Making Hunger Yield C. Robertson McClung Science 344, 699 (2014); DOI: 10.1126/science.1254135
This copy is for your personal, non-commercial use only.
Permission to republish or repurpose articles or portions of articles can be obtained by following the guidelines here. The following resources related to this article are available online at www.sciencemag.org (this information is current as of May 18, 2014 ): Updated information and services, including high-resolution figures, can be found in the online version of this article at: http://www.sciencemag.org/content/344/6185/699.full.html This article cites 15 articles, 9 of which can be accessed free: http://www.sciencemag.org/content/344/6185/699.full.html#ref-list-1 This article appears in the following subject collections: Botany http://www.sciencemag.org/cgi/collection/botany
Science (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by the American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. Copyright 2014 by the American Association for the Advancement of Science; all rights reserved. The title Science is a registered trademark of AAAS.
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PERSPECTIVES PLANT SCIENCE
A combination of approaches to develop crops with improved yields is needed to address the demands of a growing population.
Making Hunger Yield C. Robertson McClung
CREDIT: IRRI/FLICKR
T
he human population reached 1 billion in the early 1800s, roughly 12,000 years after the dawn of agriculture. However, exponential growth in the ensuing 200 years resulted in the global population exceeding 7 billion, placing enormous demands on modern agriculture. Over the past half-century, the human population has doubled but food production has more than kept pace, and the fraction of people with insufficient food has declined dramatically, from 60% in 1960 to about 15% in 2010 (1), Nonetheless, ~1 billion people remain chronically underfed and another ~2 billion suffer from micronutrient deficiencies (1, 2). It is imperative, then, to accelerate increases in agricultural production. Although the human growth rate peaked in the early 1960s, the human population is still growing and will likely plateau at around 9 billion in the middle of this century (3). Associated with this decline in growth rate is increased wealth, which boosts demand for preferred cereals such as wheat and rice and subsequently, for meat, fish, and dairy products (1). Thus, growth in population and in per capita consumption will require continued increase in agricultural production, necessitating an estimated doubling of crop production between 2005 and 2050 (4). Multiple issues compound the challenge of increasing food production. The focus will likely be on a limited set of crops, as there is a trend to homogenize the global food supply (5). Thus, the sources of larger yields must be found within or developed from a reduced base of genetic and agronomic diversity. In addition, a sizable fraction of the available arable land is lost each year to development, salinity, or nutritional degradation, and simply cultivating more land is unattractive due to the release of greenhouse gases associated with the conversion of new land into agriculture (2). There is also a need to make agriculture more sustainable—excess water use, unsustainable soil management, and fertilizer leaching all must be addressed (2). Moreover, climate change, particularly rising temperatures, is likely to slow increases in agricultural production (6). Department of Biological Sciences, Dartmouth College, Hanover, NH, USA. E-mail: c.robertson.mcclung@ dartmouth.edu
Overachieving crop. Submergent-tolerant rice was generated through DNA marker–assisted breeding (15).
Given the enormity of the challenge, it is instructive to examine the reasons behind the dramatic rise in agricultural yield over the past 70 years. The manipulation of plant architecture has been a major focus. The “Green Revolution” between the 1940s and 1960s saw the development of wheat varieties that combined resistance to rust fungus with semi-dwarfism. Shorter, stronger stems boosted grain yield from increased nitrogen inputs, and permitted increased allocation of biomass to the seed rather than the vegetative parts (harvest index) without lodging (collapse of the stem when it can no longer support the seed weight) (7). A similar strategy produced greater rice and maize yields. In part, these increases resulted from nitrogen fertilization, but another key factor has been a steady rise in planting densities. Newer varieties do not yield more grain per plant, but greater planting density yields more grain per field. A critical contribution of genetic improvement through conventional breeding has been the ability of newer varieties to tolerate the biotic and abiotic stresses associated with increased planting density (8). These advances were achieved without knowledge of the molecular mechanisms responsible for the improvements in plant growth and productivity. However, it is now known that the reduced plant stature of wheat
and rice resulted from alterations in hormone signaling pathways (7). Understanding the underlying molecular mechanism(s) and alleles (alternate versions of the same gene) that confer trait(s) of interest makes possible the determination of combinations of alleles from multiple genes that confer the desired combination of traits in a single plant variety. This DNA-marker-assisted breeding has been enabled by genomic technologies that facilitate the integration of highthroughput determination of allele combinations (genotyping) with high-throughput trait measurement (phenotyping) (9). This approach allows efficient genetic identification of plants that carry desired traits and is now being used to improve maize, rice, soybean, and wheat (see the figure). The availability of genomic resources enables conventional breeding, but also transgenic modification. The introduction of a single transgene (a gene from a different organism or a modified version of a gene from the same organism) can confer a desired property, such as herbicide or pest resistance; without appropriate control measures, crop losses to diseases, weeds, and pests, both before and after harvest, can total 50% or more (10). By conventional breeding, individual resistance genes are introduced from wild varieties, but resistance often
www.sciencemag.org SCIENCE VOL 344 16 MAY 2014 Published by AAAS
699
PERSPECTIVES breaks down rapidly as the pests or pathogens evolve to evade or overcome the resistance gene. Transgenic approaches allow the simultaneous introduction of multiple different resistance genes (stacking) into a single plant variety, which generates more durable resistance in a desired variety. This strategy is analogous to the use of drug combinations (cocktails) when treating diseases like tuberculosis and HIV infection, and has proven effective both in disease treatment and in preventing the emergence of multidrugresistant bacteria and viruses. Transgenic modification also permits the alteration of specific biochemical pathways and genetic networks. Examples can be found among efforts to enhance nutrition, including the genetic modification of “golden rice” to increase its beta-carotene content (11). The overexpression of a transcription factor from the flowering plant Arabidopsis thaliana in soybean dramatically boosts grain yield by extending the length of time of vegetative development. The result is a larger plant capable of supporting greater seed yield (12). Improved water-use and nitrogen-use efficiencies are attractive targets to increase yields while
reducing unsustainable inputs such as irrigation water and nitrogen fertilizer (6). More audacious goals include the transgenic engineering of rice (and other C3 crops) to introduce C4 metabolism—a more efficient carbon fixation pathway—and thereby increase photosynthetic capacity (13). Although the “intelligent breeding” approach that is guided by DNA markers has been much less controversial, there remains considerable public opposition to the deployment of genetically modified organisms (GMOs), especially in the food supply. One consequence has been the focus of regulatory agencies on the technology to develop the plant rather than on the properties of the engineered plant itself. This regulatory morass has delayed the availability of golden rice more than a decade at a probable cost of tens of millions of lives (6, 14). Efforts to address concerns about the safety of GMOs have chiefly focused on evidencebased refutation of claims of real and potential adverse outcomes (6), but have not alleviated concerns. The scientific community is understandably reluctant to move beyond evidence-based logic, but must explore new approaches to advocate GMOs.
In seeking new crops to sustainably feed an expanding world population, there is compelling need for a multipronged approach that includes traditional breeding, molecular breeding, and genetic modification. We need to accelerate this new green revolution in the lab, in the field, and through better communication outside the scientific community if we are to address the nearly 3 billion chronically undernourished people worldwide. References 1. H. C. J. Godfray et al., Science 327, 812 (2010). 2. H. C. J. Godfray, T. Garnett, Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20120273 (2014). 3. W. Lutz, S. K C, Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 2779 (2010). 4. D. Tilman, C. Balzer, J. Hill, B. L. Befort, Proc. Natl. Acad. Sci. U.S.A. 108, 20260 (2011). 5. C. K. Khoury et al., Proc. Natl. Acad. Sci. U.S.A. 111, 4001 (2014). 6. N. V. Fedoroff et al., Science 327, 833 (2010). 7. P. Hedden, Trends Genet. 19, 5 (2003). 8. D. N. Duvick, Maydica 50, 193 (2005). 9. L. Cabrera-Bosquet et al., J. Integr. Plant Biol. 54, 312 (2012). 10. J. D. G. Jones et al., Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20130087 (2014). 11. T. Johns, P. B. Eyzaguirre, Food Policy 32, 1 (2007). 12. S. B. Preuss et al., PLOS ONE 7, e30717 (2012). 13. S. von Caemmerer et al., Science 336, 1671 (2012). 14. B. Alberts et al., Science 341, 1320 (2013). 15. J. Bailey-Serres et al., Rice 3, 138 (2010). 10.1126/science.1254135
GEOPHYSICS
Recognizing Foreshocks from the 1 April 2014 Chile Earthquake
Seismic activity preceding recent large earthquakes, including the 1 April 2014 earthquake in Chile, hints that some large earthquakes may potentially be predictable.
Emily E. Brodsky and Thorne Lay
A
re there measurable, distinctive precursors that can warn us in advance of the planet’s largest earthquakes? Foreshocks have long been considered the most promising candidates for predicting earthquakes. At least half of large earthquakes have foreshocks, but these foreshocks are difficult or even impossible to distinguish from non-precursory seismic activity. The foreshocks for the 1 April 2014 Chile event and other recent large earthquakes suggest that observable precursors may exist before large earthquakes. Statistical models of interacting earthquakes suggest that big earthquakes are most likely to happen when regional earthquake activity is already high (1–4). However, the same models also indicate that the Department of Earth and Planetary Sciences, University of California, Santa Cruz, CA 95064, USA. E-mail: brodsky@ pmc.ucsc.edu; [email protected]
700
probability of any given earthquake being a foreshock is low, because small earthquakes are often not followed by large ones. Data for the 2011 Mw 9.0 Tohoku, Japan, earthquake suggest that detectable precursory processes may occur for some large plate boundary earthquakes. Twentythree days before the earthquake, a series of smaller earthquakes began, migrating toward the future mainshock hypocentral region at a rate of several kilometers per day; then, 2 days before the mainshock, a Mw 7.3 earthquake struck within 10 km of the mainshock nucleation site (see the figure, panel A). Data from geodetic instruments recovered from the sea floor after the Mw 9.0 earthquake showed that the fault had slipped slowly during the foreshock sequence (5, 6). No additional slow slip was detected on the fault immediately before the mainshock (7). Bouchon et al. have recently suggested that ~70% of interplate earthquakes are preceded
by similar sequences extending to months prior to mainshocks (8). It seems that some large earthquakes might be predictable. This newfound optimism is tempered by two major scientific and practical concerns. First, it remains difficult to distinguish elevated earthquake activity prior to a mainshock from earthquake swarms that do not culminate in a major event (9). The foreshocks of Tohoku may have been a random cluster that then triggered the mainshock (10). If so, the predictive value of the foreshocks is limited because such random clusters will often not trigger large mainshocks. However, the slow slip inferred from the seafloor geodetic data is a more widespread, and hence potentially more predictable, precursory process. Unfortunately, the sea-floor data are too sparse to allow a unique interpretation of the apparent slip. The scarcity of ocean floor measurements highlights the second, practical bar-
16 MAY 2014 VOL 344 SCIENCE www.sciencemag.org Published by AAAS
This copy is for your personal, non-commercial use only.
Permission to republish or repurpose articles or portions of articles can be obtained by following the guidelines here. The following resources related to this article are available online at www.sciencemag.org (this information is current as of May 18, 2014 ): Updated information and services, including high-resolution figures, can be found in the online version of this article at: http://www.sciencemag.org/content/344/6185/699.full.html This article cites 15 articles, 9 of which can be accessed free: http://www.sciencemag.org/content/344/6185/699.full.html#ref-list-1 This article appears in the following subject collections: Botany http://www.sciencemag.org/cgi/collection/botany
Science (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by the American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. Copyright 2014 by the American Association for the Advancement of Science; all rights reserved. The title Science is a registered trademark of AAAS.
Downloaded from www.sciencemag.org on May 18, 2014
If you wish to distribute this article to others, you can order high-quality copies for your colleagues, clients, or customers by clicking here.
PERSPECTIVES PLANT SCIENCE
A combination of approaches to develop crops with improved yields is needed to address the demands of a growing population.
Making Hunger Yield C. Robertson McClung
CREDIT: IRRI/FLICKR
T
he human population reached 1 billion in the early 1800s, roughly 12,000 years after the dawn of agriculture. However, exponential growth in the ensuing 200 years resulted in the global population exceeding 7 billion, placing enormous demands on modern agriculture. Over the past half-century, the human population has doubled but food production has more than kept pace, and the fraction of people with insufficient food has declined dramatically, from 60% in 1960 to about 15% in 2010 (1), Nonetheless, ~1 billion people remain chronically underfed and another ~2 billion suffer from micronutrient deficiencies (1, 2). It is imperative, then, to accelerate increases in agricultural production. Although the human growth rate peaked in the early 1960s, the human population is still growing and will likely plateau at around 9 billion in the middle of this century (3). Associated with this decline in growth rate is increased wealth, which boosts demand for preferred cereals such as wheat and rice and subsequently, for meat, fish, and dairy products (1). Thus, growth in population and in per capita consumption will require continued increase in agricultural production, necessitating an estimated doubling of crop production between 2005 and 2050 (4). Multiple issues compound the challenge of increasing food production. The focus will likely be on a limited set of crops, as there is a trend to homogenize the global food supply (5). Thus, the sources of larger yields must be found within or developed from a reduced base of genetic and agronomic diversity. In addition, a sizable fraction of the available arable land is lost each year to development, salinity, or nutritional degradation, and simply cultivating more land is unattractive due to the release of greenhouse gases associated with the conversion of new land into agriculture (2). There is also a need to make agriculture more sustainable—excess water use, unsustainable soil management, and fertilizer leaching all must be addressed (2). Moreover, climate change, particularly rising temperatures, is likely to slow increases in agricultural production (6). Department of Biological Sciences, Dartmouth College, Hanover, NH, USA. E-mail: c.robertson.mcclung@ dartmouth.edu
Overachieving crop. Submergent-tolerant rice was generated through DNA marker–assisted breeding (15).
Given the enormity of the challenge, it is instructive to examine the reasons behind the dramatic rise in agricultural yield over the past 70 years. The manipulation of plant architecture has been a major focus. The “Green Revolution” between the 1940s and 1960s saw the development of wheat varieties that combined resistance to rust fungus with semi-dwarfism. Shorter, stronger stems boosted grain yield from increased nitrogen inputs, and permitted increased allocation of biomass to the seed rather than the vegetative parts (harvest index) without lodging (collapse of the stem when it can no longer support the seed weight) (7). A similar strategy produced greater rice and maize yields. In part, these increases resulted from nitrogen fertilization, but another key factor has been a steady rise in planting densities. Newer varieties do not yield more grain per plant, but greater planting density yields more grain per field. A critical contribution of genetic improvement through conventional breeding has been the ability of newer varieties to tolerate the biotic and abiotic stresses associated with increased planting density (8). These advances were achieved without knowledge of the molecular mechanisms responsible for the improvements in plant growth and productivity. However, it is now known that the reduced plant stature of wheat
and rice resulted from alterations in hormone signaling pathways (7). Understanding the underlying molecular mechanism(s) and alleles (alternate versions of the same gene) that confer trait(s) of interest makes possible the determination of combinations of alleles from multiple genes that confer the desired combination of traits in a single plant variety. This DNA-marker-assisted breeding has been enabled by genomic technologies that facilitate the integration of highthroughput determination of allele combinations (genotyping) with high-throughput trait measurement (phenotyping) (9). This approach allows efficient genetic identification of plants that carry desired traits and is now being used to improve maize, rice, soybean, and wheat (see the figure). The availability of genomic resources enables conventional breeding, but also transgenic modification. The introduction of a single transgene (a gene from a different organism or a modified version of a gene from the same organism) can confer a desired property, such as herbicide or pest resistance; without appropriate control measures, crop losses to diseases, weeds, and pests, both before and after harvest, can total 50% or more (10). By conventional breeding, individual resistance genes are introduced from wild varieties, but resistance often
www.sciencemag.org SCIENCE VOL 344 16 MAY 2014 Published by AAAS
699
PERSPECTIVES breaks down rapidly as the pests or pathogens evolve to evade or overcome the resistance gene. Transgenic approaches allow the simultaneous introduction of multiple different resistance genes (stacking) into a single plant variety, which generates more durable resistance in a desired variety. This strategy is analogous to the use of drug combinations (cocktails) when treating diseases like tuberculosis and HIV infection, and has proven effective both in disease treatment and in preventing the emergence of multidrugresistant bacteria and viruses. Transgenic modification also permits the alteration of specific biochemical pathways and genetic networks. Examples can be found among efforts to enhance nutrition, including the genetic modification of “golden rice” to increase its beta-carotene content (11). The overexpression of a transcription factor from the flowering plant Arabidopsis thaliana in soybean dramatically boosts grain yield by extending the length of time of vegetative development. The result is a larger plant capable of supporting greater seed yield (12). Improved water-use and nitrogen-use efficiencies are attractive targets to increase yields while
reducing unsustainable inputs such as irrigation water and nitrogen fertilizer (6). More audacious goals include the transgenic engineering of rice (and other C3 crops) to introduce C4 metabolism—a more efficient carbon fixation pathway—and thereby increase photosynthetic capacity (13). Although the “intelligent breeding” approach that is guided by DNA markers has been much less controversial, there remains considerable public opposition to the deployment of genetically modified organisms (GMOs), especially in the food supply. One consequence has been the focus of regulatory agencies on the technology to develop the plant rather than on the properties of the engineered plant itself. This regulatory morass has delayed the availability of golden rice more than a decade at a probable cost of tens of millions of lives (6, 14). Efforts to address concerns about the safety of GMOs have chiefly focused on evidencebased refutation of claims of real and potential adverse outcomes (6), but have not alleviated concerns. The scientific community is understandably reluctant to move beyond evidence-based logic, but must explore new approaches to advocate GMOs.
In seeking new crops to sustainably feed an expanding world population, there is compelling need for a multipronged approach that includes traditional breeding, molecular breeding, and genetic modification. We need to accelerate this new green revolution in the lab, in the field, and through better communication outside the scientific community if we are to address the nearly 3 billion chronically undernourished people worldwide. References 1. H. C. J. Godfray et al., Science 327, 812 (2010). 2. H. C. J. Godfray, T. Garnett, Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20120273 (2014). 3. W. Lutz, S. K C, Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 2779 (2010). 4. D. Tilman, C. Balzer, J. Hill, B. L. Befort, Proc. Natl. Acad. Sci. U.S.A. 108, 20260 (2011). 5. C. K. Khoury et al., Proc. Natl. Acad. Sci. U.S.A. 111, 4001 (2014). 6. N. V. Fedoroff et al., Science 327, 833 (2010). 7. P. Hedden, Trends Genet. 19, 5 (2003). 8. D. N. Duvick, Maydica 50, 193 (2005). 9. L. Cabrera-Bosquet et al., J. Integr. Plant Biol. 54, 312 (2012). 10. J. D. G. Jones et al., Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20130087 (2014). 11. T. Johns, P. B. Eyzaguirre, Food Policy 32, 1 (2007). 12. S. B. Preuss et al., PLOS ONE 7, e30717 (2012). 13. S. von Caemmerer et al., Science 336, 1671 (2012). 14. B. Alberts et al., Science 341, 1320 (2013). 15. J. Bailey-Serres et al., Rice 3, 138 (2010). 10.1126/science.1254135
GEOPHYSICS
Recognizing Foreshocks from the 1 April 2014 Chile Earthquake
Seismic activity preceding recent large earthquakes, including the 1 April 2014 earthquake in Chile, hints that some large earthquakes may potentially be predictable.
Emily E. Brodsky and Thorne Lay
A
re there measurable, distinctive precursors that can warn us in advance of the planet’s largest earthquakes? Foreshocks have long been considered the most promising candidates for predicting earthquakes. At least half of large earthquakes have foreshocks, but these foreshocks are difficult or even impossible to distinguish from non-precursory seismic activity. The foreshocks for the 1 April 2014 Chile event and other recent large earthquakes suggest that observable precursors may exist before large earthquakes. Statistical models of interacting earthquakes suggest that big earthquakes are most likely to happen when regional earthquake activity is already high (1–4). However, the same models also indicate that the Department of Earth and Planetary Sciences, University of California, Santa Cruz, CA 95064, USA. E-mail: brodsky@ pmc.ucsc.edu; [email protected]
700
probability of any given earthquake being a foreshock is low, because small earthquakes are often not followed by large ones. Data for the 2011 Mw 9.0 Tohoku, Japan, earthquake suggest that detectable precursory processes may occur for some large plate boundary earthquakes. Twentythree days before the earthquake, a series of smaller earthquakes began, migrating toward the future mainshock hypocentral region at a rate of several kilometers per day; then, 2 days before the mainshock, a Mw 7.3 earthquake struck within 10 km of the mainshock nucleation site (see the figure, panel A). Data from geodetic instruments recovered from the sea floor after the Mw 9.0 earthquake showed that the fault had slipped slowly during the foreshock sequence (5, 6). No additional slow slip was detected on the fault immediately before the mainshock (7). Bouchon et al. have recently suggested that ~70% of interplate earthquakes are preceded
by similar sequences extending to months prior to mainshocks (8). It seems that some large earthquakes might be predictable. This newfound optimism is tempered by two major scientific and practical concerns. First, it remains difficult to distinguish elevated earthquake activity prior to a mainshock from earthquake swarms that do not culminate in a major event (9). The foreshocks of Tohoku may have been a random cluster that then triggered the mainshock (10). If so, the predictive value of the foreshocks is limited because such random clusters will often not trigger large mainshocks. However, the slow slip inferred from the seafloor geodetic data is a more widespread, and hence potentially more predictable, precursory process. Unfortunately, the sea-floor data are too sparse to allow a unique interpretation of the apparent slip. The scarcity of ocean floor measurements highlights the second, practical bar-
16 MAY 2014 VOL 344 SCIENCE www.sciencemag.org Published by AAAS
