Skip to main content
Log in

Substitutes for genome differentiation in tuber-bearing Solanum: interspecific pollen-pistil incompatibility, nuclear-cytoplasmic male sterility, and endosperm

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

The cultivated potato, Solanum tuberosum L. (2n=4x=48), has a very large number of related wild and cultivated tuber-bearing species widely distributed in the Americas. These species, grouped in 16 taxonomic series, range from the diploid to the hexaploid level. Polyploid species are either disomic or polysomic, and sexual polyploidization via genetically controlled 2n gametes has played a major role in their evolution. Species are separated in nature by geographical and ecological barriers. However, there are several examples of sympatric species that share the same niches but do not readily cross (i.e., the diploids S. commersonii and S. chacoense in certain areas of Argentina). External barriers alone are, therefore, not sufficient to explain species integrity. In addition, there is no strong evidence indicating that genome differentiation is important in the group. In this review we present evidence supporting the assertion that interspecific pollen-pistil incompatibility, nuclear-cytoplasmic male sterility, and the endosperm are major forces that strengthen the external hybridization barriers allowing, at the same time and under specific circumstances, a certain amount of gene exchange without jeopardizing the integrity of the species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abdalla MMF, Hermsen JGTH (1972) Plasmons and male sterility types in Solanum verrucosum and its interspecific hybrid derivatives. Euphytica 21:209–220

    Google Scholar 

  • Arisumi T (1982) Endosperm balance numbers among New Guinea-Indonesians Impatiens species. J Hered 73:240–242

    Google Scholar 

  • Berger F (1999) Endosperm development. Curr Opin Plant Biol 2:28–32

    Article  CAS  PubMed  Google Scholar 

  • Boavida LC, Silva JP, Feijó JA (2001) Sexual reproduction in the cork oak (Quercus suber L.). II. Crossing intra-specific and interspecific barrires. Sex Plant Reprod 14:143–152

    Article  Google Scholar 

  • Boyes JW, Thompson WP (1937) The development of the endosperm and embryo in reciprocal crosses in cereals. J Genet 34:203–227

    Google Scholar 

  • Breiman A, Galun E (1990) Nuclear-mitochondrial interrelation in angiosperms. Plant Sci 71:3–19

    Article  CAS  Google Scholar 

  • Brink RA, Cooper DC (1947) The endosperm in seed development. Bot Rev 132:423–541

    Google Scholar 

  • Brown CR (1984) Tetrad sterility: a cytoplasmic-genic male sterility attractive to bumble bees. In: Winiger FA, Stockli A (eds) Abstracts of the conference papers of the 9th Trienn Conf Europ Assoc Potato Res, Interlaken, Switzerland, 1–6 July 1984, pp 101–102

  • Buck RW Jr (1960) Male sterility in interspecific hybrids of Solanum. J Hered 512:13–14

    Google Scholar 

  • Buckner B, Hyde BB (1985) Chloroplast DNA variation between the common cultivated potato (Solanum tuberosum ssp. tuberosum) and several South American relatives. Theor Appl Genet 71:527–531

    CAS  Google Scholar 

  • Camadro EL (1981) Mode of origin and evolution of wild polyploid Solanums and the development of internal barriers to hybridization. PhD thesis, University of Wisconsin, Madison

  • Camadro EL, Masuelli RW (1995) A genetic model for the endosperm balance number (EBN) in the wild potato Solanum acaule Bitt. and two related diploid species. Sex Plant Reprod 8:283–288

    Google Scholar 

  • Camadro EL, Peloquin SJ (1981) Cross-incompatibility between two sympatric polyploid Solanum species. Theor Appl Genet 60:65–70

    Google Scholar 

  • Camadro EL, Masuelli RW, Cortés MC (1992) Haploids of the wild tetraploid potato Solanum acaule ssp. acaule: generation, meiotic behavior and electrophoretic pattern for the aspartate aminotransferase system. Genome 35:431–435

    CAS  Google Scholar 

  • Camadro EL, Verde LA, Marcellán ON (1998) Pollen-pistil incompatibility in a diploid hybrid potato population with cultivated and wild germplasm. Am J Potato Res 75:81–85

    Google Scholar 

  • Cardi T, Bastia T, Monti L, Earle ED (1999) Organelle DNA and male fertility variation in Solanum spp. and interspecific somatic hybrids. Theor Appl Genet 99:819–828

    Article  CAS  Google Scholar 

  • Carputo D, Frusciante L, Peloquin SJ (2003a) The role of 2n gametes and endosperm balance number in the origin and evolution of polyploids in the tuber-bearing Solanums. Genetics 163:287–294

    CAS  PubMed  Google Scholar 

  • Carputo D, Parisi M, Consiglio F, Iovene M, Caruso G, Monti L, Frusciante L (2003b) Aneuploid hybrids from 5x–4x crosses in potato: chromosome number, fertility, morphology and yield. Am J Potato Res 80:93–101

    Google Scholar 

  • Cipar MS, Peloquin SJ, Hougas RW (1964) Variability in the expression of self-incompatibility in tuber-bearing diploid Solanum species. Am Potato J 41:155–162

    Google Scholar 

  • Dionne LA (1961) Cytoplasmic sterility in derivatives of Solanum demissum. Am Potato J 38:117–120

    Google Scholar 

  • Dodds PN, Clarke AE, Newbigin E (1996) A molecular perspective on pollination in flowering plants. Cell 85:141–144

    Article  CAS  PubMed  Google Scholar 

  • Dvorák J (1983) Evidence for genetic suppression of heterogenetic chromosome pairing in polyploid species of Solanum, sect. Petota. Can J Genet Cytol 25:530–539

    Google Scholar 

  • Ehlenfeldt MK, Hanneman RE Jr (1988) Genetic control of endosperm balance number (EBN): three additive loci in a threshold-like system. Theor Appl Genet 75:825–832

    Google Scholar 

  • Ehlenfeldt MK, Hanneman RE Jr (1992) Endosperm dosage relationships among Lycopersicon species. Theor Appl Genet 83:367–372

    Google Scholar 

  • Erazzú LE, Camadro EL, Clausen AM (1999) Pollen-style compatibility relations in natural populations of the wild diploid potato species Solanum spegazzinii Bitt. Euphytica 105:219–227

    Article  Google Scholar 

  • Evans MMS, Kermicle JL (2001) Teosinte crossing barrier1, a locus governing hybridization of teosinte with maize. Theor Appl Genet 103:259–265

    Article  CAS  Google Scholar 

  • Flor HH (1955) Host-parasite interaction in flax rust: its genetics and other implications. Phytology 45:680–685

    Google Scholar 

  • Frankel R, Galun E (1977) Pollination mechanisms, reproduction and plant breeding. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Friedman WE (1998) The evolution of double fertilization and endosperm: an “historical” perspective. Sex Plant Reprod 11:6–16

    Article  Google Scholar 

  • Fritz NK, Hanneman RE Jr (1989) Interspecific incompatibility due to stylar barriers in tuber-bearing and closely related non-tuber-bearing Solanums. Sex Plant Reprod 2:184–192

    Google Scholar 

  • Gebhardt C, Ritter E, Barone A, Debener T, Walkemeier MN, Ganal MW, Tanksley SD, Salamini F (1991) RFLP maps of potato and their alignment with the homoeologous tomato genome. Theor Appl Genet 83:49–57

    Google Scholar 

  • de Graaf BHJ, Derksen JWM, Mariani C (2001) Pollen and pistil in the progamic phase. Sex Plant Reprod 14:41–55

    Article  Google Scholar 

  • Grant V (1971) Plant speciation. Columbia University Press, New York

    Google Scholar 

  • Grun P (1973) Cytoplasmic sterilities that separate the Group Tuberosum cultivated potato from its putative tetraploid ancestor. Evolution 27:633–643

    Google Scholar 

  • Grun P (1979) Evolution of the cultivated potato: a cytoplasmic analysis. In: Hawkes JG, Lester JA, Skelding RC (eds) The biology and taxonomy of the Solanaceae. Academic, New York, pp 655–665

    Google Scholar 

  • Grun P, Aubertin M (1965) Evolutionary pathways of cytoplasmic male sterility in Solanum. Genetics 51:399–409

    Google Scholar 

  • Grun P, Aubertin M (1966) The inheritance and expression of unilateral incompatibility in Solanum. Heredity 21:131–138

    Google Scholar 

  • Grun P, Radlow A (1961) Evolution of barriers to crossing of self-incompatible with self-compatible species of Solanum. Heredity 16:137–143

    Google Scholar 

  • Hadley HH, Openshaw SJ (1980) Interspecific and intergeneric hybridization. In: Fehr WR, Hadley HH (eds) Hybridization of crop plants. Am Soc Agron Crop Sci Soc Am, Madison, Wis., pp 133–159

    Google Scholar 

  • Hanneman RE Jr (1994) Assignment of endosperm balance numbers to the tuber-bearing solanums and their close non-tuber-bearing relatives. Euphytica 74:19–25

    Google Scholar 

  • Hanneman RE Jr (1999) The reproductive biology of the potato and its implications for breeding. Potato Res 42:283–312

    Google Scholar 

  • Hanneman RE Jr, Peloquin SJ (1981) Genetic-cytoplasmic male sterility in progeny of 4x–2x crosses in cultivated potatoes. Theor Appl Genet 59:53–55

    Google Scholar 

  • Hawkes JG (1990) The potato-evolution, biodiversity and genetic resources. Belhaven Press, London

    Google Scholar 

  • Hawkes JG (1994) Origins of cultivated potatoes and species relationships. In: Bradshaw JE, Mackay GR (eds) Potato genetics. CAB International, Oxford, UK, pp 3–42

  • Hawkes JG, Jackson MT (1992) Taxonomic and evolutionary implications of the endosperm balance number hypothesis in potatoes. Theor Appl Genet 84:180–185

    Google Scholar 

  • Hermsen JG, Sawicka E (1979) Inconmpatibility and incongruity in tuber-bearing Solanum species. In: Hawkes JG, Lester RN, Skelding AD (eds) The biology and taxonomy of the Solanaceae. Academic, London, pp 435–444

    Google Scholar 

  • Hermunstad SA, Peloquin SJ (1985) Germplasm enhancement with potato haploids. J Hered 76:463–467

    Google Scholar 

  • Hijmans RJ, Spooner DM (2001) Geographic distribution of wild potato species. Am J Bot 88:2101–2112

    Google Scholar 

  • Hogenboom NG (1973) A model for incongruity in intimate partner relationships. Euphytica 22:219–233

    Google Scholar 

  • Hogenboom NG (1979) Incompatibility and incongruity in Lycopersicon. In: Hawkes JG, Lester RN, Skelding AD (eds) The biology and taxonomy of the Solanaceae. Academic Press, London, pp 435–444

    Google Scholar 

  • Hosaka K (2003) T-type chloroplast DNA in Solanum tuberosum L. spp. tuberosum was conferred from some populations of S. tarijense Hawkes. Am J Potato Res 80:21–23

    CAS  Google Scholar 

  • Hosaka K, Hanneman RE Jr (1998) Genetics of self-compatibility in a self-incompatible wild diploid potato species Solanum chacoense.2. Localization of an S locus inhibitor (Sli) gene on the potato genome using DNA markers. Euphytica 103:265–271

    Article  CAS  Google Scholar 

  • Huamán Z, Spooner DM (2002) Reclassification of landrace populations of cultivated potatoes (Solanum sect. Petota). Am J Bot 89: 947–965

    Google Scholar 

  • Ispizúa VN, Camadro EL, Clausen AM (1999) Pre-zygotic breeding barriers between the wild diploid potato species Solanum maglia and S. kurtzianum from Argentina. Gen Res Crop Evol 46:243–249

    Article  Google Scholar 

  • Iwanaga M, Ortiz R, Cipar MS, Peloquin SJ (1991) A restorer gene for genetic-cytoplasmic male sterility in cultivated potatoes. Am Potato J 68:19–28

    Google Scholar 

  • Johnston SA, Hanneman RE Jr (1980) Support of the endosperm balance number hypothesis utilizing some tuber-bearing Solanum species. Am Potato J 57:7–14

    Google Scholar 

  • Johnston SA, Hanneman RE Jr (1982) Manipulations of endosperm balance number overcome crossing barriers between diploid Solanum species. Science 217:446–448

    Google Scholar 

  • Johnston SA, Hanneman RE Jr (1996) Genetic control of endosperm balance number (EBN) in the Solanaceae based on trisomic and mutation analysis. Genome 39:314–321

    Google Scholar 

  • Johnston SA, Hanneman RE Jr (1999) The nature of the genetic control of Endosperm Balance Number based on aneuploid analysis in Datura. Sex Plant Reprod 12:71–75

    Article  Google Scholar 

  • Johnston SA, den Nijs TM, Peloquin SJ, Hanneman RE Jr (1980) The significance of genic balance to endosperm development in interspecific crosses. Theor Appl Genet 57:5–9

    Google Scholar 

  • Katsiosis A, Hanneman RE Jr, Forsberg RA (1995) Endosperm balance number and the polar-nuclei activation hypotheses for endosperm development in interspecific crosses of Solanaceae and Gramineae, respectively. Theor Appl Genet 91:848–855

    Google Scholar 

  • Kaul MLH (1988) Male sterility in higher plants. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Koopmans A (1959) Changes in sex in the flowers of the hybrid Solanum rybinii × S. chacoense. IV. Further data from the reciprocal cross S. chacoense × S. rybinii. Genetica 30:384–390

    CAS  PubMed  Google Scholar 

  • Lamm R (1941) Varying cytological behavior in reciprocal Solanum crosses. Hereditas 27:202–208

    Google Scholar 

  • Lamm R (1953) Investigations on some tuber-bearing Solanum hybrids. Hereditas 39:97–112

    Google Scholar 

  • Lester RN, Kang JH (1998) Embryo and endosperm function and failure in Solanum species and hybrids. Ann Bot 82:445–453

    Article  Google Scholar 

  • Lin BY (1975) Parental effects on gene expression in maize development. PhD thesis, University of Wisconsin, Madison

  • Lössl A, Adler N, Horn R, Frei U, Wenzel G (1999) Chondriome type characterization of potato: mt α, β, γ, δ, ε and novel plastid mitochondrial configurations in somatic hybrids. Theor Appl Genet 99:1–10

    Article  Google Scholar 

  • Marcellán ON, Camadro EL (1996) Self- and cross-incompatibility in Asparagus officinalis and A. densiflorus cv. Sprengeri. Can J Bot 74:1621–1625

    Google Scholar 

  • Masuelli RW, Camadro EL (1997) Crossability relationships among wild potato species with different ploidies and endosperm balance numbers (EBN). Euphytica 94:227–235

    Article  Google Scholar 

  • Matsubayashi M (1991) Phylogenetic relationships in the potato and its related species. In: Tsuchiya T, Gupta PK (eds) Chromosome engineering in plants: genetics, breeding, evolution, Part B. Elsevier, Amsterdam, pp 93–118

  • den Nijs TPM, Peloquin SJ (1977) 2n gametes in potato species and their function in sexual polyploidization. Euphytica 26:585–600

    Google Scholar 

  • Ochoa CM (1992) Determinations of chromosome number (2n) and endosperm balance number (EBN) in some little known tuber-bearing Solanum species. Phytologia 73:180–182

    Google Scholar 

  • Ortiz R (1998) Plant Breeding via ploidy manipulations. In: Janick J (ed) Plant breeding reviews, vol 16. Wiley, New York, pp 15–86

  • Ortiz R, Ehlenfeldt MK (1992) The importance of endosperm balance number in potato breeding and evolution of tuber-bearing Solanum species. Euphytica 60:105–113

    Google Scholar 

  • Parrott WA, Smith RR (1986) Evidence for the existence of endosperm balance number in the true clover (Trifolium spp.). Can J Genet Cytol 28:581–586

    Google Scholar 

  • Peloquin SJ, Boiteux L, Carputo D (1999) Meiotic mutants of the potato: valuable variants. Genetics 153:1493–1499

    CAS  PubMed  Google Scholar 

  • Raimondi JP, Camadro EL (2003) Crossability relationships between the common potato, Solanum tuberosum ssp. tuberosum, and its wild diploid relatives S. kurtzianum and S. ruiz-lealii. Gen Res Crop Evol 50:307–314

    Article  CAS  Google Scholar 

  • Raimondi JP, Sala RG, Camadro EL (2003) Crossing relations among the wild potato species Solanum kurtzianum, S. chacoense and S. ruiz-lealii from Argentina. Euphytica 132:287–295

    Article  Google Scholar 

  • Rivard SR, Cappadocia M, Landry BS (1996) A comparison of RFLP maps based on anther culture derived, selfed, and hybrid progenies of Solanum chacoense. Genome 39:611–621

    CAS  Google Scholar 

  • Ross RW, Peloquin SJ, Hougas W (1964) Fertility of hybrids from Solanum phureja and haploid S. tuberosum matings. Eur Potato J 7:81–89

    Google Scholar 

  • Sala CA (1993) Incompatibilidad cruzada entre cinco especies tuberosas de Solanum Solanaceae). Darwiniana 32:15–25

    Google Scholar 

  • Santini M, Camadro EL, Marcellán ON, Erazzú LE (2000) Agronomic characterization of diploid hybrid families derived from crosses between haploids of the common potato and three wild Argentinean tuber-bearing species. Am J Potato Res 77:211–218

    Google Scholar 

  • Scotti N, Monti L, Cardi T (2003) Organelle DNA variation in parental Solanum spp. genotypes and nuclear-cytoplasmic interactions in Solanum tuberosum (+) S. commersonii somatic hybrid-backcross progeny. Theor Appl Genet 108:87–97

    Article  CAS  PubMed  Google Scholar 

  • Simpson GG (1961) Principles of animal taxonomy. Columbia University Press, New York

    Google Scholar 

  • Singh AK, Salamini F, Uhrigh H (1989) Chromosome pairing in 14 F1 hybrids among 11 diploid potato species. J Gen Breed 43:1–6

    CAS  Google Scholar 

  • Spooner DM, Van den Berg RG (1992) An analysis of recent taxonomic concepts in wild potatoes (Solanum sect. Petota). Gen Res Crop Evol 39:23–27

    Google Scholar 

  • Spooner DM, Van den Berg RG, Rodríguez A, Bamberg J, Hijmans RJ, Lara-Cabrera SI (2004) Wild potatoes (Solanum sect. Petota) of North and Central America. Syst Bot Monogr 68 (in press)

  • Stebbins L (1950) Variation and evolution in plants. Columbia University Press, New York

    Google Scholar 

  • Stone LS, Göring DR (2001) The molecular biology of self-incompatibility systems in flowering plants. Plant Cell Tissue Organ Cult 67:93–114

    Article  CAS  Google Scholar 

  • Summers D, Grun P (1981) Reproduction isolation barriers to gene exchange between Solanum chacoense and Solanum commersonii (Solanaceae). Am J Bot 68:1240–1248

    Google Scholar 

  • Thompson RD, Kirch H-H (1992) The S-locus of flowering plants: when self-rejection is self interest. Trends Genet 8:381–387

    CAS  PubMed  Google Scholar 

  • Tucci M, Carputo D, Bile G, Frusciante L (1996) Male fertility and freezing tolerance of hybrids involving Solanum tuberosum haploids and diploid Solanum species. Potato Res 39:345–353

    Google Scholar 

  • Ugent D (1966) Hybrid weed complexes in Solanum section Tuberarium. PhD thesis, University of Wisconsin, Madison

  • Valentine DH (1956) Studies in British primulas. V. The inheritance of seed compatibility. New Phytol 55:305–318

    Google Scholar 

  • Williams EG, Knox RB, Rouse JL (1982) Pollination subsystems distinguished by pollen arrest after incompatible interspecific crosses in Rhododendron (Ericaceae). J Cell Sci 53:255–277

    Google Scholar 

  • Zhang E, Palmer RG (1990) The ms mutation in soybean: involvement of gametes in crosses with tetraploid soybeans. Theor Appl Genet 80:172–176

    Google Scholar 

Download references

Acknowledgements

This is contribution No. 76 from DISSPA. E.L.C had a leave of absence from INTA and UNMdP.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. Carputo.

Additional information

Communicated by G. Wenzel

Rights and permissions

Reprints and permissions

About this article

Cite this article

Camadro, E.L., Carputo, D. & Peloquin, S.J. Substitutes for genome differentiation in tuber-bearing Solanum: interspecific pollen-pistil incompatibility, nuclear-cytoplasmic male sterility, and endosperm. Theor Appl Genet 109, 1369–1376 (2004). https://doi.org/10.1007/s00122-004-1753-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-004-1753-2

Keywords

Navigation