S, Lee J, Rudd JJ, Geiler C, Kauppinen S, Rasmussen
LITERATURE CITED G, Scheel D, Nürnberger T (2002) Pep-13, a plant defense-inducing
Abrahamian M, Ah-Fong AM, Davis C, Andreeva K, Judelson HS (2016) pathogen-associated pattern from Phytophthora transglutaminases.
Gene expression and silencing studies in Phytophthora infestans reveal EMBO J 21: 6681–6688
Cai Q, Qiao L, Wang M, He B, Lin FM, Palmquist J, Huang SD, Jin H
infection-specific nutrient transporters and a role for the nitrate reduc-
(2018) Plants send small RNAs in extracellular vesicles to fungal path-
tase pathway in plant pathogenesis. PLoS Pathog 12: e1006097
ogen to silence virulence genes. Science 360: 1126–1129
Ah-Fong AM, Judelson HS (2011) New role for Cdc14 phosphatase: Lo-
Caillaud MC, Piquerez SJM, Fabro G, Steinbrenner J, Ishaque N, Beynon
calization to basal bodies in the oomycete Phytophthora and its evolu-
J, Jones JDG (2012) Subcellular localization of the Hpa RxLR effector
tionary coinheritance with eukaryotic flagella. PLoS ONE 6: e16725
repertoire identifies a tonoplast-associated protein HaRxL17 that confers
Ah-Fong AM, Kim KS, Judelson HS (2017a) RNA-seq of life stages of the
enhanced plant susceptibility. Plant J 69: 252–265
oomycete Phytophthora infestans reveals dynamic changes in metabolic,
Caillaud MC, Wirthmueller L, Sklenar J, Findlay K, Piquerez SJM, Jones
signal transduction, and pathogenesis genes and a major role for cal- AME, Robatzek S, Jones JDG, Faulkner C (2014) The plasmodesmal
cium signaling in development. BMC Genomics 18: 198 protein PDLP1 localises to haustoria-associated membranes during
Ah-Fong AMV, Shrivastava J, Judelson HS (2017b) Lifestyle, gene gain downy mildew infection and regulates callose deposition. PLoS Pathog
and loss, and transcriptional remodeling cause divergence in the tran- 10: e1004496
scriptomes of Phytophthora infestans and Pythium ultimum during potato Carzaniga R, Bowyer P, O’Connell RJ (2001) Production of extracellular
tuber colonization. BMC Genomics 18: 764 matrices during development of infection structures by the downy
Albert I, Böhm H, Albert M, Feiler CE, Imkampe J, Wallmeroth N, mildew Peronospora parasitica. New Phytol 149: 83–93
Brancato C, Raaymakers TM, Oome S, Zhang H, et al (2015) An RLP23- Champouret N, Bouwmeester K, Rietman H, van der Lee T, Maliepaard
SOBIR1-BAK1 complex mediates NLP-triggered immunity. Nat Plants C, Heupink A, van de Vondervoort PJ, Jacobsen E, Visser RG, van der
1: 15140 Vossen EA, et al (2009) Phytophthora infestans isolates lacking class I ipiO
Allègre M, Daire X, Héloir MC, Trouvelot S, Mercier L, Adrian M, variants are virulent on Rpi-blb1 potato. Mol Plant Microbe Interact 22:
Pugin A (2007) Stomatal deregulation in Plasmopara viticola-infected 1535–1545
grapevine leaves. New Phytol 173: 832–840 Chang YH, Yan HZ, Liou RF (2015) A novel elicitor protein from Phy-
Aram K, Rizzo DM (2018) Distinct trophic specializations affect how tophthora parasitica induces plant basal immunity and systemic acquired
Phytophthora ramorum and clade 6 Phytophthora spp. colonize and persist resistance. Mol Plant Pathol 16: 123–136
on Umbellularia californica leaves in streams. Phytopathology 108: Chen Y, Halterman DA (2017) Determination of virulence contribution
858–869 from Phytophthora infestans effector Ipi-O4 in a resistant potato host
Avrova AO, Boevink PC, Young V, Grenville-Briggs LJ, van West P, containing the RB gene. Physiol Mol Plant Pathol 100: 30–34
Birch PR, Whisson SC (2008) A novel Phytophthora infestans haustorium- Dagdas YF, Belhaj K, Maqbool A, Chaparro-Garcia A, Pandey P, Petre B,
specific membrane protein is required for infection of potato. Cell Mi- Tabassum N, Cruz-Mireles N, Hughes RK, Sklenar J, et al (2016) An
crobiol 10: 2271–2284 effector of the Irish potato famine pathogen antagonizes a host au-
Barros J, Serk H, Granlund I, Pesquet E (2015) The cell biology of ligni- tophagy cargo receptor. eLife 5: e10856
fication in higher plants. Ann Bot 115: 1053–1074 Dagdas YF, Pandey P, Tumtas Y, Sanguankiattichai N, Belhaj K, Duggan
Beakes GW, Glockling SL, Sekimoto S (2012) The evolutionary phylogeny C, Leary AY, Segretin ME, Contreras MP, Savage Z, et al (2018) Host
autophagy machinery is diverted to the pathogen interface to mediate
of the oomycete “fungi.” Protoplasma 249: 3–19
Bednarek P, Schneider B, Svatos A, Oldham NJ, Hahlbrock K (2005) focal defense responses against the Irish potato famine pathogen. eLife
7: e37476
Structural complexity, differential response to infection, and tissue
Dale ML, Irwin JAG (1991) Stomata as an infection court for Phytophthora
specificity of indolic and phenylpropanoid secondary metabolism in
megasperma f. sp. medicaginis in chickpea and a histological study of
Arabidopsis roots. Plant Physiol 138: 1058–1070
infection. Phytopathology 81: 375–379
Benhamou N, le Floch G, Vallance J, Gerbore J, Grizard D, Rey P (2012)
Deacon JW, Donaldson SP (1993) Molecular recognition in the homing
Pythium oligandrum: An example of opportunistic success. Microbiology
responses of zoosporic fungi, with special reference to Pythium and
158: 2679–2694
Phytophthora. Mycol Res 97: 1153–1171
Bircher U, Hohl HR (1997) Environmental signalling during induction of
Derevnina L, Dagdas YF, De la Concepcion JC, Bialas A, Kellner R, Petre
appressorium formation in Phytophthora. Mycol Res 101: 395–402 B, Domazakis E, Du J, Wu CH, Lin X, et al (2016) Nine things to know
Blackman LM, Cullerne DP, Torreña P, Taylor J, Hardham AR (2015) about elicitins. New Phytol 212: 888–895
RNA-seq analysis of the expression of genes encoding cell wall de- Domazakis E, Wouters D, Visser RGF, Kamoun S, Joosten MHAJ,
grading enzymes during infection of lupin (Lupinus angustifolius) by Vleeshouwers VGAA (2018) The ELR-SOBIR1 complex functions as a
Phytophthora parasitica. PLoS ONE 10: e0136899 two-component receptor-like kinase to mount defense against Phytoph-
Blanco FA, Judelson HS (2005) A bZIP transcription factor from Phytoph- thora infestans. Mol Plant Microbe Interact 31: 795–802
thora interacts with a protein kinase and is required for zoospore mo- Dong S, Stam R, Cano LM, Song J, Sklenar J, Yoshida K, Bozkurt TO,
tility and plant infection. Mol Microbiol 56: 638–648 Oliva R, Liu Z, Tian M, et al (2014) Effector specialization in a lineage of
Böhm H, Albert I, Oome S, Raaymakers TM, Van den Ackerveken G, the Irish potato famine pathogen. Science 343: 552–555
Nürnberger T (2014) A conserved peptide pattern from a widespread Du Y, Mpina MH, Birch PRJ, Bouwmeester K, Govers F (2015) Phytoph-
microbial virulence factor triggers pattern-induced immunity in Arabi- thora infestans RXLR effector AVR1 interacts with exocyst component
dopsis. PLoS Pathog 10: e1004491 Sec5 to manipulate plant immunity. Plant Physiol 169: 1975–1990

Ekchaweng K, Evangelisti E, Schornack S, Tian M, Churngchow N (2017) Jack ALH, Nelson EB (2018) A seed-recruited microbiome protects devel-
The plant defense and pathogen counterdefense mediated by Hevea oping seedlings from disease by altering homing responses of Pythium
brasiliensis serine protease HbSPA and Phytophthora palmivora extracel- aphanidermatum zoospores. Plant Soil 422: 209–222
lular protease inhibitor PpEPI10. PLoS ONE 12: e0175795 Jahan SN, Åsman AK, Corcoran P, Fogelqvist J, Vetukuri RR, Dixelius C
El-Hamalawi ZA, Erwin DC (1986) Components in alfalfa Medicago sativa (2015) Plant-mediated gene silencing restricts growth of the potato late
root extract and root exudate that increase oospore germination of blight pathogen Phytophthora infestans. J Exp Bot 66: 2785–2794
Phytophthora megasperma f. sp. medicaginis. Phytopathology 76: 508–513 Judelson HS (2017) Metabolic diversity and novelties in the oomycetes.
Elliott CG (1989) Some aspects of nitrogen nutrition and reproduction in Annu Rev Microbiol 71: 21–39
Phytophthora. Mycol Res 92: 34–44 Judelson HS, Shrivastava J, Manson J (2012) Decay of genes encoding the
Evangelisti E, Govetto B, Minet-Kebdani N, Kuhn ML, Attard A, Ponchet oomycete flagellar proteome in the downy mildew Hyaloperonospora
M, Panabières F, Gourgues M (2013) The Phytophthora parasitica RXLR arabidopsidis. PLoS ONE 7: e47624
effector penetration-specific effector 1 favours Arabidopsis thaliana in- Kamoun S, Furzer O, Jones JD, Judelson HS, Ali GS, Dalio RJ, Roy SG,
fection by interfering with auxin physiology. New Phytol 199: 476–489 Schena L, Zambounis A, Panabières F, et al (2015) The top 10 oomycete
Evangelisti E, Gogleva A, Hainaux T, Doumane M, Tulin F, Quan C, pathogens in molecular plant pathology. Mol Plant Pathol 16: 413–434

Yunusov T, Floch K, Schornack S (2017) Time-resolved dual tran- Kaschani F, Shabab M, Bozkurt T, Shindo T, Schornack S, Gu C, Ilyas M,
scriptomics reveal early induced Nicotiana benthamiana root genes and Win J, Kamoun S, van der Hoorn RA (2010) An effector-targeted pro-
conserved infection-promoting Phytophthora palmivora effectors. BMC tease contributes to defense against Phytophthora infestans and is under
Biol 15: 39 diversifying selection in natural hosts. Plant Physiol 154: 1794–1804
Farrell GM, Preece TF, Wren MJ (1969) Effects of infection by Phytophthora Kebdani N, Pieuchot L, Deleury E, Panabières F, Le Berre JY, Gourgues
infestans on the stomata of potato leaves. Ann Appl Biol 63: 265–275 M (2010) Cellular and molecular characterization of Phytophthora para-
Fawke S, Doumane M, Schornack S (2015) Oomycete interactions with sitica appressorium-mediated penetration. New Phytol 185: 248–257
plants: Infection strategies and resistance principles. Microbiol Mol Biol Kemen E, Gardiner A, Schultz-Larsen T, Kemen AC, Balmuth AL,
Rev 79: 263–280 Robert-Seilaniantz A, Bailey K, Holub E, Studholme DJ, Maclean D,
Feng BZ, Zhu XP, Fu L, Lv RF, Storey D, Tooley P, Zhang XG (2014) et al (2011) Gene gain and loss during evolution of obligate parasitism in
Characterization of necrosis-inducing NLP proteins in Phytophthora the white rust pathogen of Arabidopsis thaliana. PLoS Biol 9: e1001094
capsici. BMC Plant Biol 14: 126 Kiefer B, Riemann M, Büche C, Kassemeyer HH, Nick P (2002) The host
Galiana E, Rivière MP, Pagnotta S, Baudouin E, Panabières F, Gounon P, guides morphogenesis and stomatal targeting in the grapevine pathogen
Boudier L (2005) Plant-induced cell death in the oomycete pathogen Plasmopara viticola. Planta 215: 387–393
Phytophthora parasitica. Cell Microbiol 7: 1365–1378 Kong P, Hong C (2016) Soil bacteria as sources of virulence signal pro-
Gaulin E, Jauneau A, Villalba F, Rickauer M, Esquerré-Tugayé MT, viders promoting plant infection by Phytophthora pathogens. Sci Rep 6:
Bottin A (2002) The CBEL glycoprotein of Phytophthora parasitica var- 33239
nicotianae is involved in cell wall deposition and adhesion to cellulosic Kots K, Meijer HJG, Bouwmeester K, Govers F, Ketelaar T (2017) Fila-
substrates. J Cell Sci 115: 4565–4575 mentous actin accumulates during plant cell penetration and cell wall
Govindarajulu M, Epstein L, Wroblewski T, Michelmore RW (2015) Host- plug formation in Phytophthora infestans. Cell Mol Life Sci 74: 909–920
induced gene silencing inhibits the biotrophic pathogen causing downy Kourelis J, van der Hoorn RAL (2018) Defended to the nines: 25 years of
mildew of lettuce. Plant Biotechnol J 13: 875–883 resistance gene cloning identifies nine mechanisms for R protein func-
Granke LL, Windstam ST, Hoch HC, Smart CD, Hausbeck MK (2009) tion. Plant Cell 30: 285–299
Dispersal and movement mechanisms of Phytophthora capsici sporangia. Lamour K, Kamoun S (2009) Oomycete Genetics and Genomics: Diversity,
Phytopathology 99: 1258–1264 Interactions, and Research Tools. John Wiley and Sons, Hoboken, NJ
Gravel V, Antoun H, Tweddell RJ (2007) Effect of indole-acetic acid (IAA) Larousse M, Govetto B, Séassau A, Etienne C, Industri B,
on the development of symptoms caused by Pythium ultimum on tomato Theodorakopoulos N, Deleury E, Ponchet M, Panabières F, Galiana E
plants. Eur J Plant Pathol 119: 457–462 (2014) Characterization of PPMUCL1/2/3, three members of a new
Gui YJ, Chen JY, Zhang DD, Li NY, Li TG, Zhang WQ, Wang XY, Short oomycete-specific mucin-like protein family residing in Phytophthora
DPG, Li L, Guo W, et al (2017) Verticillium dahliae manipulates plant parasitica biofilm. Protist 165: 275–292
immunity by glycoside hydrolase 12 proteins in conjunction with Latijnhouwers M, Ligterink W, Vleeshouwers VGAA, van West P,
carbohydrate-binding module 1. Environ Microbiol 19: 1914–1932 Govers F (2004) A Galpha subunit controls zoospore motility and vir-
Guillier C, Gamm M, Lucchi G, Truntzer C, Pecqueur D, Ducoroy P, ulence in the potato late blight pathogen Phytophthora infestans. Mol
Adrian M, Héloir MC (2015) Toward the identification of two glyco- Microbiol 51: 925–936
proteins involved in the stomatal deregulation of downy mildew- Lenarčič T, Albert I, Böhm H, Hodnik V, Pirc K, Zavec AB, Podobnik M,
infected grapevine leaves. Mol Plant Microbe Interact 28: 1227–1236 Pahovnik D, Žagar E, Pruitt R, et al (2017) Eudicot plant-specific
Hahn MG, Bonhoff A, Grisebach H (1985) Quantitative localization of the sphingolipids determine host selectivity of microbial NLP cytolysins.
phytoalexin glyceollin I in relation to fungal hyphae in soybean roots Science 358: 1431–1434
infected with Phytophthora megasperma f. sp. glycinea. Plant Physiol 77: Li J, Staiger CJ (2018) Understanding cytoskeletal dynamics during the
591–601 plant immune response. Annu Rev Phytopathol 56: 513–533
Halim VA, Altmann S, Ellinger D, Eschen-Lippold L, Miersch O, Scheel Li A, Wang Y, Tao K, Dong S, Huang Q, Dai T, Zheng X, Wang Y (2010)
D, Rosahl S (2009) PAMP-induced defense responses in potato require PsSAK1, a stress-activated MAP kinase of Phytophthora sojae, is required
both salicylic acid and jasmonic acid. Plant J 57: 230–242 for zoospore viability and infection of soybean. Mol Plant Microbe In-
Hosseini S, Heyman F, Olsson U, Broberg A, Jensen DF, Karlsson M teract 23: 1022–1031
(2014) Zoospore chemotaxis of closely related legume-root infecting Li A, Zhang M, Wang Y, Li D, Liu X, Tao K, Ye W, Wang Y (2014) PsMPK1,
Phytophthora species towards host isoflavones. Plant Pathol 63: 708–714 an SLT2-type mitogen-activated protein kinase, is required for hyphal
Hosseini S, Elfstrand M, Heyman F, Jensen DF, Karlsson M (2015) De- growth, zoosporogenesis, cell wall integrity, and pathogenicity in Phy-
ciphering common and specific transcriptional immune responses in pea tophthora sojae. Fungal Genet Biol 65: 14–24
towards the oomycete pathogens Aphanomyces euteiches and Phytoph- Lioussanne L, Jolicoeur M, St-Arnaud M (2008) Mycorrhizal colonization
thora pisi. BMC Genomics 16: 627 with Glomus intraradices and development stage of transformed tomato
Hua C, Wang Y, Zheng X, Dou D, Zhang Z, Govers F, Wang Y (2008) A roots significantly modify the chemotactic response of zoospores of the
Phytophthora sojae G-protein alpha subunit is involved in chemotaxis to pathogen Phytophthora nicotianae. Soil Biol Biochem 40: 2217–2224
soybean isoflavones. Eukaryot Cell 7: 2133–2140 Liu T, Song T, Zhang X, Yuan H, Su L, Li W, Xu J, Liu S, Chen L, Chen T,
Inada N, Betsuyaku S, Shimada TL, Ebine K, Ito E, Kutsuna N, Hasezawa et al (2014) Unconventionally secreted effectors of two filamentous
S, Takano Y, Fukuda H, Nakano A, et al (2016) Modulation of plant pathogens target plant salicylate biosynthesis. Nat Commun 5: 4686
RAB GTPase-mediated membrane trafficking pathway at the interface Lu YJ, Schornack S, Spallek T, Geldner N, Chory J, Schellmann S,
between plants and obligate biotrophic pathogens. Plant Cell Physiol 57: Schumacher K, Kamoun S, Robatzek S (2012) Patterns of plant sub-
1854–1864 cellular responses to successful oomycete infections reveal differences in

host cell reprogramming and endocytic trafficking. Cell Microbiol 14: Saijo Y, Loo EP, Yasuda S (2018) Pattern recognition receptors and sig-
682–697 naling in plant-microbe interactions. Plant J 93: 592–613
Ma Z, Zhu L, Song T, Wang Y, Zhang Q, Xia Y, Qiu M, Lin Y, Li H, Kong Sandrock RW, Vanetten HD (1998) Fungal sensitivity to and enzymatic
L, et al (2017) A paralogous decoy protects Phytophthora sojae apoplastic degradation of the phytoanticipin alpha-tomatine. Phytopathology 88:
effector PsXEG1 from a host inhibitor. Science 355: 710–714 137–143
Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH Schlatter D, Kinkel L, Thomashow L, Weller D, Paulitz T (2017) Disease
oxidases. Trends Plant Sci 17: 9–15 suppressive soils: New insights from the soil microbiome. Phytopa-
McCarren KL, McComb JA, Shearer BL, Hardy GESJ (2005) The role of thology 107: 1284–1297
chlamydospores of Phytophthora cinnamomi: A review. Australasian Sekizaki H, Yokosawa R, Chinen C, Adachi H, Yamane Y (1993) Studies
Plant Pathology 34: 333–338 on zoospore attracting activity. II. Synthesis of isoflavones and their
Mélida H, Sandoval-Sierra JV, Diéguez-Uribeondo J, Bulone V (2013) attracting activity to Aphanomyces euteiches zoospore. Biol Pharm Bull
Analyses of extracellular carbohydrates in oomycetes unveil the exis- 16: 698–701
tence of three different cell wall types. Eukaryot Cell 12: 194–203 Shang H, Grau CR, Peters RD (2000) Oospore germination of Aphanomyces
Mellersh DG, Heath MC (2002) Nonhost resistance to rust fungi in Ara- euteiches in root exudates and on the rhizoplanes of crop plants. Plant

bidopsis. Plant Biol 2002: 127 Dis 84: 994–998
Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant Sharma R, Xia X, Cano LM, Evangelisti E, Kemen E, Judelson H, Oome S,
stomata function in innate immunity against bacterial invasion. Cell 126: Sambles C, van den Hoogen DJ, Kitner M, et al (2015) Genome anal-
969–980 yses of the sunflower pathogen Plasmopara halstedii provide insights into
Mims CW, Richardson EA, Holt BF, Dangl JL (2004) Ultrastructure of the effector evolution in downy mildews and Phytophthora. BMC Genomics
host-pathogen interface in Arabidopsis thaliana leaves infected by the 16: 741
downy mildew Hyaloperonospora parasitica. Can J Bot 82: 1001–1008 Song J, Win J, Tian M, Schornack S, Kaschani F, Ilyas M, van der Hoorn
Morris PF, Bone E, Tyler BM (1998) Chemotropic and contact responses of RAL, Kamoun S (2009) Apoplastic effectors secreted by two unrelated
Phytophthora sojae hyphae to soybean isoflavonoids and artificial sub- eukaryotic plant pathogens target the tomato defense protease Rcr3.
strates. Plant Physiol 117: 1171–1178 Proc Natl Acad Sci USA 106: 1654–1659
Mostowfizadeh-Ghalamfarsa R, Hussaini K, Ghasemi-Fasaei R (2018) Song T, Ma Z, Shen D, Li Q, Li W, Su L, Ye T, Zhang M, Wang Y, Dou D
Effects of calcium salts in controlling Phytophthora pistaciae, the causal (2015) An oomycete CRN effector reprograms expression of plant HSP
agent of pistachio gummosis. Eur J Plant Pathol 151: 475–485 genes by targeting their promoters. PLoS Pathog 11: e1005348
Nars A, Lafitte C, Chabaud M, Drouillard S, Mélida H, Danoun S, Le Soylu S (2004) Ultrastructural characterisation of the host-pathogen inter-
Costaouëc T, Rey T, Benedetti J, Bulone V, et al (2013) Aphanomyces face in white blister-infected Arabidopsis leaves. Mycopathologia 158:
euteiches cell wall fractions containing novel glucan-chitosaccharides 457–464
induce defense genes and nuclear calcium oscillations in the plant host Staswick PE, Yuen GY, Lehman CC (1998) Jasmonate signaling mutants of
Medicago truncatula. PLoS ONE 8: e75039 Arabidopsis are susceptible to the soil fungus Pythium irregulare. Plant J
Nelson EB (1987) Rapid germination of sporangia of Pythium spp. in re- 15: 747–754
sponse to volatiles from germinating seeds. Phytopathology 77: Stossel P (1983) In vitro effects of glyceollin on Phytophthora megasperma f.
1108–1112 sp. glycinea. Phytopathology 73: 1603–1607
Ning Y, Liu W, Wang GL (2017) Balancing immunity and yield in crop Takemoto D, Jones DA, Hardham AR (2003) GFP-tagging of cell compo-
plants. Trends Plant Sci 22: 1069–1079 nents reveals the dynamics of subcellular re-organization in response to
Pham J, Stam R, Heredia VM, Csukai M, Huitema E (2018) An NMRA-like infection of Arabidopsis by oomycete pathogens. Plant J 33: 775–792
protein regulates gene expression in Phytophthora capsici to drive the Takenaka S, Yamaguchi K, Masunaka A, Hase S, Inoue T, Takahashi H
infection cycle on tomato. Mol Plant Microbe Interact 31: 665–677 (2011) Implications of oligomeric forms of POD-1 and POD-2 proteins
Pittis JE, Shattock RC (1994) Viability, germination and infection potential isolated from cell walls of the biocontrol agent Pythium oligandrum in
of oospores of Phytophthora infestans. Plant Pathol 43: 387–396 relation to their ability to induce defense reactions in tomato. J Plant
Ploch S, Thines M (2011) Obligate biotrophic pathogens of the genus Al- Physiol 168: 1972–1979
bugo are widespread as asymptomatic endophytes in natural popula- Taylor TN, Krings M, Kerp H (2006) Hassiella monospora gen. et sp. nov., a
tions of Brassicaceae. Mol Ecol 20: 3692–3699 microfungus from the 400 million year old Rhynie chert. Mycol Res 110:
Raaijmakers JM, De Bruijn I, Nybroe O, Ongena M (2010) Natural 628–632
functions of lipopeptides from Bacillus and Pseudomonas: More than Tomczynska I, Stumpe M, Mauch F (2018) A conserved RxLR effector
surfactants and antibiotics. FEMS Microbiol Rev 34: 1037–1062 interacts with host RABA-type GTPases to inhibit vesicle-mediated se-
Rasoolizadeh A, Labbé C, Sonah H, Deshmukh RK, Belzile F, Menzies cretion of antimicrobial proteins. Plant J 95: 187–203
JG, Bélanger RR (2018) Silicon protects soybean plants against Phy- Trusch F, Loebach L, Wawra S, Durward E, Wuensch A, Iberahim NA, de
tophthora sojae by interfering with effector-receptor expression. BMC Bruijn I, MacKenzie K, Willems A, Toloczko A, et al (2018) Cell entry
Plant Biol 18: 97 of a host-targeting protein of oomycetes requires gp96. Nat Commun 9:
Resjö S, Brus M, Ali A, Meijer HJG, Sandin M, Govers F, Levander F, 2347
Grenville-Briggs L, Andreasson E (2017) Proteomic analysis of Phy- van den Hoogen DJ, Meijer HJG, Seidl MF, Govers F (2018) The ancient
tophthora infestans reveals the importance of cell wall proteins in path- link between G-protein-coupled receptors and C-terminal phospholipid
ogenicity. Mol Cell Proteomics 16: 1958–1971 kinase domains. MBio 9: e02119-17
Rey T, Chatterjee A, Buttay M, Toulotte J, Schornack S (2015) Medicago Wang Y, Wang Y (2018) Phytophthora sojae effectors orchestrate warfare
truncatula symbiosis mutants affected in the interaction with a bio- with host immunity. Curr Opin Microbiol 46: 7–13
trophic root pathogen. New Phytol 206: 497–500 Wang S, Boevink PC, Welsh L, Zhang R, Whisson SC, Birch PRJ (2017)
Rin S, Mizuno Y, Shibata Y, Fushimi M, Katou S, Sato I, Chiba S, Delivery of cytoplasmic and apoplastic effectors from Phytophthora in-
Kawakita K, Takemoto D (2017) EIN2-mediated signaling is involved in festans haustoria by distinct secretion pathways. New Phytol 216:
pre-invasion defense in Nicotiana benthamiana against potato late blight 205–215
pathogen, Phytophthora infestans. Plant Signal Behav 12: e1300733 Wang Y, Bouwmeester K, van de Mortel JE, Shan W, Govers F (2013) A
Robinson SM, Bostock RM (2015) b-Glucans and eicosapolyenoic acids as novel Arabidopsis-oomycete pathosystem: Differential interactions with
MAMPs in plant-oomycete interactions: Past and present. Front Plant Phytophthora capsici reveal a role for camalexin, indole glucosinolates
Sci 5: 797 and salicylic acid in defence. Plant Cell Environ 36: 1192–1203
Robold AV, Hardham AR (2005) During attachment Phytophthora spores Wang Y, Xu Y, Sun Y, Wang H, Qi J, Wan B, Ye W, Lin Y, Shao Y, Dong S,
secrete proteins containing thrombospondin type 1 repeats. Curr Genet et al (2018) Leucine-rich repeat receptor-like gene screen reveals that
47: 307–315 Nicotiana RXEG1 regulates glycoside hydrolase 12 MAMP detection. Nat
Rodenburg SYA, Seidl MF, de Ridder D, Govers F (2018) Genome-wide Commun 9: 594
characterization of Phytophthora infestans metabolism: A systems biology Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, Gilroy
approach. Mol Plant Pathol 19: 1403–1413 EM, Armstrong MR, Grouffaud S, van West P, Chapman S, et al (2007)

A translocation signal for delivery of oomycete effector proteins into Yu X, Tang J, Wang Q, Ye W, Tao K, Duan S, Lu C, Yang X, Dong S,
host plant cells. Nature 450: 115–118 Zheng X, et al (2012) The RxLR effector Avh241 from Phytophthora sojae
Willocquet L, Savary S, Yuen J (2017) Multiscale phenotyping and decision requires plasma membrane localization to induce plant cell death. New
strategies in breeding for resistance. Trends Plant Sci 22: 420–432 Phytol 196: 247–260
Windstam S, Nelson EB (2008) Differential interference with Pythium ul- Zerillo MM, Adhikari BN, Hamilton JP, Buell CR, Lévesque CA, Tisserat
timum sporangial activation and germination by Enterobacter cloacae in N (2013) Carbohydrate-active enzymes in Pythium and their role in plant
the corn and cucumber spermospheres. Appl Environ Microbiol 74: cell wall and storage polysaccharide degradation. PLoS ONE 8: e72572
4285–4291 Zhang W, Blackman LM, Hardham AR (2013) Transient fusion and se-
Xiang Q, Judelson HS (2014) Myb transcription factors and light regulate lective secretion of vesicle proteins in Phytophthora nicotianae zoospores.
sporulation in the oomycete Phytophthora infestans. PLoS ONE 9: e92086 PeerJ 1: e221
Yang X, Zhao W, Hua C, Zheng X, Jing M, Li D, Govers F, Meijer HJG, Zhang X, Zhai C, Hua C, Qiu M, Hao Y, Nie P, Ye W, Wang Y (2016)
Wang Y (2013) Chemotaxis and oospore formation in Phytophthora sojae PsHint1, associated with the G-protein a subunit PsGPA1, is required
are controlled by G-protein-coupled receptors with a phosphatidylino- for the chemotaxis and pathogenicity of Phytophthora sojae. Mol Plant
sitol phosphate kinase domain. Mol Microbiol 88: 382–394 Pathol 17: 272–285

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Update on Plant-Oomycete Interactions

Exchanges at the Plant-Oomycete Interface That

Howard S. Judelson,2,3 and Audrey M. V. Ah-Fong

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BOX 1. A Diversity of Infectious Propagules

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BOX 2. Other Microbes at the Interface: Friend

A plant-oomycete interaction does not zoospores (Kong and Hong, 2016).

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1202 Plant Physiol. Vol. 179, 2019

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(Ah-Fong et al., 2017a). NMRA also was proposed to

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1208 Plant Physiol. Vol. 179, 2019

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Plant Physiol. Vol. 179, 2019 1209

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1210 Plant Physiol. Vol. 179, 2019

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Plant Physiol. Vol. 179, 2019 1211

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