Abstract
Both interspecific and intraspecific mechanisms restrict the exchange of genes between plants. Much research has focused on self incompatibility (SI), an intraspecific barrier, but research on interspecific barriers lags behind. We are using crosses betweenLycopersicon esculentum andL. pennellii as a model with which to study interspecific crossing barriers. The crossL. esculentum×L. pennellii is successful, but the reciprocal cross fails. Since the cross can be successfully made in one direction but not the other, gross genomic imbalance or chromosomal abnormality are precluded as causes. We showed that the lack of seed set observed in the crossL. pennellii×L. esculentum is due to the inability of pollen tubes to grow more than 2–3 mm into the style, whereas S1 crosses show continued slow pollen tube growth but, also, fail to set seed. These results indicate that the unilateral response is a barrier distinct from SI, differing from SI in the timing and location of expression in the style. We therefore suggest that this unilateral response in theL. pennellii×L. esculentum cross is more accurately referred to as “unilateral incongruity” (UI) rather than interspecific incompatibility. Periclinal chimeras were used to determine the tissues involved in UI. The results of crosses with the available chimeras indicate that the female parent must beL. pennellii at either LI (layer 1) or both LI and LII (layer 2) and the male parent must beL. esculentum at either LII or both LI and LII to observe UI similar to that seen in theL. pennellii×L. esculentum cross. Pollinations with a mixture of pollen fromL. pennellii and from transgenicL. esculentum plants harboring a pollen-specific GUS reporter gene marker were used to ascertain whether the growth of the pollen tubes of either species was modified as a possible means of overcoming UI. We found no evidence of communication between the two types of pollen tubes to either enhance or restrict all pollen tube growth.
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References
Abdalla MMF, Hermsen JGT (1972) Unilateral incompatibility: hypotheses, debate and its implications for plant breeding. Euphytica 21:32–47
Ascher PD (1976) Self-incompatibility systems in floriculture crops. Acta Hortic 63:205–215
Ascher PD (1984) Self-incompatibility. In: Sink KC (ed) Petunia. Springer, Berlin Heidelberg New York, pp 92–110
Ascher PD (1986) Incompatibility and incongruity: two mechanisms preventing gene transfer between taxa. In: Linskens HF, Heslop-Harrison J (eds) Cellular interactions. Springer, Berlin Heidelberg New York, pp 251–256
Boodley JW, Sheldrake JJ (1982) Cornell peat-like mixes for commercial plant growing. Information Bulletin no. 43. Cornell Cooperative Extension, Cornell University, Ithaca, NY
Chetelat RT, DeVerna JW (1991) Expression of unilateral incompatibility in pollen ofLycopersicon pennellii is determined by major loci on chromosomes 1, 6 and 10. Theor Appl Genet 82:704–712
Cresti M, Ciampolini F, Sarfatti G (1980) Ultrastructural investigations onLycopersicon peruvianum pollen activation and pollen tube organization after self- and cross-pollination. Planta 150:211–217
East EM, Mangelsdorf AJ (1925) A new interpretation of the heredity behaviour of self-sterile plants. Proc Natl Acad Sci USA 11:166–171
Gifford EM Jr, Corson GE Jr (1971) The shoot apex in seed plants. Bot Rev 37:143–229
Grant V (1994) Modes and origins of mechanical and ethological isolation in angiosperms. Proc Natl Acad Sci USA 91:3–10
Hardon JJ (1967) Unilateral incompatibility betweenSolanum pennellii andLycopersicon escutentum. Genetics 57:795–808
Herrero M, Dickinson HG (1980) Pollen tube growth following compatible and incompatible interspecific pollinations inPetunia hybrida. Planta 148:217–221
Herrero M, Dickinson HG (1981) Pollen tube development inPetunia hybrida following compatible and incompatible intraspecific matings. J Cell Sci 47:365–383
Hogenboom NG (1972) Breaking breeding barriers inLycopersicon. 1. The genusLycopersicon, its breeding barriers and the importance of breaking these barriers. Euphytica 21:221–227
Hogenboom NG (1973) A model for incongruity in intimate partner relationships. Euphytica 22:219–233
Hogenboom NG (1975) Incompatibility and incongruity: two different mechanisms for the non-functioning of intimate partner relationships. Proc R Soc Lond Ser B 188:361–375
Hogenboom NG (1979) Incompatibility and incongruity inLycopersicon. In: Hawkes JG, Lester RN, Skelding AD (eds) Biology and taxonomy of the Solanaceae. Academic Press, London, pp 435–444
Hogenboom NG (1984) Incongruity: non-functioning of intercelluar and intracellular partner relationships through nonmatching information. In: Linskens HE, Heslop-Harrison J (eds) Cellular interactions. Springer, Berlin Heidelberg New York, pp 641–654
Kho YO, Baer J (1968) Observing pollen tubes by means of fluorescence. Euphytica 17:298–303
Kirk ITO, Tilney-Bassett, RAE (1978) The plastids: their chemistry, structure, growth and inheritance, 2nd edn. Elsevier/North Holland, Amsterdam
Knox RB, Williams EG, Dumas C (1986) Pollen, pistil, and reproductive function in crop plants. Plant Breed Rev 4:9–79
Kostoff D (1930) Ontogeny, genetics and cytology ofNicotiana hybrids. Genetica 12:33–139
Kuboyama T, Chung CS, Takeda G (1994) The diversity of interspecific pollen-pistil incongruity inNicotiana. Sex Plant Reprod 7:250–258
Lamm R (1950) Self-incompatibility inLycopersicon peruvianum Mill. Hereditas 36:509–511
Lewis D, Crowe LK (1958) Unilateral interspecific incompatibility in flowering plants. Heredity 12:233–256
Liedl BE, Anderson NO (1993) Reproductive barriers: identification, uses, and circumvention. Plant Breed Rev 11:11–154
Liedl BE, McCormick S, Mutschler MA (1993) A clearing technique for histochemical localization of GUS activity in pollen tubes and ovules ofLycopersicon. Plant Mol Biol Rep 11:194–201
Linskens HE, Esser KL (1957) Über eine spezifische Anfärbung der Pollenschläuche im Griffel und die Zahl der Kallosepfropfen nach Selbstung und Fremdung. Naturwissenschaften 44:16
Marcotrigiano M, Bernatzky R (1995) Arrangement of cell layers in the shoot apical meristems of periclinal chimeras influences cell fate. Plant J 7:193–202
Martin FW (1961) The inheritance of self-incompatibility in hybrids ofLycopersicon esculentum Mill.×L. chilense Dun. Genetics 46:1443–1454
Martin FW (1964) The inheritance of unilateral incompatibility inLycopersicon hirsutum. Genetics 50:459–469
McGuire DC, Rick CM (1954) Self-incompatibility in species ofLycopersicon sect. eriopersicon and hybrids withL. esculentum. Hilgardia 23:101–124
Mulcahy GB, Mulcahy DL (1983) A comparison of pollen tube growth in bi- and trinucleate pollen. In: Mulcahy DL, Ottaviano E (eds) Pollen: biology and implications for plant breeding. Elsevier Biomedical, New York, pp 29–33
Mulcahy DL, Mulcahy GB (1988) Tests of the heterosis model. Sex Plant Reprod 1:32–35
Mutschler MA, Cobb E (1985) Crosses ofLycopersicon pennellii andL. esculentum usingL. pennellii as the female parent. Rep Tomato Genet Coop 35:14
Mutschler MA, Liedl BE (1994) Interspecific crossing barriers inLycopersicon and their relationship to self-incompatibility. In: Williams EG, Clarke AE, Knox RB (eds Genetic control of self-incompatibility and reproductive development in flowering plants. Kluwer, Dordrecht, pp 164–188
Mutschler MA, Steffens JC, Tingey W (1993) Broad based insect resistance fromL. pennellii: its nature and potential for pest control in tomato. In: Yoder JI (ed) Molecular biology of tomato: fundamental advances and crop improvement. Technomic, Lancaster, Pa, pp 285–290
Nettancourt D de (1977) Incompatibility in angiosperms. Springer, Berlin Heidelberg New York
Nettancourt D de, Devreux M, Laneri U, Pacini E, Cresti M, Sarfatti G (1973) Ultrastructural aspects of unilateral interspecific incompatibility betweenLycopersicon peruvianum andL. esculentum. Caryologia 25:207–217
Nettancourt D de, Devereux M, Laneri U, Cresti M, Pacini E, Sarfatti G (1974) Genetical and ultrastructural aspects of self and cross incompatibility in interspecific hybrids between self-compatibleLycopersicon esculentum and self-incompatibleL. peruvianum. Theor Appl Genet 44:278–288
Newbigin E, Anderson MA, Clarke AE (1993) Gametophytic self-incompatibility systems. Plant Cell 5:1315–1324
Pattee HE, Stalker HT, Giesbrecht FG (1991) Comparative peg ovary and ovule ontogeny of selected cultivated and wild-typeArachis species. Bot Gaz 152:64–71
Preuss D (1994) Cell-cell interactions and the selection of plant mating partners. In: Kao T, Stephenson A (eds) Pollen-pistil interactions and pollen tube growth. American Society of Plant Physiologists, Rockville, Md, pp 77–93
Rick CM (1969) Controlled introgression of chromosomes ofSolanum pennellii intoLycopersicon esculentum: segregation and recombination. Genetics 62:753–768
Rick CM (1979) Biosystematic studies inLycopersicon and closely related species ofSolanum. In: Hawkes JG, Lester RN, Skelding AD (eds) The biology and taxonomy of the solanaceae. Academic Press, London, pp 667–677
Rivers BA, Bernatzky R (1994) Protein expression of a self-compatible allele fromLycopersicon peruvianum: introgression and behavior in a self-incompatible background. Sex Plant Reprod 7:357–362
Satina S, Blakeslee AF (1941) Periclinal chimeras inDatura stramonium in relation to development of leaf and flower. Am J Bot 28:862–871
Schlösser K (1961) Cytologische and cytochemische Untersuchungen über das Pollenschlauchwachstum selbststerilerPetunia. Z Bot 49:266–288
Sharma HC (1995) How wide can a wide cross be? Euphytica 82:43–64
Stalker HT (1980) Utilization of wild species for crop improvement. Adv Agron 33:111–147
Straub J (1946) Zur Entwicklungsphysiologie der Selbststerilität beiPetunia. Z Naturforsch 1:287–291
Stettler RF, Ager AA (1986) Mentor effects in pollen interactions. In: Linskens HF (ed) Encylopedia of plant physiology, vol 17. Springer, Berlin Heidelberg New York, pp 609–623
Stout AB (1952) Reproduction inPetunia. Mem Torrey Bot Club 20:1–202
Szymkowiak EJ, Sussex IM (1992) The internal meristem layer (L3) determines floral meristem size and carpel number in tomato periclinal chimeras. Plant Cell 4:1089–1100
Tanksley SD, Loaiza-Figueroa F (1985) Gametophytic self-incompatibility is controlled by a single major locus on chromosome 1 inLycopersicon peruvianum. Proc Natl Acad Sci USA 82:5093–5096
Taylor IB (1986) Biosystematics of the tomato. In: Atherton JG, Rudich J (eds) The tomato crop: a scientific basis for improvement. Chapman and Hall, London, pp 1–34
Tilney-Bassett RAE (1986) Plant chimeras. Edward Arnold, London
Trognitz BR, Schmiediche PE (1993) A new look at incompatibility relationships in higher plants. Sex Plant Reprod 6:183–190
Twell D, Yamaguchi J, McCormick S (1990) Pollen-specific gene expression in transgenic plants: coordinate regulation of two different tomato gene promoters during microsporogenesis. Development 109:705–713
Van Tuyl JM, Marcucci MC, Visser T (1982) Pollen and pollination experiments. VII. The effect of pollen treatment and application method on incompatibility and incongruity inLilium. Euphytica 31:613–619
Webb MC, Williams EG (1988) Effects of temperature, light, nutrients and carbon dioxide on the strength of the self-incompatibility response in detached flowers ofLycopersicon peruvianum. Ann Bot 61:395–404
Williams EG, Knox RB (1982) Quantitative analysis of pollen tube growth inLycopersicon peruvianum. J Palynol 18:65–74
Yasuda S (1934) Physiological research on self-incompatibility inPetunia violaceae. Bull Imp Coll Agric 20:1–95
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Liedl, B.E., McCormick, S. & Mutschler, M.A. Unilateral incongruity in crosses involvingLycopersicon pennellii andL. esculentum is distinct from self-incompatibility in expression, timing and location. Sexual Plant Reprod 9, 299–308 (1996). https://doi.org/10.1007/BF02152705
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DOI: https://doi.org/10.1007/BF02152705