Transgenic plants for tropical regions: Some
considerations about their development and their transfer to the small farmer
Luis Herrera-Estrella
PNAS
Vol. 96, Issue 11, 5978-5981, May 25, 1999
http://www.pnas.org/cgi/content/full/96/11/5978
http://www.pnas.org/cgi/reprint/96/11/5978
-------------------------------------------------------------------------------------------------------------------------------------------------
Luis R. Herrera Estrella, Ph.D.
Dr. Herrera Estrella is chief of the National Laboratory
of Genomics for Biodiversity, Center
for Research and Advanced Studies of the National Polytechnic Institute,
Irapuato, Mexico. He received a Ph.D. in plant molecular biology from the State
University of Ghent, Belgium, where he also conducted postgraduate research.
Among the many honors he has received are the 1984 Minoru and Ethel Tsutsui Distinguished Graduate Research Award in Science
from the New York Academy of Sciences, the 1987 Javed
Husain Award from UNESCO, the 1989 Scientific Research Prize in Natural
Sciences from the Mexican National Academy of Sciences, the 1994 Award in
Biology from the Third World Academy of Sciences, the 1998 RedBio
Medal from the Latin American Biotechnology Network, the 2000 WIPO Medal from
the World Intellectual Property Organization, and the 2002 National Award in
Science, the highest recognition given to scientists by the Mexican government.
In 2003 he was elected to the Mexican Academy of Sciences and, as a foreign
associate, to the U.S. National Academy of Sciences.
RESEARCH ABSTRACT SUMMARY:
Research in Luis Herrera Estrella's laboratory aims
to understand how plants modify the
architecture of their roots to improve their ability to obtain nutrients from
the soil.
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http://www.pnas.org/cgi/content/full/96/11/5978
http://www.pnas.org/cgi/reprint/96/11/5978
Vol. 96, Issue 11, 5978-5981, May 25, 1999
This paper was presented at the National Academy of Sciences colloquium
"Plants and Population: Is There Time?" held December 5-6, 1998, at
the
Arnold and Mabel Beckman Center in Irvine, CA.
Colloquium Paper
Transgenic plants for tropical regions: Some
considerations about their development and their transfer to the small farmer
Luis Herrera-Estrella*
Departamento de Ingeniería Genética, Centro de Investigación
y Estudios Avanzados, Apartado Postal 629 C.P. 36500 Irapuato, Guanajuato, Mexico
[]
ABSTRACT
Biotechnological applications, especially transgenic plants, probably hold the
most promise
in augmenting agricultural production in the first decades of the next
millennium. However,
the application of these technologies to the agriculture of tropical regions
where the largest
areas of low productivity are located, and where they are most needed, remains
a major challenge. In this paper, some of the important issues that need to be
considered to ensure that plant biotechnology is effectively transferred to the
developing world are discussed.
The world's population is expected to double by the year 2050, making food
security the major challenge for the next millennium. Food production will have
to be doubled or preferably tripled by the year 2050 to meet the needs of the expected
11 billion people, of whom ninety percent will reside in the developing world.
The enormity of the challenge is significantly increased by the declining
availability of water and the fact that this additional food will have to be
produced on existing agricultural land or in regions considered as marginal
soils, if we want to preserve the forested regions and the environment as a
whole.
Agricultural research and technological improvements are, and will continue to
be, required for increasing agricultural productivity. There are numerous ways
in which agricultural productivity may be increased in a sustainable way,
including the use of biological fertilizers, improved pest control, soil and water
conservation, and the use of improved plant varieties, produced by either
traditional or biotechnological means. Of these measures, biotechnological
applications, especially transgenic plant varieties, probably hold the most
promise for augmenting agricultural production and productivity, when properly integrated
into traditional systems.
The Case for Genetically Engineered Plants. The effectiveness
of transgenic plant varieties in
increasing production and lowering production cost has been demonstrated in the
cases of
virus-, insect-, and herbicide-resistant plants, in which an average increase
in production of 5% to 10%, and a saving in herbicides of up to 40% and in
insecticides of between $60 to $120 per acre, have been reported in 1996 and
1997 (1). However, these increases in productivity, impressive as they are in
terms of their economic and environmental value, will have a limited impact for
global food supply. In fact, most of the developments in transgenic crops are
aimed either at reducing production costs in agricultural areas that already
have high productivity levels or at increasing the value added to the final
product by improving, for instance, oil quality. This trend has been stimulated
by the current policies of developed countries to limit production of key
products such as cereals, meat, and dairy products because of the reductions in
international prices of these products, and to reduce the intensive use of
fertilizers and pesticides because of their deleterious effects on the environment.In a global sense, a more effective strategy would
be to increase productivity in tropical areas, where an increase in food
production is needed and where crop yields are significantly lower than those
obtained in developed countries. In tropical areas, the losses caused by pests,
diseases, and soil problems are exacerbated by climatic conditions that favor
high levels of insect pests and vectors and by the lack of the economic
resources to apply insecticides and
fertilizers and to purchase high-quality seeds.
In addition to low productivity levels, postharvest losses in tropical areas
are very high, again because of climatic conditions that favor fungal and
insect infestation and because of the lack of appropriate storage facilities. Despite
efforts to prevent preharvest and postharvest crop
losses, pests destroy over half of all world production. Preharvest
losses caused
by insects, the majority of which occur in the developing world, are calculated
at around 15% of the world's production.
Using biotechnology to produce transgenic plants that better withstand
diseases, insect attack, or unfavorable soil conditions, is not a simple task.
There are an estimated 67,000 species of insects worldwide that damage crops
and a similar or even higher number of plant pathogens. For instance, in the
case of Phaseolus vulgaris,
over 200 diseases and 200-300 species of insects can affect bean productivity
(2). These numbers give an idea of the complexity of the task that scientists
face in increasing productivity. There are of course a certain number of
diseases and insect pests that can be singled out as the most important
constraints for the production of each crop. However, it is also true that when
a particular disease or insect pest is controlled, others considered as minor
can then flourish, and themselves become major productivity constraints.
One of the major advantages of plant biotechnology is that it can generate
strategies for crop improvement that can be applied to many different crops. In
this sense, genetically
engineered virus resistance, insect resistance, and delayed ripening are good
examples of strategies that can benefit many different crops. Transgenic plants
of over 20 plant species that are resistant to more than 30 different viral diseases
have been produced by using different variations of the pathogen-derived
resistance strategy. Insect-resistant plant varieties, using thedelta-endotoxin of Bacillus thuringiensis,
have been produced for several important plant species including tobacco,
tomato, potato, cotton, walnut, maize, sugarcane, and rice. Of these, maize,
potato, and cotton are already under commercial production. It is envisaged
that these strategies can be used for many other crops important for developing
countries. Genetically engineered delayed ripening, although tested only on a
commercial scale for tomato, has an enormous potential application for tropical
fruit crops, which suffer severe losses because they ripen rapidly, and in many
developing countries there are neither appropriate storage conditions nor adequate
transportation systems to allow their efficient commercialization.
To date, most of the developments in plant gene transfer technology and the
different strategies for producing improved transgenic plant varieties have
been driven by the economic value of the species or the trait. These economic
values are in turn mainly determined by their importance to agriculture in the
developed world, particularly the United States and Western Europe. This economical
emphasis is understandable, because important investments are needed to develop,
field test, and commercialize new transgenic plant varieties. However, in terms
of global food production, it is necessary to ensure that this technology is
effectively transferred to the developing world and adapted to the local crops and/or
local varieties of crops for which it was originally developed.
Developing improved transgenic versions of local varieties or local crops is
not a trivial issue; in most, if not all, cultures, the use of specific crops
has a deep social and/or religious
meaning. Cultural preservation is just as important as environmental
preservation. Cultural aspects of technology transfer need to be considered
because simply replacing crops to
increase productivity could have an enormously negative effect for certain
cultures, and new introductions may not be accepted easily for human
consumption.
It is unfortunate that most developing countries do not have sufficient
resources to implement the biotechnological capacity needed to solve the major
problems that limit agricultural
productivity, at least not in the time frame that is required to cope with the
increasing demand for food. However, it is in the developing world that
biotechnology could have its major impact in increasing crop production,
especially in the areas of the world where yields are low because of the lack
of technology.
Plant genetic engineering could be considered a neutral technology that in
principle does not require major changes in the agricultural practices of
farmers in developing countries.
Perhaps more importantly, it has the potential to bring about great benefits to
the small farmers who lack the economic resources to purchase agrochemicals or
prevent postharvest losses because of the lack of storage facilities.
Whether there is time to increase agricultural productivity in the developing
world is a question with a complex answer, because there are many factors that
need to be taken into account to make this happen. We need to identify and establish
mechanisms of technology transfer from developed countries, from both academic institutions
and the private sector, to the developing world; there is a need to create a sufficient
number of research centers with the capability of acquiring this technology,
adapting it to local crops, and developing their own
technologies. Seed production facilities must be improved and an effective
mechanism implemented to reach subsistence farmers with this new technology. To
meet these requirements, several economic, political, and social issues must be
dealt with to ensure the general application of plant biotechnology to the
agriculture of developing countries. The discussion of these
issues goes beyond the scope of this article. However, it is my personal
opinion that it will not be technological limitations but rather political
and/or economic constraints that will
determine how successful we are in supplying food to the hundreds of millions
of people who will be malnourished in the next millennium.
Soil Acidity: A Problem for Agriculture in the Tropics. Estimates of the
world's potentially arable land resources indicate that only 10.6% of the total
land area of the world is cultivated,
and about 24.2% is considered cultivable or is potentially arable land (3-5).
Of these 2.5 billion hectares of potentially cultivable land, 68% is located in
the humid tropics (6). The acid soils of the tropics, especially in the
savannas, that historically have resisted permanent settlement and agricultural
use are considered to represent the largest remaining potential for future
agricultural development (7).There are problems limiting food production that are
specific or more significant to the agriculture of tropical and subtropical
regions, but that unfortunately have not been given sufficient importance to
deserve being considered priorities in the research being done in developed
countries. However, solutions to these problems could significantly contribute
to food production in tropical areas. Because many of these problems are common
to many developing countries and affect the productivity of a wide spectrum of
crops, transgenic strategies to solve them that can be applied to different
plant species are urgently needed.
Among the problems common to tropical regions, probably the most important is
soil acidity. On a global scale, there are two main geographical belts of acid
soils: the humid northern temperate zone that is covered by coniferous forest
and the humid tropics, which are (or in some cases were) covered mainly by
savanna and tropical rain forest. Soil acidification can develop naturally in
humid climates when basic cations are leached from
soils but can be considerably accelerated by certain farming practices and by
acid rain (8). Acidic soils comprise about 3.95 billion hectares of the
ice-free land or approximately 40% of the world's arable land. Regions with
subsoil acidity occupy about 20% of the ice-free land surface. Approximately
43% of the world's tropical land area is classified as acidic, comprising about
68% of tropical America, 38% of tropical Asia, and 27% of tropical Africa (9,
6).
Tropical Acid Soils That Could Be Used for
Agriculture. Because a great proportion of forest
land is located in acid soils, it is important to
remember that not all soils, although potentially
arable land, can be used for agriculture.
Tropical forests are invaluable with regard to
their role in local, regional, and global
ecosystems and to the biodiversity found within
them (over 90% of plant and animal species live
in forest ecosystems). Indiscriminate conversion
of tropical forest into agricultural land will
have far-reaching ecological consequences, whose
effects will certainly outweigh the potential
gain in food production. In spite of these
consequences, 11 million or so hectares of forest
are cleared every year, of which only a small
fraction is converted into productive
agricultural land, and most of it becomes unproductive grassland (6).
Policies to use acid soils for agriculture should
be directed to the acid savannas of the world
such as the Cerrado in Brazil, Los Llanos of
Venezuela and Colombia, the savannas in Africa,
and the largely anthropic savannas of tropical
Asia. These acid savannas cover an area of over
700 million hectares (which is approximately 50%
of the global area that is currently under
cultivation), and their potential in food
production for both humans and animals could
account for a large portion of that required to
satisfy the need of the growing population in the
next millennium. There are good examples in
Brazil and Asia of successful development of acid
savanna into productive land for the cultivation
of sugarcane and soybean (6). The use of
biotechnology could facilitate enormously the
conversion of low-productivity acid savannas into productive cropland.
Aluminum Toxicity. Poor crop productivity and
soil fertility in acid soils are mainly caused by
a combination of aluminum and manganese toxicity
and nutrient deficiencies (mainly deficiencies in
P, Ca, Mg, and K). Among these problems, aluminum
toxicity has been identified as the most
important constraint for crop production in acid
soils. Aluminum toxicity problems are of enormous
importance for the production of maize, sorghum,
and rice in developing countries located in
tropical areas of Asia, Africa, and Latin
America. Most maize, sorghum, and rice cultivars
currently being used are susceptible to toxic
aluminum in the soil, and decreases in yield of
up to 80% resulting from aluminum toxicity have
been extensively reported in the literature
(10-12). In particular, maize and sorghum
production is severely limited in tropical
Africa, where over 45% of the total land area in
countries such as Zaire, Zambia, and the Ivory
Coast is covered by acidic soils.
In tropical South America, aluminum toxicity is a
problem shared by several countries, where about
850 million hectares, or 66% of the region, has
acid soils. In Brazil alone, acid savannas with
low cation exchange capacity and high toxic
aluminum saturation cover 205 million hectares,
of which 112 million are suitable for maize and sorghum production (9).
Aluminum has a clear toxic effect on roots,
disturbing plant metabolism by decreasing mineral
nutrition and water absorption. The most easily
recognized symptom of Al toxicity is the
inhibition of root growth, and this has become a
widely accepted measure of Al stress in plants.
Although Al toxicity primarily restricts root
growth, given sufficient exposure, myriad
different symptoms appear on both roots and
shoots that are often mistaken for soil nutrient
deficiencies. Therefore, crop production in acid
soils is, to a great extent, limited by nutrient
uptake deficiency caused by the inhibition of
root growth and function that results from the
toxic effects of Al (13). Moreover, in some acid
soils, plant growth is affected not only by
aluminum toxicity but also by low availability of
some essential elements such as P, Ca, Mg, and
Fe, some of which form complexes with Al and
consequently are not readily available for root uptake (14).
It is well documented that many plant species
exhibit significant genetic variability in their
ability to tolerate Al. Although it is clear that
certain plant genotypes have evolved mechanisms
that confer Al resistance, the cellular and
molecular basis for Al resistance is still poorly understood (13).
Two basic strategies by which plants can tolerate
Al have been proposed: (i) the ability to exclude
Al entry into the root apex and root hairs, and
(ii) the development of mechanisms that allow the
plant to tolerate toxic concentrations of Al within the cell.
Several conceptually attractive hypotheses have
been proposed to explain how plants could exclude
Al from entering into the root. For example,
mechanisms based on alteration in rhizosphere pH,
low cell-wall cation-exchange capacity, or Al +3
efflux across the plasma membrane (13). However,
experimental evidence from several research
groups supports a mechanism that results in Al
exclusion from the root apex via the release of
Al-binding ligands such as malic
and citric
acids. When these ligands are released into the
rhizosphere, they can effectively chelate
Al+3
and prevent its entry into the root.
The potential role of organic acid release in Al
tolerance was originally proposed by Miyasaka et
al. (15). Their work showed that the root system
of an Al-tolerant snapbean cultivar grown in
Al-containing solutions released 10 times as much
citrate as an Al-sensitive cultivar grown in the
presence of Al. The most complete analysis of the
possible role of organic acids as Al+3-chelating
molecules in naturally resistant plants comes
from the work, done by Delhaize and coworkers
(16, 17), using near-isogenic wheat lines
differing at the Al tolerance locus (Alt1). These
researchers found that, on treatment with Al,
tolerant wheat varieties release 5- to 10-fold
more malate than do susceptible lines, and that
this increased capacity to excrete malate
correlated with Al resistance and Al exclusion
from the root apex. Because malic acid excretion
is located in the root apex, the amount of malic
acid excreted depended on the external Al
concentration, and the Al tolerance cosegregates
with high rates of malate excretion, Delhaize et
al. (16, 17) proposed that the Alt1 locus in
wheat encodes a component of an Al-tolerance
mechanism based on the Al-stimulated excretion of malic
acid.
The existence of Al-tolerance mechanisms based on
the excretion of organic acids has also been
reported for plant species other than wheat:
citrate in the case of maize, snap beans, and
Cassia tora (18-20), and oxalic acid for
buckwheat (Fagopyrum esculentum
Moench) (20).
An Example of How Transgenic Plants Could Improve
Productivity in Acid Soils. The production of
Al-tolerant transgenic plant varieties should be
considered an important part of crop management
strategies to increase agricultural production on
acid soils and to protect forests around strongly
acidified industrial regions.
Generation of metal-tolerant plants through
genetic engineering has been demonstrated to be a
valid approach. For instance, expression of the
alpha domain of human metallothionine IA in
transgenic tobacco plants confers cadmium resistance (21).
The production of transgenic plants with an
increased capacity to produce and/or excrete
organic acids that chelate and detoxify Al in the
rhizosphere is an appealing strategy to produce
Al-tolerant plants. The effectiveness of citric
acid in alleviating Al toxicity has also been
demonstrated by adding citrate to solutions
containing toxic levels of Al, which reverses the
inhibition of wheat root growth caused by Al
(22). Citric acid forms a strong chelate with Al,
typified by a stability constant of 5 × 108 M
-
1, which is about 700-fold greater than the
corresponding value for the malate-Al complex (23).
Citrate overproduction, therefore, appears to be
an ideal candidate to produce Al-tolerant
transgenic plants. To test whether citrate
overproduction could be achieved in transgenic
plants and to assess the impact of elevated
levels of citrate on aluminum tolerance, our
research team produced transgenic tobacco lines
that overexpress the citrate synthase
from
Pseudomonas aeruginosa in their cytoplasm (24).
To produce these plants, a chimeric gene, in
which the coding sequence of the P. aeruginosa
citrate synthase gene (25) transcriptionally
fused to the 35S promoter from the cauliflower
mosaic virus, was introduced into the genome of
tobacco plants. Biochemical analysis of these
transgenic tobacco lines showed that most of them
had elevated levels of citrate synthase and that
they contained in their roots 10-fold higher
levels of citrate and exuded five times more of
this organic acid into the rhizosphere than did their
nontransformed siblings.
Because the evidence for the role of organic acid
excretion in aluminum tolerance is rather
indirect, it was important to determine whether
the lines with elevated levels of citrate
synthesis and excretion are less or equally
susceptible than wild-type plants to phytotoxic
concentrations of Al. It was observed that the
inhibition of root growth by phytotoxic
concentrations of Al is significantly lower in
the citrate synthase overproducing lines than in the
control (24).
To test whether the same strategy could be used
in other plant species, the chimeric gene
encoding the bacterial citrate synthase was used
to transform papaya plants, a crop that is grown
in tropical areas where aluminum toxicity limits
its cultivation. It was found that transgenic
papaya plants expressing the bacterial enzyme
developed roots at concentrations of up to 150 mM
Al, whereas the controls failed to do so in concentrations above 50 mM (24).
The finding that in two different plant species
an increased capacity to produce and excrete
citrate led to Al tolerance suggests that this
strategy might be useful in many different plant species.
The production of Al-tolerant plants is just one
example of what plant biotechnology could do to
improve productivity in developing countries.
Drought-tolerant plants or plants with an
enhanced capacity to take up nutrients that are
present in tropical soils, but that are not
readily available for plant nutrition are
examples, among others, of technology that could
be produced by genetic engineering means, and
that could significantly elevate productivity.
Transfer of Technology to Developing Countries.
Most of the available technology for producing
improved transgenic plant varieties could
effectively be used to improve productivity in
developing countries. Because most, if not all,
of these technologies have been patented and
belong to private corporations, a major challenge
is to identify and establish the mechanisms to
effectively transfer this technology to
developing countries. Several avenues could be
followed: one would be the training of scientists
from developing countries in universities,
research institutes, and companies in developed
countries; a second one is to assist developing
countries in establishing their own facilities
for biotechnological research; and the third one
is to transfer technology, by means of gene
constructs or transgenic plants, from
universities or companies to the existing
research centers in the developing world.
In terms of training and capacity building,
several foundations and government agencies have
important programs. Good examples of successful
programs of this kind are the rice and cassava
programs of the Rockefeller Foundation, the
program of the Biotechnology Action Council of
the United Nations Educational, Scientific and
Cultural Organization (UNESCO) and the
International Cooperation (INCO) program of the
European Commission, among others. In particular,
the success of the Rockefeller rice biotechnology
program can be highlighted, which in a few years
stimulated biotechnological research for this
crop in the U.S. and Europe and facilitated the
establishment of rice molecular biology research
in many laboratories in many countries in the developing world.
In the short term, the direct transfer of
technology may be the most effective strategy to
implement plant biotechnology to increase
productivity in the developing world. Technology
transfer can be done by using end products
(transgenic seed) that have been developed for
the agriculture of advanced countries. Transfer
of end products in some cases will be done anyhow
if the market is of value to the companies;
however, the use of such seed will probably be
limited to intensive agriculture of a nature
similar to that for which the transgenic seed was
originally developed. It would be more
interesting if transgenic seeds were transferred
to national breeding programs, which could be
used as the basis for developing local varieties
better suited to local environment and soil conditions.
Another possibility is to transfer gene
constructs to research institutes that have the
capacity to introduce this genetic material into
local crops or varieties. How to achieve this is
still not completely clear, but a number of
mechanisms are beginning to be explored.
Transferring this technology has some problems;
for instance, when royalties can be waived and
when not. Perhaps a naive approach would be to
reach agreements in which the technology is
donated on a royalty-free basis if it will be
used only for production aimed at internal
markets of developing countries. In cases where
export is possible, royalties should of course be
paid; if the farmers can export their products,
however, they should at least have certain
capacities to share their increased income with
the providers of the technology.
To be able to meet the needs of developing
countries with technology available in public and
private institutions in developing countries, a
source of easily accessible information will be
needed, which preferentially indicates which
institutions or companies agree in principle to
donate technology. Initial attempts in this
direction have been carried out by the
International Service for the Acquisition of
Agrobiotech Applications (ISAAA). This nonprofit
organization is attempting to play the role of an
"honest broker," identifying needs in their
target countries and assisting a national
institution to reach an agreement with the
companies that have the technology that can
potentially solve the problem. An example of this
is the agreement between the Centro de
Investigación y Estudios Avanzados in Mexico and
Monsanto to develop virus-resistant potatoes for
the Mexican market (26). Having a company as a
partner makes it more likely that all the steps,
from basic research to field evaluation, are
carried out successfully. These still-limited
initiatives should be significantly enhanced to
make sure that plant biotechnology is transferred
to developing countries at an adequate pace.
To ensure effective technology transfer, each
recipient country must have a research center
with the capacity to assimilate the technology
and apply it to local crops or local varieties.
Although several developing countries, such as
Brazil, Argentina, India, and China, have at
least some of this capacity, it is clear that not
all developing countries have research institutes
with sufficient infrastructure and trained
personnel to effectively participate in this
process. It is therefore urgent that the
countries that do not have such capabilities give
priority to the establishment of research groups,
as well as the regulatory bodies required to
assess and approve the use and commercialization
of genetically modified organisms.
Even if technology is successfully transferred to
developing countries and transgenic varieties are
developed for local crops, the problem of getting
this technology to the small farmer is still an
important challenge. The government of each
country needs to implement a system for producing
and distributing transgenic seeds and any other
input, at low or no cost, to the small farmer.
Whether technology transfer to developing
countries takes place will, of course, depend on
the political will of each national government and the resources required.
[]
ACKNOWLEDGEMENTS
The work on acid soils in my laboratory was
carried out with support of the Howard Hughes
Medical Institute and the Rockefeller Foundation.
I thank June Simpson for critically reviewing this manuscript.
[]
FOOTNOTES
* To whom reprint requests should be addressed.
e-mail:
<mailto:lherrera@irapuato.ira.cinvestav.mx>lherrera@irapuato.ira.cinvestav.mx
.
[]
REFERENCES
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REFERENCES
1. James, C. (1997) Int. Ser. App. Agro. Apply Briefs 5, 1-20
.
2. Van Schoonhoven, A. & Voysest,
O. (1980) in
Bean Production Problems in the Tropics, eds.
Schwartz, M. & Pastor-Corrales, J. (Centro
Internacional de Agricultura
Tropical, Cali, Colombia), pp. 33-58.
3. U.S. President's Advisory Committee Report (1967), pp. 20-45.
4. Food and Agriculture Organization (FAO) (1991)
World Soil Resources Report 66.
5. Buringh, P., van Haenst,
H. D. & Staring, Y.
(1975) J. Exp. Bot. 24, 1189-1195 .
6. Von Uexküll, H. R. & Mutert,
E. (1995) Plant
Soil 171, 1-15
<http://www.pnas.org/cgi/content/full/96/11//cgi/external_ref?access_num=10.1007/BF00009558&link_type=DOI>[CrossRef].
7. Dunal, R. (1988) in Management and
Fertilization of Upland Crops in the Tropics, ed.
Wang, Y. (Nanjing Institute of Soil Science, Nanjing, China), pp. 1-5.
8. Kennedy, I. R. (1986) in The impact on the
Environment of Nitrogen and Sulfur Cycling, ed.
Kennedy, I. R. (Cambridge Univ. Press, Cambridge, U.K.), pp. 34-92.
9. Pandey, S., Ceballos,
H., Granados, G. &
Knapp, E. (1994) in Stress Tolerance Breeding:
Maize That Resist Insects, Drought, Low Nitrogen
and Acidic Soils. Maize Program, A Special
Report, eds. Edmeades, G. E & Deutsch, J. A.
(Centro Internacional de Mejoramiento
de Maíz y Trigo, Mexico D.
F.).
10. Brenes, E. & Pearson, R. W. (1973) Soil Sci.
116, 295-302 .
11. Lopes, A. S. & Cox, F. R. (1977) Soil Sci. Am. J. 41, 743-747 .
12. Saigusa, M., Shoji, S. & Takahashi, T. (1980)
Soil Sci. 130, 241-250 .
13. Kochian, L. V. (1995) Annu.
Rev. Plant
Physiol. Plant Mol. Biol. 46, 237-260
<http://www.pnas.org/cgi/content/full/96/11//cgi/external_ref?access_num=10.1146/annurev.pp.46.060195.001321&link_type=DOI>[CrossRef]<http://www.pnas.org/cgi/content/full/96/11//cgi/external_ref?access_num=A1995RP62200011&link_type=ISI>[ISI].
14. Haug, A. (1984) CRC Crit. Rev. Plant Sci. 1, 345-373 .
15. Miyasaka, S. C., Buta,
J. G., Howell, R. K. &
Foy, C. D. (1991) Plant Physiol. 96, 737-743
<http://www.pnas.org/cgi/content/full/96/11//cgi/ijlink?linkType=ABST&journalCode=plantphysiol&resid=96/3/737>[Abstract/Free<http://www.pnas.org/cgi/content/full/96/11//cgi/ijlink?linkType=ABST&journalCode=plantphysiol&resid=96/3/737>
Full Text].
16. Delhaize, E., Craig, S., Beaton, C. D.,
Bennet, R. J., Jagadish, V.
D. & Randall, P. J.
(1993) Plant Physiol. 103, 685-693
<http://www.pnas.org/cgi/content/full/96/11//cgi/ijlink?linkType=ABST&journalCode=plantphysiol&resid=103/3/685>[Abstract].
17. Delhaize, E. & Ryan, P. R. (1995) Plant
Physiol. 107, 315-321
<http://www.pnas.org/cgi/content/full/96/11//cgi/external_ref?access_num=A1995QH87200001&link_type=ISI>[ISI]<http://www.pnas.org/cgi/content/full/96/11//cgi/external_ref?access_num=12228360&link_type=MED>[Medline]
.
18. Pellet, D. M., Grunes, D. L. & Kochian, L. V.
(1995) Planta 196, 788-795
<http://www.pnas.org/cgi/content/full/96/11//cgi/external_ref?access_num=10.1007/BF01106775&link_type=DOI>[CrossRef]<http://www.pnas.org/cgi/content/full/96/11//cgi/external_ref?access_num=A1995RN78600023&link_type=ISI>[ISI].
19. Ma, J. F., Zheng, S. J. & Matsumoto, H.
(1997) Plant Cell Physiol. 38, 1019-1025
<http://www.pnas.org/cgi/content/full/96/11//cgi/ijlink?linkType=ABST&journalCode=pcellphys&resid=38/9/1019>[Abstract/Free<http://www.pnas.org/cgi/content/full/96/11//cgi/ijlink?linkType=ABST&journalCode=pcellphys&resid=38/9/1019>
Full Text].
20. Ma, J. F., Zheng, S. J., Matsumoto, H. &
Hiradate, S. (1997) Nature (London) 390, 569-570
<http://www.pnas.org/cgi/content/full/96/11//cgi/external_ref?access_num=9403684&link_type=MED>[Medline]
.
21. Pan, A., Tie, F., Duau, Z., Yang, M., Wang,
Z., Li, L., Chen, Z. & Ru, B. (1994) Mol. Gen.
Genet. 242, 666-674
<http://www.pnas.org/cgi/content/full/96/11//cgi/external_ref?access_num=8152417&link_type=MED>[Medline]
.
22. Ownby, J. D. & Popham,
H. R. (1989) J. Plant Physiol. 135, 588 - 591.
23. Suhayda, C. G. & Haug,
A. (1986) Physiol. Plant. 68, 189-195 .
24. De la Fuente, J. M., Ramírez-Rodríguez,
V.,
Cabrera-Ponce, J. L. & Herrera-Estrella, L.
(1997) Science 276, 1566-1568
<http://www.pnas.org/cgi/content/full/96/11//cgi/ijlink?linkType=ABST&journalCode=sci&resid=276/5318/1566>[Abstract/Free<http://www.pnas.org/cgi/content/full/96/11//cgi/ijlink?linkType=ABST&journalCode=sci&resid=276/5318/1566>
Full Text].
25. Donald, L. J., Molgat, G. F. & Duckworth, H.
W. (1989) J. Bacteriol. 171, 5542-5550
<http://www.pnas.org/cgi/content/full/96/11//cgi/ijlink?linkType=ABST&journalCode=jb&resid=171/10/5542>[Abstract/Free<http://www.pnas.org/cgi/content/full/96/11//cgi/ijlink?linkType=ABST&journalCode=jb&resid=171/10/5542>
Full Text].
26. Rivera-Bustamante, R. (1997) in Plant
Biotechnology Transfer to Developing Countries,
eds. Altman, D. & Watanabe, S., R. G. (Landes,
Austin, TX).
<http://www.pnas.org/cgi/content/full/96/11//misc/terms.shtml>Copyright
© 1999 by The National Academy of Sciences
0027-8424/99/965978-4$2.00/0
--------------------------
Prof. Dr. Luis Herrera-Estrella
Centro de Investigacion y Estudios
Avanzados, CIEA, Mexico
The Centro de Investigacion y Estudios
Avanzados
(CIEA) is a public institute, financially
supported by the Mexican federal government,
whose mission is to carry out basic research in
plant biology and to apply molecular biology and
genetic engineering techniques for the genetci
improvement of plant species of economical and/or
social importance for Mexico.
[]
The Centro de Investigacion y Estudios
Avanzados
(CIEA) is a public institute, financially
supported by the Mexican federal government,
whose mission is to carry out research and to
train students at the Ms.C. and Ph.D. level. The
Biotechnology Unit of CIEA was created in 1986 to
carry out basic research in plant biology and to
apply molecular biology and genetic engineering
techniques for the genetci improvement of plant
species of economical and/or social importance for Mexico.
Dr. Luis Herrera-Estrella a plant molecular
biologist with ample experience in the
development of plant transformation systems, the
study of gene regulation in plants and the
application of plant genetic engineering
techniques for plant improvement. Dr.
Herrera-Estrella has recently developed a
technology to produce aluminium-resistant
transgenic plants, based on the modification of
the production of organic acids, and has
published over 60 pier reviewed articles in
internationally recognised journals. Dr.
Herrera-Estrella has received awards from the New
York Academy of Science, UNESCO, TWAS and the
Mexican Academy of Sciences for his achievements
in plant biotechnology and was recently elected
as president of the International Society of Plant Molecular Biology.
Cabrera-Ponce, J.L., Lopez,L.,
Assad-Garcia, N.
Medina-Arevalo,C., Bailey, A.M. and
Herrera-Estrella, L. An efficient particle
bombardment system for the genetic transformation
of asparagus (Asparagus officinalis L. ) Plant Cell Rep
16: 255-260 (1997)
De La Fuente J.M., Ramirez-Rodriguez V.,
Cabrera-Ponce J.L. and Luis Herrera-Estrella:
Expression of a bacterial citrate synthase in the
cytoplasm of
transgenic plants leads to
aluminium tolerance. Science 276: 1566-1568. (1997)
Jofre-Garfias,A., Villegas
Sepulveda, N.,
Cabrera-Ponce, J.L., Adame-Alvarez, R.M.,
Herrera-Estrella, L. and Simpson, J.:
Agrobacterium-mediated transformation of
Amaranthus hypochondriacus:
light- and
tissue-specific expression of a pea chlorophyll
a/b-binding protein promoter. Plant Cell Reports 16: 847-852 (1997).
Valdez, M., Cabrera-Ponce, J.L., Sudhakar, D.,
Herrea-Estrella,L and Christou,
P.: Transgenic
Central American, West African and Asian elite
rice varieties resulting from particle
bombardment of foreign DNA into mature
see-derived explants utilizing three different
bombardment devices. Annals of Botany 82: 795-801 (1998)
Curatti, L, Folco, E, Desplats, P, Abratti, G,
Limones, V, Herrera-Estrella,
L, Salerno, G.:
Sucrose-phosphate synthase from Synechocystis
sp.
Strain PCC 6803: Identification of the spsA gene
and characterization of the enzyme expressed in
Escherichia coli. J Bac, Vol.180, No.24, pp.6776-6779. (1998)
De la Fuente-Martinez, JM and Herrera-Estrella,
L.: Advances in the understanding of aluminium
toxicity and the development of
aluminium-tolerant transgenic plants. Advances in
Agronomy, 1999, Vol.66, pp.103-120
Thomas R. DeGregori, Ph.D.
Professor of Economics
University of Houston
Department of Economics
204 McElhinney Hall
Houston, Texas 77204-5019
Ph. 001 - 1 - 713 743-3838
Fax 001 - 1 - 713 743-3798
Email trdegreg@uh.edu
Web homepage http://www.uh.edu/~trdegreg