Flier, W.G.

English

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  13 
Phytophtora infestans sensu lato in South America Population 
substructuring through host-specificity 
 
N. Adler1, G. Chacón1, G. Forbes1,2, W. Flier3 
 
The causal organism of late blight, Phytophthora infestans, has a pan global distribution. It is thought that P. 
infestans originates from the central highlands of Mexico where high levels of genetic variation are being 
maintained in sexually reproducing populations on both cultivated potato and several native Solanum 
species. 
Although our understanding of recent migrations and global population architecture has been improved 
considerably in recent years, little is known on the population biology of P. infestans in the Andean highlands 
of South America. The Andes are known as the center of diversity of solanaceous plant species (Spooner et al., 
1992). 
Late blight research in South America does not differ much from the rest of the world in that the majority of 
research is done on isolates obtained from potato and tomato, the cultivated host plants of greatest 
economic interest. Therefore, it is not surprising that little is known about the population biology of 
Phytophthora on other hosts. This may be one reason that the genetic diversity of clonally reproducing P. 
infestans populations in South America reported thus far is low and apparently stable (Table 1). 
 
Diversity of P. infestans on solanaceous plants 
In Ecuador, known for its highly variable ecosystems, P. infestans can be found on many host plant species 
belonging to the genus Solanum. Solanaceous plants can be subdivided in tuber-bearing (section “Petota“) 
and non tuber-bearing (“Etuberosum“) species. Ecuador offers a wide range of cultivated solanaceous hosts, 
such as potato (S. tuberousm), tomato (S. lycopersicon), tree tomato (S. betaceum), pear melon (S. muricatum) 
and naranjilla (S. quitoense) and wild species like S. andreanum, S. caripense, S. brevifolium-complex, S. 
tuquerrense and many more. There are four described clonal lineages for P. infestans, an exception to the 
general situation in South America (Table 1), which gives an indication of the diversity of P. infestans that 
might be revealed when population studies include samples from host plant species other than potato and 
tomato (Table 2). 
 
Table 1. Genetic diversity of P. infestans population in South America. 
Country Plant species studied Mating-
types 
Haplotypesa Clonal lineagesb 
Argentina Potatoes, tomatoes A1, A2 Ia, IIa AR-1, AR-2, AR-3, AR-4, AR-5, BR-1 
Bolivia Potatoes A2 Iia BR-1 
Brazil Potatoes, tomatoes A1, A2 Ia, IIa BR-1 
Chile Potatoes A1 Ib US-1 
Colombia Potatoes, tomatoes A1 Iia, Ib US-1, EC-1 
Ecuador solanaceous A1, A2 Ia, IIa, Ib, Ic US-1, EC-1, EC-2, EC-3, 
Peru Petota, tomatoes, S. caripense A1 Ia, IIa, Ib US-1, EC-1, PE-3, PE-5, PE-6 
Uruguay Potatoes A2 Iia BR-1 
Venezuela Potatoes A1 Iia, Ib US-1, EC-1 
aMitochondrial DNA haplotype 
bClonal lineage as defined by marker data. 
Sources: Deahl et al. in press, Erselius et al. 2000, Forbes et al. 1998, Gonzales Castano and Garcia 1998, Ñústez 1999, Pérez et al. 2001. 
                                                 
1 International Potato Center (CIP), Quito, Ecuador 
2 Now at International Potato Center (CIP) HQ, Peru 
3 Plant Research International, Wageningen, The Netherlands 
  14 
Table 2. Diversity of P. infestans on solanaceous plants in Ecuador. 
Lineage a Haplo- 
type b 
Mating 
type  
Gpi c Pep d Hosts 
US-1 Ib A1 86/100 92/100 S. ochrantum, S. lycopersicon, S. caripense, S. 
muricatume 
EC-1 IIa A1 90/100 96/100 S. tuberosum, all Solanum of the section ”Petota“ 
(tuber-bearing-potatoes) 
?a Ia A1 100/100 76/100 S. brevifolium-complexf, Datura bicolour 
EC-2 Ic A2 100/100 76/100 S. brevifolium-complexf, S. muricatumg 
EC-3 Ia A1 86/100 76/100 S. betaceum 
aClonal lineage as defined by marker data. The Ia mitochondrial DNA haplotype  isolates attacking S. brevifolium complex collected to date have the 
archetype EC-2 RFLP fingerprint but differ for other markers. 
bMitochondrial DNA haplotype 
cGlucose phosphate isomerase banding pattern 
dPeptidase banding pattern 
eBefore 2001 only US-1 was found on  S. muricatum.  
fHost species of this complex have not yet been identified. 
gTwo isolates with this genotype were taken from a heavily infected field of  S. muricatum near Baños. 
All isolates described so far in Ecuador can be placed in either of these clonal lineages; US-1, EC-1, EC-2 or EC-
3. However, there is some confusion as to the degree of diversity in the group of isolates described previously 
as EC-2. This will be discussed below. 
Ongoing research on the population biology of P. infestans attacking species in the genus Solanum 
demonstrates the level of host-specificity that can be found within the meta-population of P. infestans in the 
Ecuadorian highlands. In spite of a high level of diversity in the Ecuadorian meta-population of P. infestans, 
almost all the isolates coming from tuber-bearing species of Solanum (section Petota) are genetically similar, 
With only minimal polymorphism, this group, designated the EC-1 clonal lineage, is characterized by the A1 
mating type, Gpi 90/100 and Pep 96/100 allozyme genotype and the IIa mitochondrial DNA (mtDNA) 
haplotype. The diversity in P. infestans coming from the non-tuber-bearing hosts is higher (Table 2), occurring 
principally among and not within host-specific groups. One exception is the group of isolates associated with 
the S. brevifolium-complex. Plants belonging to this host-group including S. brevifolium, S. tetrapetalum, S. 
oblongifolium and few other plants that do not fit the description of these species could not always be clearly 
identified at the species level. 
To date there are at least two distinct pathogen groups associated with the S. brevifolium-complex. One has 
generally been associated with a plant phenotype tentatively identified as S. oblongifolium. This pathogen 
group is characterized by the A1 mating-type, Gpi (100/100) and Pep (76/100) allozyme genotype and the Ia 
mtDNA haplotype. A second group of isolates characterized by the same allozyme genotype, but with the A2 
mating type and Ic mtDNA haplotype (Oliva et al, 2002), is associated with other phenotypes in the host 
complex, probably S. brevifolium and S. tetrapetalum. However, host specificity within the pathogen group 
attacking S. brevifolium complex can only be considered a hypothesis at this time because of confusion about 
the identities of the different host species. 
The relationship between the two pathogen groups attacking the S. brevifolium complex is confounded even 
further by RFLP fingerprint data. The Ic mtDNA haplotype group appears to belong to the EC-2 clonal lineage 
as described previously (Ordoñez et al., 2000), but it is now generally found with an RFLP fingerprint assigned 
previously to the sub-lineage EC-2.1 (Ordoñez et al., 2000). Surprisingly, the Ia mtDNA haplotype group, which 
by mating type and mtDNA haplotype does not resemble EC-2, has the archetype RFLP fingerprint of EC-2. 
More sampling and marker evaluation is needed to determine how these two groups are related. Future 
research on isolates coming from the S. brevifolium-complex will focus on whether they are indeed isolates of 
P. infestans or if they belong to another taxon related to P. infestans. 
Isolates with the genetic profile of the Ic mtDNA haplotype group were also found in two ocassions on 
cultivated pear melon plants (S. muricatum), implying that some apparently host-specific sub-populations of 
P. infestans are still capable of successfully colonizing new hosts. Viable oospores were found in the fruits of 
pear melon after infection with isolates of opposite mating types originally obtained from this host plant. 
Sexual reproduction between apparently host specific populations of P. infestans on “bridging hosts” would 
lead to increased variability in the pathogen population, and host switching would lead to a more complex 
population structure and could be of great importance in population biology of P. infestans in Ecuador. 
In general, host specificity is still a driving force for maintaining genetic isolation between sub-populations 
(clonal lineages) of P. infestans in Ecuador (Table 3). For example, it is impossible to infect plants in the S. 
brevifolium complex (hosts of Ic mtDNA group of isolates) with P. infestans isolates obtained from a host of 
the Petota section, and vice versa. The results of cross inoculation experiments demonstrate that, in general, 
  15 
each clonal lineage, except EC-3 that is only found on S. betaceum (tree tomato) plants, is associated with 
more than one host, but rarely are hosts associated with more than one lineage. The only exception appears 
to be pear melon, where two lineages have been found causing epidemics. 
AFLP analysis divided all Ecuadorian isolates into two major clusters. The US-1 and EC-1 lineages formed one 
major cluster, while the S. brevifolium complex isolates and EC-3 isolates belonged to the second major 
cluster. Within these major clusters, AFLP analysis also discriminated among clonal lineages.  Furthermore, 
within the S. brevifolium complex group, the Ic mtDNA isolates clustered separately from the Ia mtDNA 
isolates. This is consistent with the hypothesis that two distinct groups attack the S. brevifolium complex. 
However, as noted above, these groups have similar RFLP fingerprints. 
The separation of the S. brevifolium complex group and the EC-3 lineage from the other lineages raises the 
question of origin. It is possible that these two lineages are relatives of an “ancient“ Phytophthora population 
that is indigenous to Ecuador or immigrated into Ecuador long before the first reported migration from 
Mexico took place. 
 
The sexual frontier 
In pear melon plants a coexistence of the “old“ population US-1 (A1) and the EC-2 (A2) was reported, while in 
other hosts of the section Petota the US-1 lineage was replaced by the EC-1 lineage (Forbes et al., 1997). 
Therefore gene flow between host-specific populations of P. infestans might take place in the Andes when 
bridging hosts exist.  
Apart from genetic isolation through host specificity, geographical isolation between late blight populations 
has been observed in South America. This was found at the frontier of Peru and Bolivia next to Lake Titicaca. 
The P. infestans population found in potato cultivars of Peru is of the A1 mating type and principally the EC-1 
lineage, while Bolivian isolates on potato are predominantly A2 mating type and belong to the BR-1 clonal 
lineage. No interactions were ever observed between the two clonal lineages in potato crops along the 
border between the two countries. Nonetheless, meiotic recombination of the two lineages may take place 
on other solanaceous hosts growing along the border of the lake. Although hosts generally only have one 
principal pathogen population, at least two cases of host switching have been detected so far in Ecuador. The 
EC-1 lineage is believed to have displaced US-1 on potato (Forbes, et al, 1997) and both A1 and A2 genotypes 
were found to cause epidemics on pear melon. More fieldwork and population studies should be carried out 
to determine whether sexual recombination is occurring in the region of Late Titicaca. 
Knowledge of the genetic structure of P. infestans on all Andean solanaceous hosts, especially the cultivated 
hosts, gives new insight into the historical and present changes in the pathogen population. This information 
is also important in breeding for durable resistance because the mechanisms of host specificity are not known 
and may mask or confound resistance. 
 
Table 3. Cross inoculations of sub-populations of P. infestans on different hosts (“+” = infection, ”-“  = no infections or 
hypersensitive reactions detached-leaf tests). 
       Isolates from 
 
 
Hosts 
“Petota”-   
(EC-1) 
S. brevifolium-complex 
 
S. betaceum 
(EC 3) 
S. lycopersicon, S. 
muricatum, S. caripense 
(US-1) 
“Petota“ group 
 
 
+ 
 
- 
 
- 
 
+a 
S. brevifolium - complex  
 
 
- 
 
+ 
 
- 
 
- 
 
S. betaceum 
 
 
- 
 
- 
 
+ 
 
 
US-1 group 
(S. lycopersicon, S. 
muricatum, S. caripense) 
 
+ a 
 
S. muricatumb 
 
- 
 
+ 
aUS-1 and EC-1 isolates can be cross inoculated on their alternative hosts,but are more aggressive on their primary hosts. 
bTwo isolates typical of those from S. brevifolium complex were collected from a heavily infected field of S. muricatum. 
 
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Figure 1: AFLP analysis of isolates of P. infestans isolated from different solanaceous hosts in Ecuador. 
 
  17 
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Phytophthora infestans sensu lato in South America; Population sub-structuring through host specificity

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