Abstract
Nicotiana tabacum was used as a pistillate parent and crossed with three self-compatible species, N. rustica, N. repanda and N. trigonophylla, which were previously reported to have pollen tubes unilaterally inhibited by N. tabacum pistil. Temporal and morphological observations revealed distinct differences of pollen tube behavior among these incongruous crosses. Pollen tubes of N. repanda were arrested in stigma and those of N. rustica in the middle of the style. On the other hand, pollen tubes of N. trigonophylla continued growing at a slow rate. Tubes of N. repanda and N. rustica showed morphological abnormalities such as swelling, thick wall, and irregular callose deposition. In addition, tubes of N. rustica often elongated in reverse direction and wound about in the middle of the style. Although the tubes of N. trigonophylla were apparently normal in morphology, they were distributed throughout the transmitting tissue, differing from the self-pollination of N. tabacum in which they were confined to the peripheral region of it. The diversity of pollen tube behavior indicates that physiological causes of incongruity are different among the three crosses. Bud pollination enabled pollen tubes to reach the ovary in all crosses, indicating that the N. tabacum pistil acquired its ability to inhibit foreign pollen tube elongation with its development. When interspecific hybrids between N. tabacum and the other three species were pollinated by parental species, tubes reached the ovary in all crosses, but the elongation rate of tubes slowed down and morphology was abnormal.
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References
Abdalla MMF, Hermsen JGTH (1972) Unilateral incompatibility: hypothesis, debate and its implications for plant breeding. Euphytica 21:32–47
Anderson E, Winton D De (1931) The genetic analysis of an unusual relationship between self-sterility and self-fertility in Nicotiana. Ann Mo Bot Gard 18:97–116
Atkinson AH, Heath RL, Simpson RJ, Clarke AE, Anderson MA (1993) Proteinase inhibitors in Nicotiana alata stigmas are derived from a precursor protein which is processed into five homologous inhibitors. Plant Cell 5:203–213
Camadro EL, Peloquin SJ (1981) Cross-incompatibility between two sympatric polyploid Solanum species. Theor Appl Genet 60:65–70
Chetelat RT, DeVerna JW (1991) Expression of unilateral incompatibility in pollen of Lycopersicon pennellii is determined by major loci on chromosomes 1, 6 and 10. Theor Appl Genet 82:704–712
Cheung AY, May B, Kawata EE, Gu Q, Wu H-M (1993) Characterization of cDNAs for stylar transmitting tissue-specific proline-rich proteins in tobacco. Plant Journal 3:151–160
Chung CS, Nakajima T, Takeda G (1988) Interspecific hybridization between Nicotiana trigonophylla Dun. and N. tabacum L. through ovule culture. Jpn J Breed 38:319–326
Chung CS, Takeda G, Nakajima T (1989) Overcoming of cross-incompatibility between Nicotiana tabacum L. and N. trigonophylla Dun., and characteristics of their hybrids. Proceedings of 6th International Congress of SABRAO, Tsukuba, Japan, August, pp 439–442
De Nettancourt D (1977) Incompatibility in angiosperms. Monographs on theoretical and applied genetics, vol 3. Springer, Berlin Heidelberg New York
De Nettancourt D, Devereux M, Bozzini A, Cresti M, Pacini E, Sarfatii G (1973a) Ultrastructural aspects of self-incompatibility mechanism in Lycopersicon peruvianum. J Cell Sci 12:403–419
De Nettancourt D, Devereux M, Laneri U, Pacini E, Cresti M, Sarfatii G (1973b) Ultrastructural aspects of unilateral incompatibility between Lycopersicon peruvianum and L. esculentum. Caryologia [Suppl] 25:207–217
DeVerna JW, Myers JR, Collins GB (1987) Bypassing prefertilization barriers to hybridization in Nicotiana using in vitro pollination and fertilization. Theor Appl Genet 73:665–671
Gasser CS, Budelier KA, Smith AG, Shah DM, Fraley RT (1989) Isolation of tissue-specific cDNAs from tomato pistils. Plant Cell 1:15–24
Goldman MHS, Pezzotti M, Seurinck J, Mariani C (1992) Developmental expression of tobacco pistil-specific genes encoding novel extensin-like proteins. Plant Cell 4:1041–1051
Jefferies CJ, Belcher AR (1974) A fluorescent brightener used for pollen tube identification in vivo. Stain Technol 49:199–202
Hogenboom NG (1972) Breaking breeding barriers in Lycopersicon. 4. Breakdown of unilateral incompatibility between L. peruvianum (L.) Mill. and L. esculentum Mill.
Hogenboom NG (1984) Incongruity: non-functioning of intercellular and intracellular partner relationships through nonmatching information. In: Linskens HF, Heslop-Harrison J (eds) Cellular interactions. (Encyclopedia of plant physiology, new series, vol 17) Springer, New York Berlin Heidelberg, pp 640–654
Kostoff D (1930) Ontogeny, genetics and cytology of Nicotiana hybrids. Genetica 12:33–139
Kuroiwa T, Kuroiwa H, Mita T, Fujie M (1990) Fluorescence microscopic study of the formation of giant mitochondrial nuclei in the young ovules of Pelargonium zonale. Protoplasma 158:191–194
Lewis D, Crowe LK (1958) Unilateral incompatibility in flowering plants. Heredity 12:233–256
Lotan T, Ori N, Fluhr R (1989) Pathogenesis-related proteins are developmentally regulated in tobacco flowers. Plant Cell 1:881–887
Martin FW (1968) The behavior of Lycopersicon incompatibility alleles in an alien genetic milieu. Genetics 60:101–109
Marubashi W (1985) Studies on interspecific hybridization in genus Nicotiana using test-tube fertilization. Doctoral thesis, University of Tokyo.
Marubashi W, Nakajima T (1981) Pollen tube behavior in the ovary of Nicotiana tabacum L. Jpn J Breed 31:133–140
McClure BA, Haring V, Ebert PR, Anderson MA, Simpson RJ, Sakiyama F, Clarke AE (1989) Style self-incompatibility gene products of Nicotiana alata are ribonucleases. Nature 342:955–957
Pandey KK (1969) Elements of the S-gene complex. IV. S-allele polymorphism in Nicotiana species. Heredity 24:601–619
Shintaku Y, Yamamoto K, Nakajima T (1988) Interspecific hybridization between Nicotiana repanda Willd. and N. tabacum L. through the pollen irradiation technique and the egg cell irradiation technique. Theor Appl Genet 76:293–298
Shizukuda N, Nakajima T (1982) Production of interspecific hybrids between Nicotiana rustica L. and N. tabacum L. through ovule culture. Jpn J Breed 32:371–377
Swaminathan MS, Murty BR (1957b) One-way incompatibility in some species crosses in the genus Nicotiana. Indian J Genet Plant Breed 17:23–26
Tanaka M, (1961) The effect of irradiated pollen grains on species crosses of Nicotiana. Bull Hatano Tob Exp Stat 51:1–38
Williams EG, Rouse JL (1990) Relationships of pollen size, pistil length and pollen tube growth rates in Rhododendron and their influence on hybridization. Sex Plant Reprod 3:7–17
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Kuboyama, T., Chung, C.S. & Takeda, G. The diversity of interspecific pollen-pistil incongruity in Nicotiana . Sexual Plant Reprod 7, 250–258 (1994). https://doi.org/10.1007/BF00232744
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DOI: https://doi.org/10.1007/BF00232744