Green Biotechnology for Food Security in Climate ChangeKevan MA Gartland and Jill S Gartland, Glasgow Caledonian University, Glasgow, Scotland

� 2016 Elsevier Inc. All rights reserved.

Climate Change and Food Security 1Green Biotechnology and Food Security 2Green Biotechnology Crops 2Drought Tolerance 3Salt Stress and Flooding Tolerance 6Emergent Technologies for Regulating Gene Expression in Food Crops 6Attitudes, Needs, and the Future 7References 8

Climate Change and Food Security

Climate change effects include rising temperatures and increasingly frequent extreme weather events including drought, storms, orflooding (FAO, 2014). Negative impacts on agricultural and aquacultural productivity including food crops, livestock, forestry, andfisheries are inevitable. Climate change is sometimes referred to as ‘global warming,’ although it more accurately also includes theincreasing frequency of extreme weather events and unusual variations in weather patterns. Climate change effects where and howparticular types of food can be produced, pre- and postharvest losses, and the effective range of pathogens. Nutritional properties,such as mineral and vitamin content of foods, are also likely to be affected. Quantitative estimates of the effects of climate changeinclude a 4 �C rise in mean global temperatures by 2060, which will impact greatly on yields of global crops such as rice, wheat,maize, and soya (IPCC, 2014).

Food security encompasses the ability of all people, at all times to have physical and economic access to sufficient, safe, andnutritious food to meet their dietary needs and food preferences for an active and healthy life (FAO, 2014). Four dimensions offood security have been identified, as outlined in Table 1 (Ruane and Sonnino, 2011).

More than 925 million people will be undernourished by 2020, including 16% of developing country populations. This startlingneed, combined with 40% of the global population relying on agriculture for some or all of their income (Yashveer et al., 2015;Federoff, 2015), means that climate change is probably the biggest threat to global food security. Gradual temperature increasesand extreme weather events will lead to declining yields, increased soil degradation, and pollution through nitrogen runoff asincreasing use is made of chemical fertilizers to prop up food production (Godfrey and Garnett, 2014). Wheat yields globallyhave already begun to decline (Figure 1; Goldenberg, 2014), and forecasts for sub-Saharan Africa of 22% wheat, 14% rice, and5% maize yield decreases by 2050 (Fernandez, 2011) demonstrate the scale of the threat to food security posed by climate change.

Opportunities for mitigation include enhancing adaptation to the progressive effects of climate change, better management ofglobal warming–related agricultural risks, crop substitution in altered environments, agricultural intensification, and reducingdeforestation for agricultural purposes (Vermeulen et al., 2012). Although seemingly counterintuitive, reducing deforestation by10% can save 500 million tonnes CO2 equivalents emissions over 5 years and keep more land available for food production (Smithet al., 2008).

Table 1 Dimensions of food security

Food security dimension Examples

Food availability Production and processing, tradeAccess to food Marketing and transport, incomes and buying powerUtilization of food Health status, nutritious food choices, food quality and

safety, clean water and sanitationFood system stability Ensuring physical and economic access

Sources: Food and Agriculture Organisation of the United Nations, 2011. Climate Change, Water and FoodSecurity. FAO. Water Report 36; Food and Agriculture Organisation of the United Nations, 2014. FAO SuccessStories on Climate Smart Agriculture. FAO. I3871E/1/05.14. www.fao.org/climatechange/climatesmart; Ruane,J., Sonnino, A., 2011. Agricultural biotechnologies in developing countries and their possible contribution tofood security. J. Biotechnol. 156, 356–363.

Reference Module in Food Sciences http://dx.doi.org/10.1016/B978-0-08-100596-5.03071-7 1

Green Biotechnology and Food Security

Biotechnology uses any biological systems, living organisms, or derivatives to make or modify products or processes for specific use(United Nations Convention on Biodiversity, 1992). When applied to agricultural processes, this is known as green biotechnology.Among the approaches being used in combating climate change to ensure food security, sustainable intensification and climatesmart agriculture are globally relevant. Sustainable intensification seeks to increase food production from a decreased land areathrough greater intensification and enhanced extensification of land being used in agriculture (Godfray and Garnett, 2014).Achieving this will involve ecological, genetic, and market intensification. Climate smart agriculture seeks to use breeding, techno-logical, and policy tools to increase the sustainability and resilience of food production systems; reduce greenhouse gas emissions;and enhance achievement of national food security and development goals (Conway, 2012). Green biotechnology is making signif-icant contributions to combating climate change. This contribution includes the use of technology in everything from conventionalbreeding and marker-aided selection to genetic modification and the application of genomics in agriculture. Marker-aided selectionuses a morphological, biochemical, or DNA/RNA variation markers for indirect selection or determination of an interesting trait.Examples of such traits include yield, grain size, disease resistance, stress tolerance, or some aspect of quality. Genomics appliesnucleic acids (DNA or RNA), sequencing recombinant DNA, or other bioinformatics approaches to the structure and function ofgenomes. Recent progress in agricultural genomics includes the sequencing of 65% of the complex and gene dense barley (Hordeumvulgare, Figure 2) genome by the International Barley Sequencing Consortium (Munoz-Amitriain et al., 2015).

Green Biotechnology Crops

The application of biotechnology to agriculture offers a wide range of potential advantages in aiding food security. Examples ofthese green biotechnology advantages are outlined in Table 2. Attaining the full potential of green biotechnology for food security,

Figure 2 Barley, Hordeum vulgare. Source: WikiCommons.

Figure 1 Durum wheat grains. Source: USDA Photo Services.

2 Green Biotechnology for Food Security in Climate Change

for example, through sustainable intensification and climate smart agriculture requires lessons from the first agricultural ‘green revo-lution’ to be learned (Borlaug, 2000, 2003; McKenzie and Williams, 2015). Climate change affects food production and food secu-rity globally. Temperate regions are experiencing the impact of climate change earlier than previously thought (IPCC, 2014). Whenthese changes are allied to rising global population, forecast to increase from the current 7.2 to 9.6 billion by 2050 (Federoff, 2015),expectations of 70% more food being needed appear realistic (Bruce, 2011) and the challenge to food security becomes greater(Federoff, 2015). Green biotechnology can make a valuable contribution to meeting increased food needs, through its variousforms, including genetic modification, alongside conventional and organic forms of agriculture. No single approach or agriculturalmodel can, however, be a panacea, as the needs and environments of populations around the world differ so widely.

Biotechnology crops were grown in 28 countries by more than 18 million farmers on 181 million ha in 2014, an increase of3.5% on 2013. Ninety percent of these were small, poorly resourced farmers (James, 2014). The largest plantings rangedfrom 73.1 million ha of biotechnology crops (food crops plus cotton) in the United States to 42.2 million ha in Brazil and24.3 million ha in Argentina. 20 of the 28 countries involved are developing nations, with the smallest planting being �2 haof brinjal (aka aubergine or eggplant) expressing Bacillus thuringiensis (Bt) toxins for insect resistance planted in Bangladesh,being 1 of 7 Asian countries adopting biotechnology crops (ISAAA, 2014b). Within the European Union, 5 of the 28 memberstates planted biotech maize (Figure 3), typically Bt traits (Figure 4; James, 2014). Selected current developments and applica-tions of green biotechnology to food crops will now be considered.

Drought Tolerance

Rising temperatures and increased competition for available water are important challenges for agriculture, accounting for approx-imately 70% of global water use. Extended drought yield losses can exceed 40% in rice, being particularly severe in South and South-east Asia, where 23 million ha of rice is rainfed (Figure 5; IRRI, 2015), yet requires 3000–5000 l of water to produce 1 kg of rice seed(Todaka et al., 2015).

Drought tolerance is regulated by many small-effect genetic loci, while hundreds of genes are involved in physiologicalresponses to drought (Hu and Xiong, 2014). Unraveling and manipulating drought perception, transduction ofdrought-related signals and adaptation mechanisms for increased food security remains a long-term goal (Reyes, 2009).Short-duration indica rice varieties such as Sahbhagi Dhan (literally ‘bred by collaboration’), released in India in 2010, havedelivered yield gains of 0.8–1.0 tonnes ha�1 (Dar et al., 2014). While conventional breeding has made some progress in devel-oping drought-tolerant hybrids, progress has been quickened using biotechnological tools, including marker-aided selection,genomics, and genetic modification. Transgenic rice expressing the CaMsrB2 gene performs equivalently to unmodified Ilmirice in unstressed conditions (Dhungana et al., 2015), while the Oshox24 drought-responsive promoter is a strong candidatefor drought-inducible gene expression in rice (Nakashima et al., 2014). Overexpressing the rice quantitative trait locus DeeperRooting 1 (DRO1) increased rooting depth when backcrossed into shallow rooting rice genotypes to increase yield under drought

Table 2 Contributions of green biotechnology to food security

Contribution Example References

Food production increased 33 000 tonnes drought-tolerant maize seed, providing upto 25% yield advantage under water-stressedconditions, distributed in 2013 by Drought Tolerancefor Africa Project

Abate (2014) and Zilberman et al. (2014)

Overexpression TaNF-YB4 gene in transgenic wheatimproves grain yield in 775 l containerized trials

Yadav et al. (2015)

Yield losses reduced Papaya resistant to ringspot virus Gonsalves and Gonsalves (2014) and Bruce (2011)Increased intensification Potato intensification Katoh et al. (2014) and Masiga et al. (2014)Agricultural water use reduced Drought-tolerant maize hybrids increase water use

efficiency by up to 30%Haoa et al. (2015)

Reduced soil physical damage Low/no tilling crops led to 25.9 billion kg additional soilcarbon sequestration in 2013

James (2014)

Greenhouse gas emissionsdecreased

Reduced tractor usage for tilling, spraying, irrigatingreduced CO2 emissions by 2.1 billion kg in 2013

Brookes and Barfoot (2015)

Breeding cycle time reduced Marker-aided selection, genomics Munoz-Amitriain et al. (2015)Insecticide use decreased 7.6 kilotonnes reduction in insecticide use for 2012 from

insect-resistant maizeBrookes and Barfoot (2014) and Mutuc et al. (2011)

Herbicide use decreased 203 million kg herbicide use reduction byherbicide-tolerant maize farmers 1996–2013

ISAAA (2014a)

Enhanced adaptation Drought-tolerant ‘DroughtGard’ maize planting in the USAincreased 5.5 � in 2014

James (2014)

Improved nutritional properties Pro-vitamin A in ‘Golden Rice’ Bollineni et al. (2014) and Tang et al. (2009)

Green Biotechnology for Food Security in Climate Change 3

Figure 3 Maize, Zea mays. Source: USDA Photo Services.

Figure 4 European Corn borer on maize leaf. Source: USDA Photo Services.

Figure 5 Rice, Oryza sativa. Source: USDA Photo Services.

4 Green Biotechnology for Food Security in Climate Change

stress conditions (Uga et al., 2013). DRO1 encourages downward root growth and is the first crop root quantitative trait locus tobe cloned and overexpressed in this way.

Genuity DroughtGard�maize expressing the Bacillus subtilis CspB RNA chaperone has been marketed since 2013, delivering upto 51 kg ha�1 yield enhancements (Morsy, 2015). Expressing rice trehalose-6-phosphate phosphatase in developing maize ears,under the regulation of the Mads6 promoter, reduced trehalose-6-phosphate concentration, which influences maize growth anddevelopment and increased ear spikelet sucrose concentration. Multiseason and multilocation field data demonstrated thattrehalose-6-phosphate overexpression in this way improved kernel set and harvest index, with 9–49% yield increases under non-drought or mild drought conditions and 31–123% under severe drought conditions (Nuccio et al., 2015).

Integrating findings from marker-aided selection and quantitative trait loci with genomic sequences including single nucleotidepolymorphism variations will enhance drought resistance breeding. DNA chip, microarray, and whole genome transcript profilingapproaches have increased the numbers of drought-responsive genes identified (Hu and Xiong, 2014). Extensive microarray anal-ysis of four drought-tolerant and drought-sensitive rice varieties identified 413 shared upregulated and 245 common downregu-lated genes in response to drought stress (Degenkolbe et al., 2009). Comparing drought or abscisic acid–treated sorghumtranscripts with model and major crop transcript databases revealed 50 novel drought-responsive genes (Dugas et al., 2011). Pro-teomic and metabolomic profiling have allowed 60 proteins and 37 differentially expressed metabolites to be identified indrought-stressed rice seedlings (Shu et al., 2011), while 8 metabolites were positively correlated with drought stress among21 rice cultivars (Degenkolbe et al., 2013). Epigenetic analysis of genome-wide DNA methylation patterns in rice identifiedmore than 5400 drought-responsive genes, with 75% of the chromatin folding and remodeling genes identified being downregu-lated (Shaik and Ramakrishna, 2012). MicroRNAs, short, 22-nucleotide-long single-stranded sequences, are also believed to beinvolved in regulating stress responses at the molecular level. Taken collectively, these findings illustrate the complexity, diversity,and partial nature of drought-related response knowledge from food crops (Hu and Xiong, 2014). Examples of drought responsecandidate genes, many of which were identified by integrating genomics and transgenic approaches, are shown in Table 3.

The genetically modified drought-tolerant maize MON87460 expressing cold shock Protein B, currently approved in 13 coun-tries and the European Union, and deployed in Canada, the United States, and Japan, is delivering up to 20% increased yieldsunder water-stressed conditions (Heinemann, 2013; Sammons et al., 2014; Nemali et al., 2015; ISAAA, 2015). Marker-aidedselection is widely deployed in the Water Efficient Maize for Africa project, with support from the Howard G. Buffet and Bill& Melinda Gates Foundations in sub-Saharan Africa (ISAAA, 2008; Fisher et al., 2015). Enhancing soil water extraction potentialand water use efficiency through marker-aided selection has increased grain yield by up to 24% in American drought-tolerantmaize trials (Hao et al., 2015). Combining precise knowledge of phenotypic properties with the use of genomic and trait archi-tecture data will continue to enhance maize hybrid yields incrementally (Cooper et al., 2014). Drought tolerance controlnetworks involve transcription factors, protein kinases, receptor-like kinases, and osmoprotectants, among other mechanisms(Todaka et al., 2015; see Table 3). Use of dehydration-responsive element-binding factors (Chen et al., 2013) such as OsDREB1Aenhances tolerance to a range of environmental stresses, including drought, and salt tolerance, from Australian rice trials(Hussain et al., 2014). Drought tolerance also involves increased production and vacuolar storage of a range of solutes, includingproline, glycine-betaine, mannitol, and trehalose to try and maintain water balance. Leaf wilting, abscisic acid–related stomatalclosure, and altered photosynthesis patterns are also used to decrease transpiration water losses, along with altered root growthpatterns to search for more water (ISAAA, 2013; Borrell et al., 2014). In wheat, overexpressing the CCAAT box-binding transcrip-tion factor TaNFYA-B1 stimulated enhanced root development as well as nitrate and phosphorus transporters (Qu et al., 2014).Arabidopsis ERA1 b-subunit of farnesyltransferase is involved in reversible drought tolerance induction and may be applicable toa range of crop plants to deliver higher yields than conventionally bred genotypes under water stress conditions without yielddrag in normal conditions. MicroRNAs are known to impact on a wide range of transcriptional networks. The microRNAsmiR1435, miR5024, and miR7714 have been found in water-stressed roots of the drought-tolerant wheat genotype TR39477,but are absent from drought-sensitive lines (Akpinar et al., 2015). These microRNAs may be good indicators of potentialdrought tolerance in future breeding studies.

Table 3 Drought-resistance candidate genes

Function Protein and gene Example Source and host References

Protein kinases MAP kinase OsMAPK5 Abscisic acid–inducible response Rice Xiong and Yang (2003)Transcription factors Zinc finger protein DST Stomatal aperture control regulation Rice Huang et al. (2009)Protein degradation Ubiquitin ligase OssDIR1 Drought tolerance response Rice Gao et al. (2011)Protein modification Farnesyltransferase/squalene

synthase SQS1RNAi-mediated disruption Rice Manavalan et al. (2011)

Abscisic acid metabolism Molybdenum cofactorsulfurase LOS5

Enhanced drought tolerance and yield Arabidopsis, soybean Li et al. (2013)

Osmotic adjustment Trehalose synthesis OsTPS1 Vacuolar storage Rice Li et al. (2011)Dehydrins Late embryogenesis abundant

protein HVA1

Desiccation protection Barley, wheat Sivamani et al. (2000)

Green Biotechnology for Food Security in Climate Change 5

Salt Stress and Flooding Tolerance

Salinity affects more than 20% of the world’s agricultural soils. Climate change will lead to rising sea levels, doublingsalt-contaminated areas by 2050 (IPCC, 2014). Using marker-aided selection can speed up conventional breeding processes fortraits such as salt stress. Plant responses to salt stress can be either rapid or following long-term exposure. Rapid responses mayinclude stomatal closure, inhibition of shoot elongation, and increased leaf temperature (Roy et al., 2014). Extended salt stressfrequently leads to declines in growth rate and reproductive development affecting seed formation (Julkowska and Testerink,2015). Salt tolerance mechanisms are frequently multigenic and multilocational. Studying the inheritance patterns of molecularmarkers linked to salt tolerance will be of benefit in overcoming a major obstacle to food crop production in areas likely to beflooded due to climate change (Roy et al., 2014). Introgression of the high-affinity potassium transporter gene TmHKT1;5-Afrom einkorn wheat (Triticum monococcum) into durum wheat (Triticum turgidum var. durum) lines by marker-aided selection hasproduced up to 25% yield gains under saline conditions when compared with unimproved genotypes (Munns et al., 2012; Jameset al., 2011; Munns and Gilliham, 2015). Although genetic modification approaches have yet to garner such impressive field perfor-mance in commercially important wheats, a truncated form of the T. turgidum var. durum plasma membrane Naþ/Hþ antiporterTdSOS1 gene has been shown to improve salt tolerance in the hypersensitive Arabidopsis thaliana sos1-1 genotype as shown byseed germination and seedling growth trials (Feki et al., 2014; Ji et al., 2013).

Introgression of the rice flash flood tolerance gene Sub1A into commercial indica rice lines by marker-assisted selection hasproduced yield gains of 1.0–3.0 tonnes ha�1 in India and the Philippines (Dar et al., 2014; IRRI, 2015). Unfortunately, the advan-tages conveyed by Sub1A are only effective for up to 15 days submergence in up to 20 cm of floodwater. Efforts to improve the stag-nant flood and submergence tolerance of elite rice genotypes are ongoing. The Saltol trait identified in rice is thought to be animportant contributor to genetic variation in ion uptake in saline conditions (Deinlein et al., 2014) and may prove useful inmarker-aided selection of salt- and submergence-tolerant rice varieties (Ashraf and Foolda, 2013). The International Rice ResearchInstitute, for example, has developed more than 100 salinity-tolerant elite rice lines currently being screened for use in India, Ban-gladesh, and West Africa (IRRI, 2015). Natural variation in the soybean (Glycine max, Figure 6) chromosome 3 GmSALT3 locusmodulates salinity tolerance between commercial cultivars (Guan et al., 2014). In the salt-tolerant Tiefeng 8 cultivar GmSALT3,cation/Hþ exchanger protein is preferentially expressed in phloem- and xylem-associated root cells, reducing Naþ ion accumulation.In the salt-sensitive cultivar 85-140, however, this gene is interrupted, leading to increased salt sensitivity. The salt-tolerantGmSALT3 variant, known as haplotype H1, is found extensively in salt-tolerant genotypes and has breeding potential for improvingsoybean varieties in saline conditions.

Emergent Technologies for Regulating Gene Expression in Food Crops

Among the areas where new technology is likely to influence the use and growth of food crops in response to climate change, threeapproaches stand out (see Table 4).

Gene silencing is a means of downregulating (or ‘turning off’) particular genes by overexpression of RNA sequences, known asRNAi, preventing functional expression of a gene. Although already available for several years, it is now increasingly seen as a toolfor turning off particular genes, as in the bruising-resistant Arctic� apples (Waltz, 2015) and bruising and black spot–resistantInnate� potatoes deregulated and considered safe for consumption by the United States Food and Drug Administration(Bettenhausen, 2013; USFDA, 2015). This RNAi technology can be applied using DNA from sexually compatible wild relatives

Figure 6 Soybean, Glycine max. Source: USDA Photo Services.

6 Green Biotechnology for Food Security in Climate Change

of crop plants, as in Innate� potatoes, which should make gaining regulatory acceptance easier. Future food security applicationsmay include turning off receptors to pathogen attack or stress response components, which could be of considerable value inclimate change.

Gene editing is a means of making precision, directed changes in genomes at as fine a scale level as one, or a few nucleotides(Ledford, 2015a). Two alternative systems currently provide state-of-the-art protocols for achieving these small-scale genomicchanges, using clustered regularly interspaced short palindromic repeats (CRISPR) and the CAS9 nuclease, or alternatively, transcrip-tional activator-like effector nucleases (TALENS). Precise genomic modification using CRISPR has been likened to a ‘find andreplace’ function (The Economist, 2015). CRISPR is effective in a range of food crop species, including rice (Xu et al., 2014), maize(Xang et al., 2014), and wheat (Shan et al., 2014), and provides an inexpensive toolkit approach for any genome (Xang et al., 2014).CRISPR has already been used to produce herbicide-resistant canola (oil seed rape) in Canada. Using CRISPR in agriculture will notrequire regulation in many countries, although the European Union has not yet formed a consolidated position on CRISPR.TALENS uses an alternative nuclease system to precision edit genomes, based on fusions of transcription activator-like effectorswith target DNA-binding domains and an endonuclease cleavage domain (Li et al., 2014). Just like CRISPR/CAS9, varyingDNA-binding domain sequences allow different genomic targets to be addressed. The TALENS system has been effective in riceand in conferring powdery mildew resistance to wheat (Wang et al., 2014). Although some concerns relating to controlling thespread of CRISR-edited sequences throughout wild populations have been expressed (Camacho et al., 2014; Ledford, 2015b),precision editing of genomes will become widely used in agriculture. Targets relevant to food security in climate change includemodulating stomatal closure, ion transporters, stress receptors, and components of signal transduction in environmental stressresponses (Hu and Xiong, 2014).

RNA spraying technology topically applies specific synthetic RNA to the surfaces, e.g., leaves of plants to control plant responsesor stimulate pathogen resistance. Several agricultural biotechnology companies are believed to be investigating RNA spraying tech-nology, including BioDirect� insect and virus control, developed by Monsanto, to combat Colorado potato beetle and tospovirusoutbreaks (Regalado, 2015). RNA spraying removes the need to use genetic modification in such applications, as no change to theplant genome takes place. Instead, take-up of the sprayed synthetic RNA by plant cells takes place, silencing particular genes tempo-rarily, until the effect wears off, typically from a few days to 3 months. Difficulties include developing efficient ways to penetrateplant cells and identifying suitable gene sequences to use. Whether spraying should always be done after stressing, either bioticsuch as pathogen attack, or abiotic, such as salt or drought stress occurs, or can be done preemptively is not yet clear. The specificityof the gene silencing effect is likely to make this approach highly valuable and cost-effective in the future. Recent advances inlarge-scale RNA synthesis mean that field spraying consumable costs of as little as $5/acre may be achievable (Regalado, 2015).Since climate change means that crop hosts are likely to face new pathogen threats, or more widely distributed pathogens, usingRNA sprays to prevent attacks, limit losses, or combat weed spread will contribute to food security through maintaining yieldsor preventing postharvest losses (Shaner and Beckie, 2014). As global temperatures rise, this may lead to a wider spread of patho-gens such as the citrus greening Candidatus liberibacter in fruit trees, causing the loss of millions of citrus fruit trees each year. SprayingRNA only when needed could be more cost-effective and less environmentally damaging than current intensive chemical control ofthe Asian citrus psyllid vector (Robinson et al., 2014).

Attitudes, Needs, and the Future

Green biotechnology tools are and will continue to make positive contributions to enhancing food security during climatechange, alongside a range of other means to ensure food availability, access to food for all, efficient utilization of food resources,and a stable global food commodity trading system. The extent to which green biotechnology will help to achieve this is depen-dent on several factors, including the rate of technological development, governmental and public acceptance of novel biotech-nologies, and the costs of climate change effected food crops to consumers. For the increasing numbers of undernourishedpeople, as the global population grows toward 9.6 billion by 2050 (Federoff, 2015), particularly in the developing nations,choices about how a food crop has been produced are likely to be an unaffordable luxury. Producing enough food to meetthe needs of the growing world population, reducing pre- and postharvest losses, and enhancing access to food for all must surelybe a laudable aim for mankind.

Table 4 Novel biotechnological approaches for altering gene expression in food crops

Approach Opportunity References

Gene silencing Nonbrowning Arctic® apples, Innate® bruising-resistantpotatoes by RNA interference (RNAi)

Bettenhausen (2013), Ricroch and Hénard-Damave(2015), and USFDA (2015)

Gene editing CRISPR-Cas9 Shan et al. (2014)Transcription activator-like effector nucleases (TALENS)in rice

Li et al. (2014)

RNA spraying BioDirect® RNA interference applications Regalado (2015)

Green Biotechnology for Food Security in Climate Change 7

References

Abate, T., Davis, N., Regasa, M., et al., 2014. DTMA moves to the next level: welcoming DTMASS. Q. Bull. Drought Toler. Maize Afr. Proj. 3, 1–2.Akpinar, B.A., Kantar, M., Budak, H., 2015. Root precursors of microRNAs in wild emmer and modern wheats show major differences in response to drought stress. Funct. Integr.

Genom. http://dx.doi.org/10.1007/s1-142-015-0453-0.Ashraf, M., Foolda, M.R., 2013. Crop breeding for salt tolerance in the era of molecular markers and marker-assisted selection. Plant Breed. 132, 10–20.Bettenhausen, C., 2013. Engineered apples near approval. Chem. Eng. News 91, 31–33.Bollineni, H., Gopala, K.S., Sundaram, R., et al., 2014. Marker assisted biofortification of rice with pro-vitamin A using transgenic Golden Rice lines: progress and prospects. Indian

J. Genet. Plant Breed. 74, 624–630.Borlaug, N.E., 2000. Ending world hunger: the promise of biotechnology and the threat of antiscience zealotry. Plant Physiol. 124, 487–490.Borlaug, N.E., 2003. Feeding a World of 10 Billion People: The Tva/lfdc Legacy. International Fertilizer Development. ISBN: 978–0880901444.Borrell, A.K., Mullet, J.E., George-Jaeggli, B., van Oosterom, E.J., Hammer, G.L., Klein, P.E., Jordan, D.R., 2014. Drought adaptation of stay-green sorghum is associated with

canopy development, leaf anatomy, root growth, and water uptake. J. Exp. Bot. http://dx.doi.org/10.1093/jxb/eru232.Brookes, G., Barfoot, P., 2014. GM Crops: Global Socio-economic and Environmental Impacts 1996–2012. PG Economics Ltd, UK.Brookes, G., Barfoot, P., 2015. Global income and production impacts of using GM crop technology 1996–2013. GM Crops Food 6, 13–46.Bruce, T.J.A., 2011. GM as a route for delivery of sustainable crop protection. J. Exp. Bot. 63, 537–541.Camacho, A., Van Deynze, A., Chi-Ham, C., Bennett, A.B., 2014. Genetically engineered crops that fly under the US regulatory radar. Nat. Biotechnol. 32, 1087–1091.Chen, Y., Yang, J., Wang, Z., Zhang, H., Mao, X., et al., 2013. Gene structures, classification, and expression models of the DREB transcription factor subfamily in Populus

trichocarpa. Sci. World J. 2013, article 954640.Conway, G., 2012. One Billion Hungry, Can We Feed the World. Cornell University Press, Ithaca, NY.Cooper, M., Gho, C., Leafgren, R., Tang, T., Messna, C., 2014. Breeding drought-tolerant maize hybrids for the US corn-belt: discovery to product. J. Exp. Bot. http://dx.doi.org/

10.1093/jxb/eru064.Dar, M.H., Singh, S., Singh, U.S., Zaidi, N.W., Ismail, A.M., 2014. Stress tolerant rice varieties – making headway in India. SATSA Mukhaptra Annu. Tech. Issue 18, 1–14.Deinlein, U., Stephen, A.B., Horie, T., Luo, W., Xu, G., Schroeder, J.I., 2014. Plant salt-tolerance mechanisms. Trends Plant Sci. 19, 371–379.Degenkolbe, T., Do, P.T., Zuther, E., Repsilber, D., Walther, D., et al., 2009. Expression profiling of rice cultivars differing in their tolerance to long-term drought stress. Plant Mol.

Biol. 69, 133–153.Degenkolbe, T., Do, P.T., Kopka, J., Zuther, E., Hincha, D.K., Kohl, K.I., 2013. Identification of drought tolerance markers in a diverse population of rice cultivars by expression and

metabolite profiling. PLoS One 8, e63637.Dhungana, S.K., Kim, B.-R., Son, J.-H., Shin, D.-H., 2015. Comparative study of CaMsrB2 gene containing drought-tolerant transgenic rice (Oryza sativa L.) and non-transgenic

counterpart. J. Agron. Crop Sci. 201, 10–16.Dugas, D., Monaco, M., Olsen, A., Klein, R., Kumari, S., et al., 2011. Functional annotation of the transcriptome of Sorghum bicolor in response to osmotic stress and abscisic acid.

BMC Genom. 12, 514.Federoff, N.V., 2015. Food in a future of 10 billion. Agric. Food Secur. 4, 11.Feki, K., Quintero, F.J., Khoudi, H., Leidl, E.O., Masmoudi, K., Pardo, J.M., 2014. A constitutively active form of a durum wheat Naþ/Hþ antiporter SOS1 confers high salt tolerance

in transgenic Arabidopsis. Plant Cell Rep. 33, 277–288.Fernandez, J.W., July 2011. Biotech addresses food security, climate change: potential economic growth engine. Biotech Now 1–2.Fisher, M., Abate, T., Lunduka, R.W., Asnake, W., Alemayehu, Y., et al., 2015. Drought tolerant maize for farmer adaptation to drought in sub-Saharan Africa: determinants of

adoption in eastern and southern Africa. Climatic Change. http://dx.doi.org/10.1007/s10584-015-1459-2.Food and Agriculture Organisation of the United Nations, 2011. Climate Change, Water and Food Security. FAO. Water Report 36.Food and Agriculture Organisation of the United Nations, 2014. FAO Success Stories on Climate Smart Agriculture. FAO. I3871E/1/05.14. www.fao.org/climatechange/climatesmart.Gao, T., Wu, Y., Zhang, Y., Liu, L., Ning, Y., et al., 2011. OsDIR1 overexpression greatly improves drought tolerance in transgenic rice. Plant Mol. Biol. 76, 145–156.Godfray, H.C.J., Garnett, T., 2014. Food security and sustainable intensification. Philos. Trans. R. Soc. B 369, 20120273.Goldenberg, S., March 31, 2014. Climate Change a Threat to Security, Food and Humankind – IPCC Report. Guardian, pp. 1–2.Gonsalves, C.V., Gonsalves, D., 2014. The Hawaii papaya story. In: Smyth, S.J., Phillips, P.W.B., Castle, D. (Eds.), Handbook on Agriculture, Biotechnology and Development.

Edward Elgar, Northampton, MA, pp. 642–660.Guan, R., Qu, Y., Guo, Y., Liu, Y., Jiang, J., Chen, J., Ren, Y., Liu, G., Tian, L., Jin, L., Liu, Z., Hong, H., Chang, R., Gilliham, M., Qiu, L., 2014. Salinity tolerance in soybean is

modulated by natural variation in GmSALT3. Plant J. 80, 937–950.Haoa, B., Xuea, Q., Mareka, T.H., et al., 2015. Soil water extraction, water use, and grain yield by drought-tolerant maize on the Texas High Plains. Agric. Water Manag. 155, 11–21.Heinemann, J.A., 2013. Genetic Engineering and Biotechnology for Food Security and for Climate Change Mitigation and Adaptation: Potential and Risks, vol. 17. Third World

Network Biotechnology & Biosafety Series. ISBN: 978-967-5412-92-9.Hu, H., Xiong, L., 2014. Genetic engineering and breeding of drought-resistant crops. Annu. Rev. Plant Biol. 65, 715–741.Huang, X.-Y., Chao, D.-Y., Gao, J.-P., Zhu, M.-Z., Shi, M., Lin, H.-X., 2009. A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal

aperture control. Genes Dev. 23, 1805–1817.Hussain, Z., Ali, S., Hayat, Z., Zia, M.A., Iqbal, A., et al., 2014. Agrobacterium mediated transformation of DREB1A gene for improved drought tolerance in rice cultivars (Oryza sativa L.).

Aust. J. Crop Sci. 8, 1114–1123.Inter-Governmental Panel on Climate Change, 2014. Fifth Assessment Report.International Rice Research Institute, 2015. Climate Change-Ready Rice. IRRI Press, Manila, Philippines.International Service for the Acquisition of Agri-Biotech Applications, 2008. Biotechnology for the Development of Drought Tolerant Crops. ISAAA. Pocket K No. 32.International Service for the Acquisition of Agri-Biotech Applications, 2013. Biotechnology and Climate Change. ISAAA. Pocket K No. 43.International Service for the Acquisition of Agri-Biotech Applications, 2014a. Documented Benefits of GM Crops. ISAAA. Pocket K No. 5.International Service for the Acquisition of Agri-Biotech Applications, 2014b. The Status of Commercialized Bt Brinjal in Bangladesh. ISAAA. Brief 47.International Service for the Acquisition of Agri-Biotech Applications, 2015. GM Crop Approvals Database.James, C., 2014. Global Status of Commercialized Biotech/GM Crops: 2014. International Service for the Acquisition of Agri-Biotech Applications.James, R.A., Blake, C., Byrt, C.S., Munns, R., 2011. Major genes for Naþ exclusion Nax1 and Nax2 (wheat HKT1;4 and HKT1;5) decrease Naþ accumulation in bread wheat under

saline and waterlogged conditions. J. Exp. Bot. 62, 2939–2947.Ji, H., Pardo, J.M., Batelli, G., Van Oosten, M.J., Bressan, R.A., et al., 2013. The Salt Overly Sensitive (SOS) pathway: established and emerging roles. Mol. Plant. 6, 275–286.Julkowska, M.M., Testerink, C., 2015. Tuning plant signalling and growth to survive salt. Trends Plant Sci. http://dx.doi.org/10.1016/j.tplants.2015.06.008.Katoh, A., Ashida, H., Kasajima, I., Shigeoka, S., Yokota, A., 2014. Potato yield enhancement through intensification of sink and source performances. Breed. Sci. 65, 77–84.Ledford, H., 2015a. CRISPR, the disruptor. Nature 522, 20–24.Ledford, H., 2015b. Caution urged over DNA editing in wild. Nature 524, 16.Li, H.-W., Zang, B.-S., Deng, X.-W., Wang, X.-P., 2011. Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice. Planta 234,

1007–1018.

8 Green Biotechnology for Food Security in Climate Change

Li, Y., Zhang, J., Zhang, J., Hao, L., Hua, J., et al., 2013. Expression of an Arabidopsis molybdenum cofactor sulphurase gene in soybean enhances drought tolerance and increasesyield under field conditions. Plant Biotechnol. J. 11, 747–758.

Li, T., Liu, B., Chen, C.H., Yang, B., 2014. TALEN utilization in rice genome modifications. Methods 69, 9–16.Manavalan, L.P., Chen, X., Clarker, J., Salmeron, J., Nguyen, H.T., 2011. RNAi-mediated disruption of squalene synthase improves drought tolerance and yield in rice. J. Exp. Bot.

63, 163–175.Masiga, C.W., Mugoya, C., Ali, R., et al., 2014. Enhanced utilisation of biotechnology research and development innovations in Eastern and Central Africa for agro-ecological

intensification. In: Challenges and Opportunities for Agricultural Intensification of the Humid Highland Systems of Sub-saharan Africa, pp. 97–104.McKenzie, F.C., Williams, J., 2015. Sustainable food production: constraints, challenges and choices by 2050. Food Secur. 7, 221–233.Morsy, M., 2015. Microbial symbionts: a potential bio-boom. J. Investig. Genom. 2, 00015.Munns, R., Gilliham, M., 2015. Salinity tolerance of crops – what is the cost? New Phytol. http://dx.doi.org/10.1111/nph.13519.Munns, R., James, R.A., Xu, B., Athman, A., Conn, S.J., Jordans, C., Byrt, C.S., Hare, R.A., Tyerman, S.D., Tester, M., Piett, D., Gilliham, M., 2012. Wheat grain yield on saline soils

is improved by an ancestral Naþ transporter gene. Nat. Biotechnol. 30, 360–364.Munoz-Amitriain, M., Lonardi, S., Luo, M.C., et al., 2015. Sequencing of 15 622 gene-bearing BACs clarifies the gene-dense regions of the barley genome. Plant J. http://

dx.doi.org/10.1111/tpj.12959.Mutuc, E.M., Rejesus, R.M., Yorobe, J.M., 2011. Yields, insect productivity, and Bt corn: evidence from damage abatement models in the Philippines. J. Agrobiotechnol. Manag.

Econ. 14, 1–19.Nakashima, K., Jan, A., Todaka, D., Maruyama, K., Goto, S., et al., 2014. Comparative functional analysis of six drought-responsive promoters in transgenic rice. Planta 239,

47–60.Nemali, K.S., Bonin, C., Dohleman, F.G., Stephens, M., Reeves, W.R., et al., 2015. Physiological responses related to increased grain yield under drought in the first

biotechnology-derived drought tolerant maize. Plant Cell Environ. 38, 1866–1880.Nuccio, M.L., Wu, J., Mowers, R., Zhou, H.-P., Meghji, M., et al., 2015. Expression of trehalose-6-phosphate phosphatase in maize ears improves yield in well-watered and drought

conditions. Nat. Biotechnol. 33, 862–869.Qu, B., He, X., Wang, J., Zhao, Y., Teng, W., Shao, A., Zhao, X., Ma, W., Wang, J., Li, B., Li, Z., Tong, Y., 2014. A wheat CCAAT box-binding transcription factor increases the grain

yield of wheat with less fertilizer input. Plant Physiol. 167, 411–423.Regalado, A., August 11, 2015. The next great GMO debate. MIT Technol. Rev.Reyes, L., 2009. Overcoming the toughest stress. Rice Today 8, 30–32.Ricroch, A.E., Hénard-Damave, M.C., 2015. Next biotech plants: new traits, crops, developers and technologies for addressing global challenges. Crit. Rev. Biotechnol. http://

dx.doi.org/10.3109/07388551.2015.1004521.Robinson, K.E., Worrall, E.A., Mitter, N., 2014. Double stranded RNA expression and its topical application for non-transgenic resistance to plant viruses. J. Plant Biochem.

Biotechnol. 23, 231–237.Roy, S.J., Negrao, S., Tester, M., 2014. Salt resistant crop plants. Curr. Opin. Biotechnol. 26, 115–124.Ruane, J., Sonnino, A., 2011. Agricultural biotechnologies in developing countries and their possible contribution to food security. J. Biotechnol. 156, 356–363.Sammons, B., Whitsel, J., Stork, L.G., Reeves, W., Horak, M., 2014. Characterisation of drought-tolerant maize MON87460 for use in environmental risk assessment. Crop Sci. 54,

719–729.Shaik, R., Ramakrishna, W., 2012. Bioinformatic analysis of epigenetic and microRNA mediated regulation of drought responsive genes. PLoS One 7, e49331.Shan, Q., Wang, Y., Li, J., Gao, C., 2014. Genome editing in rice and wheat using the CRISPR/Cas system. Nat. Protoc. 9, 2395–2410.Shaner, D.L., Beckie, H.J., 2014. The future of weed control and technology. Pest Manag. Sci. 70, 1329–1339.Shu, L., Lou, Q., Ma, C., Ding, W., Zhou, J., et al., 2011. Genetic, proteomic and metabolic analysis of the regulation of energy storage in rice seedlings in response to drought.

Proteomics 11, 4122–4138.Sivamani, E., Bahieldin, A., Wraith, J.M., Al-Niemi, T., Dyer, W.E., et al., 2000. Improved biomass productivity and water use efficiency under water deficit conditions in transgenic

wheat constitutively expressing the barley HVA1 gene. Plant Sci. 155, 1–9.Smith, P., Martino, D., Cai, Z., Gwary, D., Janzen, H., et al., 2008. Greenhouse gas mitigation in agriculture. Phil. Trans. Roy. Soc. B 363, 789–813.The Economist, August 22, 2015. The age of the red pen. Economist. ISSN: 0013-0613.Tang, G., Qin, J., Dolnikowski, G.G., Russel, R.M., Grusak, R.M., 2009. Golden rice is an effective source of vitamin A. Am. J. Clin. Nutr. 89, 1776–1783.Todaka, D., Shinozaki, K., Yamaguchi-Shinozaki, K., 2015. Recent advances in the dissection of drought-stress regulatory networks and strategies for development of

drought-tolerant transgenic rice plants. Front. Plant Sci. 6 article 84.Uga, Y., Sugimoto, K., Ogawa, S., Rane, J., Ishitani, M., et al., 2013. Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions.

Nat. Genet. 45, 1097–1102.United Nations Convention on Biodiversity, 1992. Article 2.United States Food & Drug Administration, 2015. FDA Concludes Arctic Apples and Innate Potatoes Are Safe for Consumption. Biotechnology Consultation Agency Response Letters

BNF00132, BNF00141.Vermeulen, S.J., Aggarwal, P.K., Ainslie, A., et al., 2012. Options for support to agriculture and food security under climate change. Environ. Sci. Policy 15, 136–144.Waltz, E., 2015. Non-browning GM apple approved for market. Nat. Biotechnol. 33, 326–327.Wang, Y., Cheng, X., Shan, Q., Zhang, Y., Liu, J., et al., 2014. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery

mildew. Nat. Biotechnol. 32, 947–951.Xang, H.-L., Dong, L., Wang, Z.-P., Zhang, H.-Y., Han, C.-Y., et al., 2014. A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol. 14, 327.Xiong, L., Yang, Y., 2003. Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid – inducible mitogen-activated protein kinase. Plant Cell

15, 745–759.Xu, R.F., Li, H., Qin, R.Y., Li, J., Qiu, C.H., et al., 2014. Generation of inheritable and ‘transgene clean’ targeted genome-modified rice in later generations using CRISPR/Cas9

system. Sci. Rep. 5, 11491.Yadav, D., Shavrukov, Y., Bazanova, N., Chirkova, L., Borisjuk, N., Kovalchuk, N., Ismagul, A., Parent, B., Langridge, P., Hrmova, M., Lopato, S., 2015. Constitutive overexpression

of the TaNF-YB4 gene in transgenic wheat significantly improves grain yield. J. Exp. Bot. http://dx.doi.org/10.1093/jxb/erv370.Yashveer, S., Singh, V., Kaswan, V., Kaushik, A., Tokas, J., 2015. Green biotechnology, nanotechnology and bio-fortification: perspectives on novel environment-friendly crop

improvement strategies. Biotechnol. Genet. Eng. Rev. 30, 113–126.Zilberman, D., Kaplan, S., Kim, E., Sexton, S., Barrows, G., 2014. Biotechnology and food security. J. Int. Aff. 67 (2).

Green Biotechnology for Food Security in Climate Change 9