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Pollen competitive ability in maize: within population variability and response to selection

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Male gametophytic selection can play a special role in the evolution of higher plant populations. The main assumption — gametophytic-sporophytic gene expression of a large portion of a plant's genes — has been proven by a number of studies. Population analyses have revealed a large amount of variability for male gametophytic fitness. However, the data available do not prove that at least a portion of this variability is due to postmeiotic gene expression. This paper reports the analysis of a synthetic population of maize based on a gametophytic selection experiment, carried out according to a recurrent scheme. After two cycles of selection, the response was evaluated for gametophytic and sporophytic traits. A parameter representing pollen viability and time to germination, although showing a large amount of genetic variability, was not affected by gametophytic selection, indicating that this variability is largely sporophytically controlled. Pollen tube growth rate was significantly affected by gametophytic selection: 21.6% of the genetical variability was released by selection. Correlated response for sporophytic traits was observed for mean kernel weight: 15.67% of the variability was released. The results are a direct demonstration that pollen competitive ability due to pollen tube growth rate and kernel development are controlled, to a considerable extent, by genes expressed in both tissues. They also indicate that gametophytic selection in higher plants can produce a higher evolution rate than sporophytic selection; it can thus serve to regulate the amount of genetic variability in the populations by removing a large amount of the genetic load produced by recombination.

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References

  • Beker WA (1975) Manual of quantitative genetics. Washington State University Press, Pullman

    Google Scholar 

  • Bianchi A, Lorenzoni C (1975) Gametophytic factors in Zea mays. In: Mulcahy DL (ed) Gamete competition in plants and animals. North Holland, Amsterdam, pp 257–263

    Google Scholar 

  • Brewbaker HL (1971) Pollen enzymes and isoenzymes. In: Heslop-Harrison J (ed) Pollen development and physiology. Butterworth, London, pp 156–170

    Google Scholar 

  • Brink RA, MacGillvrary JH (1924) Segregation of the waxy character in maize pollen and differential development of the male gametophyte. Am J Bot 11:465–469

    Google Scholar 

  • Clegg MT, Kahler AL, Allard RW (1978) Estimation of life cycle component of selection in an experimental plant population. Genetics 89:765–792

    Google Scholar 

  • Darwin C (1877) The different forms of flowers on plants of the same species. Appleton, New York

    Google Scholar 

  • Dickinson DB, Hopper JE, Davies MD (1973) A study of pollen enzymes involved in sugar nucleotide formation. In: Loewus F (ed) Biogenesis of plant cell wall polysaccharides. Academic Press, New York, pp 29–48

    Google Scholar 

  • Falconer DS (1961) Introduction to quantitative genetics. Oliver and Boyd, Edinburgh London

    Google Scholar 

  • Goodnight JH, Speed FM (1978) Computing expected mean squares. SAS Institute, Cary NC

    Google Scholar 

  • Grizzle JE, Starmer CF, Kock GG (1969) Analysis of categorical data by linear models. Biometrics 25:489–504

    Google Scholar 

  • Haldane JB (1932) The cause of evolution. Harper and Row, New York

    Google Scholar 

  • Haldane JB (1957) The cost of natural selection. J Genet 55:511–524

    Google Scholar 

  • Harding J (1975) Models for gamete competition and self fertilization as components of natural selection in populations of higher plants. In: Mulcahy DL (ed) Gamete competition in plants and animals. North-Holland, Amsterdam, pp 243–255

    Google Scholar 

  • Harding J, Tucker CL (1969) Quantitative studies on mating system. II. Method for the estimation of male gametophytic selective values and differential outcrossing rates. Evolution 23:85–95

    Google Scholar 

  • Heslop-Harrison J (1979) The forgotten generation: some thoughts on the genetics and physiology of Angiosperm gametophytes. In: Davies DR, Hopwood DA (eds) The plant genome. 4th Innes Symp, Norwich, pp 1–14

  • Heslop-Harrison J, Heslop-Harrison Y (1970) Evaluation of pollen viability by enzymatically induced fluorescence; intracellular hydrolysis of fluoroscein diacetate. Stain Techn 45:115–120

    Google Scholar 

  • Heslop-Harrison J, Heslop-Harrison Y, Knox RB, Howlett B (1973) Pollen wall proteins: gametophytic and sporophytic fraction in pollen wall of Malvaceae. Ann Bot 37:403–412

    Google Scholar 

  • Heslop-Harrison Y, Reger BJ, Heslop-Harrison J (1984) The pollen-stigma interaction in the grasses. 6. The stigma (“silk”) of Zea mays L. as host to the pollens of Sorghum bicolor L. (Moench) and Pennisetum americanum L. (Leeke). Acta Bot Neerl 227:205–227

    Google Scholar 

  • House RL, Nelson OE (1958) Tracer study of pollen-tube growth in cross-sterile maize. J Hered 49:18–21

    Google Scholar 

  • Johnson CM, Mulcahy DL (1978) Male gametophyte in maize. 2. Pollen vigour in inbred plants. Theor Appl Genet 51:211–215

    Google Scholar 

  • Jones DF (1928) Selective fertilization. University of Chicago Press, Chicago

    Google Scholar 

  • Kiesselbach TA (1949) The structure and reproduction of corn. University of Nebraska, Lincoln

    Google Scholar 

  • Kock GG, Landis JR, Freeman JL, Freeman DH, Lehnen RG (1977) A general methodology for the analysis of experiments with repeated measurement of categorical data. Biometrics 33:133–158

    Google Scholar 

  • Lee TD (1984) Patterns of fruit maturation: a gametophyte competition hypothesis. Am Nat 123:427–432

    Google Scholar 

  • Mascarenhas JP (1975) The biochemistry of angiosperm pollen development. Bot Rev 41:259–314

    Google Scholar 

  • Mascarenhas JP, Mermelstein J (1981) Messenger RNAs: their utilization and degradation during pollen germination and tube growth. Acta Soc Bot Pol 50:13–20

    Google Scholar 

  • Mascarenhas NT, Bashe D, Eisenberg A, Willing RP, Xiao CM, Mascarenhas JP (1984) Messenger RNA in corn pollen and protein synthesis during germination and pollen tube growth. Theor Appl Genet 68:323–326

    Google Scholar 

  • McKenna M, Mulcahy DL (1983) Ecological aspects of gametophytic competition in Dianthus chinensis. In: Mulcahy DL, Ottaviano E (eds) Pollen: biology and implications in plant breeding. Elsevier, New York, pp 414–424

    Google Scholar 

  • Moore CW, Creech RG (1972) Genetic fine structure analysis of amylose-extender locus in Zea mays L. Genetics 70:611–619

    Google Scholar 

  • Mulcahy DL (1971) A correlation between gametophytic and sporophytic characteristics in Zea mays L. Science 171:1155–1156

    Google Scholar 

  • Mulcahy DL (1974) Correlation between speed of pollen tube growth and seedling weight in Zea mays L. Nature 249:491–492

    Google Scholar 

  • Mulcahy DL (1979) The rise of the Angiosperms: a genecological factor. Science 206:20–23

    Google Scholar 

  • Mulcahy DL (1983) Manipulation of gametophytic population. In: Lange W, Zeven AC, Hogenboom NG (eds) Efficiency in plant breeding. Proc 10th EUCARPIA Congr, Pudoc, Wageningen, pp 167–179

    Google Scholar 

  • Mulcahy DL, Mulcahy GB, Ottaviano E (1975) Sporophytic expression of gametophytic competition in Petunia hybrida. In: Mulcahy DL (ed) Gamete competition in plants and animals. North Holland, Amsterdam, pp 227–232

    Google Scholar 

  • Mulcahy DL, Mulcahy GB, Ottaviano E (1978) Further evidence that gametophytic selection modifies the genetic quality of the sporophyte. Soc Bot Fr Actual Bot 1–2:57–60

    Google Scholar 

  • Nelson OE (1952) Non reciprocal cross sterility in maize. Genetics 37:101–124

    Google Scholar 

  • Ottaviano E, Mulcahy DL (1986) Gametophytic selection as a factor of crop plant evolution. In: Barigozzi C (ed) The origin and domestication of cultivated plants. Elsevier, Amsterdam, pp 101–120

    Google Scholar 

  • Ottaviano E, Sari-Gorla M (1979) Genetic variability of male gametophyte in maize. Pollen genotype and pollen-style interaction. In: Israeli-Italian Joint Meeting Genet Breed Crop Plants. Monogr Genet Agraria IV, Roma, pp 89–106

  • Ottaviano E, Sari-Gorla M, Mulcahy DL (1980) Pollen tube growth rate in Zea mays: implications for genetic improvement of crops. Science 210:437–438

    Google Scholar 

  • Ottaviano E, Sari-Gorla M, Pé M (1982) Male gametophytic selection in maize. Theor Appl Genet 63:249–254

    Google Scholar 

  • Ottaviano E, Sari-Gorla M, Arenari I (1983) Male gametophyte competitive ability in maize. Selection and implications with regard to the breeding system. In: Mulcahy DL, Ottaviano E (eds) Pollen: biology and implications for plant breeding. Elsevier, New York, pp 367–373

    Google Scholar 

  • Ottaviano E, Petroni D, Pé E (1988) Gametophytic expression of genes controlling endosperm development in maize. Theor Appl Genet 75:252–258

    Google Scholar 

  • Paterniani E (1969) Selection for reproductive isolation between two populations of maize, Zea mays L. Evolution 23:534–547

    Google Scholar 

  • Pearce SC (1983) The agricultural field experiments. Wiley, New York

    Google Scholar 

  • Pfahler PL (1965) Fertilization ability of maize pollen grain. 1. Pollen sources. Genetics 52:513–526

    Google Scholar 

  • Pfahler PL (1967) Fertilization ability of maize pollen grains. 2. Pollen genotype, female sporophyte and pollen storage interactions. Genetics 57:513–521

    Google Scholar 

  • Pfahler PL (1975) Factors affecting male transmission in maize (Zea mays L.). In: Mulcahy DL (ed) Gamete competition in plants and animals. North Holland, Amsterdam, pp 115–124

    Google Scholar 

  • Pfahler PL (1983) Comparative effectiveness of pollen genotype selection in higher plants. In: Mulcahy DL, Ottaviano E (eds) Pollen: biology and implication for plant breeding, Elsevier, New York, pp 361–366

    Google Scholar 

  • Rao CR (1973) Linear statistical inference and its applications. Wiley, New York

    Google Scholar 

  • Sacher R, Mulcahy DL, Staples R (1983) Developmental selection for salt tolerance during self pollination of Licopersicon x Solarium F1 for salt tolerance of F2. In: Mulcahy DL, Ottaviano E (eds) Pollen: biology and implications for plant breeding. Elsevier, New York, pp 329–334

    Google Scholar 

  • Sadras VO, Hall AJ, Schlichter TM (1985) Kernel set of the uppermost ear of maize. 1. Quantification of some aspects of floral biology. Maydica 30:37–48

    Google Scholar 

  • Sari-Gorla M, Ottaviano E, Faini D (1975) Genetic variability of gametophytic growth rate in maize. Theor Appl Genet 46:289–294

    Google Scholar 

  • Sari-Gorla M, Frova C, Binelli G, Ottaviano E (1986) The extent of gametophytic-sporophytic gene expression in maize. Theor Appl Genet 72:42–47

    Google Scholar 

  • Schlichting CD, Stephenson AG, Davis LE, Winsor JA (1987) Pollen competition and offspring variance. Evol Trend Plant 1:35–39

    Google Scholar 

  • Schwartz D (1960) The analysis of a case of cross-sterility in maize. Proc Natl Acad Sci 36:719–724

    Google Scholar 

  • Searcy KB, Mulcahy DL (1985a) Pollen selection and the gametophytic expression of metal tolerance in Silene dioica (Caryophyllaceae) and Mimulus guttatus (Scrophulariaceae). Am J Bot 72:1700–1706

    Google Scholar 

  • Searcy KB, Mulcahy DL (1985b) Pollen tube competition and selection for metal tolerance in Silene dioica (Caryophillaceae) and Mimulus guttatus (Scrophulariaceae). Am J Bot 72:1695–1699

    Google Scholar 

  • Searle SR (1971) Linear models. Wiley, New York

    Google Scholar 

  • Ter-Avanesian DV (1978) The effect of varying the number of pollen grains used in fertilization. Theor Appl Genet 52:77–79

    Google Scholar 

  • Tanksley SD, Zamir D, Rick CM (1981) Evidence for extensive overlap of sporophytic and gametophytic gene expression in Lycopersicion esculentum. Science 213:453–455

    Google Scholar 

  • Vasek FC, Harding J (1976) Outcrossing in natural populations. 5. Analysis of outcrossing, inbreeding and selection in Clarkia exilis and Clarkia tembloriensis. Evolution 30:403–411

    Google Scholar 

  • Willing RP, Mascarenhas JP (1984) Analysis of complexity and diversity of mRNAs from pollen and shoots of Tradescantia. Plant Physiol 75:865–868

    Google Scholar 

  • Yamada M, Murakami K (1983) Superiority in gamete competition of pollen derived from F1 plant in maize. In: Mulcahy DL, Ottaviano E (eds) Pollen: biology and implications for plant breeding. Elsevier, New York, pp 389–395

    Google Scholar 

  • Zamir D (1983) Pollen gene expression and selection: applications in plant breeding. In: Tanksley SD, Orton JJ (eds) Isozymes in plant genetics and breeding. Elsevier, Amsterdam, pp 313–330

    Google Scholar 

  • Zamir D, Vallejos EC (1983) Temperature effects on haploid selection of tomato microspores and pollen grains. In: Mulcahy DL, Ottaviano E (eds) Pollen: Biology and Implication for Plant Breeding. Elsevier, New York, pp 335–341

    Google Scholar 

  • Zamir D, Tanksley SD, Jones RA (1981) Low temperature effect on selective fertilization by pollen mixture of wild cultivated tomato species. Theor Appl Genet 59:235–238

    Google Scholar 

  • Zamir D, Tanksley SD, Jones RA (1982) Haploid selection for low temperature tolerance of tomato pollen. Genetics 101:129–137

    Google Scholar 

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Authors and Affiliations

  1. Dipartimento di Genetica e di Biologia dei Microrganismi, Università di Milano, Via Celoria 26, I-20133, Milano, Italy

    E. Ottaviano, M. Sari-Gorla & M. Villa

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  1. E. Ottaviano
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  2. M. Sari-Gorla
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  3. M. Villa
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Communicated by P. L. Pfahler

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Ottaviano, E., Sari-Gorla, M. & Villa, M. Pollen competitive ability in maize: within population variability and response to selection. Theoret. Appl. Genetics 76, 601–608 (1988). https://doi.org/10.1007/BF00260915

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