Plant Breeding 101, 261-2~8 (1988)@ 1988 Paul Parey Scientific Publishers, Berlin and HamburgISSN 0179-9541

School of Biological Sciences, University of Birmingham (U.K.

The Importance of the Bolivian Wild Potato Speciesin Breeding for Globodera pallida Resistance

M. T. JACKSON, G. HAWKES, BEATRICE S. MALE-KAYIWA and N. W. M. WANYERA

With one figure and 2 tables

Received August 3, 1988/ Accepted August 7; 1988

AbstractScreening for resistance to the potato cyst nematode,Globodera pallida, in potatoes from Bolivia, wascarried out in 1983 and 1984, using a mixture of fournematode populations representing pathotypes Pat.Paz and Pa}. From the 66 accessions of 17 species andsubspecies evaluated, highly resistant genotypeswere identified in 21 accessions from seven species.All had Pf/Pi values of 2 or less, whereas the suscepti-ble control, Solanum tuberosum cv. 'Desiree', hadPf/Pi values of more than 20 in both tests. Twodiploid wild species, S. brevicaule and S. leptophyes,showed the best resistant. The geographical distribu-tion of resistant populations and the evolution ofresistance in wild potato populations are discussed.

Key words: Solanum spec. -Globodera pallida-potato cyst nematode -potato breeding -geneticresources -wild species -resistance screening -evaluation studies -phytogeography

Resistance to the potato cyst nematode,Globodera pallida (Stone) Mulvey & Stone, isone of the principal objectives of potato breed-ing in the United Kingdom. Early work onresistance breeding concentrated on G. ros-tochiensis (Woll.), after resistance had beenidentified in Solanum vernei from north-westArgentina, and in S. tuberosum ssp. andigena(ELLENBY 1948, 1952). Even so, resistant Euro-pean varieties were unknown before 1950 (VANSOEST et al. 1983 b). Since the recognition oftwo Globodera species in the early 1970s, therehas been a concerted effort in Europe andSouth America to identify and use sources of

resistance to G. pallida. These breeding effortshave paralleled germplasm collecting activitiesthroughout the Andes of South America, butmore particularly in Bolivia.

It is true that until the 1970s, the wildpotatoes of Bolivia were less well known andunderstood biologically than those of othercountries of South and Central America, eventhough some of the species that occur inBolivia do have distributions which spreadnorthwards into Peru, and southwards intoArgentina. What is clear, however, is that thematerial collected in Bolivia has shown consid-erable promise as a source of cyst nematoderesistance genes. Through evaluation studies ofmaterial collected in Bolivia in 1980 (VAN SOESTet al. 1983a), not only is there a much betterunderstanding of the taxonomic and evolution-ary relationships and distribution of the Boli-vian wild species (HAWKES and H]ERTING 1988)but genotypes resistant to G. pallida have beenidentified (VAN SOEST et al. 1983 b, CHAVEZ1984, DELLAERT and HOEKSTRA 1987, CHAVEZ etal. 1988).

There are 35 species and subspecies of wildpotatoes in Bolivia (HAWKES and H]ERTING1988). Although the best sources of resistanceto G. pallida have been found in species fromSeries Tuberosa, which are closest biologicallyto the cultivated potatoes, other species fromSeries Acaulia, Circaeifolia and Megistacrolobahave also shown resistance. The apparent con-centration of resistance genes to both G. palli-da and G. rostochiensis in north-west Argenti-na has been commented upon by STONE (1979).

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264 JACKSON, HAWKES, MALE-KAYIWA and WANYERA

organic matter, it is reliable, efficient and widelyused.

In the 1983 test, resistance screening was based onthree seedlings from each accession, whereas in the1984 test, screening was carried out on five seedlings.The resistance of each seedling was determined onthe basis of the ability of cyst nematodes to repro-duce on potato plants, using the Pf/Pi ratio, where Piis the initial nematode population (i.e. number ofcysts added as inoculum) and Pf the final population(i.e. number of cysts recovered after senescence ofthe potato plant). Plants with a Pf/Pi ratio of less than2 were regarded as resistant. Accurate counts weremade up to three times the initial inoculum, butabove this only estimates were made. TheS. tuberosum cultivar 'Desiree' was used as a suscep-tible control, although in this case plants were grownfrom tubers.

HAM 164 where the results for the 1984 test(mean Pf/Pi = 3) were higher than in 1983(mean Pf/Pi = 1), and upon which this acces-sion was selected for a second evaluation. Allother species and accessions showed muchhigher multiplication of cysts, and althoughthe Pf/Pi values never reached those on cv.'Desiree', it was relatively easy nevertheless todiscriminate these genotypes as susceptible topotato cyst nematodes.

The levels of resistance found in certainBolivian wild potato species to G. pallidapathotypes Pal, Pal and Pa3 is impressive andextensive. Clearly the best resistance is foundin S. brevicaule and S. leptophyes, and in all butone accession of S. sparsipilum. The low levelof cyst nematode multiplication on genotypesof these species, relative to that which wastypical of the susceptible control variety 'De-siree', indicates that the resistance of thesespecies is worthy of further investigation. Theimportance of the S. brevicaule genotypes isstrengthened by the results from other screen-ing tests. The S. brevicaule accessions used inthe present study against three G. pallidapathotypes were the same as those screened byCHAVEZ (1984) and reported by CHAVEZ et al.(1988) against pathotypes P4A and P5A. Al-though SCURRAH and FRANCO (1985) equatedP4A and P5A with pathotypes Pal and Pa3respectively, the nematode populations usedby CHAVEZ were altogether different fromthose used here. Even so, CHAVEZ et al. (1988)reported a very high frequency of resistantgenotypes in the S. brevicaule material, whichindicates its very high breeding value. It isinteresting also to mention those species suchas S. alandiae, S. berthaultii, S. microdontum,S. okadae, S. violaceimarmoratum andS. toralapanum which gave low resistance val-ues. The first three of these are from loweraltitudes. Can we assume that G. pallida hasnot been present in such altitudes and that thespecies have not evolved protective mecha-nisms to combat it? Species such as S. okadae,S. violaceimarmoratum and S. circaeifoliumssp. quimense grow in the very high rainfallceja forest region, and again, the nematodesmay not have been present in this phytogeog-raphical region. It is more difficult even tohazard a guess at the apparent lack of resistancein S. toralapanum, since this species is veryfrequent in the same region as S. brevicaule,

ResultsAssessment of resistance to cyst nematodes

Apparent broad spectrum resistance to G. pal-lida pathotypes Pal' Pal and Pa3 was identifiedin 21 accessions (Table 2), representing sevenspecies from three taxonomic series. All hadmean Pf/Pi ratios of 2 or less in one or bothtests, and in fact only two accessions, S. suc-Tense HAM 089 and S. sparsipilum HHA 6670had scores of 2, in the 1984 test. In contrast theS. tuberosum cultivar "Desiree' had Pf/Pi valuesof more than 20, which clearly demonstrate itsextreme susceptibility to this mixture of cystnematode populations. In the light of this mul-tiplication of cysts on a susceptible host plant,the resistance shown by the thirteen accessionstested in both years of S. brevicaule, S. lep-tophyes, S. sparsipilum, S. sucrense andS. megistacrolobum is even more impressive.Pf/Pi values were obtained for one test only forthe remaining apparent resistant accessions be-longing to S. brevicaule, S. sparsipilum,S. tuberosum ssp. andigena and S. acaule.Conflicting values were obtained for S. neocar-denasii, S. oplocense, S. acaule and S. cir-caeifolium ssp. quimense. In the case ofS. neocardenasii (HHA 6496), original seedwas available only for the 1983 test, whereasseed from sib-matings had to be used in 1984.In the first test, the mean Pf/Pi value was 3, butin 1984 it was only 1. The same pattern wasalso shown by S. acaule HHA 6604 and S. cir-caeifolium ssp. quimense HHA 6532. How-ever this trend was reversed in S. oplocense

cyst multiplication on cv. 'Desiree' were madeon the basis of the latter grown from tubers.PHILLIPS (1984, 1985) has outlined some of theinherent dangers in assessing quantitative re-sistance to cyst nematodes, including the effectof initial population density on the reproduc-

which is extremely promising in its G. pallidaresistance. These are questions which cannotyet be answered.

Undoubtedly, the screening tests themselvescan be open to criticism, since they were car-ried out on seedlings, but comparisons with

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266

JACKSON, HAWKES, MALE-KAYIWA and WANYERA

tion of G. pallida, and that in these experi-ments results can be variable because of geno-type-environment interactions, due to thepolygenic nature of resistance (SCURRAH andFRANCO 1985). Although some nematologistshave criticized the use of seedlings in resistancetesting, because of the restricted root systemrelative to that from a vegetatively-propagatedplant, the validity of seedling tests has beenconfirmed by PHILLIPS and DALE (1982). Theimportant consideration which must be bornein mind is that an efficient screening pro-gramme must quickly identify promisinggenotypes, or to put it in other words, it isnecessary to eliminate at an early stage allsusceptible materials. Any clones which sur-vive a rigorous test can be evaluated againusing tubers. It is therefore important to setselection criteria which allow the breederrapidly to achieve this objective. Only in thisway is it possible to screen germplasm for cystnematode resistance, bearing in mind that re-sistance to this parasite is only one of manypriorities in potato breeding.

Geographical distribution of resistant species

In order adequately to describe the geographi-cal distribution of resistant species, it is neces-sary to comment upon the phytogeography ofBolivian wild species. They are found within abelt which runs north-south through centralBolivia (Fig. 1), with a concentration ofspecies in the Departments of Chuquisaca (19species and subspecies), La Paz (17) andCochabamba (18), and fewer in Potosi (14),Santa Cruz (10), Tarija (9) and aruro (5)(HAWKES and H]ERTING 1988). No wild specieshave been found in the lowland tropical de-partments of Beni and Pando. The low numberof species in aruro can be explained by its highaltitude, with most of the area of the depart-ment covered by high dry puna steppe, oftenwith saline soils unsuitable for potatoes.HAWKES and H]ERTING (1988) account for thepotato richness of the other departments as areflection of the range of altitude and ecologi-cal zones favourable for potatoes. In thepresent study, most of the accessions whichshowed resistance to G. pallida were collectedin the area immediately to the north and southof Cochabamba, although other resistantmaterials

were found in locations further to thenorth-west, and to the south and east (Fig. 1).

Nevertheless, most of the accessions studiedfall along a broad line north-west to south-eastfrom La Paz to the region between Sucre andSanta Cruz. All the S. brevicaule and S. lep-tophyes materials came from the Cochabambaregion, as did the majority of the S. sparsipilumaccessions. These results at first sight seem toconflict with those of VAN SOEST et al. (1983b).However, closer inspection shows that theseauthors did not show S. brevicaule on theirmap, even though they noted Pa3 resistance intheir Table 2. They also screened a very largeamount of material from Oruro and Potosi,southwards to the Argentine border. We hadonly three accessions (two of,S. sucrense andone of S. oplocense) from that region. Thesethree results fit well into the VAN SOEST et al.pattern as shown in their map. Again, ourS. sparsipilum and S. leptophyes results accordwith the VAN SOEST et al. resistance distribu-tion for those species. On the whole then, ourresults agree well with the VAN SOEST et al.(1983 b) work, but add an interesting new di-mension in terms of the high incidence ofG. pallida resistance in S. brevicaule, So lep-tophyes and S. sparsipilum, especially in the LaPaz and Cochabamba regions.

Another point worth mentioning is that allthe S. brevicaule collections were found at veryhigh altitudes (3650-3850 m) and from twogeneral areas, both near Cochabamba. TheS. leptophyes collections were from slightlylower altitudes (3200-3530 m) to the north ofPotosi. The S. sparsipilum collections werefrom still lower altitudes (2380-3300 m), andwere all from the Cochabamba valley region.

DiscussionThe evolution of resistance to potato cystnematodes in wild and cultivated plant popula-tions is worthy of some consideration. Culti-vated potatoes have originated from wildspecies, although it is not possible to say withcomplete certainty which these species were.We can only surmise their identity based uponthe results of biosystematic studies of the culti-gens and their wild relatives (HAWKES 1978).The co-evolution of potato cyst nematodes andtheir hosts has been reviewed by STONE (1985).Co-evolution suggests that resistance in planthosts and virulence in nematodes is controlledby genes acting on a gene-for-gene basis. Such

The Importance of the Boli"ian Wild Potato Species 267

the existence of resistance genes in wild potatopopulations is very hard to explain, based onour present knowledge. If, as STONE (1987) hasindicated, resistance to potato cyst nematodesevolved through co-evolution during geologi-cal time, the nature and distribution of thehost-parasite interaction may well have beenmore extensive in the past than can be ac-counted for at the present time. Whatever maybe the answer to this problem the evidence forresistance in wild potato species from Bolivia isof considerable importance from a breedingand genetic resources point of view. Resistanceto G. pallida derived from S. tuberosum ssp.andigena and S. vernei may prove vulnerableto selection for virulence, and as a consequ-ence, STONE (1985) argued for the breedingbase for resistance to this parasite to be wide-ned to include other sources. In this light theresistance identified in S. brevicaule, S. lep-tophyes and S. sparsipilum is important forpotato breeding, as is that in S. sucrense be-cause it is easier to cross with S. tuberosum. AsCHAVEZ et al. (1988) have shown, such resist-ance can be transferred to hybrid progenieswith S. tuberosum. The need for continuedscreening cannot be emphasized too strongly.

interactions have been observed in relation tomajor resistance genes HI and Hz (PARRO1T1982). However, such straightforward expla-nations cannot account for the variation invirulence which is encountered in G. pallidapopulations, and the polygenic nature of re-sistance to this nematode in potato species.One of the reasons why the pathotype conceptof nematode populations, which describesraces of a nematode species distinguished byinherited ability or inability to reproduce onspecified lines of a host-plant species that em-body different genes for resistance to thenematode (STONE 1985), is now being ques-tioned because it is proving impossible to par-tition the variability of G. pallida populationswithin such a concept (STONE 1987). Accordingto STONE (1985) the evolution of wild plantpopulations with resistance genes to nematodeparasitism, and wild nematode populationswith virulence genes and pathotypes, is a pro-cess which occurred in geological time. Theoutcome of this process is that we have avail-able wild and cultivated potatoes which displayresistance to potato cyst nematodes.

When we look at the distribution of Globo-dera populations throughout the Andes, it isapparent that most populations north of LakeTiticaca are G. pallida, whereas those to thesouth are mainly G. rostochiensis (EVANS et al.1975). Why is it then, that wild species fromBolivia, considerably to the south of LakeTiticaca, such as S. brevicaule and S. leptophy-es, show such good resistance to a wide rangeof G. pallida populations, which in the workreported by CHAVEZ et al. (1988), came fromcentral and northern Peru, and in the workpresented here, were British nematode popula-tions? Furthermore, what are the actual selec-tion pressures for resistance in nature?BROCHER (1961) reported finding cystnematode on wild potatoes in Argentina. Thevalidity of this report must, however, be ques-tioned. In a detailed survey carried out in Peruand Bolivia in 1978, during the growing sea-son, over 220 soil samples associated with cul-tivated and wild tuber-bearing Solanumspecies, as well as other solanaceous plants,were collected (EVANS, personal communica-tion). Whereas cysts and females were foundassociated with cultivated potatoes, this wasnot so with wild species, except in one or twodoubtful cases. In the light of such evidence,

ZusammenfassungDie Bedeutung bolivianischer Kartoffel-Wildarten fur die Resistenzzuchtung gegenGJobodera pallida

Es wurden in den J ahren 1983 und 1984 beiKartoffeln aus Bolivien Priifungen auf Resi-stenz gegen den cystenbildenden NematodenGlobodera pallida durchgefiihrt. Hierbei wur-de cine Mischung aus 4 Nematoden-Populatio-nen mit den Pathotypen Pal, Pal und Pa3 ver-wendet. Van 66 Herkiinften aus 17 Arten undUnterarten erwiesen sich 21 Herkiinfte aus 7Arten als hochresistent. 1m Gegensatz zur an-falligen Kontrollsorte 'Desiree' aus Solanumtuberosum, bei der Pf/Pi-Werte van iiber 20 zuverzeichnen waren, lagen die entsprechendenWerte der als hochresistent erkannten Her-kiinfte bei 2 und darunter. Die hochste Resi-stenz wurde bei den Arten S. brevicaule undS. leptophyes festgestellt. Die geographischeVerbreitung der Resistenz und ihre Evolutionin den Kartoffel- Wildarten werden diskutiert.

The authors are grateful for facilities and help pro-vided at Rothamsted Experimental Station by thelate Dr. ALAN STONE and by Miss D. PARROTT. Thework was carried out under the terms of MAFFLicence PHF 78A/57 (126). The University of Bir-mingham Potato Collection is now held underquarantine in Scotland. Further informacion aboutthis material may be obtained from MTJ.

PARROTT, D. M., 1982: Evidence for gene-for-generelationships between resistance gene HI from Sol-anum tuberosum ssp. andigena and a gene inGlobodera rostochiensis and between H2 fromS. multidissectum and a gene in G. pallida.Nematologica 27, 372-384.

PHILLIPS, M. S., 1984: The effect of initial popula-tion density on the reproduction of Globoderapallida on partially resistant potato clones derivedfrom Solanum vernei. Nematologica 30, 57-65.

--, 1985: Environmental differences and theireffect on the assessment of quantitative resistance topotato cyst nematodes. EPPO Bulletin 15,179-183.

--, and M. F, B. DALE, 1982: Assessing potatoseedling progenies for resistance to the white potatocyst nematode. J. Agric. Sci., Cambridge 99,67-70.

STONE, A. R., 1979: Co-evolution of nematodes andplants. Symp. Bot. Upsal. XXII 4, 46-61.

--, 1985: Co-evolution of potato cyst nematodesand their hosts: implications for pathotypes andresistance. EPPO Bulletin 15, 131-137.

--, 1987: Genetic systems in plant pathogenicnematodes and their hosts. In: P. R. DAY and G. J.JELLIS (eds.), Genetics and Plant Pathogenesis. Ox-ford: Blackwell Scientific Publications.

SCURRAH, M. M. DE, and J. FRANCO, 1985: Breed-ing for resistance to Globodera pallida at CIP.EPPO Bulletin 15, 167-173.

VAN SOEST, L. J. M., J. G. HAWKES, and W.HONDELMANN, 1983a: Potato collecting expedi-tion to Bolivia and the importance of Boliviangermplasm for plant breeding. Z. Pflanzenziichtg.91, 154-168.

--, H. J. RUMPENHORST, and C. A. HUijSMAN,1983 b: Resistance to potato cyst-nematodes intuber-bearing Solanum species and its geographicaldistribution. Euphytica 32, 65-74.

Authors' addresses: M. T. JACKSON, Plant GeneticsGroup, School of Biological Sciences, University ofBirmingham, P.O. Box 363, Birmingham, B15 2TT;J. G. HAWKES, c/o Earth Sciences, University ofBirmingham (U.K.); B. S. MALE-KAYIWA andN. M. W. W ANYERA, Kawanda Research Station,P.O. Box 7065, Kampala (Uganda).

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CHAVEZ, R., 1984: The use of wide crosses in potatobreeding. Ph. D. thesis, Univ. of Birmingham,U.K.

--, M. T. JACKSON, P. E. SCHMIEDICHE, and J.FRANCO, 1988: The importance of wild potatospecies resistant to the potato cyst nematode,Globodera pallida, pathotypes P~ and PsA, inpotato breeding. I. Resistance studies. Euphytica27,9-14.

DELLAERT, L. M. W., and R. HOEKSTRA, 1987:Resistance to potato cyst nematodes, Globoderassp., in wild and primitive Solanum species. PotatoRes. 30, 579-587.

ELLENBY, C., 1948: Resistance to the potato-rooteelworm. Nature 162, 704.

--, 1952: Resistance to the potato-root eelwormHeterodera rostochiensis Woll. Nature 170, 1016.

EVANS, K., J. FRANCO, and M. M. DE SCURRAH,1975: Distribution of species of potato cyst-nematodes in South America. Nematologica 21,365-369.

HAWKES, J. G., 1978: Biosystematics of the potato.In: P. M. HARRIS (ed.), The Potato Crop -TheScientific Basis for Improvement. London: Chap-man and Hall.

--, and J. P. HjERTING, 1988: The Potatoes ofBolivia -Their Breeding Value and EvolutionaryRelationships. Oxford: Clarendon Press.

JACKSON, M. T., 1988: Vavilov's Law of Homolo-gous Series -is it relevant to potatoes? Bot. J.Linn. Soc. (in press).