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Editorial overview: Synthetic plant biology: the roots of a
bio-based society
Birger Lindberg Møller and R George Ratcliffe
Current Opinion in Biotechnology 2014, 26:ix–xvi
For a complete overview see the Issue
0958-1669/$ – see front matter, Published by Elsevier
Ltd.
http://dx.doi.org/10.1016/j.copbio.2014.02.016
Birger Lindberg Møller1,2
1
Department of Plant and Environmental
Sciences, Plant Biochemistry Laboratory,
University of Copenhagen, Denmark
2
Carlsberg Laboratory, Copenhagen, Denmark
e-mail: [email protected],
[email protected]
Birger Lindberg Møller is professor at the Plant
Biochemistry Laboratory, University of Copenhagen
(UCPH). He is Head of the Carlsberg Laboratory,
director of the VILLUM research centre ‘Plant
Plasticity’ and director of the synthetic biology
research centre ‘bioSYNergy’ funded by the UCPH
Excellence Programme for Interdisciplinary Research.
Member of the Danish Council for Research and
Innovation Policy. Recipient of an ERC Advanced
Grant in 2012. Recipient of the VKR Research Prize in
2007, the largest Danish Research Award.
R George Ratcliffe
Department of Plant Sciences, University of
Oxford, United Kingdom
e-mail: [email protected]
R George Ratcliffe is a professor in the Department of
Plant Sciences at the University of Oxford and a Fellow
in Biochemistry at New College, Oxford. He has a longstanding interest in heterotrophic plant metabolism,
particularly mitochondrial metabolism, with a focus on
the organization and function of the central metabolic
network. He uses metabolic flux analysis to measure
and predict the response of metabolic phenotypes to
genetic and abiotic perturbations.
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Humanity faces three major challenges in the 21st century: food security,
availability of renewable energy, and environmental degradation. These
three challenges are inter-linked and plants will be essential in counteracting them with science-based solutions (Figure 1).
All our food is derived from plants, either directly or indirectly via animal
production. The process of photosynthesis enables plants to convert solar
energy into chemical energy in the form of biomass that may be converted
into renewable biofuels. Due to climate change, the need to develop
sustainable robust agricultural systems is of utmost importance to avoid
continued destruction of previously arable land (Figure 2). Inter-disciplinary
research, including constructive engagement and dialogue with politicians,
bio-ethicists, the general public and other stakeholders, is obviously essential in addressing these complex challenges, but excellent research within
plant biology is going to be instrumental. This calls for increased investment
in plant research. Likewise, plant researchers around the globe need to take
charge in spurring the interest of young talented students to choose plant
biology as their favorite discipline.
We are privileged by the numerous technological advances that we have at
our disposal. Entire genome sequences of crop plants are now available at
reasonable cost, transcriptome libraries and proteomics facilitate studies of
developmental and environmental impacts, and bio-imaging techniques
based on electron microscopy and mass spectrometry facilitate elucidation
of plant plasticity. Nevertheless, the challenges to be addressed remain
highly complex and interlinked, while the multidisciplinary approaches that
are required dictate new ways of collaboration to ensure that basic and
applied research is interconnected with engineering, and advanced in ways
acceptable to the end users and thus to the benefit of society. It is ironic that
the technological advances that formed the basis for the Green Revolution in
the 1970s, such as the use of synthetic fertilizers, chemical control of
herbivores and diseases, mechanization and the development of semi-dwarf
high-yielding crop varieties, resulted in overproduction of foods in the
industrialized world, created economic imbalances that caused governmental and private investment in plant research and production to decrease,
especially within the EU. As a consequence, what has been achieved is tiny
in comparison with what could have been done. More humans are alive
today than have ever died, and we are in a situation where we have to make
up for two decades in which solid foundations to address the challenges we
are now facing could have been built. A similar overshoot in plant productivity in the years to come is highly unlikely. A burgeoning middle class,
a wealth-related switch towards animal products, and the use of plant crops
for bioenergy production renders the demand for crop products and biomass
immense (Figure 3). In addition, plant biologists and breeders will face the
Current Opinion in Biotechnology 2014, 26:ix–xvi
x Plant biotechnology
Figure 1
Current Opinion in Biotechnology
Painting by Peter Bruegel the Elder entitled ‘The Harvest’ from 1565. The painting illustrates the labor intensive harvest progressing in a wheat field.
The panoramic view testifies that monocultures have been an important part of food production for centuries and transform the landscape. Note that
the height of the wheat plants almost matched the height of the harvesters. As part of the Green Revolution in the 1970’ the expression of semi-dwarf
genes resulting in less tall plants greatly increased yield.
increasing challenge of developing new crop varieties that
are able to cope with the extreme weather changes
associated with the expected changes in global climate
(Figure 4).
This volume of Current Opinion in Plant Biology provides an overview of current research in areas that are
expected to provide science-based solutions to these
challenges. Future directions of the research within these
areas are outlined as an inspiration to other researchers.
Molecular breeding is the most direct way to gain access
to a desired phenotype and the available tools continue to
evolve under the selection pressures of cost, precision and
scope. Effective genetic screens to identify the single
plant within a large natural population that carries a
specific desired trait and advances within genetic engineering technologies are important complementary
approaches. Plastid transformation is a less established
technology with great promise, and the review by
Current Opinion in Biotechnology 2014, 26:ix–xvi
Bock describes the recent technological developments
that have greatly increased the power of the approach.
This is reflected in the extensive and diverse range of
applications summarized in the article, leading the author
to conclude that the commercialization of the technology
is imminent (Figure 5). It is particularly helpful that
plastid DNA is not transmitted through pollen in most
species, enabling plastid transformation to offer biological
containment of the traits introduced.
Reconfiguring the plant cell extracellular matrix has
emerged as a major objective for the biofuels sector
and four papers review progress in this area. First,
researchers from the Bacic laboratory discuss the unprecedented complex challenges facing plant breeders and
biotechnologists in their efforts to engineer designer
walls. Changing individual components poses a challenge
in itself since the changes have to be compatible with wall
assembly and re-modeling, and with feed-back loops
monitoring cell wall integrity following biotic and abiotic
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Editorial overview: Synthetic plant biology: the roots of a bio-based society Møller, Ratcliffe xi
Figure 2
Current Opinion in Biotechnology
Painting by Henri Rousseau entitled ‘The Dream’ from 1910. This painting features a nude woman surveying the spectacular undestroyed landscape of
lush jungle with stylized flowers and animals. Not a single leaf has been chewed up by an insect! The biodiversity is rich in such an environment and to
survive, the indigenous people living in such habitats need to possess a detailed knowledge of the plants available for food and medication.
Unfortunately, this basic knowledge of the virtues of plants tends to be lost in our industrialized societies as do these kinds of habitats and biodiversity
in general.
challenges. The authors discuss the integrity-sensor role
of the plant cell wall as an additional control level that
needs to be understood to optimize the plant cell wall
properties for specific agro-industrial applications in a
predictable and effective manner.
Secondly, Burton and Fincher discuss the recent advances
in research on the structure and synthesis of cellulosic and
non-cellulosic wall polysaccharides. Efficient conversion
of these constituents from crop plant residues into renewable fuels, and human health benefits derived from ingestion of dietary fibers from cereal grains, are major research
objectives. The resolved three dimensional structure of a
bacterial cellulose synthase guides studies on the plant
enzymes. Plants only tolerate small overall changes in
their cellulose content but are less sensitive to engineering of their non-cellulosic polysaccharides. This offers
promising avenues for development of cereals producing
dietary fibers with increased health benefits.
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Thirdly, Rennie and Scheller outline advances with respect
to the genes involved in xylan biosynthesis, the complex
substitution pattern of the xylan backbone, and with
respect to glycosidase mediated re-modeling of the xylan
polysaccharide and its interactions with other cell wall
polymers. The different pentoses contained within the
xylan polymer are not easily fermented by microorganisms
and their presence presents an obstacle to attempts to
convert biomass into biofuels. Recent attempts to complement mutants deficient in xylan synthesis with functional
versions of the mutated gene under the control of a vesselspecific promoter produced plants with no adverse phenotypic properties, yet with a much reduced xylan content
and thus improved characteristics for biofuel production.
Fourth, the research group of Loque´report on the exciting
work in which researchers have developed more elaborate
approaches for lignin modification and employed tissuespecific promoters to reduce the risk of disturbing other
Current Opinion in Biotechnology 2014, 26:ix–xvi
xii
Plant biotechnology
Figure 3
Current Opinion in Biotechnology
Painting by Vincent van Gogh entitled ‘Enclosed field with rising sun’ from 1889. In this dramatic impressionist painting of a wheat field, van Gogh
expresses his connection to nature and communicates his sense of the meaning of life using wheat fields as a metaphor for the life cycle of humans.
Van Gogh considers photosynthesis as mediated by ‘the good God Sun’. Life should be considered as sowing time and not harvest. Most present day
investors in agriculture and other business fields act like we are always in the harvesting period and so do not make long term investments in the future.
These decisions often fail to recognize how exposed we are to nature’s powerful forces and how dependent humanity is on plants.
phenylpropanoid-derived pathways in non-lignified tissues. Transgenic plants incorporating new lignin monomers and with reduced lignin content in selected tissues
have now been obtained. The synthetic biology and
genome editing approaches used to re-route the lignin
pathway and to introduce new monolignols into the lignin
polymer may also be applicable to attempts to achieve
highly targeted modifications of the cellulose and hemicellulose content. In combination, the research has the
potential to facilitate the design of crops with optimized
lignin, cellulose and hemi-cellulose content and distribution while retaining traits such as physical stability and
defense characteristics.
Microbial biotechnology constitutes an alternative route
to renewable fuels (Figure 5). The research group of Jones
discusses the potential of microbial technology to offer
routes to the production of renewable jet fuels. The
production would encompass microbial synthesis of linear
Current Opinion in Biotechnology 2014, 26:ix–xvi
and branched medium chain length alkanes derived from
fatty acid biosynthesis. The fatty acid would be enzymatically converted into aldehydes and decarboxylated
into alkanes by the action of the recently identified
aldehyde deformylating oxygenase. Optimization of the
activity and stability of this soluble non-heme di-iron
enzyme constitutes a major challenge. It may be possible
to couple photosynthetic electron transport directly to
the alkane producing enzyme system to speed up reaction
rates. If successful this approach will simplify jet fuel
production with major environmental, social and economic
benefits.
Plant growth is another major area that attracts, and
indeed needs, the attention of plant biotechnologists.
Improving nutrient use efficiency and resistance to
abiotic stress remain two of the most important challenges and this special issue highlights work in three
areas.
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Editorial overview: Synthetic plant biology: the roots of a bio-based society Møller, Ratcliffe xiii
Figure 4
UNIVERSITY OF COPENHAGEN
Villum Research Center for Plant Plasticity
Current Opinion in Biotechnology
Breeding of forage sorghum in a field at Toowoomba, Queensland. Forage sorghum is cultivated as fodder for ruminants and is gaining increased
importance because of its drought tolerance and high yield potential. The breeder is bagging the panicles of the sorghum plants with desired
phenotypes to avoid cross-pollination. Photo: Peter Stuart, Toowoomba.
First, Oldroyd and Dixon describe the great strides that
have been made in our understanding of symbiotic nitrogen fixation, particularly in delineating the signaling
pathway that links the perception of a Nod factor by a
root hair to the development of the nodule that harbors
the nitrogen-fixing bacteria in the legume symbiosis.
Sufficient progress has been made to discern how it might
be possible to engineer the entire legume symbiosis itself,
or failing that nitrogenase activity, into cereals. It is not
expected that either option will be easy to implement —
the article mentions a timescale of perhaps two decades — but even incremental progress towards the ultimate goal could lead to a useful gain in productivity on
the many nitrogen poor soils that have been pressed into
agricultural use.
Secondly, Cabello et al. tackle the huge problem of abiotic
stress and provide a compelling holistic analysis that
identifies multiple intervention points throughout the
cascade of events that leads to the response of the plant
to the stresses caused by water shortage, salinity,
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temperature or light. The authors argue that re-engineering the regulatory mechanisms that fine tune or
modulate the stress response offers the best prospect
for increasing stress tolerance without detrimental
effects on growth or development. Multiple engineering
strategies are available and substantial progress has been
made in constructing stress-tolerant genotypes. As a
specific example, introduction of cyanobacterial flavodoxins has been used to complement the loss of ferredoxin that occurs under adverse environmental
conditions leading to improved stress tolerance in
tobacco plants.
In a second article on abiotic stress, Roy et al. look at the
increasing problem of salt stress in agricultural soils. The
article provides a comprehensive account of the many
genes that have been studied in search of salt-tolerance,
including genes for the signaling and regulatory pathways
that mediate the response to salt stress, and highlights the
difficulty of predicting the performance of promising
engineered genotypes under field conditions. It is salutary
Current Opinion in Biotechnology 2014, 26:ix–xvi
xiv Plant biotechnology
Figure 5
Current Opinion in Biotechnology
Systems for sustainable production of medicinal and other high-value compounds in microalgae grown in photo-bioreactors are being developed
using the approaches of synthetic biology. Eventually, these pioneering efforts are expected to offer an alternative to present day production based on
fossil fuels. Photo: Theodor Fahrendorf, NovaGreen, Berlin.
to note that a shortage of quantitative data from field trials
means that it is still not possible to draw conclusions about
the best approach for specific crops. On a more positive
note introgression of a gene that promotes the exclusion
of sodium ions into durum wheat has increased yield by
25% on saline soils, demonstrating that tangible agricultural benefits are emerging from the increased mechanistic understanding of salt stress in plants.
Serendipity apart, and the value of this unpredictable
ingredient should never be underestimated in biotechnology, progress in manipulating the outputs of the plant
metabolic network will continue to depend on an everdeepening understanding of how these complex organisms function in a changing world. Three articles highlight areas in which recent progress has the potential to
influence future plant engineering efforts.
The push-pull farming concept highlights the complexity of the factors that can influence crop productivity in
the field, while at the same time providing an example
of the benefits of translational research. Pickett et al.
provide an update on the development of this very
successful crop protection strategy in sub-Saharan Africa
and discuss ways in which the approach could be
extended to mainstream arable farming. Here the aim
is to refine and extend the concept by using the tools of
plant breeding and engineering to optimize the attractant and repellent properties of the companion plants in
mixed seed beds.
First, in a special issue that happens to be largely devoid
of updates on the manipulation of CO2 assimilation,
Shikanai describes the contribution of cyclic electron
transport around photosystem I to the regulation of
photosynthesis. Recent work has provided mechanistic
insights into the electron transport pathway between
ferredoxin and plastoquinone, and this raises the possibility of being able to control and possibly optimize the
balance between ATP and NADPH production in illuminated leaves. Where this might lead is unclear, but as
the author points out up-regulation of cyclic electron
transport supported by photosystem I is a feature of C4
Current Opinion in Biotechnology 2014, 26:ix–xvi
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Editorial overview: Synthetic plant biology: the roots of a bio-based society Møller, Ratcliffe xv
Figure 6
Current Opinion in Biotechnology
Painting by Paul Gauguin entitled ‘The blue tree trunks’ from 1888. Gauguin spent part of his life at Tahiti to leave civilization and enjoy primitivism.
Juxtaposition of complementary colors has a dramatic effect. The vineyards behind the blue tree trunks span the entire width of the canvas, almost
becoming threatening, and it remains a mystery how the two people in the foreground are going to reach the end of the path at the horizon. As a postimpressionist, Gauguin used nature as a breeding ground and develops it into a synthetic nature from which to abstract figures and models, modules,
symbols and ideas. He states that he does not invent the entire picture. On the contrary, he finds it in nature and only disentangles it and use the
modules in new combinations. This is how synthetic biology should be developed and progress, based on excellent research within plant biology,
inter-disciplinary approaches and aesthetics. In this way we may proceed to the end of the path shown on the painting without causing too much
damage. In ‘‘Notes Synthetiques’’ (c. 1888) Gauguin has expressed why he considers paintings to be composed of more modules in comparison to
any other form of arts.
leaf metabolism that allows the bundle sheath cells to
meet the ATP demand for photosynthesis, and this may
well be a useful strategy for satisfying the bioenergetic
requirements of re-engineered chloroplasts.
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Secondly, Nu¨tzmann and Osbourn provide a timely update
on the identification of increasing numbers of gene clusters that encode the enzymes required for pathways of
specialized metabolism in plants. The biotechnological
Current Opinion in Biotechnology 2014, 26:ix–xvi
xvi Plant biotechnology
significance of these gene clusters is both obvious and
uncertain — obvious in the sense that transformation
with a gene cluster might provide a convenient route to
heterologous expression of a useful metabolite; but
uncertain because the biosynthetic genes usually only
comprise a small fraction of the DNA within a cluster,
raising questions about the functionality or otherwise of
the intervening sequences. The importance of coinheritance to avoid accumulation of toxic intermediates
may be a key factor favoring cluster formation. The
development of methods for the systematic identification of gene clusters in plant genomes and research
into their functional architecture are now pressing
objectives, but this essential underpinning activity
can be expected to run in parallel with a more empirical
analysis of the potential value of both naturally occurring and edited gene clusters for applications in synthetic biology.
Finally, Junker charts recent developments in analyzing
the flux distributions in plant metabolic networks. It is the
metabolic fluxes through the network that deliver the
outputs that biotechnologists seek to optimize, and flux
maps are used routinely in microbial metabolic engineering. It is not so easy to implement the in silico techniques
of constraints-based metabolic modelling or the experimental methods of 13C metabolic flux analysis to multicellular organisms with multiple internal compartments,
but the strategies and protocols continue to evolve and
Junker highlights recent progress that is increasing the
usefulness of the fluxes predicted by flux balance
analysis, and the speed with which flux maps of central
carbon metabolism can be determined from labeling
experiments. These developments increase the likelihood of significant applications in plant metabolic engineering in the foreseeable future.
Conclusion
The approaches needed to address the challenges the
global community is facing with respect to food and
Current Opinion in Biotechnology 2014, 26:ix–xvi
energy supply, while avoiding deterioration of the
environment, will be highly interdisciplinary. Relevant
expertise in the university sector includes genetics, biochemistry, physiology, biotechnology, synthetic biology,
breeding, agronomy, and agricultural engineering. The
private sector companies can stack desired traits in their
large scale breeding programs.
To advance the relevant university research, increased
funding for research on crop plants is essential. University
researchers carrying out fundamental research on model
plants have easy access to high impact plant journals for
their results and thus compete efficiently for grants.
Research on crop plants is typically more time-consuming
and does not offer easy access to the highest impact
journals in the field. Plant biologists working on crop
plants may in theory profit from the results generated
using model plants, but a funding gap has typically
blocked exploitation of the results obtained in model
plants. Neither industry nor the research councils and
universities have shown strong interest in supporting
this time-consuming and costly translational work. Fortunately foundations such as the Bill and Melinda
Gates Foundation have recently undertaken the task of
shepherding basic plant biology research into the development of elite cultivars and products. However,
the potential capabilities for genetic improvement in crop
plants remain poorly exploited.
Plant biology is going to be an essential research discipline in the next few decades (Figure 6). The need for top
researchers to enter the field and to pass on their expertise
and enthusiasm to the next generation through active
teaching efforts and engagement in communication with
society through all relevant media is essential for success.
If we meet these challenges, plant biology will advance at
both the basic and applied levels to the benefit of the
entire global community and future generations. It is
vitally important to be successful. Otherwise the likely
future is grim.
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