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Pitfalls of Transgene Containment in Chloroplast

As transgenic contamination is becoming a big issue, biotech companies are proposing to put transgenes in the chloroplast genome instead of the nuclear genome in order to prevent them from spreading. Prof. Joe Cummins reveals the pitfalls.

The majority of proposals for preventing the spread of transgenes by putting them into chloroplasts assume that chloroplasts are maternally inherited, and absent from pollen. Where this may be true for the specific transgenic plant variety involved, little or no consideration has been given to the pollination of chloroplast transgenic crops by weedy relatives. The resulting hybrids could then either transmit transgenes maternally, or possibly, through both ovule (containing the female germ cell) and pollen. Pollination of a chloroplast transgenic crop by non-transgenic varieties, or with a variety containing nuclear transgenes, may also alter nuclear-cytoplasmic balance, leading to altered chloroplast transmission.

In fact, plastids (general term that includes chloroplasts) are inherited strictly maternally, exclusively paternally, or bi-parentally, depending on the species and the variety within a species and other factors. Gymnosperms have mainly paternal (pollen) transmission while most flowering plants seem to have maternal inheritance. About one third of the flowering plants investigated, however, have displayed bi-parental inheritance to some degree [1]. Among the flowering plants, rye shows paternal inheritance [1], and predominantly paternal inheritance has been observed in chaparral [2]. Alfalfa has predominantly paternal inheritance with both biparental and maternal variants [3,4]. The medicinal herb damiana has clearly paternal inheritance [5] as does kiwi [6]. Experiments with calla lilies showed that nuclear-cytoplasmic interactions determined the transmission of plastids. Interspecific hybrids showed maternal chloroplast transmission in the F1 generation but from either maternal or paternal parents in the backcross [7]. Even plants that appear to have clear maternal plastid transmission may show leakage of pollen transmission [8], a frequency of one transgenic chloroplast containing pollen granule in 100 or 1000 could lead to significant transgenic pollution of nearby crops or weeds.

Thus, the claim that chloroplasts are maternally inherited and transgenic chloroplasts can thereby contain the release of polluting transgenic pollen is by no means always valid. The numerous crops or wild plants that show bi-parental or paternal inheritance of plastids means that each crop must be carefully studied. When a transgenic chloroplast crop plant is fertilized by weed pollen, a hybrid weed with maternal chloroplast inheritance results, but as the nuclear-cytoplasmic relationship has also been altered, this may result in weeds that show either paternal or biparental inheritance. For example, canola has weedy relatives in Canada with which it could form hybrids: birdsrape mustard in eastern Canada, feral B. rapa in western Canada, and wild radish (Raphanus raphanistrum L). A few crop-weed hybrids can quickly establish transgenic weeds.

In conclusion, the proposal to contain trangenes by putting them into chloroplast need a great deal more investigations on the inheritance of chloroplasts and the consequences of hybridisation carefully considered. Chloroplast transgenes offer the advantage of producing multiple gene copies that are not so much affected by gene silencing (neither pre-transcriptional nor posttranscriptional silencing) and a potential to transform the genome using homologous recombination, which is not possible with nuclear transgenes. But the use of chloroplasts to prevent gene spread rests on rather shaky grounds.

Article first published 19/06/02


References

  1. Mogensen L and Rusche M. Occurrence of plastids in rye sperm cells. Am J. Bot. 2000, 87, 1189-92.
  2. Yang T, Yang Y, and Xiong Z. Paternal inheritance of chloroplast DNA in interspecific hybrids in the Genus Larrea. Am. J. Bot. 2000, 87, 1458-2000.
  3. Schumann C and Hamcock J. Paternal inheritance of plastids in Medicago sativa. Theor and Appl Genet 1991, 78, 863-66.
  4. Rusche M, Mogensen H, Zhu T and SmithT. The zygote and prembryo of alfalfa. Protoplasma 1995, 189,88-100
  5. Cipriani G,Testolin R and Morgante M. Paternal inheritance of plastids in interspecific hybrids of the genus Actinidia revealed by PCR -amplification of chloroplast DNA fragments. Mol and Gen Genet 1995, 247,693-97.
  6. Tustolin R and Cipriani G. Paternal inheritance of chloroplast DNA and maternal inheritance and maternal inheritance of mitochondrial DNA in the genus Actinidia. Theor and Appl Genet 1997, 94, 897-903.
  7. Yao J and Cohen D. Multiple gene control of pastime-genome incompatibility and plastid DNA inheritance in interspecific hybrids of Zantedeschia. Theor. Appl Genet. 2000, 101,400-6.
  8. Avri A and Edelman M. Direct selection for paternal inheritance of paternal inheritance of chloroplasts in sexual crosses of Nicotiana Direct selection for paternal inheritance of chloroplasts in sexual progeny of Nicotiana. Mol Gen Genet 1991, 225,273-7

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