host specificity, host specialization and host jump of
TRANSCRIPT
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Host specificity, host specialization and host jump of Phytophthora
species: a review
Alejandra González Ruiz, Martha Cárdenas, Silvia Restrepo
Resumen
Los oomicetes taxonómicamente son un grupo extendido de fitopatógenos. Entre ellos, los
miembros del género Phytophthora han sido reconocidos como los patógenos más
importantes y destructivos de diversos hospederos. El oomicete mejor estudiado es
Phytophthora infestans, incluido en el clado 1c de Phytophthora. Dentro de este clado seis
especies se han reportado como las especies hermanas más cercanas a P. infestans,
incluyendo la especie recientemente descrita P. betacei. Esta especie es la causante de la
enfermedad del tizón tardío en el tomate de árbol (Solanum betacum) en la región andina y
ha sido considerada como un punto focal relevante debido a la continua expansión de dicha
enfermedad en Colombia. Se revisa la información actual de los términos relacionados con
el rango de hospedero, la especificidad de hospedero, la especialización de hospedero y el
salto de los mismos dentro de las especies de oomicetes y Phytophthora, con el fin de
proporcionar un marco que contribuya a la comprensión de la biología de P. betacei. En este
trabajo se concluye que: i) no hay ningún parámetro para la categorización del rango de
hospederos de un patógeno; ii) patógenos especializados secretan efectores muy específicos
que les permiten mantener su condición de especialistas; iii) la especialización del hospedero
puede ser mediada por la adaptación y favorecida por la actividad humana; iv) la distancia
filogenética entre las especies de hospederos y los cambios en el genoma del patógeno son
factores que contribuyen a los eventos de salto de hospedero; y v) el estrecho rango de P.
betacei podría ser explicado por un salto de hospedero y ser mediado por la actividad de sus
efectores, lo que requiere una validación experimental.
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Abstract
The oomycetes are, taxonomically, a widespread group of phytopathogens. Among these,
members of the genus Phytophthora have been recognized as the most important and
destructive pathogens of diverse hosts. The best-studied oomycete is Phytophthora infestans,
comprised in the Phytophthora clade 1c. Within this clade six species have been reported as
the closest known relatives of P. infestans, including the recently described P. betacei. This
species causes the late blight disease in tree tomato (Solanum betacum) in the Andean region
and has been considered as a relevant focal point due to the continued expansion of the
disease in Colombia. The present-day state of knowledge of the host range, host specificity,
host specialization and host jump within oomycetes and Phytophthora species is revisited to
provide a framework that contributes with the understanding of P. betacei biology. This
review concludes: i) there is no parameter for the categorization of the host range of a
pathogen; ii) specialist pathogens secrete highly specific effectors that allow them to maintain
their specialist condition; iii) host specialization can be mediated by adaptation and aided by
human activity; iv) phylogenetic distance between host species and changes in the genome
of the pathogen are factors that contribute to host jump events; and v) the narrow range of P.
betacei could be explained by a host jump and be mediated by its effectors activity which
requires experimental validation.
Key words: host range, host specificity, host specialization, host jump, Phytophthora spp.
I. Introduction
The oomycetes are a diverse group of filamentous microorganisms present in a wide
variety of ecosystems, such as marine, freshwater, and terrestrial environments (Wang et al.,
2020). These microorganisms were historically regarded as part of the basal fungal lineage.
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Nonetheless, they are no longer considered to be true fungi, but fungi-like protists sometimes
called pseudofungi (Cavalier-Smith, 1987). Like other plant pathogens, oomycetes
manipulate their hosts by secreting an arsenal of proteins, known as effectors, which target
plant molecules and alter plant processes (Thines and Kamoun 2010). Prior analyses have
identified an extremely large superfamily of apoplastic and cytoplasmic effectors in
oomycetes, which contribute to virulence (or aggressiveness) by suppressing plant defense
responses (Shen et al., 2017; Stukenbrock & Bataillon, 2012).
Oomycetes have evolved a wide diversity of infectious lifestyles and they can be
biotrophic, necrotrophic, or hemibiotrophic (Pais et al., 2013). According to Gilbert et al,
oomycetes have a significantly higher tendency for host specialization (2012) and their
ecological characteristics have been studied in terms of specialization to particular host
species (Restrepo et al., 2014). Oomycetes can be host specific or can exhibit a wide host
range (Birch et al., 2006). Many members of this family are important and destructive
pathogens of diverse hosts including crop plants, natural forests, fish, insects and,
occasionally, humans (Fawke et al., 2015). Important oomycete plant pathogens include the
downy mildews of the genera Peronospora and members of the Phytophthora, Albugo,
Pythium and Phytopythium genera (Kamoun, 2003; Rujirawat et al., 2018)
Phytophthora species are the most economically damaging invasive plant pathogens
worldwide (Drenth et al., 2006; W. Fry, 2008; Jafari et al., 2020; F. Martin et al., 2012). In
the United States, the economic damage overall to crops has an approximate cost of $10
billion of dollars (Tyler, 2007). Phytophthora infestans, for example, the causal agent of late
blight disease of potato have caused significant worldwide agricultural losses estimated to
exceed $6,7 billion annually (Fukamachi et al., 2019; Vargas et al., 2009). Similarly, the
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soybean root and stem rot agent P. sojae causes around $1–2 billion in losses worldwide per
year (Tyler, 2007).
To date, this genus has been considered as a paraphyletic group comprising 10 clades, with
more than 150 recognized species (Cooke et al., 2000; Mideros et al., 2018; Yang et al.,
2017), and approximately 1000 described hosts (T. H. Wang et al., 2020). Phytophthora
infestans and the closely related species P. mirabilis, P. ipomoeae, P. phaseoli, P. andina
and P. betacei comprise Phytophthora clade 1c (Blair et al., 2008; Cooke et al., 2000; Kroon
et al., 2004; Mideros et al., 2018; Yang et al., 2017). Phytophthora infestans is a species
complex and has a broad host range within the Solanaceae family including potato, tomato
and tree tomato (Forbes et al., 2013, 2016), whilst P. mirabilis has a narrow host range
limited to Mirabilis jalapa (4 o’clock weeds) (Coaker, 2014; Galindo-A., 1985; Goodwin et
al., 2016). Phytophthora ipomoeae infects two morning glory species Ipomoea
longipedunculata and I. purpurea (Badillo-Ponce et al., 2004; Flier et al., 2002).
Phytophthora phaseoli has a narrow host range restricted primarily to lima bean (Kunjeti et
al., 2012). Phytophthora andina, is the pathogen of several members of the Solanaceae
family including tree tomato (Forbes et al., 2016; Gómez-Alpizar et al., 2008) and P. betacei,
a newly described plant pathogen that causes the late blight disease only on Solanum
betaceum Cav. in Colombia (Mideros et al., 2018).
As previously mentioned, P. betacei was recently proposed as a new species within the
clade 1c (Mideros et al., 2018). The authors stated that P. betacei might display host
specificity for tree tomato because until now no other hosts have been identified (Mideros et
al., 2018). These observations highlight the need of understanding the new pathogen biology,
considering that recent outbreaks on tree tomato in Ecuador, Peru and the southern region of
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Colombia, have been reported (Mideros et al., 2018). However, there is little evidence
regarding how these pathogens can set a suitable host range breadth and the conditions in
which they undergo a specialization event. Therefore, the aim of this study is to revisit the
notion of host range, host specificity, host specialization and host jump within oomycetes
and Phytophthora species to provide a framework that can contribute with the understanding
of the pathogen biology of Phytophthora clade 1c members, including recently described P.
betacei.
II. Definitions
Which information is currently available?
One central question in oomycete research is to understand how the host-pathogen
interaction works, and which information is known and available. The number of studies of
host range, host specificity, host specialization and host jump within oomycetes has
fluctuated in the last ten years (Figure 1). Although data is not abundant, we can see that the
scientific community has indeed a strong interest in “host range” within oomycetes.
A short summary of the main information related to the four definitions is described
in the chart below. The Scopus database and its search engine were used to obtain the
publications related to the main concepts of interest for this study: host range, host specificity,
host specialization and host jump within oomycetes plant pathogens. The comprehensive
search was carried out using the previously mentioned terms as keywords, each at a time.
Afterwards, the research papers were refined from year 2010 onwards. The search was
conducted from March to July 2020.
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Figure 1. Year over year comparison of the number of studies of host range, host specificity, host jump and host
specialization within oomycete species. Data was obtained from Scopus data base by using “oomycete” and “host range”,
“host specificity”, “host specialization” and “host jump” as key words.
Host range
The host range is defined as the number of host species that can be infected by a
pathogen (Schulze-Lefert & Panstruga, 2011). This is a trait determined by both its potential
hosts and the evolutionary history of a pathogen (Poulin & Keeney, 2008). In nature, some
pathogens are highly specialized, known as specialists, which can only infect one or a few
members of a single species (Barrett et al., 2009), whereas the generalists can infect several
unrelated host species. The specialist and generalist pathogens have been associated with a
narrow and a broad host range, respectively (Woolhouse et al. 2001). Obligate biotrophic
pathogens have been associated with narrower host ranges than facultative necrotrophic
pathogens (Oliver & Ipcho, 2004). Phytophthora capsici, for example, infects a broad range
of vegetable crops worldwide, including crops in North and South America, Asia, Africa and
Europe (Lamour et al., 2012). In contrast, the soybean pathogen Phytophthora sojae displays
a narrow host range and infects only soybean (Savidor et al., 2008; Tyler, 2007). However,
there are some exceptions on an obligate biotrophic pathogen displaying a narrow host range,
such as Plasmopara viticola, an obligate biotrophic pathogen that has a wide host range with
hosts widely distributed geographically in North America (Rouxel et al., 2014).
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Pathogens with either a narrow or broad host range are often closely related and can
be found within the same phylogenetic pathogen lineage (Gilbert & Webb, 2007). In fact, the
capacity of most pathogens to infect multiple hosts decreases with the phylogenetic distance
among host species (Poulin et al., 2011). According to this, some authors have proposed that
molecular phylogenetic analysis and cross-inoculations may predict how to determine a
potential host range (O’Hanlon et al., 2017; Reis et al., 2018; Telle et al., 2011). Although a
standard methodology has not been described yet, experimental inoculations have generally
used detached leaves to evaluate the infection on every host under controlled conditions
(Rouxel et al., 2013).
It is important to emphasize that host range measurement is not straightforward;
neither the actual number of hosts nor the phylogenetic distance among host species have
been directly associated with the host range. A recent review indicated that perhaps infecting
less than 10 plant genera could be a suitable number for a narrow host range (Morris &
Moury, 2019). However, there is lack of evidence regarding the measurement of the host
range breadth. As a result, more studies are needed to evaluate major drivers behind host
range breadth of pathogens.
Host specificity
Host specificity implies an interaction between a specific host and a pathogen
(Hermens 1982). In other terms, this interaction is a relationship in which a pathogen derives
its nutrition from a plant, and is limited to a particular host or group of related species, but
does not occur on other unrelated plants in the same habitat (Poulin & Keeney, 2008; Zhou
& Hyde, 2001). Nevertheless, the pathogen adaptation to a specific host interaction has
intrigued plant pathologists. Generalist pathogens have multiple effectors to overcome the
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resistance mechanisms encountered among host species (Friesen et al., 2008; Jones & Dangl,
2006). In contrast, pathogens with a narrow host range secrete highly specific effectors that
promote disease in a single host species (Birch et al., 2006; Chisholm et al., 2006). Thus,
molecular models have been developed to understand the basis of host specificity, and the
role of conserved effectors both in pathogen biology and in essential virulence functions
(Flor, 1971; Mestre et al., 2016).
To surpass host response, oomycetes use specific effectors which includes the RxLR
class, containing an RxLR followed by (D)EER motif, and the Crinkler (CRN) class,
containing a FLAK translocation motif (Bos et al., 2003; Panstruga, 2009). In fact, some
authors have suggested that conserved CRN and RxLR effectors among certain species from
the Plasmopora genus might play important roles in the pathogen biology (Mestre et al.,
2016). Likewise in Phytophthora pisi and P. sojae proteomic analyses were performed, in
which several proteins were identified as probable pathogenicity factors (Hosseini et al.,
2015).
As previously mentioned, the recognition of effectors can elucidate the pathogen
biology and limit further virulence (Oliveira-Garcia & Valent, 2015). Recent studies have
also used experimental inoculations to identify some factors involved in host specificity
(Mestre et al., 2016). However, under laboratory conditions host specificity has shown that
it can break down when new hosts and pathogens are brought together (Poulin & Keeney,
2008). This suggest that experimental and molecular studies are valid methods to understand
more about the pathogen biology and how can host switches be possible, considering the
tight association between host specificity and the likelihood of ‘jumping’ to a novel host
(Dobson & Foufopoulos, 2001).
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Host specialization
Host specialization events are commonly found in the plant-pathogen interaction and
have been considered as processes of adaptation in which lineages evolve to infect a narrower
range of hosts than related lineages (Benevenuto et al., 2018; Navaud et al., 2018). Some
studies suggest that specialization occurs not only because some hosts are inherently more
suitable than others (Fry, 1996). In fact, in most cases when a new specialist pathogen appear,
this process could be mediated by adaptation, interspecific competition or favored by an
ecological event (Benevenuto et al., 2018; Restrepo et al., 2014). Whenever a new specialist
pathogen appears the specialization can take the form of host specificity and be associated
with a speciation event (Barrett et al., 2009; Johnson et al., 2009; Parker & Gilbert, 2004)
In contrast with host range expansion, in which a pathogen can infect both its novel and
ancestral host, a host shift speciation event has been related with the “speciation by
specialization onto a novel host”, when a pathogen speciates on a new host and cannot infect
its ancestral host (Giraud et al., 2010). Biotrophic pathogens such as grapevine downy
mildews, for example, have been used in cross-pathogenicity tests to support the hypothesis
that they can diversify by host plant specialization and have linages with both narrow and
broad host ranges (Rouxel et al., 2013). Other studies have used network approaches as useful
tools to analyze host-pathogen interactions because the statistical structure within these
networks provides a standardized framework for describing and quantifying patterns of
specialization in such interactions (Barrett et al., 2015; Vacher et al., 2008; Valverde et al.,
2020). Finally, studies have focused on describing that hybridization might be responsible
for some of these adaptation events, such as in Phytophthora species (Brasier, 2000; Giraud
et al., 2008; Jung et al., 2017).
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Host jump
Host jump events have been defined as the “colonization of a new host species that is
phylogenetically distantly related to the species of the contemporary host range” (Schulze-
Lefert & Panstruga, 2011). In other words, a pathogen has the ability to jump from its original
host into a novel host, adapt to a narrower host range and thereby becomes a new pathogen
(Borah et al., 2018). These events are part of the evolutionary history of most pathogens and
can result in new dead end infections (Longdon et al., 2014). The primary cause of a host
jump is still under study. Nonetheless, previous studies have analyzed some factors that could
be related to this event. A ‘‘phylogenetic distance effect’’ was found to be important in order
to predict the susceptibility of a potential host (Engelstädter & Fortuna, 2019). The authors
explained that the shorter the phylogenetic distance between the novel and original host the
higher the probability to be a potential host (Engelstädter & Fortuna, 2019; Foster, 2019), as
close relatives of the natural host provide a similar environment to the pathogen in which the
infection can occur efficiently (Longdon et al., 2014).
Host jumps have been associated with several changes in the genome of the pathogen,
including genome rearrangements, hybridization, horizontal gene transfer, positive selection,
partial or total gene deletion, and amino acid substitutions (Morris & Moury, 2019; Sharma
et al., 2014). However, genetic relationships to other host species are not the only predictor
of how susceptible a potential host might be to a new pathogen, but it could also be fostered
by inherent flexibility in microbial specificity due to environmental factors that can modulate
the molecular interactions (Morris & Moury, 2019).
The diversity of oomycete pathogens has been considered a result of the changes that
have occurred after adaptation to a new host by host jumps rather than host specialization
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(Navaud et al., 2018). This is the case of the downy mildew pathogens which have diversify
by host jumps, and later by co-speciation (Sharma et al., 2014) and many other cases,
including some Phytophthora species in which interspecific hybridization have contributed
to host jumps and host-range expansions (Depotter et al., 2016). Those events differ from
jumping from one host to another, in which the pathogens have the possibility to infect a new
host and its host of origin (Rouxel et al., 2013). Although there is a lack of information about
the patterns of effector diversification after host jump events, comparative analyses of host
phylogenies have shown that in some cases gen loss rather than gene gain could be related
with a host jump (Longdon et al., 2014; Sharma et al., 2014).
Despite the limited information regarding host range, host specificity, host specialization
and host jump, the following section explores a few examples of how these approaches can
be supported by the Phytophthora genus pathogens and their hosts.
III. Phytophthora genus
Phytophthora species cause enormous economic losses on crop species as well as
environmental damage in natural ecosystems (Davison, 1998). The impact caused by
Phytophthora species has continuously increased in recent years and the number of species
known in the genus has doubled during the past decades (Yang et al., 2017). Phytophthora
species, the most studied genus within oomycetes (Figure 2), can easily overcome the plant
resistance by asexual and sexual reproduction (Aylor et al., 2001; Kroon et al., 2012). Some
species can produce uninucleate motile zoospores that can be released under flooding
conditions and swim towards plant roots (Hardham & Blackman, 2010). In P. sojae, for
example, in a chemotactical manner the zoospores are attracted towards soybean isoflavones
which may be involved in host specificity (Hosseini et al., 2015). The chemotactical
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attraction has also been related to the presumption of the adaptation to soybean as a host
(Hosseini et al., 2015).
Figure 2. Year over year comparison of the number of studies within the most remarkable pathogens within oomycetes.
Data were obtained from Scopus data base by using “Oomycete” and “Phytophthora”, “Pythium”, “Downy mildew” and
“Albugo” as key words.
Phytophthora species are distinguished by producing apoplastic effectors such as cell
wall-degrading enzymes (CWDEs), enzyme inhibitors and elicitins which are secreted to the
extracellular space of the host, and cytoplasmic effectors like RxLR and CRN that are
translocated to the host cytoplasm (Armitage et al., 2018). Those effectors promote several
diseases in a great variety of plants (Birch et al., 2009). Thus, previous studies have focused
on the understanding of the pathogen biology by analyzing the role of cytoplasmic and
apoplastic effectors that may contribute to the virulence of those diseases (Chepsergon et al.,
2020). The narrow host range pathogen P. sojae, for example, present two apoplastic
effectors (PsAvh240 and PsXEG1) that suppress soybean immunity and promote virulence
by an specific interaction with host secreted enzymes (Guo et al., 2019; Ma et al., 2017). In
contrast, 16 out of 21 secreted cysteine proteases were induced during the infection stage and
displayed an important role in P. parasitica pathogenesis within various species of Nicotiana
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(Zhang et al., 2020). In this study, the authors stated that all the secreted cysteine proteases
were highly conserved among different P. parasitica strains, and that some of these proteases
were conserved among three different Phytophthora species (Zhang et al., 2020).
On the other hand, few specific apoplastic effectors have been associated with the
preference of some pathogen species over certain hosts. Other cytoplasmic effectors have
been involved in pathogenicity, either eliciting or suppressing defenses (Bos et al., 2009;
Tyler et al., 2006; Zhang et al., 2015). In a recent study, P. sojae displayed 22 out of 400
candidate RxLR effectors that were able to suppress INF-1 induced cell death and the wide
host range pathogen P. parasitica 172 candidate RxLR effectors (Dalio et al., 2018; Wang et
al., 2011). Although these pathogens have a distinct host range breadth, the high number of
secreted proteins has been involved in virulence and probably shaped by host specialization
(Dalio et al., 2018). In fact, even though the ability of the RxLR effectors to move from
different sites of the host cell has shown that those proteins have an important association
with the virulence activity of the pathogen, the whole knowledge of both the cytoplasmic and
apoplastic effectors remains vague and is a theme that still requires much research
(Chepsergon et al., 2020).
Host specialization within Phytophthora species has also been related to hybridization
events. This is particularly important because in contrast to their parents, hybrids have the
possibility to explore new environments resulting in infection of new host species, even
species their parents were not able to infect (Brasier, 1995). In other words, hybrids can
change their host range breadth as well as the specificity their parents had, and even
developed new features related to the host specialization events. Previous studies identified
that P. andina emerged via hybridization between P. infestans and another unknown
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Phytophthora species (Goss et al., 2011). Despite their shared morphology P. andina is
genetically distinct from P. infestans and their host range breadth differences suggested that
it is probable that hybridization led to host range expansion or shifts (Brasier et al., 1999;
Goss et al., 2011).
Other examples of host specialization have been related to some Phytophthora
species, such as P. nicotianae, P. palmivora and P. sojae. For instance, in P. nicotianae
populations the continuous planting of two varieties of the host (Php and Phl) have caused a
shift in the pathogen from race 0 to race 1, as well as an increase in the virulence (Sullivan
et al., 2010). For this reason authors have stated that it might be possible that host
specialization of P. nicotianae occurs more frequently in intensive farming systems (Biasi et
al., 2016). Phytophthora palmivora, for example, causes significant diseases on a wide range
of host plants and some individual isolates vary in their virulence on cacao. However, a recent
study has determined that this pathogen has expanded its genetic capacity, resulting in better
adaptation to a wider diversity of host interactions (Ali et al., 2017). In P. sojae, a specific
chemotaxis displayed between its zoospores and soybean isoflavones have been associated
to the adaptation to soybean as a host, as mentioned before (Hosseini et al., 2015; Morris &
Ward, 1992).
Jumping from one host to another has let some Phytophthora species the opportunity
of spreading throughout more regions by infecting new hosts, including Phytophthora
infestans. This species has been considered one of the most damaging agricultural plant
pathogen and studies have focused mainly on identifying the mechanisms involved in the
host range, host specificity, host specialization and host jump events. Although there is not
much related information a summary of the topic is presented in the next section.
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IV. Phytophthora clade c1
As of today, six species comprise the Phytophthora clade 1c including one of the most
well-known oomycetes, the causal agent of potato and tomato late blight and the Irish potato
famine in the mid-nineteenth century, Phytophthora infestans (Birch & Whisson, 2001;
Cooke et al., 2000; Forbes et al., 2013; Haas et al., 2009; Kroon et al., 2012). This
hemibiotrophic pathogen attacks wild tuber-bearing and other solanaceous species, and has
become a ‘model system’ for the study of oomycete plant-pathogen interaction (Guo et al.,
2017; Judelson, 1997; Mideros et al., 2018; Seidl et al., 2019; Tyler, 2007). Phytophthora
infestans has also been reported evolving rapidly to overcome resistant potato varieties (Chen
et al., 2018).
Within the clade 1c, P. infestans is the only member that has a broad host range
contrary to the narrower host ranges its closest relatives display (Birch & Whisson, 2001).
Phytophthora mirabilis, P. ipomoeae and P. phaseoli, for example, have a very restricted
host range, infecting only one or a few plant species. Similarly, P. andina and P. betacei
display a narrow host range but form part of a monophyletic clade with P. infestans (Mideros
et al., 2018). A recent study showed that the triad P. infestans, P. andina and P. betacei
display both genetic and morphological differences. Nonetheless, an evaluation of host
preferences identified that P. betacei cannot infect neither tomatoes nor potatoes but revealed
the highest fitness on tree tomatoes compare to its closest relatives P. andina and P. infestans
(Mideros et al., 2018).
Within the clade 1c, some molecular studies have shown that using the internal
transcribed spacer (ITS) region is an useful tool to clarify the relationships among
Phytophthora species (Blair et al., 2008; Kroon et al., 2004; Mideros et al., 2018; Vargas et
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al., 2009). In central Mexico, for example, some authors pointed out that these species
evolved through host jumps followed by adaptive specialization on different botanical
families (Grünwald & Flier, 2005; Raffaele et al., 2010). Similarly, interspecies hybridization
has been studied showing that these events can lead to changes in host range, the loss of sex,
and subsequent speciation (Martin et al., 2016). However, the information related to
hybridization events has mainly been associated with geographical distribution of both, the
host and the pathogen (Martin et al., 2016).
In general, many pathogens such as P. infestans, secrete effector proteins that alter
host physiology and facilitate infection (Kamoun, 2006). For instance, the apoplastic effector
EPIC1 has been studied in great detail because it is abundantly secreted during infection of
tomato and inhibits extracellular papain-like proteases (including RCR3), which control key
processes at different levels of plant defense (Misas-Villamil et al., 2016). A recent study
described that 82 effectors are involved in the positive selection between P. infestans and P.
mirabilis (Coaker, 2014). The P. mirabilis EPIC1 ortholog (PmEPIC1), for example, has
evolved to function in Mirabilis jalapa infection, following the split between P. mirabilis
and P. infestans (Dong et al., 2014). In other words, the jump from Solanum species to
Mirabilis jalapa and subsequent specialization involved amino acid substitutions in protease
inhibitors that allowed this EPIC1 ortholog to participate in the infection process (Dong et
al., 2014). These results highlight that protease inhibitors have played important roles in
adaptation of P. mirabilis, and that effector proteins are important for adaptation to a new
host, supporting the hypothesis of effector specialization after a host jump (Chepsergon et
al., 2020; Coaker, 2014; Dong et al., 2014).
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Within Phytophthora clade 1c species, it has also been proposed that some
Phytophthora species are driven by hybridization (Delcán & Brasier, 2001; Depotter et al.,
2016). This is particularly the case of P. andina, initially referred to as P. infestans but
reclassified as P. andina (Oliva et al., 2010). The origin of P. andina has been related with
two different factors: a common ancestor between this specie and P. infestans, and a result
of an interspecific hybridization between P. infestans and another unknown Phytophthora
species also belonging to Phytophthora clade 1c (Gómez-Alpizar et al., 2008; Goss et al.,
2011). The very close relationship between these two species was associated with, among
other reasons, their restricted distribution across the Andean region (Cárdenas et al., 2011;
Gómez-Alpizar et al., 2008; Oliva et al., 2010). In Ecuador, for example, P. andina occurs
sympatrically with P. infestans on Solanum betaceum (Cárdenas et al., 2011; Gómez-Alpizar
et al., 2008; Oliva et al., 2010). As described before, P. andina is a pathogen on various
Solanum species, and has recently been included in a monophyletic clade with P. infestans
and P. betacei (Mideros et al., 2018). The authors have stated that the three species are
reciprocally monophyletic with no recent gene flow, which might suggest a strong host
specialization within these species (Mideros et al., 2018).
At the moment, few studies have described P. betacei biology. Some authors have
focused on the differential pathogenicity of P. betacei on different cultivars of its natural host
S. betaceum by using detached leaf assays. Other authors have recently identified some
apoplastic and cytoplasmic effectors that were suggested to play an important role in host
specificity of this species (Rojas-Estevez et al., 2020). In this study, a comparison between
P. betacei and some other Phytophthora species determined that P. betacei produces several
unique effectors that might allow it to easily colonize tomato tree than other hosts (Rojas-
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Estevez et al., 2020). Although this study showed which protein effectors might be involved
in host specificity of P. betacei, both molecular and experimental analyses are required to
corroborate the information already presented.
V. Future perspectives
In this review a detailed study of the monophyletic Phytophthora clade 1c (P.
infestans, P. andina and P. betacei) is suggested in order to determine the relationship P.
betacei biology has with the definitions already presented for host range, host specificity,
host specialization and host jump events. It is considered that studying in more depth this
monophyletic clade could help into determining the main characteristics of P. betacei
biology, because the closer the phylogenetic relationship, the easier to find similar features
between species, as it was observed in Rojas-Estevez et al (2020) study. Although a part of
the P. betacei effector profile was already described, the lack of information raises a series
of questions about the specific effectors involved in its restricted host range or the possibility
that a host jump event has occurred resulting in host specialization. Specifically, we need to
ask (a) Is the presence of an EPIC1 ortholog, as found in P. mirabilis, involved in
pathogenicity and specificity within P. betacei species? Or (b) Is P. betacei the result of an
interspecific hybridization event, as it was reported for its closest known relative P. andina
and several other Phytophthora species? And finally, (c) Has host jump occurred over time,
and are the shifts predictable based on phylogenetic distance from known hosts?
In summary, oomycete plant-pathogen interactions are as diverse as the features
within its members. Although, our understanding of newly described pathogens’ biology
such as P. betacei is still vague, a big progress has been done in recent years highlighting the
characteristics involved in host range, host specificity, host specialization and host jump
19
events within its closest known relatives. In this review, the main purpose was to summarize
the information available for this plant-pathogen interaction, starting from more general
examples within oomycetes to some specific cases already known within Phytophthora clade
1c. It is clear that further studies are required, and thus this compilation might help future
researchers into designing and creating new methodologies to validate the hypotheses related
to interspecific hybridization or host jump events. For example, testing could include host
pathogenicity assays and comparative genome analyses of sister species.
VI. Conclusions
The oomycetes are a widespread group of microorganisms that includes some of the most
important pathogens of plants. Among these, members of the genus Phytophthora have been
recognized as the most economically damaging in natural ecosystems. Within this genus,
recently described P. betacei has become a pathogen of relevant concern because its biology
is unknown and late blight epidemics on tree tomatoes have increased in several regions of
Colombia.
A deeper and applied understanding of host range, host specificity, host specialization and
host jump has proven to be a valuable tool in explaining plant-pathogen interaction. The
literature review of these concepts for the specific case of P. betacei biology allows to draw
the following conclusions:
• There is no parameter for the categorization of the host range (wide or narrow) of a
pathogen, in terms of numbers or phylogenetic relationships of hosts.
• Specialist pathogens secrete highly specific effectors that allow them to maintain
their specialist condition.
20
• Host specialization can be mediated by adaptation and aided by human activity.
• Phylogenetic distance between host species and changes in the genome of the
pathogen are some of the factors that contribute to host jump events.
• The narrow range of P. betacei could be explained by a host jump and be mediated
by the activity of its effectors which requires experimental validation.
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