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Review

Phytophthora sansomeana, an Emerging Threat to Soybean Production

by
Christopher Evan Detranaltes
1,
Jianxin Ma
2 and
Guohong Cai
1,3,*
1
Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907, USA
2
Department of Agronomy, Purdue University, West Lafayette, IN 47907, USA
3
Crop Production and Pest Control Research Unit, Agricultural Research Services, United States Department of Agriculture, West Lafayette, IN 47907, USA
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(8), 1769; https://doi.org/10.3390/agronomy12081769
Submission received: 9 June 2022 / Revised: 7 July 2022 / Accepted: 22 July 2022 / Published: 28 July 2022
(This article belongs to the Special Issue Advances in Soybean Phytophthora Diseases Research)
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Abstract

:
In 1990, new Phytophthora strains, later recognized as a new species, Phytophthora sansomeana, were found to cause Phytophthora root rot (PRR) in soybean in addition to P. sojae. The emergence and spread of a second pathogen causing PRR poses a significant threat to soybean production. While genetic resistance to P. sojae has been developed and widely deployed as a management tool, these varieties appear largely ineffective at controlling P. sansomeana, which has a broad host-range and can infect and survive on non-leguminous hosts including fir trees, Rosaceous fruit trees, maize, and several herbaceous weeds. This contributes potential for broad distributions worldwide across both agricultural and natural ecosystems. Despite having been studied since the 1980s under a variety of informal designations, little is known about the epidemiology, host-interactions, and management of this emergent pathogen. Due to the lack of management options, increased frequency of first reports in new geographic areas, and the overall limited body of knowledge surrounding this novel pathogen, P. sansomeana warrants more research attention from both biological and disease management perspectives. The aim of this review is to summarize the hosts, distribution, pathogenicity, and current management strategies of P. sansomeana and to provide a concise record of where it has been studied under other informal designations. Its role in PRR of soybean is emphasized due to the economic magnitude of PRR-associated losses and its well-documented aggressiveness as a soybean pathogen.

1. Introduction

Since the 1990s concern has been rising about a new causal agent of Phytophthora root rot (PRR) in soybean across the Midwest. Phytophthora sojae (Kaufm. and Gerd.) has long been attributed as the cause of PRR in soybean [1]. However, in 1990 an outbreak of what was initially thought to be P. sojae (then P. megasperma (Drechs.) f. sp. glycinea (T.L. Kuan and Erwin)) occurred in Indiana [2]. Although it is morphologically similar to P. sojae, the pathogen failed to produce race-classifiable results when inoculated on a set of P. sojae differentials. In 2009, the pathogen isolates from soybean, as well as isolates from Douglas-fir in Oregon and wild carrot, white clover, and white cockle in New York, were recognized as a novel species designated Phytophthora sansomeana (E.M. Hansen and Reeser) based on a combination of morphological observations, host interactions, and molecular phylogenetics [3]. Isolates from soybean, Douglas-fir, and a few agricultural weeds long suspected to be distinct species from the P. megasperma sensu lato clade were all reidentified as belonging to this species.
It has been more than a decade since P. sansomeana was formally designated. The scope of this review is to summarize published findings on P. sansomeana, both before and after its formal nomenclatural designation, with an emphasis on its role as a soybean pathogen. A record of the various published research articles in which P. sansomeana was referred to by other designations or as unknown Phytophthora spp. is presented, in the hopes of bringing clarity to where P. sansomeana has been studied under other nomenclature. A current list of hosts and population distribution as of the time of this writing is also presented; this is followed by a summary of what is known related to the genetics, pathogenicity, and disease management of this pathogen.

2. Nomenclature

Phytophthora megasperma was first described by Dreschler from hollyhock in 1931 as a novel Phytophthora species possessing large oogonia and oospores and mostly paragynous antheridia [4]. By 1936 the species description was expanded to encompass isolates with smaller oospores and different host specificities [5]. A variety of isolates were later lumped into P. megasperma sensu lato that possessed similar morphology but were genetically unrelated, forming a conglomerate polyphyletic clade in which P. sansomeana was included. Observations by Hansen and colleagues found evidence that the clade encompassed 9 distinct subgroups potentially representing emergent species based on a combination of chromosome number, nuclear DNA content, morphology, electrophoretic patterns of total proteins, and host pathogenicity [6]. P. sansomeana was separated from other subgroups and given its formal species designation in 2009 (Hansen et al., 2009) based on a combination of unique morphological traits, host pathogenicity, and sequences of the internal transcribed spacer (ITS) region of the ribosomal RNA gene. This nomenclature has since been widely adopted in the literature.
Many observations have been made of P. sansomeana isolates identified under a variety of informal designations and subgroups of P. megasperma used throughout individual studies. Hansen and Hamm noticed that some isolates of P. megasperma isolated from Douglas-fir caused more severe necrosis of taproots after inoculation on two-year-old trees than other P. megasperma isolates from alfalfa, soybean, or clover [7]. Additionally, these same isolates caused the stem collapse and death of soybean seedlings after hypocotyl inoculation and could be distinguished from the legume-derived isolates by oogonial diameter in combination with sporangial length; they were designated P. megasperma D1. Later, these same D1 isolates were observed to have unique chromosome number, faster growth rate, and distinguishable electrophoretic pattern of total proteins. They were relabeled the DF protein group [6], which was later reidentified as P. sansomeana [3]. Reeser reported an outbreak of Phytophthora root rot in soybean in Indiana, which did not respond to any of the known Rps genes conferring resistance to the suspected causal agent P. megasperma f. sp. glycinea (now P. sojae). These isolates were designated P. megasperma f. sp glycinea race non-classifiable [2] and again later confirmed to be P. sansomeana [3]. Förster and Coffey examined 194 isolates of Phytophthora for differences in mitochondrial DNA restriction fragment length polymorphisms (RFLPs) and referred to what was later discovered to be P. sansomeana isolates as P. megasperma mtDNA group F1 [8].
The informal designations used throughout the literature to describe isolates of P. sansomeana are summarized in Table 1. The isolates that were reviewed and confirmed to be misidentifications of P. sansomeana in the original species description are highlighted [3]. As such P. sansomeana was not first discovered in 2009: rather, it had been isolated from various hosts as far back as the 1980s and perhaps even earlier. Multiple distinct species have since been discerned from the P. megasperma sensu latu clade, while P. megasperma sensu Dreschler remains valid as P. megasperma sensu strictu.
Phylogenies based on molecular data were used to delineate species and examine the relationship between the Phytophthora species, including P. sansomeana and others derived from the P. megasperma sensu lato polyphyletic clade (Figure 1). Cooke et al. used ITS sequences to assemble a 10 clade Phytophthora tree in an attempt to resolve Phytophthora relationships [12]. This phylogeny and later expansions have been widely adopted in the literature to group Phytophthora species (see [13,14,15]). Hansen et al. placed P. sansomeana into Cooke’s clade 8, which was shared by nine other species including P. dreschleri, P. cryptogea, P. erythroseptica, P. trifolii, P. medicaginis, P. syringae, P. primulae, and P. porri. They also noted that isolates from New York and the Midwest showed consistent ITS polymorphisms indicating related but distinct populations within the US [3]. More recently, Martin et al. looked at 92 species and 17 provisional species of Phytophthora using sequences from four mitochondrial loci and seven nuclear loci and reaffirmed P. sansomeana’s position in clade 8a using the isolate from white cockle reidentified by Hansen et al. [14]. It shared this position with six other Phytophthora species, including P. cryptogea, P. kelmania, P. drechsleri, P. erythroseptica, P. medicaginis, and P. trifolii. Since then, evidence of further subgroups, novel species, and interspecific hybridization within this clade has emerged [15,16,17,18]. As such, the total list of Phytophthora species that should be included in clade 8a and therefore considered closely related to P. sansomeana may not yet be fully resolved and is likely to expand.

3. Morphology and Identification

Hansen et al. noted that P. sansomeana keys to P. megasperma in Waterhouse’s morphological group V, and that additional morphological features, host preference, and growth characteristics must be observed for accurate identification [3].
The species has nonpapillate sporangia and oogonia averaging 39–45 µm depending on the host they are formed on. In Hamm and Hansen’s key, P. sansomeana (as P. megasperma—Group 1) could be distinguished from other morphologically similar isolates of P. megasperma sensu lato by a combination of average oogonia size less than 44 µm and sporangial length to width ratio of 1.4–1.6:1 [10]. This key was built with a subset of Phytophthora isolates attacking conifer trees in the Pacific Northwest and may need verification for use across the whole of the Phytophthora genus or on different hosts. Of the species now distinguished from P. megasperma sensu Waterhouse, Hansen et al. observed that P. sansomeana has the fastest growth rate at 7–10 mm/day at 25 °C on carrot agar [3]. Its optimal growth temperature is 27 °C. When distinguishing Phytophthoras isolated from soybean, P. sansomeana grows well on potato dextrose agar (PDA) while P. sojae has extremely limited growth on this media [19].
As with many Phytophthora species, identification of this species from morphology alone may be difficult or impossible. Molecular identification protocols are available for corroboration of a morphological identification. ITS sequencing is a reliable option and has been shown to distinguish P. sansomeana from closely related species and even identify potential hybrids [3]. The entirety of the ITS region can be sequenced to capture all potential polymorphisms and is readily amplified using ITS1/4 [20] for pure samples or DC6 and ITS4 for selective amplification of the ITS region from members of the Peronosporales and Pythiales [21]. Sequencing and BLAST search against nucleotide databases can corroborate morphological identifications, especially when type specimen sequences are available. Additionally, a real-time PCR protocol has been developed for species-level detection of P. sansomeana from soybean [22]. The qPCR probes developed in this study can distinguish between P. sojae and P. sansomeana, which makes it an important tool for judging the relative contributions of each species associated with PRR outbreaks in soybean.

4. Hosts and Distribution

P. sansomeana is primarily known as a pathogen of soybean and other legumes but it has a broad host range and is widely reported globally (Table 2). On soybean, P. sansomeana has been reported to cause PRR or be associated with rotted roots in 10 US states including Iowa, Illinois, Indiana, Kansas, Michigan, Minnesota, Nebraska, Ohio, South Dakota, and Wisconsin, in addition to Canada and China [2,23,24,25,26,27]. It’s host range suggests it is pathogenic to both monocotyledonous and dicotyledonous hosts, woody and herbaceous species, and has been reported to affect both root and recently foliage tissues, though only in a single host thus far. Reports of P. sansomeana on various hosts from around the world have been increasing since its formal designation as a unique species in 2009. Its ability as a non-specialized pathogen to parasitize hosts from a variety of natural and agricultural ecosystems means it is likely capable of broad distribution worldwide. Across hosts, P. sansomeana is frequently the cause of root rot or rots of other belowground plant structures (i.e., rhizomes). P. sansomeana is soilborne and is recoverable by baiting as well as direct isolation from infected tissues [28]. The production of oospores may help it survive long-term or overwinter in adverse soil conditions.
Epidemiological data that sheds light on the invasive potential of P. sansomeana has arisen almost exclusively from outbreaks of PRR in soybean and is limited primarily to first reports and new detections across counties in individual US states. The 1990 epidemic from Indiana, which serves as the first report of the pathogen for the state, is described as having emerged in soybean fields scattered across many of the state’s counties in a single season [2,3]; P. sansomeana has since been routinely detected across the state. Since its first detection in Wisconsin in 2012, reports of P. sansomeana infections of soybean have spread to 15 counties, with new detections from three counties in 2020 alone [40]. P. sansomeana is additionally reported on maize and multiple fir species, indicating the pathogen’s ability to utilize multiple economic crops as hosts to survive and spread once introduced. However, whether P. sansomeana reports are purely a result of pathogen dispersal or also a byproduct of increased detection accuracy is difficult to determine, especially due to frequent misidentifications of the pathogen prior to 2009. Where P. sansomeana has become naturalized and where it may have originated will require further studies of population structure and diversity across multiple geographic regions.

5. Disease Symptoms and Pathogenicity

5.1. On Soybean

It is now known that the causal agent of PRR outbreaks in soybean may be either P. sojae or P. sansomeana; how much P. sansomeana contributes relative to P. sojae in causing PRR epidemics and at what growth stages in soybean remain unknown. When first reported in Wisconsin, P. sansomeana was recovered from 49 symptomatic plants (V1–V4) at a rate of only 6% [25]. In some Illinois counties, however, P. sansomeana (referred to as an unknown Phytophthora species [19]) was recovered from soil baiting assays as often as 70% of the time [28]. Whether all these populations were contributing to PRR is unclear, however fields from which P. sansomeana was recovered had histories of seedling disease and at least some of the isolates were pathogenic when inoculated on P. sojae differentials. Whether Rps genes conferring resistance to P. sojae are ineffective at providing resistance to P. sansomeana is likely [2,28] but has not been thoroughly tested.
In the field, distinguishing the two pathogens can be difficult. Late in the growing season, P. sojae typically causes a necrosis of the stem that emerges from the soil line and spreads upward after the seedling stage in soybean [19]. P. sansomeana appears to primarily cause wilting as an aboveground symptom with the stem lesion usually absent in infected hosts [3]. An accurate discernment of the two pathogens from field symptoms alone is unlikely before the onset of stem lesion formation and may remain impossible without further diagnostic evidence. There may also be potential for emergent effects from double infection with both P. sojae and P. sansomeana. Rojas et al. reported the discovery of two field samples testing positive for both species in PCR based assays. They noted that P. sansomeana mostly concentrated in the tap roots while P. sojae preferentially colonized the lateral roots in both cases [22]. Double infection in combination with P. sojae may reduce the usefulness of stem lesions as a pathognomonic symptom.
P. sojae is also known to be a potent seed and seedling pathogen implicated in pre-emergence and post-emergence damping off long before the stem lesion symptom is produced. The relative contribution that P. sansomeana may make during Phytophthora-induced seedling disease outbreaks in the field is unknown. Nevertheless, seed plate assays suggest that P. sansomeana causes significantly more severe seed rot scores than P. sojae [24]. It is therefore possible that P. sansomeana plays a greater role as a seed pathogen than in adult plant infections, which could help explain its relatively low isolation rate from symptomatic hosts later in the season [25] despite high frequency of recovery in soil baiting assays [28]. The increased availability of conventional and real-time PCR protocols that differentiate between the two species may help to disentangle the relative contributions of each pathogen to PRR [20,41]

5.2. On Non-Soybean Hosts

On trees P. sansomeana causes root and collar rot symptoms of varying severity depending on the host. In conifer species infected trees typically become progressively more chlorotic, stunted, and may die off as infections age [29]. In Abies species branch flagging and wilting of the younger shoots was observed [30]. In Rosaceous trees, fruit production may be stunted or ceased entirely [35]. On maize P. sansomeana causes wilting and stunting and may be related to emergence problems [38], though interestingly, reports from this host lag behind that of soybean in the U.S. and globally. P. sansomeana was also recently isolated from leaf lesions in taro [42]. Artificial inoculation yielded the same lesions as seen on field hosts on detached leaves. It appears that P. sansomeana infects belowground or aboveground tissues on a host-by-host basis.

6. Genetic Variability

The mitochondrial genome of P. sansomeana has been sequenced and annotated [43]. Interspecific comparison showed genes of similar structure and order as Phytophthora species selected from clades 1, 7, 8, and 9, including conserved respiratory complex, ATP synthase, and ribosomal RNA protein genes. The genome closely resembles that of Phytophthora ramorum (clade 8c), differing only in an inversion of the section covering nad5, nad6 and trnRUCU. Other members of clade 8 or subclade 8a were not included in the analysis. P. sansomeana carries in its mitochondrial genome a unique ORF encoding an unknown protein of 402 amino acids in length not seen in the 10 other Phytophthora species included in the analysis. An annotated nuclear genome sequence is in preparation (Cai, unpublished data).
Intraspecific variation in the ITS sequence has been observed across populations of P. sansomeana. Hansen et al. reported that isolates of P. sansomeana were polymorphic at eight loci in the 826 bp long sequences analyzed between isolates from weedy hosts in New York and isolates from soybeans from the Midwest [3]. They noted that isolates from Douglas-fir may have been the result of hybridization between these two populations due to the presence of double peaks in sequence chromatogram that resembled both populations. Whether all P. sansomeana strains infecting Douglas-fir are a result of hybridization is unclear, since isolates recovered from weedy-type parent population also readily cause disease when inoculated on Douglas-fir just the same as apparent hybrid strains [3].
The species also appears to readily hybridize with other members of Phytophthora subclade 8a. Hybrids have been identified from Iran and Bulgaria with P. sansomeana acting as the paternal parent in both cases of suspected sexual recombination with the species P. pseudocryptogea and P. kelmania, respectively [16,17]. The two hybrids with P. pseudocryptogea were isolated from beet, while the hybrid with P. kelmania was recovered from Rhododendron leaf baits in a freshwater river. All three hybrids produced only asexual sporangia and neither oogonia nor antheridia. Hybrids otherwise shared morphological features of both parents. P. sansomeana has been reported to be pathogenic to maize, however the hybrid of P. sansomeana and P. kelmania was unable to infect maize seedlings, indicating that hybridization may change host specificity or that pathogenicity on maize may be strain specific in P. sansomeana [16]. Interestingly, in both cases where hybrids have been isolated, P. sansomeana has yet to be reported, indicating either that it has been present and so far unreported or that the hybrid originated elsewhere and was transported to the region.

7. Disease Management

Research on the control of P. sansomeana is still emerging and several studies have investigated genetic resistance in soybean and chemical control in lab studies. Two small effect quantitative trait loci (QTLs) were found to confer partial resistance to P. sansomeana in soybean [44]: these two loci showed isolate specificity when tested against seven isolates including one isolate that overcame both QTLs. The authors noted that only one replicate of inoculated trials could be completed per isolate due to seed limitations, so whether this is evidence for a potential virulence/avirulence structure or an artifact of environmental fluctuations between tests is uncertain. Biocontrol measures and other non-chemical management strategies are unstudied in reference to this pathogen.
Seed treatment was found to significantly reduce root rot in soybean seed plate assays after inoculation with P. sansomeana [24]. Soybean seeds treated with combinations of metalaxyl and ethaboxam, pyraclostrobin and metalaxyl, or mefenoxam alone significantly reduced disease severity compared to nontreated controls. Importantly, these treatments were also effective against P. sojae suggesting one seed treatment formulation could control both pathogens. Previous findings of metalaxyl sensitivity in P. sansomeana corroborate the susceptibility of this species to this chemical control measure [7]. P. sansomeana isolates recovered from corn are similarly susceptible to both ethaboxam and mefenoxam [39]. Seed treatment may therefore be a useful tool in managing P. sansomeana associated losses while genetic resistance and other components of integrated pest management are investigated and developed.
Although both species cause PRR in soybeans, it is unclear if P. sojae control measures aside from seed treatment will similarly manage P. sansomeana due to fundamental differences in host specificity and the absence of typical race reactions on soybean differentials for P. sojae resistance. For instance, crop rotation with corn may be ineffective in reducing primary inoculum available for soybean infections due to the ability of P. sansomeana isolates to infect maize [38]. Further, Rps genes conferring resistance to P. sojae appear to provide no protection against P. sansomeana.

8. Conclusions

Though P. sansomeana has been studied since the 1980s, this nomenclature was unavailable until 2009. The formal designation of P. sansomeana as its own species has been widely adopted and has brought clarity to research on the pathogen since 2009. Molecular methods for the detection of P. sansomeana should help in identifying the pathogen and the development of epidemiological and disease management studies across hosts.
P. sansomeana has been isolated from and shown to be pathogenic to many other plant hosts (Table 2), including other economic species such as maize, alfalfa, Christmas trees, Douglas-fir for timber, and several fruit trees. Many important food and economic crops could therefore benefit from increased research on P. sansomeana and its control. Chemical control of P. sansomeana has been studied, while research into genetic resistance or tolerance is severely limited [24,39,44]. The development of integrated pest management practices for this disease will require further research into cultural, genetic, and biocontrol measures to reduce disease severity across hosts.
Outside of corn and soybean, research into P. sansomeana has focused largely on identification and not control. It has been noted that while P. sansomeana is less frequently isolated from apple trees, in pathogenicity trials it caused worse necrosis of rootstock segments measured by total length from the inoculation point than more frequently occurring species, including P. cactorum, P. cryptogea, P. syringae, and P. plurivora [35]. The heightened threat P. sansomeana may pose among already wide-spread Phytophthora pathogens warrants increased attention to the control and management of this pathogen. P. sansomeana’s broad host range may facilitate survival on unsuspected hosts once introduced into a new area, so care should be taken to manage dispersal of this pathogen to new areas.

Author Contributions

Conceptualization, G.C.; methodology, G.C. and C.E.D.; writing—original draft preparation, C.E.D.; writing—review and editing, G.C. and J.M.; supervision, G.C.; project administration, G.C.; funding acquisition, G.C. and J.M. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Indiana Soybean Alliance (https://indianasoybean.com/).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data are presented within this article.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 12 01769 g001 550
Figure 1. Phylogenetic tree showing P. sansomeana’s position in subclade 8a based on seven genetic markers including: 60S Ribosomal protein L10 (60S); beta-tubulin (Btub); elongation factor 1 alpha (EF1α); enolase (Enl); heat shock protein 90 (HSP90); 28S ribosomal DNA (28S); and tigA gene fusion protein (TigA). Values at nodes represent bootstrap values for maximum likelihood and maximum parsimony, and Bayesian posterior probabilities in percentage. Asterisks represent 100% support between all three analyses. Figure reproduced from Yang et al. [15] under Creative Commons CC BY license from Springer Nature.
Figure 1. Phylogenetic tree showing P. sansomeana’s position in subclade 8a based on seven genetic markers including: 60S Ribosomal protein L10 (60S); beta-tubulin (Btub); elongation factor 1 alpha (EF1α); enolase (Enl); heat shock protein 90 (HSP90); 28S ribosomal DNA (28S); and tigA gene fusion protein (TigA). Values at nodes represent bootstrap values for maximum likelihood and maximum parsimony, and Bayesian posterior probabilities in percentage. Asterisks represent 100% support between all three analyses. Figure reproduced from Yang et al. [15] under Creative Commons CC BY license from Springer Nature.
Agronomy 12 01769 g001
Table
Table 2. Hosts and distribution of Phytophthora sansomeana.
Table 2. Hosts and distribution of Phytophthora sansomeana.
HostCommon NameFamilyIsolation LocationsKoch’s Criteria aPublicationsDesignation
Abies amabilisPacific silver firPinaceae P[29]Phytophthora megasperma Group 1
Abies concolorWhite firPinaceae P[29]Phytophthora megasperma Group 1
Abies fraseriFraser firPinaceaeNorth Carolina, New York, Wisconsin, Michigan (USA)K[30,31]Phytophthora sansomeana
Abies magnifica var. shastensisShast red firPinaceae P[29]Phytophthora megasperma Group 1
Abies proceraNoble firPinaceae P[29]Phytophthora megasperma Group 1
Atractylodes macrocephalaBai ZhuAsteraceaeKoreaI + P[32]Phytophthora sansomeana
Chamaecyparis lawsoniaLawson cypressCupressaceaeEuropeI[33]Phytophthora sansomeana
Daucus carotaWild carrotApiaceaeNew York (USA)I [6]Phytophthora megasperma DF protein group
Gerbera spp.African daisyAsteraceaeJapanR[34]Phytophthora sansomeana
Glycine maxSoybeanFabaceaeOntario (CA), China, Iowa, Illinois, Indiana, Kansas, Michigan, Minnesota, Nebraska, Ohio, South Dakota, Wisconsin (USA)K[2,23,24,25,26,27]Phytophthora sansomeana
Malus domesticaCommon appleRosaceaeCzech RepublicK[35]Phytophthora sansomeana
Medicago sativaAlfalfaFabaceae P[9]Phytophthora megasperma Douglas-fir Group 1
Pisum sativaField peaFabaceaeAlberta (CA)K[36]Phytophthora sansomeana
Prunus domesticaEuropean plumRosaceaeEuropeI[33]Phytophthora sansomeana
Prunus insitiaSt. Julien plumRosaceae P[35]Phytophthora sansomeana
Prunus mahalebMahaleb cherryRosaceae P[11]Phytophthora megasperma DF1
Pseudotsuga menziesiiDouglas-firPinaceaeOregon (USA)K[7,9]Phytophthora megasperma Douglas-fir Group 1; Phytophthora megasperma DF1
Pyrus communisCommon pearRosaceaeCzech RepublicI [35]Phytophthora sansomeana
Silene latifolia subsp. Alba White cockleCaryophyllaceaeNew York (USA)I [6,8] bPhytophthora megasperma DF protein group; Phytophthora megasperma mtDNA Group F1
Wasabia japonicaWasabiBrassicaceaeBritish Columbia (CA)K[37]Phytophthora sansomeana
Zea maysMaizePoaceaeMichigan, Ohio (USA)K[38,39]Phytophthora sansomeana
a K = isolation + pathogenicity + reisolation, I = isolation only, P = pathogenicity only, R = reidentification. b as Lychnis alba.
Table
Table 1. Nomenclature and informal designations of Phytopthora sansomeana isolates prior to species description by Hansen et al., 2009.
Table 1. Nomenclature and informal designations of Phytopthora sansomeana isolates prior to species description by Hansen et al., 2009.
SpeciesDesignationIsolatesPublication
Phytophthora megaspermaDouglas-fir Group 1Hamm 284; Hamm 304 *; Hamm 306; Hamm 385; Hamm B2-17 *; Hamm B3A *[9]
Phytophthora megaspermaDouglas-fir D1Hamm 345 *; Hamm B2-17 *; Hamm B3A *[7]
Phytophthora megaspermaDFHamm 304 *; Hamm 345 *; Hamm B2-17 *; Hamm B3A *; Stack Car2(86) *; Stack WCl(75) *[6]
Phytophthora megaspermaGroup 1 [10]
Phytophthora megaspermaDF1Hamm 304 *; Hamm 306[11]
Phytophthora megasperma f. sp. glycineaRace non-classifiable20 isolates including OSU 1819B *, 2323 *, 2516A *, 9284 *[2]
Phytophthora megaspermamtDNA group F1Hamm 304 *; Hamm 306; Hamm B3A *; IMI280906; Stack Car2(86) *; Stack WCl(75) *[8]
* Later reidentified as P. sansomeana in [3].
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Detranaltes, C.E.; Ma, J.; Cai, G. Phytophthora sansomeana, an Emerging Threat to Soybean Production. Agronomy 2022, 12, 1769. https://doi.org/10.3390/agronomy12081769

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Detranaltes CE, Ma J, Cai G. Phytophthora sansomeana, an Emerging Threat to Soybean Production. Agronomy. 2022; 12(8):1769. https://doi.org/10.3390/agronomy12081769

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Detranaltes, Christopher Evan, Jianxin Ma, and Guohong Cai. 2022. "Phytophthora sansomeana, an Emerging Threat to Soybean Production" Agronomy 12, no. 8: 1769. https://doi.org/10.3390/agronomy12081769

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