Challenges and prospects of endosperm balance number in potato (Solanum tuberosum) improvement

JAI GOPAL

doi:10.56093/ijas.v84i9.43407

Authors

JAI GOPAL Directorate of Onion and Garlic Research, Rajgurunagar, Pune, Maharashtra 410 505

https://doi.org/10.56093/ijas.v84i9.43407

Keywords:

2n gametes, Interspecific crosses, Ploidy manipulation, Potatoes, Seed development, Solanum species and Speciation

Abstract

Endosperm Balance Number (EBN) is a genome-specific ploidy, which is not necessarily equivalent to the chromosome ploidy. The EBN is the ‘effective ploidy’ that determines crossability in Solanum species. It varies from 1 to 4 and the two Solanum species are crossable if they have the same EBN so that maternal to paternal ratio of EBN in the endosperm is 2:1. However, a number of significant exceptions to this rule have been observed in potato (Solanum tuberosum L.). EBNs have been experimentally assigned to a number of Solanum species after crosses with standard species whose EBN was arbitrarily established. Neither specific genes nor the molecular basis of EBN have been established in potato, but 2-3 unlinked loci with equal additive effects are known to determine the EBN in Solanum species. EBN acts as a powerful isolating mechanism in the sexual reproduction of Solanum species. EBN incompatibility played an important role in the speciation of polyploids from diploids, complementing the role of 2n gametes in the polyploidy evolution of potato species. EBN has great predictive value for planning interpsecific crosses in potato. EBN of a species can be modified through sexual or somatic polyploidization. This has facilitated the transfer of useful disease and pest resistance genes from 1 EBN and 2EBN wild species to 4EBN cultivated potatoes. Besides direct, indirect gene transfer through bridge species from otherwise incompatible Solanum species has been accomplished for improving cultivated potatoes. The concept, inheritance and role of EBN in speciation, and its prospects in potato varietal improvement are reviewed in this paper. The problems associated in transfer of useful traits from wild species to cultivated potatoes due to EBN barriers are also highlighted.

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References

Adiwilaga K D and Brown C R. 1991. Use of 2n pollen-producing triploid hybrids to introduce tetraploid Mexican wild species germplasm to cultivated tetraploid potato gene pool. Theoretical and Applied Genetics 81: 645–62. DOI: https://doi.org/10.1007/BF00226732

Amaya A and Matsubayashi M. 1981. Effects of chromosome doubling and a chemical immunosuppressant on crossability between Solanum and its related diploid species. Science Report Faculty of Agriculture, Kobe University 14: 253–63.

Bamberg J B. 1994. Allelism of endosperm balance number (EBN) in Solanum acaule Bitt. and other wild potato species. Theoretical and Applied Genetics 89: 682–6. DOI: https://doi.org/10.1007/BF00223705

Bamberg J B and Hanneman R E Jr. 1990. Allelism of endosperm balance number (EBN) in Mexican tuber-bearing Solanum species. Theoretical and Applied Genetics 80: 161–6. DOI: https://doi.org/10.1007/BF00224380

Bamberg J B, Hanneman Jr. R E, Palta J P and Harbage J F. 1994. Using disomic 4x (2EBN) potato species germplasm via bridge species Solanum commersonii. Genome 37: 866–70. DOI: https://doi.org/10.1139/g94-122

Boyes J W and Thompson W P. 1937. The development of the endosperm and embryo in reciprocal crosses in cereals. Journal of Genetics 34: 203–27. DOI: https://doi.org/10.1007/BF02982263

Brink R A and Cooper D C. 1947. The endosperm in seed development. Botanical Review 132: 423–541. DOI: https://doi.org/10.1007/BF02861549

Brown C R. 1988. Characteristics of 2n pollen producing triploid hybrids between Solanum stoloniferrum and cultivated diploid potatoes. American Potato Journal 65: 75–84. DOI: https://doi.org/10.1007/BF02867455

Brown C R and Adiwilaga K D. 1990. Introgression of Solanum acaule germplasm from the endosperm balance number 2 gene pool into the cultivated endosperm balance number 4 potato gene pool via triplandroids. Genome 33: 273–8. DOI: https://doi.org/10.1139/g90-042

Cai X K, Spooner D M and Jansky S H. 2011. A test of taxonomic and biogeographic predictivity: resistance to potato virus Y in wild relatives of the cultivated potato. Phytopathology 101: 1 074–80. DOI: https://doi.org/10.1094/PHYTO-02-11-0060

Camadro E L and Espinillo J C. 1990. Germplasm transfer from the wild tetraploid species Solanum acaule Bitt. to the cultivated potato S. tuberosum L. using 2n eggs. American Potato Journal 67: 737–49. DOI: https://doi.org/10.1007/BF03044524

Camadro E L and Masuelli R W. 1995. A genetic model for the endosperm balance number (EBN) in the wild potato Solanum acaule Bitt. and two related diploid species. Sexual Plant Reproduction 8: 283–8. DOI: https://doi.org/10.1007/BF00229385

Camadro E L, Erazzu L E, Maune J F and Bedogni M C. 2012. A genetic approach to the species problem in wild potato. Plant Biology 14: 543–54. DOI: https://doi.org/10.1111/j.1438-8677.2012.00563.x

Carputo D, Cardi L, Frusciante L and Peloquin S J. 1995. Male fertility and cytology of triploid hybrids between frost tolerant Solanum commersonii (2n = 4x = 48, 2EBN) and Phureja- Tuberosum haploid hybrids (2n = 2x = 24, 2EBN). Euphytica 83: 123–9. DOI: https://doi.org/10.1007/BF01678039

Carputo D, Barone A, Cardi T, Sebastiano A and Frusciante L. 1997. Endosperm balance number manipulation for direct in vivo germplasm introgression to potato from a sexually isolated relative (Solanum commersonii Dun.) Proceedings of National Academy of Sciences, USA 94: 12 013–7. DOI: https://doi.org/10.1073/pnas.94.22.12013

Carroll C P. 1975. The inheritance and expression of sterility in hybrids of dihaploid and cultivated diploid potatoes. Genetics 45: 149–62. DOI: https://doi.org/10.1007/BF01517192

Chavez R, Brown C R and Iwanaga M. 1988. Application of interspecific sesquiploidy to introgression of PLRV resistance from non-tuber-bearing Solanum etuberosum to cultivated potato germplasm. Theoretical and Applied Genetics 76: 497– 500. DOI: https://doi.org/10.1007/BF00260898

Clugston D B. 1988. ‘Embryo culture and protoplast fusion for the introduction of Mexican wild species germplasm into the cultivated potato’. Ph D Thesis, University of Birmingham, UK.

Cornejo P, Camadro E L and Masuelli R W. 2012. Molecular bases of the postzygotic barriers in interpsecific crosses between the wild potato species Solanum acaule and S. commersonii. Genome 55: 605–14. DOI: https://doi.org/10.1139/g2012-047

den Nijs T P M and Peloquin S J. 1977. 2n gametes in potato species and their function in sexual polyploidization. Euphytica 26: 585–600. DOI: https://doi.org/10.1007/BF00021684

Dionne L A. 1963. Studies on the use of Solanum acaule as a bridge between Solanum tuberosum and species in the series Bulbocastana, Cardiophylla, and Pinnatisecta. Euphytica 12: 263–9. DOI: https://doi.org/10.1007/BF00027461

Ehlenfeldt M K and Hanneman R E Jr. 1988a. Genetic control of endosperm balance number (EBN): three additive loci in a threshold-like system. Theoretical and Applied Genetics 68: 155–61. DOI: https://doi.org/10.1007/BF00258041

Ehlenfeldt M K and Hanneman R E Jr. 1988b. The transfer of synaptic gene (sy-2) from 1EBN Solanum commersonii Dun. to 2EBN germplasm. Euphytica 37: 181–7. DOI: https://doi.org/10.1007/BF00036856

Ehlenfeldt M K and Ortiz R. 1995. Evidence on the nature and origins of endosperm dosage requirements in Solanum and other angiosperm genera. Sexual Plant Reproduction 8: 189– 96. DOI: https://doi.org/10.1007/BF00228936

Gopal J and Khurana SM Paul. 2006. Handbook of Potato Production, Improvement and Post Harvest Management, p 605. Food Product Press, New York, London, Oxford. DOI: https://doi.org/10.1201/9780429246623

Hanneman R E Jr. 1994. Assignment of endosperm balance numbers to the tuber-bearing Solanums and their close non- tuber-bearing relatives. Euphytica 74: 19–25. DOI: https://doi.org/10.1007/BF00033762

Hanneman R E Jr. and Bamberg J B. 1986. Inventory of tuber- bearing Solanum species. Univ Wisconsin Research Bulletin 533.

Hanneman R E Jr. and Peloquin S J. 1968. Ploidy levels of progeny from diploid-tetraploid crosses in the potato. American Potato Journal 45: 255–61. DOI: https://doi.org/10.1007/BF02849919

Hawkes J G. 1990. The potato – Evolution, Biodiversity and Genetic Resources. Belhaven Press, London.

Hawkes J G and Jackson M T. 1992. Taxonomic and evolutionary implications of the endosperm balance number hypothesis in potatoes. Theoretical and Applied Genetics 84: 180–5. DOI: https://doi.org/10.1007/BF00223998

Hayes R J and Thill C A. 2002. Introgression of cold (4 C) chipping from 2x (2 endosperm balance number) potato species into 4x (4EBN) cultivated potato using sexual polyploidization. American Journal of Potato Research 79: 421–31. DOI: https://doi.org/10.1007/BF02871687

Hayes R J, Dinu I I and Thill C A. 2005. Unilateral and bilateral hybridization barriers in inter-series crosses of 4x 2EBN Solanum stoloniferum, S. pinnatisectum, S. cardiophyllum, and 2x 2EBN S. tuberosum haploids and haploid-species hybrids. Sexual Plant Reproduction 17: 303–11. DOI: https://doi.org/10.1007/s00497-005-0244-1

Hermsen J G Th. 1987. Efficient utilization of wild and primitive species in potato breeding. The Production of New Potato Varieties: Technological Advances, pp 172–85. DOI: https://doi.org/10.1017/CBO9780511895463.040

Jellis G J and Richardson D E (Eds). Cambridge University Press, England Hermsen J G Th and Taylor L M. 1979. Successful hybridization of non-tuberous Solanum tuberosum Lind.and tuber-bearing S. pinnatisectum Dun. Euphytica 28: 1–7. DOI: https://doi.org/10.1007/BF00029166

Hermundstad S A and Peloquin S J. 1985. Germplasm enhancement with potato hybrids. Journal of Heredity 76: 463–7. DOI: https://doi.org/10.1093/oxfordjournals.jhered.a110146

Hermundstad S A and Peloquin S J. 1986. Tuber yield and tuber traits of haploid-wild species hybrids. Potato Research 29: 289–97. DOI: https://doi.org/10.1007/BF02359958

Irikura Y. 1968. Studies on interspecific crosses of tuber-bearing Solanums. 1. Overcoming cross-incompatibility between Solanum tuberosum and other Solanum species by means of induced polyploids and haploids. Hokkaido National Agricultural Experimental Station Research Bulletin 92: 21–37.

Jackson M T, Rowe P R and Hawkes J G. 1978. Crossability relationships of Andean potato varieties of three ploidy levels. Euphytica 27: 541–55. DOI: https://doi.org/10.1007/BF00043180

Jansky S. 2006. Overcoming hybridization barriers in potato. Plant Breeding 1125: 1–12. DOI: https://doi.org/10.1111/j.1439-0523.2006.01178.x

Jansky S and Hamernik A. 2009. The introgression of 2x 1EBN Solanum species into the cultivated potato using Solanum verrucossum as a bridge. Genetic Resources and Crop Evolution 56: 1 107–15. DOI: https://doi.org/10.1007/s10722-009-9433-3

Jansky S H, Simon R and Spooner D M. 2009. A test of taxonomic predictivity: resistance to the Colorado potato beetle in wild relatives of cultivated potato. Journal of Economic Entomology 102: 422–31. DOI: https://doi.org/10.1603/029.102.0155

Janssen G J W, van Norel A, Verkerk-Bakker B, Janssen R and Hoogendoorn J. 1997. Introgression of resistance to root-knot nematodes from wild Central American Solanum species into S. tuberosum ssp. tuberosum.Theoretical and Applied Genetics 95: 490–6. DOI: https://doi.org/10.1007/s001220050588

Johnston S A and Hanneman R E Jr. 1980. Support of the endosperm balance number hypothesis utilizing some tuber-bearing Solanum species. American Potato Journal 57: 7–14. DOI: https://doi.org/10.1007/BF02852750

Johnston S A and Hanneman R E Jr. 1982. Manipulation of endosperm balance number to overcome crossing barriers between diploid Solanum species. Science 217: 446–8. DOI: https://doi.org/10.1126/science.217.4558.446

Johnston S A and Hanneman R E Jr. 1995. The genetics of triploid formation and its relationship to endosperm balance number in potato. Genome 38: 60–7. DOI: https://doi.org/10.1139/g95-007

Johnston S A and Hanneman R E Jr. 1996. Genetic control of endosperm balance number (EBN) in the Solanaceae based on trisomic and mutation analysis. Genome 39: 314–21. DOI: https://doi.org/10.1139/g96-042

Johnston S A, den Nijs A P M, Peloquin S J and Hanneman R E Jr. 1980. The significance of genetic balance to endosperm development in interspecific crosses. Theoretical and Applied Genetics 57: 5–9. DOI: https://doi.org/10.1007/BF00276002

Kameraj A Ya, Vavilova M A, Zhitlova N A and Ivanova V N. 1978. Interspecific hybridization of the potato involving wild species of the series Acaulia Juz. Bulletin of Applied Botany, Genetics and Breeding 62: 115–38.

Lamm R. 1953. Investigations on some tuber-bearing Solanum hybrids. Hereditas 39: 97–112. DOI: https://doi.org/10.1111/j.1601-5223.1953.tb03404.x

Lee H and Cooper D C. 1958. Seed development following hybridization between diploid Solanum species from Mexico, Central and South America. American Journal of Botany 45: 104–10. DOI: https://doi.org/10.1002/j.1537-2197.1958.tb13117.x

Louwes K M, Hockestra R and Matthejj W M. 1992. Interspecific hybridization between the cultivated potato Solanum tuberosum sub-species tuberosum L. and the wild species S. circaeifolium subsp. circaeifolium Bitter exhibiting resistance to Phytophtora infestans (Mont.) de Bary and Globodera pallida (Stone) Behrens. 2. Sexual hybrids. Theoretical and Applied Genetics 84: 362–70. DOI: https://doi.org/10.1007/BF00229495

Marks G E. 1966. The enigma of triploid potatoes. Euphytica 15: 285–90. DOI: https://doi.org/10.1007/BF00022170

Masuelli R W and Camadro E L. 1997. Crossability relationships among wild potato species with different ploidies and endosperm balance numbers (EBN). Euphytica 94: 227–35.

Masuelli R W, Camadro E L, Mendiburu A O. 1992. 2n gametes in Solanum commersonii and cytological mechanisms of triplandroid formation in triploid hybrids of Solanum commersonii × Solanum gourlayi. Genome 35: 864–69. DOI: https://doi.org/10.1139/g92-131

Matsubayashi M. 1982. Species differentiation in Solanum, Sect Petota. XI. Genomic relationships between S. acaule and certain diploid Commersoniana species. Science Report Faculty of Agriculture, Kobe University 15: 23–33.

McHale N A and Lauer F I. 1981. Inheritance of tuber traits from Phureja in diploid Phureja-Tuberosum hybrids. American Potato Journal 58: 93–102. DOI: https://doi.org/10.1007/BF02854378

Novy R G and Hanneman Jr. R E. 1991. Hybridization between GP. Tuberosum haploids and 1EBN wild potato species. American Potato Journal 68: 151–69. DOI: https://doi.org/10.1007/BF02853896

Ochoa C M. 1992. Determinations of chromosome number (2n) and endosperm balance number (EBN) in some little known tuber-bearing Solanum species. Phytologia 73: 180-82. DOI: https://doi.org/10.5962/bhl.part.4134

Panahandeh J, Valizadeh M, Khosroshahly M, Yermishin A P, Khoei F R and Mahna N. 2008. Microsporogenesis and crossing behavior of a tetraploid, interspecific inter-EBN hybrid potato. Scientia Horticulturae 116: 348–353. DOI: https://doi.org/10.1016/j.scienta.2008.02.006

Peloquin S J and Ortiz R. 1992. Techniques for introgressing unadapted germplasm to breeding population Plant Breeding in the 1990s, pp 485–507. Stalker H T and Murphy J P (Eds). CAB International, Wallingford, UK.

Peloquin S J, Yerk G L, Werner J E and Darmo E. 1989. Potato breeding with haploids and 2n gametes. Genome 31: 1 000–4. DOI: https://doi.org/10.1139/g89-174

Raimondi J P and Camadro E L. 2003. Crossability relationships between the common potato, Solanum tuberosum spp. tuberosum and its wild diploid relatives S. kurtzianum and S. ruiz-lealii. Genetic Resources and Crop Evolution 50: 307–14.

Ramanna M S and Abdalla M M F. 1970. Fertility, late blight resistance, and genome relationship in an interspecific hybrid, Solanum polytrichon Rydb. × Solanum phureja Juz et. Buk. Euphytica 19: 317–26. DOI: https://doi.org/10.1007/BF01904209

Ross R W, Peloquin S J and Hougas R W. 1964. Fertility of hybrids from Solanum phureja and haploid S. tuberosum matings. European Potato Journal 7: 81–9. DOI: https://doi.org/10.1007/BF02414417

Rousselle-Bourgeois F and Rousselle P. 1992. Creation et selection de populations diploid de pomme de terre (Solanum tuberosum L.) Agronomie 12: 59–67. DOI: https://doi.org/10.1051/agro:19920105

Sanetomo R, Ono S and Hosaka K. 2011. Characterization of crossability in the crosses between S. demissum and S. tuberosum and the F1 and BC1 progenies. American Journal of Potato Research 88: 500–10. DOI: https://doi.org/10.1007/s12230-011-9217-0

Serquen F C and Peloquin S J. 1996. Variation for agronomic and processing traits in Solanum tuberosum haploids x wild species hybrids. Euphytica 89: 185–91. DOI: https://doi.org/10.1007/BF00034604

Scotti N, Cozzolino S and Cardi T. 2007. Mitochondrial DNA variation in cultivated and wild potato species (Solanum spp.) Genome 50: 706–13. DOI: https://doi.org/10.1139/G07-042

Sliwka J, Jakuczun H, Chmielarz M, Hara-Skrzypiec A, Tomczynska I, Killan A and Zimnoch-Guzowska E. 2012. A resistance gene against potato late blight originating from Solanum x michoacanum maps to potato chromosome VII. Theoretical and Applied Genetics 124: 397–406. DOI: https://doi.org/10.1007/s00122-011-1715-4

Spooner D M and Salas A. 2006. Structure, biosystematics and genetic resources. (In) Handbook of Potato Production, Improvement and Postharvest Management, pp 1–39. Gopal J and Khurana S M Paul (Eds). Food Product Press, New York, London, Oxford.

Swaminathan M S. 1951. Notes on induced polyploids in the tuber-baring Solanum species and their crossability with S. tuberosum. American Potato Journal 28: 472–89. DOI: https://doi.org/10.1007/BF02854980

Tarn T R and Hawkes J G. 1986. Cytogenetic studies and the occurrence of triploidy in the wild potato species Solanum commersonni Dun. Euphytica 35: 293–302. DOI: https://doi.org/10.1007/BF00028567

Tucci M, Carputo D, Bile G and Frusciante L. 1996. Male fertility and freezing tolerance of hybrids involving Solanum tuberosum haploids and diploid Solanum species. Potato Research 39: 345–53. DOI: https://doi.org/10.1007/BF02357938

Valentine D H. 1956. Studies in British primulas. V. The inheritance of seed compatibility. New Phytologist 55: 305–18. DOI: https://doi.org/10.1111/j.1469-8137.1956.tb05290.x

Wangenheim KH von. 1955. Zur Ursache der Kreuzungssch wierigkeiten zwischen Solanum tuberosum L und S. acaule Bitt. Bzw. S. stoloniferum Schlechtd. Et Bouche. Zeitschrift ferPflanzenzuchtung 34: 7–48.

Wangenheim KH von, Peloquin S J, Hougas R W. 1960. Embryological investigations on the formation of haploids in the potato (S. tuberosum). Zournal Vererbungsl 91: 391–9. DOI: https://doi.org/10.1007/BF00888395

Wang Mi Qia, Allefs S, Berg R G van-den, Vleeshouwers V G A A, Vossen E A G van-der and Vosman B. 2008. Allele mining in Solanum: conserved homologues of Rpi-blbl are identified in Solanum stoloniferum. Theoretical and Applied Genetics 116: 933–43. DOI: https://doi.org/10.1007/s00122-008-0725-3

Watanabe K, Arbizu C and Schmiediche P E. 1992. Potato germplasm enhancement with disomic tetraploid Solanum acuale.I. Efficiency of introgression. Genome 35: 53–7. DOI: https://doi.org/10.1139/g92-009

Watanabe K N, Orrillo M, Vega S, Iwagana M, Ortiz R, Freyre R, Yerk G, Peloquin S J and Ishiki K. 1995. Selection of diploid potato clones from diploid (haploid x wild species) F1 hybrid families for short day conditions. Breeding Science 45: 341–7. DOI: https://doi.org/10.1270/jsbbs1951.45.341

Yerk G L and Peloquin S J. 1989. Evaluation of tuber traits of 10 2x (2EBN) wild species through haploid x wild species hybrids. American Potato Journal 66: 731–9. DOI: https://doi.org/10.1007/BF02896829