Main issues in the ALAP - 2010 presentation “Controversy on the origin of S.

tuberosum
ssp. tuberosum” by Humberto A. Mendoza.

The author: A geneticist working in potato breeding for 35 years, 24 at CIP, 16 leading its
Breeding and Genetics Department. Duties: Breeding for disease resistance and adaptation to
diverse environments using adg, tbr, Neo tbr, stn, phu and gon. As a student he worked in day
length reaction: Physiology (France) and Genetics (US) and also at US collaborated in the long
day adaptation of diploid sps. stn and phu. (All underscoring and bolding are mine)
.
The subject: It is accepted that ssp. tbr originated from long day adaptation of adg migrating to
Europe starting in the XVI century. Solid scientific support came in 1960-80 with the creation of
Neo tbr germplasm very close to the ssp. tbr from a large number of true seed samples of the
ssp. adg introduced in Scotland and New York. Neo tbr combine genes for long day adaptation
with high yield, good tuber traits and several disease resistances present in adg but not in tbr.

The controversy: Papers by Ghislain and Spooner in the 2008 ALAP’s Meeting - Argentina and
2009 in TAG, based on SSR and plastid DNA marker analysis, concluded that “Neo tuberosum
originated mainly from southern Chile landraces instead of ssp. andigena”.

Presentation Objectives: To demonstrate that (1). This conclusion was sustained on six
invalid suppositions and (2). Their wide inferences were incorrect and some false.

First supposition: “adg tuberizes poorly in long days and rapid selection for long-day
tuberization was a big part of the long controversy on the origin of European potatoes”

Based on the false idea that all Andean potatoes have a “short day reaction” for tuberization, The
authors ignored that adg has ample variability for day length reaction (Mendoza and Haynes,
1976 and 1977 and several other authors they cited).

Mendoza and Haynes (1977) showed that day length reaction for tuberization was controlled by
one locus with two alleles and complete dominance, i.e., Pi = short day (SD) and pi = long day
(LD). Also, one of the five adg cultivars used had a LD reaction as the tbr progenitors. Thus, adg
clones have 5 genotypes: PiPiPiPi, PiPiPipi, PiPipipi, Pipipip, with SD reaction and pipipipi LD
reaction. Selfed seed of PiPipipi, Pipipipi and pipipipi adg genotypes produce 16.6, 50 and 100%
respectively of clones showing LD reaction for tuberization

Conclusion: These genetic results supported the rapid progress in “long day adaptation” of the
Neo tbr populations derived from the “short day andigena” discarding the first supposition.

Second supposition: Arguing that tbr: pollen flow into the adg initial population changed its
make up “A rapid selection against original adg clones after unintended hybridization with
ssp. tbr”. (Probably they meant “a rapid replacement of genes of adg by tbr genes”)

This is untenable as only a forced mass artificial fertilization of adg females with tbr pollen
for 3 to 4 continuous generations could have rapidly replaced original adg genes for tbr
genes in the Neo tbr population and absolutely not by unintended pollen flow.

Simmonds (1966) stated that initiation of the first Neo tbr population was at “some hundreds of
yards” from tbr cultivars and that out-pollination “was infrequent and probably non-existent”.

The following facts reinforce Simmonds statement that unintended pollen flow would have had
insignificant or no effects on the genetic make up of the andigena population.

(a). Lack of synchrony in flowering time (adg flowers later than commercial tbr cultivars),
(b). Near 90% commercial tuberosum cultivars do not shed pollen or have male sterility,
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(c). Near 80% or higher of berry set in andigena fields come from selfing,
These three irrefutable facts are sufficient to dismiss this argument.
(d). The adg cytoplasm was maintained in Neo tbr as pollen does not carry extra nuclear factors,
(e). Neo tbr high frequency of resistance genes to P. infestans, S. scabies, S. endobioticum, G.
rostochiensis, PVX, PVY, PLRV, etc., all from adg further invalidate the supposition.
(f). Also, dozens of crosses we made within Neo tbr segregated for some adg like plant and tuber
traits confirming that Neo tbr originated from adg. This rarely happened in crosses tbr x tbr.
(g). Discussions on bumblebee foraging-flaying habits are irrelevant by the previous facts.

Conclusion: These facts invalidate this supposition that also shows unawareness on potato
reproductive biology and the large number of Neo tbr traits directly originating from adg.

Third supposition: Identity errors in the adg entries from the Commonwealth Potato Collection
(CPC) used to build the Neo tbr population. “This collection may have misidentified
accessions of tbr as adg as in the early collection days all tetraploid landraces from the
highland Andes were included into adg” (Trying to imply that Neo tbr has tbr cytoplasm.).

(a). Tbr cultivars are not cultivated in the high Andes due to poor tuber yield and quality,
(b). Tbr cultivars flower poorly or not at all in the high Andes due to short days and low Tº.
(c). Because of (a) and (b), likelihood of spontaneous tbr x adg hybrids is nil,
(d). It is doubtful that the prestigious Commonwealth Potato Collection would have freely
distributed seed of “suspicious” tbr like clones as if they were adg.

Conclusion: This supposition is so improbable that can not even be considered.

Fourth supposition: Presence of volunteers or ssp. tbr plants from tubers left from the
previous crop in the adg field (again trying to imply a tbr cytoplasm in Neo tbr).

(a). Experienced geneticists never replant experiments in fields where potatoes were grown,
(b). Also, it would be very rare that the well known John Innes Institute would allow it,
(c). Tuber survival after the freezing winter temperatures is very low,
(d). Even if a few tbr volunteers growing in the adg field would have been promptly rouged out.

Conclusion: This weak supposition doesn’t merit any further comment.

Fifth supposition: Based on the rapid phenotypic change observed in Neo tbr. It ignored the
adg variability for day length reaction and basic genetic features “A plausible explanation could
be that desirable features of a cultivated potato (adaptation to long-days, superficial eyes,
oblong tubers, etc.) are present mainly in the tbr germplasm and rarely in adg”

(a). Simmonds and Plaisted stated that early selection cycles of Neo tbr populations concentrated
in the ability to yield under long days and not in tuberosum like plant and tuber characteristics,
(b).This supposition ignores that adg germplasm is highly heterozygous for many traits including
day length reaction, plant type, tuber shape, deep of eyes, etc. This was evident in crosses and
selfings within adg that segregated for long day adaptation and tuber characters,
(c). Also, Mendoza and Haynes (1976 and 1977) showed that among the “short day potatoes”
growing under 11, 13, 15 and 17 hour day lengths, there existed ample variability for day length
reaction and some adg cultivars photo periodically behaved as tbr cultivars do.

Conclusion: Suggests unawareness of genetics and breeding behavior of adg, tbr and Neo tbr.

An additional unchallenged issue covered in my ALAP – 2010 presentation:

Dr. F. L. Haynes at North Carolina, USA adapted diploid stn and phu to long days. After 5 to 6
cycles of selection results were as successful as those obtained with Neo tbr. As Frank’s student
during five years I collaborated in his work and later used his materials to build some of CIP’s
advanced populations. This also proved the “short day” Andean potatoes ample variability for day
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length reaction and rapid response to selection for adaptation. Haynes’ results can’t be contested
by arguments of unintended pollen flow, volunteers or errors in the founder phu-stn seed stocks.
Reflections on short day potato adaptation to high latitude environments.

Adaptation to 45 to 60ºN latitudes didn’t only involve ability to produce at 15 to 17 hour days but
also adapt to different temperature and soil regimes, light intensity and their interactions, etc. This
process should have required several genetic changes to readjust to the new environment.

As discussed before, among phu and adg cultivars under 11, 13, 15 and 17 hour day lengths,
there was ample variability and some adg behaved as tbr cultivars (Mendoza and Haynes, 1976).

In crosses and selfings within adg it was found that short day reaction was dominant over long
day and under control of a single locus. Also, adg germplasm was highly heterozygous at that
locus and segregated for long day adaptation (Mendoza and Haynes, 1977).

Plaisted’s Neo tbr and Haynes’ long day adapted diploid phu-stn tuberize and produce well under
the higher day and night temperatures of tropical lowlands in Peru where native adg, phu and stn
cultivars do very poorly (Mendoza, 1976, Mendoza and Estrada,1979 and Mendoza, 1980).

Reciprocal crosses (tbr x Neo tbr) and (Neo tbr x tbr) showed differences. The former with higher
frequency of earlier maturing clones with foliage and tuber type closer to tbr. This suggests that
tbr cytoplasm may have also evolved having more important effects than previously thought. The
same differences were observed in reciprocal crosses (tbr x adg) and (adg x tbr) in Peru.

High frequency of chloroplast marker T in tbr and adg derived Chilean landraces vs a low
frequency in native adg may also suggest evolutionary cytoplasm changes in the adaptation
process to higher latitudes with all their environmental elements different from those of the Andes.

Analysis of Ghislain and Spooner results, inferences and conclusions

We composed Figure Nº 1 with results by Ghislain and Spooner (2008 and 2009) and Spooner et
al (2007). The comparison shows contradictions and confusion leading to the following remarks.

(a).The left side picture grouped adg differently from tbr (Chilotanum group). However, the right
side picture showed the contrary grouping together landraces from southern Chile within adg.

(b).The left side picture shows errors in two pure adg check cultivars: ICA Nevada is not adg
as its parents were two S. phureja cultivars: Also, San Antonio Abad was a cross of {(tbr x adg) x
adg} with a tbr cytoplasm and tbr genes. So, their grouping with adg appears incorrect.

(c). The left side picture grouped ssp. tbr with a small sample of six Neo tbr and 15 Neo tbr
derived clones. Inference: “The high frequency of the plastid marker in variety and lines
derived from Neo tbr reflects also the importance of ssp. tbr into their pedigrees”

This sixth supposition was already dismissed: Neo tbr has adg cytoplasm and a large
number of adg genes for plant and tuber traits and disease resistances not present in tbr.

(d). The right side picture grouped Chilean landraces with adg, but these were separated in two
taxonomic groups: Chilotanum and Andigenum despite their phenotypic similarity in plant and
tuber traits and genetic behavior. Chilean landraces (15) and adg cultivars (15) used as females
crossed to the same adg pollen did not show any difference in tuber yield. Moreover, their
segregating progenies showed the same plant and tuber traits and time of maturity (Mendoza,
unpublished results). This supports the hypothesis that Southern Chile potatoes evolved from the
ssp. andigena after adaptation to the intermediate day lengths of 14 to 15 hours.
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(e). Moreover, the right side picture suggests that the power of genetic markers might have
limitations separating species as adg is grouped with several S. chaucha and S. stenotomum
cultivars and the “pure adg” check San Antonio Abad that has tbr cytoplasm and tbr genes.

Results were: (R1). All six pure Neo tbr clones and 12 Neo tbr derived lines grouped with tbr,
(R2). T plastid tbr marker was in one of six pure Neo tbr clones and seven of 12 Neo tbr lines.
Conclusion: “Neo tbr originated mainly from south Chile landraces instead of ssp. adg”

We reject this conclusion on the following undeniable genetic evidences;

(R1). This would have required a high frequency of tbr genes in Neo tbr. The authors said that
this was due to unintended pollen flow from tbr fields. We demonstrated that this argument
was untenable and can’t ignore the large number of well known adg genes in Neo tbr.

(R2). The fact that seven of 12 Neo tbr clones had the T chloroplast marker would mean that
about half of Neo tbr has tbr cytoplasm and that Simmonds and Plaisted’s work was a bluff. Given
that Neo tbr has adg cytoplasm this result confirm our hypothesis “the adaptation to higher
latitudes probably also involved evolutionary cytoplasm readjustments”
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Paradoxically, additional research results published by Ghislain, Spooner and others, based on
SSR and cytoplasm markers as the only methodology, gave an excellent and unexpected support
for our proposed cytoplasm evolution.
“Results of SSR analysis of 19 Canary Islands native cultivars showed that these were
distributed in the ssps. adg and tbr and the triploid S. chaucha” (Ghislain and Spooner,
2008, Rios, Spooner and Ghislain, 2007)

Five ancient Canary Islands cultivars all with the T chloroplast marker grouped within the Chilean
cluster. The Andean cluster grouped one 4x cultivar and two triploid S. chaucha cultivars with the
T chloroplast marker and 11 tetraploid cultivars with the X chloroplast adg marker. In summary,
of the 19 cultivars 14 grouped with Andean materials including three with the T chloroplast marker
and five with the T marker grouped with Chilean landraces.

The authors instead of discussing the reason of the two Andean triploid S. chaucha cultivars with
the T chloroplast marker said “Curiously, two of the chaucha had the T marker of tbr despite
that 150 Andean S. chaucha cultivars did not show it”

Given that S. chaucha has never been found in southern Chile, “the curiosity” of finding two
chaucha cultivars with the T marker of tbr has an evolutionary meaning supporting our previous
argument “High frequency of chloroplast marker T in tbr and adg derived Chilean landraces vs
low frequency in native Andean adg suggested evolutionary cytoplasm changes in the adaptation
to higher latitudes with all their environmental elements different from those of the Andes”.

All nine pictures in Figure Nº 2 show the typical adg tuber traits. The authors thru marker analysis
inferred that five of the 17 ancient Canary Island tetraploid cultivars originated in southern Chile
and 12 in the central Andes. (1). Given the similarity of their tuber type this would support that
Chilean landraces originated of adg migrating south as many taxonomists proposed and we
agree, and (2). This also supports our cytoplasm hypothesis of the change of the X chloroplast
marker to T type as an evolutionary event in the adaptation of adg to high latitude environments.

The basic differences between Chilean and Andean adg landraces are: (a). Chilean potatoes
are adapted to 14-15 hour day lengths of and andigena to 12-13 hours, and (b). The former has a
high frequency of the chloroplast marker T while adg has lower frequency.
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To us both differences instead of inherent traits of southern Chile potatoes are consequences of
the evolution of adg materials migrating to Chile. The same argument holds for the evolution of
the adg introduced to Europe starting in the mid XVI century.
Conclusion: This research based on genetic markers is an excellent support as an intermediate
step in the adg gradual chromosome and cytoplasm factor evolution in its way to continental
Europe towards the development of the European Solanum tuberosum ssp. tuberosum.

“SSR marker analysis of 32 Indian cultivars of which a few are believed to be remnants of
the supposedly old adg cultivars. Results showed that all 32 cultivars grouped with native
southern Chile cultivars and not with adg” (Spooner et al. 2005, Ghislain and Spooner, 2008).

This statement ignored important points about the origin and traits of Indian varieties.

(a). Potatoes introduced to India came from Europe and not from South America..
(b). Day length wasn’t a problem in adaptation of potatoes to India as 80% of its production is
made in the winter under short day length (< than 12 hours).
(c). Five out of the 32 varieties showed the X chloroplast marker of adg (Kufri Jawahar, Lalmutti,
Phulwa, Gulabia and Kufri Megha) and the other 27 the T from tbr.
(d). Indian records show that most Kufri varieties were released after 1958 and several have a
tbr European or US variety as female and adg as male progenitors. Their plant and tuber type
resembles more to tbr x adg hybrids rather than to tbr (Fig. 2). Moreover, the T chloroplast
marker came from their tbr female progenitor and not from Chilean landraces as suggested.
(e). Most Indian varieties have resistance to late blight and some to frost, wart and viruses
diseases. These genes originated from adg and not from Chilean landraces.

Conclusion: This research based on genetic marker analysis of modern Indian potato varieties
showed once more the change of the adg X type chloroplast marker to the tbr T type.

Additionally, this does not have any thing to do with the origin of the early European potatoes as
the analysis has been made on mostly modern varieties.
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“Implications of invalidating the Neo tuberosum hypothesis” (Ghislain and Spooner, 2008)

The SSR and chloroplast marker analysis didn’t invalidate anything. Denying the existence,
evolutionary and breeding significance of Neo tbr based on unfounded arguments is
unacceptable.

1. “The theory of adaptation of short day potatoes to long days sustaining that adg
cultivars were adapted to European long days and after the great 1840 famine produced by
late blight these were improved with Chilean landraces is invalidated”

(a). The existence of Neo tbr populations originated of selection for adaptation to high latitude
environments of widely diverse true seed samples of andigena stands still. Then, the Ghislain
and Spooner (2008 and 2009) arguments denying its existence are unfounded and unacceptable.

(b). Spooner et al (2005) inferences based on genetic marker analysis of modern Indian potato
varieties do not have anything to do with the origin of the early European potatoes.

(c). Likewise, Rios, Ghislain and Spooner (2008) conclusions on the origin of the European potato
based on genetic marker analysis of Canary Island landraces are also unacceptable. On the
contrary, it is a valuable evolutionary proof reinforcing the accepted theory on the andigena origin
of the European potatoes that we support.

(d). It is not possible to reach drastic conclusions solely based on SSR and chloroplast marker
analysis denying solid evolutionary, reproductive biology, genetic and breeding evidences.

(e). One strong argument of those who believe the ssp. tuberosum originated from Chile was a
Goodrich (1863) statement. “In 1851, I received 8 varieties from Panama, supposedly coming
from Chile. I grew one of them as Rough Purple Chile. It was progenitor of Garnet Chile. The
other seven were too late for this climate, one of them for one month and the rest probably for two
or three months”.

The last statement indicates that the eight varieties came from the Andean zone instead of Chile.
If they would have been from Chiloe (42º30’ S) with a photo period near 15 hours similar to that of
New York all would have tuberized normally even if later discarded for other reasons.

2. “The genetic base of CIP’s improved varieties continue being narrow as it has not taken
benefit of the diversity existing in the ssp. adg (except the population B1)”

This shows a total lack of knowledge of CIP’s breeding work ignoring the large number of widely
diverse new varieties released in the developing world with genes for resistance and adaptation
from andigena, native and Neo tbr, tbr, cultivated diploids and some wild species. Apparently, the
pedigree books were not carefully analyzed or were not understood. It is unfortunate that being
the first author a CIP staff member and the second a close cooperator, made such a serious and
unfounded statement without previously verifying and discussing its validity with CIP breeders.

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Ghislain, M, G. Núñez, M. Herrera, M. and D. M. Spooner. 2009. The single Andigenum origin of Neo-
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