You are on page 1of 8

PDFlib PLOP: PDF Linearization, Optimization, Protection

Page inserted by evaluation version


www.pdflib.com sales@pdflib.com

Efivironmental Impact from


Plant Biotechnology
SIMON w. J. BRIGHT," ANDREW J. GREEN LAND,^
CLAIRE M. HALPIN,",d WOLFGANG W. SCHUCH," AND
JAMES M. DUNWELL",'
aZeneca Plant Science,
bZeneca Agrochemicals, and
'Zeneca Seeds
Jealott's Hill Research Station
Bracknell, Berks, RG42 6EY, UK
The environmental impact of plant biotechnology has been widely debated since
the first reports of gene transfer to plants in 1982. Three aspects have been
emphasized: the potential benefits, the potential risks, and the nature of the consequences of gene transfer in general. Much progress has been made in addressing
these topics. In North America the first products have come t o the market with
USDA clearance, and the release of transgenic plants in limited experimental
quantities is routine for both private companies and public researchers. The focus
is shifting to a measured assessment of specific risks of particular products and
to evaluating and capturing the environmental benefits that are on offer.

RISK ASSESSMENTS OF TRANSGENIC PLANTS


This area has been a major source of research activity in both public and
private laboratories, spawning a series of coordinated programs,' international
symposia,2and international harmonization initiative^.^,^ Risk can be broken down
into Hazard (the actual harm or damage that might occur) multiplied by Likelihood
(the probability of occurrence of the event). Viewed in this light, most of the
research in the area has focused on trying to measure likelihood.
Pollen transfer to neighboring crops and wild relatives has been a s ~ e s s e d . ~ - ~
In our studies, we observed the pollination behavior of transgenic tobacco and
oilseed rape lines. Pollen movement to neighboring plants was detected by marker
gene e x p r e ~ s i o n .The
~ , ~ frequency of gene transfer to neighboring plants decreases
rapidly with distance (FIG. l), a result in keeping with other transgenic cr0ps~7~
and with the biology of these crops. It seems reasonable to generalize that the
fact that a plant is transgenic does not a priori alter the fate or function of pollen.
Another characteristic of interest is "weediness." The hazard identified is that
transgenic plants may become more competitive in wild or disturbed habitats and
thus become weeds.'O.'' One study of oilseed rape and other crops concluded that
this did not occur in the transgenic lines studied.12 No observations of enhanced
weediness or survival have been reported from numerous field releases, although
Present address: Department of Biologial Science, University of Dundee, Dundee,
DDl 4HN, UK.
e Present address: Department of Agricultural Botany, University of Reading, Reading
RG6 2AS, UK.
99

ANNALS NEW YORK ACADEMY OF SCIENCES

100

G
8

v1

0.002

0.001

&

10

21

interpretation of this is open to debate.13 It does seem reasonable to generalize


once again that transgenic lines are not u priori likely to be more weedy. Indeed,
crop traits that have been selected for by breeders over multiple generations (large
seeds, uniform germination, and response to high inputs) might militate against
those crops becoming successful weeds. The availability of gene transfer methods
actually offers a new tool selectively to alter individual plant fitness components
to assess the contribution of particular factors to plant survival.
A third potential hazard has been thought of as the possibility of horizontal
gene transfer either from plants to soil microorganisms or amongst soil microflora.
Current experimental results suggest that the likelihood of these transfers is low
as it has proved difficult to demonstrate in practice.14
~ several
In a thought-provoking overview of the topic in 1994 D e ~ h a y e s drew
conclusions which remain valid today. (1) Some basic principles of biology were
rediscovered with transgenic lines. ( 2 ) Negative results from risk assessment can
only indicate a low likelihood, not a negative one. (3) Scientific assessment of
risks for the purposes of regulation does not equate with public perceptions. This
remains an issue in Europe.
Partly as a consequence of the research and regulatory activity over the last
5 years, regulatory regimens that focus, for the most part, on scientific evaluation
of products are now in place in North America and Europe. In North America
there have been clearances for the sale of tomato, cotton, soybean, canola, and
maize lines. The situation in Europe is less rosy; no crops have currently completed
the full Part C clearance required for growth and placing on the market throughout Europe although several applications are under review.

ENVIRONMENTAL BENEFITS IN AGRONOMY


OF TRANSGENIC PLANTS
Transgenic plants offer the potential to give additional choices for the farmer
to provide cost-effective control of bacterial, viral, and fungal diseases and insect
pests; examples are cited in other articles in this volume. The existing contribution
of conventional plant breeding in this area should not be ignored. Indeed, high
technology before gene transfer often involved introgression of genes across spe-

BRIGHT ef al.: PLANT BIOTECHNOLOGY AND THE ENVIRONMENT

101

cies and genus barriers using sophisticated crossing and embryo rescue methods.
Notable successes, for instance, were the introduction of rust resistance from
Aegilops and Agropyon species into bread wheat Triticum aestiuum and bacterial
and nematode resistances from wild tomato species (Lycopersicon hirsutum,
L . peruuianurn) into the cultivated form, L . esculentum. Essentially the transgenic
approach allows complete access to genes from other organisms to be used without
regard to sexual barriers in order to provide plants with appropriate resistances.
The products of these gene transfers can then be seen as complementing or
substituting the existing genetic or chemical capacities. The earliest examples of
the technology are virus, insect, and herbicide resistances discussed elsewhere
in this volume. For the purposes of this paper, the environmental impacts come
in three forms. Firstly, by increasing the genetic component of the crop package
the potential to use less chemicals can be realized. This is a specific goal of
agricultural policy in some countries such as Denmark (government policy, however, does not always equate with environmental benefit). Secondly, by giving
additional routes to crop protection the successful maintenance of useful chemical
and genetic resistances against the development of resistances in the pest or
disease is made more feasible. l6 Finally, by increasing yields or productivity the
total environmental load from agriculture may be reduced. This may also be seen
in a capacity to tolerate stressful or marginal environments.
At Zeneca we have a program to examine the use of plant-derived antifungal
proteins in transgenic crops. Many plant seeds were screened in collaboration
with W. Broekaert's laboratory in Leuven for the presence of antifungal proteins.
Several classes of protein were identified and their amino acid and DNA sequences
determined (TABLEl).17-2n These proteins are small (25-60 amino acids) with
several disulfide bridges. Tertiary structure of a protein from radish has been
determined.2n-21
Antifungal activity of these proteins has been assessed in uitro. On a molar
basis they can be as effective as a chemical fungicide, having I,, values of 80-400
nM in uitro (TABLE1). They are effective as sprays and look promising when
expressed in transgenic plant leaves.22

ENVIRONMENTAL BENEFITS OF TRANSGENIC PLANTS


BEYOND THE FIELD
We can look forward to a complete DNA sequence of Arabidopsis early in
the next century. Much more rapidly will come an understanding of the major
TABLE 1. Biological Activity of Several Classes of Small, Cysteine-Rich

Antifungal Proteins"
Source Species

AFP

Class

Size (kDa)

IC,, (nM)

Mirabilis jalapa
Amaranthus cauduzus
Raphanus sativus
Dahlia merckii
Allium cepa
Impatiens balsamina

Mj-AMP2
Ac-AMP2
Rs-AFP2
Dm-AMP1
Ace-AMP1
Ib-AMP2

Mirabilis type
Hevein type
Plant defensin
Plant defensin
nsLTP typeh
Impatiens type

4
3
5
5
9
2.5

400
250
3 00
<I50
<80
<300

Ii Assays were performed in microplate cultures using an isolate of Fusarium oxysgorum


from banana; ICso = protein concentration required to inhibit fungal growth by 50%.
nsLTP = nonspecific lipid transfer protein.

ANNALS NEW YORK ACADEMY OF SCIENCES

102

genes controlling the raw material quality of the major agricultural commodities
as both foods and industrial feedstocks. This is already heralded in the work
described elsewhere in this volume on the genes determining the chain length and
desaturation of fatty acids and those determining the quantity and quality of starch.
From this work it can be seen that three clear environmental benefits are within
sight. Firstly, improvements in harvested yield and productivity will relieve the
agricultural load on land and resources. Secondly, plants as renewable resources
will provide tailor-made products for bulk and specialty needs of industry (the
financial case, on the other hand, is less clear depending on the cost of competing
technological solutions, the price of oil, and other political considerations). Finally,
the end products can be made in a way that reduces processing costs and environmental load.
As an example of this latter application, Zeneca has been working on the
modification of lignin with a group of European laboratories coordinated by Professor Boudet in Toulouse. Lignin is a complex and heterogeneous polymer with
structural and waterproofing functions. It is made from the polymerization of
monomer components derived from the phenylpropanoid pathway.23Genes specifying two enzymes in this pathway, cinnamyl alcohol dehydrogenase (CAD) and
cinnamyl-o-rnethyl transferase (COMT), have been cloned from a number of spec i e ~ . ~ ,In ~tobacco plants in which CAD or COMT was reduced to less than 5%
of control values by introduced transgenes, the lignin structure was altered.26v27
For the low-CAD plants, this was shown to translate into an improvement in the
chemical extractability of the lignin. This produces better quality pulp and is
estimated to require less chlorine to bleach the final pulp.26 We are currently
examining the effect of reducing the expression of these genes in transgenic poplar
in the field.

FUTURE OPPORTUNITIES: PHYTOREMEDIATION AND THE STUDY


OF PLANT ECOLOGY
Two research avenues that are not covered elsewhere in this symposium deserve mention as having potential for applied use of transgenic technology.
Phytoremediation is a branch of Bioremediation that focuses on the special
benefits that plants can offer to the problems of pollution of soil, aqueous waste
streams, and ground
Considerable literature exists on plants that can
tolerate soils with high metal content such as those in the spoil heaps of mines.31
This is an area where the conventional use of adapted plants can go hand in hand
with the development of new plants specifically adapted to bind, accumulate, or
extract particular metal^.'^ The field is in its infancy; plants with introduced metalbinding capacity were recently made.32The incorporation of an Escherichia coli
mercuric reductase gene into Arabidopsis to confer the capacity to grow on mercuric salts and evolve Hg seems an excellent harbinger of the technical potential
for metabolism of metals and organic pollutants. In practice the problems of
dealing with pollution are large and intractable enough to indicate that all avenues
should be explored.
On a more fundamental level, the science of plant ecology must surely benefit
from the advent of transgenic plants. Early studies on ecology of transgenic linesI2
brought together expertise from very different disciplines. Now it seems that
transgenics can perhaps offer the ecologist interesting tools to change, one gene
at a time, plants of known ecology in order to assess the contribution of different

BRIGHT ef al.: PLANT BIOTECHNOLOGY AND THE ENVIRONMENT

FIGURE 2. Density-dependent elongation responses of the stems of wild-type


(0)and phyd-expressing tobacco plants
( 0 ) .Redrawn from ref. 34.

103

- 0.6

0.6

Log. Leaf Area Index

factors to growth, survival, seed dispersal, and reproductive success. An early


indication of the potential of this approach comes from the use of plants overexpressing the phyA gene which alters their capacity to sense their neighbors
and respond to shading by increasing internode length (FIG.2).34The identification
of genes that trigger flowering responses35will provide a further set of tools for
this research area.

CONCLUSIONS
From an environmental point of view, the first dozen years of research with
transgenic plants has focused mostly on the environmental risks that might be
incurred. During this time the base of understanding has moved forward so that
the hazards of particular products rather than transgenic plants in general are the
focus of regulatory review and scientific discussion. In addition, as the first products come to the market, attention has also shifted to the positive environmental
benefits to be gained in both agronomics and downstream of the farm gate. Although the commercialization of transgenic plants is in its infancy, it is clear
that great opportunities exist to have a positive environmental impact from plant
biotechnology throughout the world.
REFERENCES
ECONOMIDIS,
I. 1992. Biosafety research in the European Community: Results and
perspectives. In Proceedings of the 2nd International Symposium on the Biosafety
Results of Field Tests of Genetically Modified Plants and Microorganisms. R. Casper
& J. Landsmann, Eds.: 135-140. Goslar. Braunschweig. Germany.
2. JONES, D. D., Ed. 1994. Proceedings of the 3rd International Symposium on the Biosafety Results of Field Tests of Genetically Modified Plants and Microorganisms.
558 pp. University of California. Division of Agriculture and Natural Resources,
Oakland, CA.
3. MOFFAT,A. 1994. Developing nations adapt biotech for own needs. Science 265:
186- 187.
4. DICKSON,D. 1995. Biosafety code gathers pace through bilateral agreements. Nature
317: 94.
5 . DALE,P. J. 1994. The impact of hybrids between genetically modified crop plants and
their related species: General considerations. Molec. Ecol. 3: 31-36.
1.

104

10.

11.

12.
13.

14.

15.

16.
17.

18.

19.

20.
21.

22.

23.
24.

ANNALS NEW YORK ACADEMY OF SCIENCES


ROGERS,H . J. & H.C. PARKES.1995.Transgenic plants and the environment. J. Exp.
Bot. 46: 467-488.
PAUL,E. M., G. B. LEWIS& J. M. DUNWELL.1991. The pollination of genetically
modified plants. Acta Hortic. 288: 425-428.
PAUL,E. M., C. THOMSON& J. M. DUNWELL.1995. Gene dispersal from genetically
modified oil seed rape in the field. Euphytica 81: 283-289.
MCPARTLAN,
H. C. & P. J. DALE. 1994. An assessment of gene transfer by pollen
from field-grown transgenic potatoes to non-transgenic potatoes and related species.
Transgenic. Res. 3: 216-225.
DARMENCY,
H. 1994.The impact of hybrids between genetically modified crop plants
and their related species: Introgression and weediness. Mol. Ecol. 3: 27-40.
RAYBOULD,
A. F. & A. J. GRAY. 1994. Will hybrids of genetically modified crops
invade natural communities? Trends Ecol. Evol. 9: 85-89.
CRAWLEY,M. J., R. S . HAILS,M. REES, D. KOHN& J. BUXTON.1993. Ecology of
transgenic oilseed rape in natural habitats. Nature 363: 620-622.
MELLON,M. & J. RISSLER.1995.Transgenic crops: USDA data on small scale tests
contribute little to commercial risk assessment. Bio/Technology 13: 96.
SMALLA,K., F. GEBHARD,
J. D. VANELSAS,A. MATZK& J. SCHIEMANN.
1994.
Bacterial communities influenced by transgenic plants. In Proceedings of the 3rd
International Symposium on the Biosafety Results of Field Tests of Genetically
Modified Plants and Micro-organisms. D. D. Jones, Ed.: 157-167. University of
California, Division of Agriculture and Natural Resources, Oakland, CA.
DESHAYES,
A. F. 1994. Environmental and social impacts of GMO's: What have we
learned from the past few years? I n Proceedings of the 3rd International Symposium
on the Biosafety Results of Field Tests of Genetically Modified Plants and Microorganisms. D. D. Jones, Ed.: 5-19. University of California, Division of Agriculture
and Natural Resources, Oakland, CA.
ALTMAN,D. W. & J. H. BENEDICT.1996.Transgenic plants for durable insect resistance: Case study for cotton with Bacillus rhurigirnsis genes. N.Y. Acad. Sci.,
this volume.
CAMMUE,B. P. A,, M. F. C. DE BOLLE,F. R. G. TERRAS,P. PROOST,J. VAN
& W. F. BROEKAERT.
1992. Isolation and
DAMME,S. B . REES,J. VANDERLEYDEN
characterisation of a novel class of plant antimicrobial peptides from Mirabilisjafopa
L. seeds. J. Biol. Chem. 267: 2228-2233.
TERRAS,F. R. G., S . TORREKENS,
F. VANLEUVEN,
R. W. OSBORN,
J. VANDERLEYDEN,
B. P. A. CAMMUE
& W. F. BROEKAERT.
1993.A new family of basic cysteine-rich
antifungal proteins from Brassicaceale species. FEBS Lett. 316: 233-240.
OSBORN,R. W., G. W. SAMBLANX,
K. THEVISSON,
I. GODERIS,S . TORREKENS,
F. VAN LEUVEN,S. ATTENBOROUGH,
S. B. REES & W. F. BROEKAERT.
1995.
Isolation and characterisation of plant defensins from seeds of Asteraceae Fabaceae,
Hippocastanaceae and Saxifragaceae. FEBS Lett. 368: 257-262.
BROEKAERT,
W. F.,F. R. G. TERRAS,B. P. A. CAMMUE& R. W.OSBORN.1995.
Plant defensins: Novel antimicrobial peptides as components of the host defence
system. Plant Physiol. 108: 1353-1358.
FANT,F., L.SANTOS,K. BOULEZ,W. VRANKEN,
J. C. MARTINS& F. A. M. BORREMANS. 1994. The solution structure by 'H-NMR of a plant antifungal protein from
radish seeds, Rs AFPI. In Abstracts of the 12th European Experimental NMR
Conference. L. P. Ingman, J. Jokisaari & J. Lounila, Eds.: 247.
TERRAS,F. R. G., K. EGGERMONT,
V. KOVALEVA,
N. RAIKHEL,R. W. OSBORN,
S . TORREKENS,
F. VANLEUVEN,
A. K. KESTER,S. B. REES,J. VANDERLEYDEN,
B . P. A. CAMMUE
& W. F. BROEKAERT.
1995.Small cysteine-rich antifungal proteins
from radish (Raphanus Satiurns. L.) Their role in hose defence. Plant Cell 7: 573-588.
DEAN,J. F. D. & K. E. L. ERIKSSON.1992. Biotechnological modification of lignin
structure and composition in forest trees. Holzforschung 4 6 135-147.
KINGHT,M. E., C. HALPIN& W. W. SCHUCH.
1992.Identificationand characterisation
of cDNA clones encoding cinnamyl alcohol dehydrogenase from tobacco. Plant Mol.
Biol. 1 9 793-XOl.

BRIGHT et al.: PLANT BIOTECHNOLOGY AND THE ENVIRONMENT

105

& B. FRITIG.
1992. Regulationofenzymesinvolved
25. JAECK,E., B. DUMAS,P. GEOFFREY
in lignin biosynthesis: Induction of 0-methyltransferase mRNAs during the hypersensitive reaction of tobacco to tobacco mosaic virus. Mol. Plant-Microbe Interact.
4: 294-300.
M. M. CAMPBELL,A. M. BOUDET,
26. HALPIN,C., M. E. KNIGHT,G. A. FOXON,
J. BOON, B. CHABBERT,M. T. TOLLIER
& W. W. SCHUCH.
1994. Manipulation
of lignin quality by down regulation of cinnamyl alcohol dehydrogenase. Plant J.
6: 339-350.
R., N. FAVET,F. MARTZ,B. CHABBERT,
M.-T. TOLLIER,B. MONTIES,
27. ATANASSOVA,
B. FRITIG
& M. LEGRAND.
1995. Altered lignin composition in transgenic tobacco
expressing 0-methyl-transferase sequences in sense and antisense orientation.
Plant J. 8: 465-477.
S. M. 1994. Environmental biotechnology. Bio/Technology 12: 133828. EDGINGTON,
1342.
N. P. B. A. KUMAR,V. DUSHENKOV,
B. D. ENSLEY,
29. SALT,D. E., M. BLAYLOCK,
I. CHET & I. RASKIN.1995. Phytoremediation: A novel strategy for the removal of
toxic metals from the environment using plants. Bio/Technology 13: 468-474.
S. D., W. R. BERTI& J. W. HUANG.1995. Phytoremediationofcontami30. CUNNINGHAM,
nated soils. Trends Biotechnol. 13: 393-397.
1979. The use of metal tolerant plant populations
31. SMITH,R. A. H . & A . D. BRADSHAW.
for the reclamation of metalliferous waste. J. Appl. Ecol. 16: 595-612.
32. PAN,A., M. YANG,F. TIE, L. L I , 2. CHEN& B. Ru. 1994. Expression of mouse
metallothionein-I gene confers cadmium resistance in transgenic tobacco plants.
Plant Mol. Biol. 24: 341-351.
33. RUGH,C. L., H. D. WILDE,S. A. MERKLE& R. B. MEAGHER.1995. Genetic transformation of Arabidopsis thaliana with an engineered bacterial gene for mercuric reductase. Plant Physiol. 108: S23.
C. L., A. L. SCOPEL,E. T. JORDAN & R. D. VIERSTRA.1994. Signalling
34. BALLARE,
among neighbouring plants and the development of size in equalities in plant populations. Proc. Natl. Acad. Sci. USA 91: 10094-10098.
~ . A developmental switch sufficient for flower initiation
35. WEIGEL,D. & 0. N r ~ s s o 1995.
in diverse plants. Nature 377: 495-500.

You might also like