The Omics Revolution in Agricultural Research - ACS Publications

Subscriber access provided by BOSTON UNIV

Perspective

Omics revolution in agricultural research Jeanette Van Emon J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.5b04515 • Publication Date (Web): 15 Oct 2015 Downloaded from http://pubs.acs.org on October 18, 2015

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

Journal of Agricultural and Food Chemistry is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 32

Journal of Agricultural and Food Chemistry

The Omics Revolution in Agricultural Research

1 2

Jeanette M. Van Emon*

3 4 5

National Exposure Research Laboratory, United States Environmental Protection Agency, Las Vegas, NV 89119, United States

6 7 8

*Corresponding author (Tel: 702-798-2154; Fax: 702-798-2243: E-mail: [email protected])

9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25

1 ACS Paragon Plus Environment


26 27 28 29 30 31 32 33 34 35 36 37

ABSTRACT: The Agrochemicals Division co-sponsored the 13th International Union of Pure and Applied Chemistry International Congress of Pesticide Chemistry held as part of the 248th National Meeting and Exposition of the American Chemical Society in San Francisco, CA, August 10-14, 2014. The topic of the Congress was Crop, Environment, and Public Health Protection; Technologies for a Changing World. Over 1000 delegates participated in the Congress with interactive scientific programming in nine major topic areas including the challenges and opportunities of agricultural biotechnology. Plenary speakers addressed global issues related to the Congress theme prior to the daily technical sessions. The plenary lecture addressing the challenges and opportunities that omic technologies provide agricultural research is presented here. The plenary lecture provided the diverse audience with information on a complex subject to stimulate research ideas and provide a glimpse of the impact of omics on agricultural research.

38 39 40 41

KEYWORDS: agricultural research, biotech crops, genetic modifications, genomics, metabolomics, omics, plant breeding, plant transcriptomics, proteomics, transgenic crops

42 43 44 45 46 47 48 49 50 51 52 53 54 55 2 ACS Paragon Plus Environment

Page 2 of 32

Page 3 of 32


56

INTRODUCTION

57

Omics can inform you if the steak you are about to enjoy will be tender and juicy; if your glass

58

of wine will be sweet or dry before your first sip; and can provide you a genetic map to growing

59

the deepest-red tomato possible. The panomic arsenal of omic tools is enhancing the quality,

60

taste, and nutritional composition of food crops; increasing agricultural production for food, feed

61

and energy; playing a significant role in crop protection; and significantly impacting agricultural

62

economics. Through the use of genomics, proteomics, transcriptomics, and metabolomics, the

63

consistency and predictability in plant breeding have been improved, reducing the time and

64

expense of producing better quality food crops that are resistant to stress but still exhibit a high

65

nutritional value. Omics has provided insights to the molecular mechanisms of insect resistance

66

to pesticides, and the tolerance of plants to herbicides for better pest management. Linking

67

genes to traits provides more scientific certainty leading to improved cultivars and understanding

68

the mechanisms of insect and weed resistance. Omics enables a systems biology approach

69

towards understanding the complex interactions between genes, proteins, and metabolites within

70

the resulting phenotype. This integrated approach relies heavily on chemical analytical methods,

71

bioinformatics and computational analysis, and many disciplines of biology, leading to crop

72

protection and improvements.

73

The National Agricultural Biotechnology Council in its report “Vision for Agricultural Research

74

and Development in the 21st Century” outlined its plan for developing a sustainable biobased

75

economy.¹ The Council urged agricultural research and development programs to look beyond

76

food, feed and fiber production and to address sustainable biobased industries. This in part

77

would, create rural and urban job opportunities; improve the quality of air, water and soil;



78

improve the healthfulness of food; and produce human health-related products in plants,

79

microbes and animals.¹ Good ideas but how do we get there?

80

81

Early Crop Improvement Techniques

82

The genetic makeup of plants has been intentionally altered since the initial start of agriculture,

83

estimated to have its beginnings 8,000 – 10,000 years ago. The evolution of crop domestication,

84

which was essentially genetic manipulation, was based on selective breeding to produce better

85

plants and animals and resulted in genetic modifications, although not recognized at the time. In

86

these early experiments, only the seeds from the best looking plants were saved for the next

87

planting cycle. Traits such as higher yields, pest and disease resistance, larger fruits or

88

vegetables, and faster growth, were commonly selected.

89

bred for higher yields of milk and meat.

90

Luther Burbank developed the “plumcot” by crossing plums with apricots, 100 years ago, and

91

described the process in his 1921 book “How Plants are Trained to Work for Man: Fruit

92

Improvement.”² Plumcots are still on the market today along with many other hybrids including

93

more from plums and apricots. Broccoflower another well-known genetic modification is said to

94

have more vitamins than either the broccoli or cauliflower parent. Products of plant genetic

95

manipulations based on chemical treatment and radiation are also well-known commodities.

96

When the seeds from seeded watermelons are treated with colchicine a triploid seed is produced

97

that is sterile, leading to no seeds in the fruit. This may be convenient for eating but it takes

98

away one of the pleasures of eating watermelon – the seed spitting contests.

Farm animals were also selectively


Page 4 of 32

Page 5 of 32

99


During mutation breeding, plants are exposed to γ-rays, protons, neutrons, and α- and β- particles

100

to induce mutations to obtain the desired traits. Chemicals such as sodium azide and ethyl

101

methanesulphonate are also used to produce mutagenic plants. Over 3200 mutagenic plant

102

varietals have been officially released between 1930 and 2014.³ Of this number, over 1,000

103

mutant varietals are of major staple crops being grown worldwide. After World War II, giant

104

“gamma gardens” sprang up on government installations in several countries to support peaceful

105

uses of atomic energy. A popular variety of red grapefruit was created via thermal neutron

106

radiation at Brookhaven National Laboratory.4 Plants developed via mutagenic processes or

107

cross breeding, possess random, multiple and unspecific genetic changes often leading to

108

thousands of undesirable plants to finally obtain the ones with the desired traits. These

109

nonspecific genetic manipulations have a high potential to result in unintended and perhaps

110

adverse compositional changes. However, the successful products of these genetic

111

manipulations have led to searches for more efficient and controllable ways to transfer genetic

112

traits among plants, while lowering risks of adverse mutations using precision genetic

113

modifications.

114

115

Omic Technologies

116

The suffix omics has been attached to many fields of study, instantly conferring buzzword status

117

and attention (Figure 1). The world of omics is quickly becoming a vast field and impossible to

118

cover properly in just one paper. Several global omics technologies (Figure 2) are presented here

119

in relation to agricultural research applications.



120

Omics can enable the further expansion of agricultural research in food, health, energy, chemical

121

feedstock and specialty chemicals, while helping to preserve, enhance and remediate the

122

environment. Omic technologies focus on key traits of interest with precision. Omics can lead to

123

enhancement of the nutritional properties of food for consumer benefit, such as a tomato that is

124

high in lycopene, fruit with delayed ripening characteristics, and produce with potent antioxidant

125

capabilities.5

126

Omics enables us to learn more about the genes and biochemical pathways that control such

127

attributes for added health benefits, moving beyond basic nutrition and into the development of

128

functional foods. For example, seed oils that do not produce trans-fats but rather contain heart

129

healthy omega-3 fatty acids, or cassava melons with increased protein content to help fight

130

malnutrition. Improvements in protein quality and content for better human and animal

131

nutrition, increased vitamin and mineral levels to address nutrient deficiencies, and reduction of

132

allergens and of anti-nutritional substances that diminish food quality can all be explored through

133

omics. Foodomics, another omics term, encompasses studies of food and nutrition through

134

integrated omic approaches.6 Foodomics advances the trend of linking food and health, and may

135

eventually lead to a larger role for nutrition in preventing disease.7 Foodomics may also lead to

136

the development of food for medicinal purposes based on an individual’s genotype and may

137

determine the effect of bioactive compounds in foods on molecular pathways.7

138

Omic technologies allow the visualization or monitoring of all of the changes that take place

139

when the genetics, nutritional state, or environment of an organism is altered.8 Thus, revealing an

140

understanding of the alterations in plant metabolism resulting from environmental interactions.

141

Omics can provide insights into species that we thought we knew everything about. The central

142

Asian wild apple was long thought to be the main progenitor of the domesticated apple. 6 ACS Paragon Plus Environment

Page 6 of 32

Page 7 of 32


143

However, using genomic markers it has been found that the European crabapple made an

144

unexpectedly large contribution to the genome of the domestic apple Malus domestica.9 The

145

genetic probing into the lives of plants can be quite fruitful. Studies on cultivated tomatoes

146

revealed genetic changes over time through early domestication and modern plant breeding that

147

has led to today’s cultivars being much larger than their wild relatives.10

148

Using omics, the genes responsible for proteins that confer or block the desired traits can be

149

determined. Once these genes have been identified they can be silenced in a plant or introduced

150

from one plant to another or from another species making a transgenic plant (Figure 3). Thus, a

151

transgenic plant contains a gene or genes (i.e., transgenes) which have been artificially inserted

152

rather than the plant acquiring them through pollination. Transgenic crop varieties possess a

153

variety of useful agronomic traits.5 By inserting one or two target genes that encode for specific

154

desirable traits into crop plants in vitro, new plant varieties with specified traits are developed in

155

a more precise manner than conventional plant breeding.

156

In the 1980s researchers developed more precise and controllable methods of genetic engineering

157

to create plants with desirable traits. In 1990, the U.S. Food and Drug Administration (FDA)

158

approved the first genetically engineered food ingredient for human consumption, the enzyme

159

chymosin, which is used in 70% or more of the cheese making in the U.S.11 In 1994, the

160

FlavrSavr™ tomato, was the first genetically engineered food approved for human consumption

161

in the U.S. The FlavrSavr™ was developed to have more flavor and to have a longer shelf-life.

162

Rice fortified with beta carotene, known as golden rice, appeared in 1999 to prevent blindness

163

due to a lack of vitamin A.12 Some of the other first biotechnology products to be

164

commercialized were modifications that make insect, virus and weed control easier or more



165

efficient. These modified traits now account for the majority of soybeans, cotton and corn grown

166

in the US.5, 11

167

Genomics: Genomics is a good entry point for the omics field, particularly as the omics

168

nomenclature started with the coining of the word genomics. A plant’s domestication and

169

breeding history are recorded in its genome.10 The completion of the sequence of the first plant

170

genome, Arabidopsis thaliana (i.e., thale cress), ushered in the post genomic era in plant

171

research. The Human Genome Project revealed that there are about 20,500 human genes, while

172

Arabidopsis thaliana is reported to have 25,498 genes.13,14 These genomes were completed

173

along with the rice genome in the early 2000s.15 Databases of genetic sequences have been

174

compiled based on submissions from researchers to foster collaborations. GenBank™ is an

175

annotated collection of publicly available DNA sequences that is frequently updated to provide

176

the latest DNA sequence information.16

177

Genomics provides knowledge-based approaches for crop plant biotechnology, enabling precise

178

and controllable methods for molecular breeding and marker-assisted selection, accelerating the

179

development of new crop varieties. However, time is not the only advantage as new attributes

180

not imagined before the omics era, can be introduced into plants, such as the production of

181

biopharmaceuticals and industrial compounds.5 Gene expression studies identify functional gene

182

products that give rise to the phenotype, which is information that can be used for plant

183

improvements. By adding a specific gene or genes to a plant, or knocking down a gene with

184

RNAi, the desirable phenotype can be produced more quickly than through traditional plant

185

breeding.


Page 8 of 32

Page 9 of 32


186

Transcriptomics: The complete set of RNA, also known as the transcriptome, is edited and

187

becomes mRNA, which carries information to the ribosome, the protein factory of the cell,

188

translating the message into protein. Transcriptomics has been described as expression profiling,

189

as it is a study of the expression levels of mRNAs in a given cell population. Unlike the genome,

190

which is roughly fixed for a given cell line, with the exception of mutations, the transcriptome is

191

dynamic as it is essentially a reflection of the genes that are actively expressed at any given time

192

under various conditions. Transcriptomics determines how the pattern of gene expression

193

changes due to internal and external factors such as biotic and abiotic stress. Transcriptomics is

194

a powerful tool for understanding biological systems. Transcriptomic techniques such as next-

195

generation sequencing (NGS) provide capability for furthering the understanding of the

196

functional elements of the genome.17

197

Proteomics: Proteins are everywhere in plants and are responsible for many cell functions.

198

Through proteomics it can be determined whether expression of mRNA results in protein

199

synthesis to further illuminate gene function. The hundreds of thousands of distinct proteins in

200

plants play key functional roles for texture, yield, flavor, and nutritional value of virtually all

201

food products.18 Through protein expression profiling, proteins can be identified at a specific

202

time as a result of expression to a stimulus such as disease and insect infestation, or temperature

203

and drought, further elucidating the function of particular proteins. Comparative proteomics can

204

determine the molecular mechanisms for susceptibility or resistance to enhance resistance traits.

205

Protein patterns have been used to study the foam stabilization of Champagne and sparkling

206

wines, the effect of fungal pathogens on grapes, wine authentication and to determine if grapes

207

were indeed grown in the appropriate appellation.19 Proteomics can also enhance the



208

understanding of mechanisms of resistance, mode of action, and biodegradation of pesticides,

209

aiding in the discovery of new effective and safe pesticides.

210

Translational plant proteomics is an expansion of proteomics from expression to functional,

211

structural and finally the translation and manifestation of desired traits. Through translational

212

proteomics the outcomes of proteomics for food authenticity; food security and safety; energy

213

sustainability; human health; increased economic values; and environmental stewardship can be

214

applied.20

215

Metabolomics: Metabolomics is the study of chemical processes providing a linkage between

216

genotypes and phenotypes.21 Proteomics identifies the gene products produced, while

217

metabolomic studies determine whether the expressed proteins are metabolically active and

218

identifies biochemical processes and the roles of the resulting various metabolites. The

219

metabolome is dynamic and subject to environmental and internal conditions. The simultaneous

220

monitoring of metabolic networks enables the association of changes resulting from biotic or

221

abiotic stress which can aid in the development of improved crop varieties and a basic

222

understanding of systems biology.21 Metabolic profiling provides an instantaneous picture of

223

what is occurring in the cell such as during fruit ripening, identifying key compounds important

224

for imparting taste and aroma. Monitoring changes in metabolite patterns can lead to quality

225

improvements for nutrition and plant health.22 Changes in the metabolome can also help to

226

distinguish the mode of action of pesticides providing critical information for new pesticide

227

discoveries.

228

Metabolomics can provide an indication of the equivalency or compositional similarity between

229

conventional and altered plants and determine if undesirable changes have occurred in the


Page 10 of 32

Page 11 of 32


230

overall metabolite composition. Metabolic profiling through mass spectrometry (MS) and

231

nuclear magnetic resonance (NMR) analyses have been used to ascertain metabolic responses to

232

herbicides, investigate metabolic regulation and metabolite changes related to environmental

233

conditions of light, temperature, humidity, soil type, salinity, fertilizers, pests and pesticides, and

234

genetic perturbations.21, 22 The in-depth analysis of metabolites may be helpful for developing

235

new pesticides, decreasing pesticide usage, increasing nutritive values or assist with other key

236

traits.

237

238

Methods of Analysis

239

The field of omics and particularly proteomics has been driven by major improvements in MS

240

instrumentation, advanced data analysis, bioinformatics and rapid analytical methods such as

241

DNA microarrays to screen thousands of samples within a short time. High-resolution NMR

242

spectroscopy has also been applied to omic studies. However, complex spectra are often

243

obtained, and it is typically not as sensitive as MS. An in-depth review of NMR theory and its

244

applications to omics has been published.23 Numerous hyphenated techniques have been used to

245

analyze transgenic food for safety and risk assessments.5, 24, 25 Advances in large-scale data

246

generation, requires concomitant advances in bioinformatic tools to process in-depth information

247

essential for the comparative studies of genes and protein expression and regulation.

248

The two major analytical proteomic approaches are termed top down and bottom up. In a top-

249

down approach intact proteins are analyzed by mass spectrometry. The bottom-up approach

250

(commonly referred to as shotgun proteomics) starts with a proteolytic digestion followed by

251

separation of the resulting peptides with detection by MS/MS. The masses of the resulting 11 ACS Paragon Plus Environment


252

peptides are compared with theoretical peptide masses. Search engines are used to match the

253

spectra generated by the MS/MS analysis with peptides from a target protein sequence database.

254

Matrix-assisted laser desorption ionization (MALDI) imaging enables the visualization of the

255

spatial distribution of proteins and metabolites. The proteome of the common apple was

256

determined using two-dimensional polyacrylamide gel electrophoresis and matrix-assisted laser

257

desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS/MS). These types of

258

proteomic studies further the understanding of the genetic regulation of fruit ripening and the

259

changes that occur during storage to identify key parameters for maintaining nutrition upon

260

storage and to prevent spoilage.26 MALDI-TOF MS/MS has shown application for the

261

authentication of foods, critical for food safety, quality assurance, and international trade. The

262

geographical origins of several honeys were differentiated based on individual protein

263

fingerprints using MALDI-TOF MS/MS.27 The approach of using MS profiles of proteins can be

264

applied to other food commodities to satisfy quality assurance requirements such as for verifying

265

the country of origin. Although wines are not known for their protein content, proteins are

266

important factors in the quality of individual wines. In addition to the effect of wine proteins on

267

foaming, important for sparkling wines, they also influence astringency, color stability, and other

268

factors leading to the overall quality of the wine.19 Proteomic studies can provide a quality

269

assurance measure for this often expensive commodity. Two-dimensional electrophoresis (2-

270

DE) with immunochemical and tandem mass spectrometry detection can highlight differences in

271

protein profiles of wine from healthy and diseased grapes.19

272

Interfacing mass spectrometry with protein databases provides not only protein characterization

273

but also mapping of post-translational and other chemical modifications, and determines

274

interactions between proteins and ligands, providing data to address issues of food quality, 12 ACS Paragon Plus Environment

Page 12 of 32

Page 13 of 32


275

safety, traceability and structure/function relationships of food proteins and peptides.28

276

Proteomic software, such as Scaffold, enables in-depth visualization of the data and clusters

277

similar proteins with shared peptides for comparisons.

278

Advances in analytical methods will further advance the applications of omics. Second

279

generation proteomics employs stable isotope labeling of amino acids in cell culture (SILACS)

280

and other quantitative methods for high throughput measurement of protein dynamics and

281

interactions rather than just identification by MS. Third generation techniques look at and

282

compare entire proteomics over time and space which require large capacity data analysis.

283

Accelerator MS has proven useful for metabolic profiling in humans and it is anticipated that it

284

will play an increasing role in plant metabolomics.

285

286

Omics Opportunities, Applications, and Research

287

Herbicide and Insect Resistance: Herbicides typically work by binding to plant enzymes to

288

inhibit their action. Crops modified to make different proteins or target sites that are not

289

inhibited by a particular chemical can provide herbicide resistance to the crop, leaving weeds

290

vulnerable. For example, plants that are resistant to glyphosate have been engineered to express

291

a different protein that is not inhibited by the herbicide. The planting of herbicide resistant (HT)

292

soybeans, cotton, and corn has dramatically risen in the U.S. since when they were first

293

introduced.

294

The soil bacterium Bacillus thuringiensis (Bt) produces a protein that is toxic to specific insect

295

pests (i.e., corn rootworm, corn earworm, European corn borer, and cotton bollworm). The

296

insertion of this gene into corn and cotton plants provides protection from these pests throughout 13 ACS Paragon Plus Environment


297

the plant’s lifespan. Two different traits can be combined (i.e., stacked) in the same plant such

298

as HT with BT for added benefit. The stacked traits of both HT and BT traits accounted for 79%

299

of the cotton grown in the U.S. in 2014 and 76% of corn was stacked.29

300

Omics also enables the study of the evolution of herbicide and insecticide resistance and the

301

biochemical and molecular mechanisms underlying resistance. Gene amplification studies

302

provide information on resistance evolution, chemical selectivity, and the link between resistance

303

and host plant adaptation.30 Such studies can lead to more efficient pesticides closely allied with

304

defense mechanisms of insects and plants and enable more tailored crop protection strategies.

305

Food Safety: Omic techniques can be applied throughout each food processing step (from raw

306

materials to end products) to maintain quality; improve shelf life predictions; and signal

307

microbial contamination in real time to improve facility sanitation and increase safety assurance.

308

Food authenticity and adulterations, allergen detection (peptide markers), biomarkers for meat

309

tenderness, and protein profiles, can all be determined through omics.28

310

Edible Vaccines: An alternative to an injection for vaccination would be to enjoy a fruit or

311

vegetable engineered to produce a vaccine. Tomatoes and bananas have been reported to

312

produce vaccines in their fruit to diphtheria, pertussis, polio, measles, tetanus, tuberculosis, and

313

hepatitis B.5 These edible vaccines could lead to low-cost protection particularly in poorer

314

countries with low vaccination rates to provide community immunity and livestock protection.31

315

Plantibodies: Antibodies produced in planta can yield gram level amounts in just a few weeks, a

316

significant advantage over other procedures.32 A comparison of therapeutic monoclonal

317

antibodies produced from plants with antibodies produced conventionally showed that the

318

plantibodies could fight the West Nile virus infection in mice as well as the more conventional 14 ACS Paragon Plus Environment

Page 14 of 32

Page 15 of 32


319

and costly version of the same antibody grown in mammalian cells.33 Antibodies from the leaves

320

of a transgenic tobacco plant were found to neutralize various types of rabies viruses.34 Clinical

321

trials of anti-HIV plantibodies have already been approved in the United Kingdom. The

322

potential for plant-based antibodies to provide the same therapeutic benefits at a lower cost is

323

extremely attractive and opens vast areas of the world to better health care. Plants as bioreactors

324

for the production of therapeutic proteins have several advantages, including the lack of animal

325

pathogenic contaminants, low cost of production and ease of agricultural scale-up.

326

Another genetically modified strain of tobacco produces an antibody for the environmental toxin

327

microcystin. The plants secrete the antibody from their roots and bind the toxin extracting it

328

from the environment.35 One can envision the use of such plants for reducing the bioavailability

329

of toxins, remediating contaminated water or soils, and giving new meaning to the term

330

phytoremediation.

331

Plants as Synthetic Chemists: With a little encouragement, plants are excellent synthetic

332

chemists for a wide range of compounds. Biotech crops have enabled an increase in the oleic

333

acid content of vegetable oils, with a simultaneous reduction in polyunsaturated fatty acids.

334

This shift in ratios conferred the added advantage of increasing the stability of the vegetable oil

335

and ultimately the processed foods. While traditional plant breeding allowed a modest increase

336

in oleic acid, biotechnology was necessary to achieve the higher levels (75 – 80%) desired.36

337

Through gene silencing, high oleic (78%) and high stearic (40%) acid cottonseed oils have been

338

produced.37

339

In addition to these synthetic capabilities, as well as producing antibodies, vaccines and other

340

biological compounds (e.g., human serum albumin, cytokines, human growth hormone, 15 ACS Paragon Plus Environment


341

pancreatic lipases) plants can also produce industrial compounds. Plants can outperform bacteria

342

in post-translational modifications of proteins and are being considered as vehicles for producing

343

plastics, polymers and other industrial building blocks.38

344 345

Human Exposure Assessment: Omics can significantly contribute to our knowledge of

346

biomarkers of exposure. Stable isotope labeling of amino acids in cell culture (SILAC) with

347

HPLC-MS/MS detection is a proteomic approach useful for determining biomarkers of exposure

348

and for linking exposure to molecular initiating events and finally to adverse outcome pathways

349

(AOPs).39 In the SILAC approach either C12 or C13-labeled amino acids are added to the growth

350

media of separately cultured, but identical, cell lines giving rise to cells containing either light or

351

heavy protein chains. A comparative analysis provides a measurement of protein dynamics and

352

interactions rather than just identification of proteins. Linking omics and genetic data to

353

pharmacokinetic and pharmacodynamic exposure models can provide in depth ecological and

354

human health risk assessments.

355

Energy Sustainability: Changing climate, rising fuel prices, and an increased desire for using

356

renewable energy sources will drive this research further. For example, cultivation of a non-

357

domesticated oilseed shrub which grows in adverse conditions can produce oil that is easily

358

converted to biodiesel. Maize, sugarcane and rapeseed can be major sources of green energy

359

particularly through modification. The development of cost-competitive advanced biofuels from

360

non-food biomass resources may reduce greenhouse gas emissions by 50% or more versus

361

petroleum-based alternatives.40 Transcriptome profiling, whole genome sequencing and

362

molecular markers are approaches being investigated for developing Jatropha curcas Linn.

363

(another non-domesticated shrub) as a sustainable biofuel crop.41 Another potential is African 16 ACS Paragon Plus Environment

Page 16 of 32

Page 17 of 32


364

grain sorghum that requires minimal fertilizer and water compared to cereal crops and has

365

readily fermentable sugars. Proteomic data from molecular breeding studies can assist with the

366

further utilization of plants as sources of sustainable production of biofuels without reducing

367

food production.

368

Bioeconomy: The National Research Council report on research and commercialization of

369

biobased industrial products provides a foundation for the National Bioeconomy Blueprint.42, 43

370

The blueprint highlights several key areas for supporting research and development investments

371

to foster a bioeconomy, including facilitating the transition of new translational products from

372

research lab to market, while protecting human and environmental health.

373

The growth of today’s U.S. bioeconomy is due in large part to the development of omic

374

technologies. According to the USDA, U.S. revenues in 2010 from genetically modified food

375

crops were approximately $76 billion and revenues from fuels, materials, chemicals, and

376

industrial enzymes derived from genetically modified systems, were approximately $100

377

billion.44

378 379

Continuing Trends

380

Global studies support the contribution biotech crops have made to food security and

381

sustainability, while positively impacting the environment by increasing crop production with a

382

reduction in pesticide usage, decreasing CO2 emissions, conserving biodiversity, and helping

383

small and resource poor farmers become self-sufficient.29 Confining cultivation to cropland saves

384

forest and protects biodiversity. The US continued to be the largest commercial grower of

385

biotech crops with 73.1 million hectares (40% of global share) devoted to maize, soybean and



386

cotton, followed by Brazil and Argentina (24.3 million hectares); India (11.6 million hectares of

387

Bt cotton) and Canada with 11.5 million hectares.29

388

In 2014, 18 million farmers, of which 90% were poor with small farms, planted a record 81

389

million hectares of biotech crops in 28 countries. Over 15 million hectares of Bt cotton in 2014

390

were planted by small-scale farmers in China and India and 415,000 small-scale farmers in the

391

Philippines benefited from biotech maize.29 Bangladesh planted BT eggplant for the first time in

392

2014 and is field testing biotech potatoes and exploring biotech cotton and rice.29 Indonesia

393

planted drought tolerant sugarcane, Brazil a HT soybean and Viet Nam approved biotech maize.

394

All of these plantings are contributing to a more stable food supply worldwide. The US recently

395

approved a reduced lignin alfalfa with higher digestibility and yield and a potato that when fried

396

produces 50-70% less acrylamide. The potato does not contain genes from other species but

397

fragments of a related wild potato DNA that silence the potato’s own genes for production of

398

certain enzymes.

399

Need for Continued Crop Improvements

400

Projections on world population growth coupled with a shrinking amount of prime agricultural

401

land that is forcing the use of sub-optimal land for crops, indicates the continued need for

402

improvements in agriculture.45 Climate change and the impact of agriculture on climate change

403

is also a factor.46 Climate change is normal, but the rate of change in recent years exceeds

404

normal.47 Climate change affects several aspects of agriculture including soil warming and

405

increasing soil respiration. The development of plants with attributes of drought and salt

406

tolerance, and early maturation will help to address the trend of declining rainfall and increasing

407

temperatures in agricultural areas and overcome the increased susceptibilities to disease and


Page 18 of 32

Page 19 of 32


408

pests.40 Plants that are more efficient in fixing nitrogen would need less nitrogenous fertilizer

409

reducing the contribution of fertilizers to greenhouse gas emissions and the accelerated

410

eutrophication of waterways.48

411

Accomplishments and Challenges for Omics

412

Omics won’t produce a vegetable such as Minnesota Cuke of Veggie Tales fame but it can

413

provide potential health benefits to consumers, contribute to a stable food and energy supply,

414

help preserve and protect the environment, benefit farmers and help eliminate world hunger.

415

Omics has furthered our understanding of pesticide biodegradation, and the mechanisms of

416

pesticide resistance and metabolism, leading to the development of more effective and safer

417

pesticides and the identification of biomarkers to determine human and environmental

418

exposures.49 The increased knowledge and insights gained from plant genomics are leading to

419

unexpected discoveries and conceptual advances in understanding plant biology. The DOE

420

Office of Biological and Environmental Research is a program providing a predictive, systems-

421

level understanding of plants.50 Through the advances made by omics, large scale collections of

422

proteins (proteomes), interactions between proteins (interactomes), metabolites (metabolomes),

423

and collections of observable characteristics (phenomes), is enabling a systems biology approach

424

for understanding plants from the single cell to the mature plant not only during development,

425

but importantly under changing environmental conditions.51

426

Omics has increased our ability to feed a hungry world, particularly populations that live in less

427

than ideal agricultural regions. Regulators, however, are faced with balancing the enthusiasm of

428

researchers who want their new products to be immediately on the market, with public interest

429

groups and consumers who urge caution and do not want modern genetically enhanced foods.



430

The U.S. approach for evaluating products from biotechnology is a coordinated, risk based

431

system to ensure public safety and the continuing development of biotech products.52 The policy

432

focuses on the product of genetic modification, not the process itself; considers genetic modified

433

products to be on a continuum with existing products and therefore employs existing statues for

434

their review.52 In short, the regulations are based on proving substantial equivalence. Recalling

435

Burbank’s plant breeding experiments, the terms plumcot and apriplum have both been used for

436

various fruits derived from plum and apricot parents and are considered equivalent. Thus, the

437

concept of substantial equivalence is not new to plant breeding. Prior to commercialization of a

438

transgenic crop, thousands of genes and transformation events are evaluated. In addition to

439

determining the equivalence of the transgenic with a traditional crop, a safety assessment of the

440

gene and protein product is performed. Among other parameters, the performance of the

441

transgenic plant and the environmental impact of its cultivation are also determined.53

442

Compositional analysis comparisons between transgenic and traditional crops are an important

443

aspect of the safety and risk assessment process.54, 55 Compositional analyses can detect

444

unintended changes which can occur with any genetic manipulation process.56

445

Agricultural researchers must engage the consumers of their research products particularly as

446

demographics have transitioned away from agriculture in developed countries. This increasing

447

disconnect has brought a renewed consumer interest in food production which is not always

448

answered by sound science and is often fueled by misconceptions. Ironically, some certified

449

organic brands, whose companies support strict labeling or outright bans on biotech crops, sell

450

certified organic products that were developed using both chemical and nuclear mutagenesis

451

without reference to this genetic manipulation.4


Page 20 of 32

Page 21 of 32


452

Consumer interest in agricultural practices must be addressed with fact and not opinion, and

453

must be used to benefit agricultural research for both industrialized and agrarian based societies,

454

without hindering a hungry world from feeding itself. A systems approach of sound science,

455

social ramifications, and economic considerations is needed for understanding and embracing

456

products of omics research. Sociological implications differ between industrialized and agrarian

457

nations and must be defined and addressed. There needs to be close collaborations and

458

cooperation between scientists, regulators and the public. Many scientists have voiced concerns

459

that their research is not automatically embraced and unfortunately blame regulators while doing

460

little or nothing to educate the public, the potential consumers of their research. Scientists in

461

omics research need to do their part by dispelling opinions with facts. The modification of

462

biological organisms through any process can carry potential safety risks, raising issues which

463

must be defined and addressed in a manner to satisfy consumers. To ensure biosafety, scientific

464

expertise must be applied to the analysis of biotech crops, their progeny and anticipated

465

environmental interactions for a sound risk assessment, which ironically can be accomplished, in

466

part, with omic studies.57

467

Global organizations have greatly facilitated cooperation among researchers. Both the Human

468

Genome Project and the sequencing of the rice genome were completed earlier than anticipated

469

due to widespread collaborations. Websites such www.gmoanswers.com and

470

www.biotechbenefits.croplife.org provide public forums for discussion and vetting information

471

on biotech crops. The importance of a public forum to engage scientists and the public regarding

472

the safety of biotech crops cannot be over emphasized. A recognized center for researching the

473

safety of biotech crops could also provide opportunity for scientists to interact with the public so

474

that informed decisions can be made at all levels of engagement.48 21 ACS Paragon Plus Environment


475

We can see that omics can revolutionize agricultural research in many exciting areas and fulfill

476

the National Agricultural Biotechnology Council’s vision for the future of agriculture. The omics

477

pipeline is full of promise including more functional foods such as tomatoes with high levels of

478

flavonols to reduce health risks, foods with higher levels of phytosterols to reduce cholesterol,

479

and plants for producing drugs to address specific health issues. Drought tolerant maize, arsenic-

480

tolerant plants, low lignin trees for paper making, longer bananas with a longer shelf-life, plants

481

that can fix ambient N2, and plants with increased bioluminescence to provide lighting are all

482

potentials. Wine with increased resveratrol for the reduction of oxidized lipids in vivo would be

483

welcomed by enophiles. However, silencing the gene responsible for caffeine production in

484

coffee plants may not be so readily embraced particularly at 6:00 in the morning.58

485 486

Notice: The United States Environmental Protection Agency through its Office of Research and

487

Development has provided administrative review of this article and has approved for publication. The

488

views expressed in this article are those of the author and do not necessarily reflect the views or policies

489

of the U.S. EPA. Mention of trade names or commercial products does not constitute endorsement or

490

recommendation for use.

491 492 493 494 495 496 497 22 ACS Paragon Plus Environment

Page 22 of 32

Page 23 of 32

498 499 500 501 502 503 504 505 506 507 508 509 510 511 512 513 514 515 516 517 518 519 520 521 522 523 524 525 526 527 528 529 530 531 532 533 534 535 536 537


References 1. National Agricultural Biotechnology Council. Vision for Agricultural Research and Development in the 21st Century. http://nabc.cals.cornell.edu/Publications/WhitePapers/NABCvision.pdf 2. Burbank, L. Fruit Improvement. In How Plants are Trained to Work for Man; P.F. Collier & Son Company: New York, NY, 1921; Vol. 3, 85. 3. United Nations Report of the Food and Agriculture Organization, International Atomic Energy Agency. Plant Breeding and Genetics Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture. (http://www-naweb.iaea.org/nafa/pbg/index.html) (03/17/2015) 4. Fedoroff, N.V.; Brown, N.M. In Mendel in the Kitchen, Joseph Henry Press: Washington, DC, 2004. 5. Ahmad, P.; Ashraf, M.; Younis, M.; Hu, X. Kumar, A.; Akram, N.A.; Al-Qurainy, F. Role of transgenic plants in agriculture and biopharming. Biotechnol. Adv. 2012, 30, 524–540. 6. Ibáñez, C.; Simó, C.; Garcia-Cañas, V.; Cifuentes, A.; Castro-Puyana, M. Metabolomics, peptidomics and proteomics applications of capillary electrophoresis-mass spectrometry in foodomics: a review. Anal. Chim. Acta. 2013, 802, 1-13. 7. Garcia-Cañas, V.; Simó, C.; Herrero, M.; Ibáñez, E.; Cifuentes, A. Present and future challenges in food analysis: foodomics. Anal. Chem. 2012, 84, 10150-10159. 8. Chassy, B.M. Can-omics inform a food safety assessment? Regul. Toxicol. Pharm. 2010, 58, S62-S70 9. Cornille, A.; Gladieux, P.; Smulders, M.J.M.; Roldán-Ruiz, I.; Laurens, F.; Le Cam, B.; Nersesyan, A.; Clavel, J.; Olonova, M.; Feugey, L.; Gabrielyan, I.; Zhang, X.-G.; Tenaillon, M.I.; Giraud, T. New insight into the history of domesticated apple: secondary contribution of the European wild apple to the genome of cultivated varieties. PLOS Genet. 2012, 8(5), e1002703. 10. Lin, T.; Zhu, G.; Zhang, J.; Xu, X.; Yu, Q.; Zheng, Z.; Zhang, Z.; Lun, Y.; Li, S.; Wang, X.; Huang, Z.; Li, Junming.; Zhang, C.; Wang, T.; Zhang, Yuyang; Wang, A.; Zhang, Yancong; Lin, K.; Li, C.; Xiong, G.; Xue, Y.; Mazzucato, A.; Causse, M.; Fei, Z.; Giovannoni, J.J.; Chetelat, R.T.; Zamir, D.; Städler, T.; Li, Jingfu.; Ye, Z.; Du, Y.;



538 539 540 541 542 543

Hurang, S. Genomic analyses provide insights into the history of tomato breeding. Nat. Genet. 2014, 46(11), 1220-1226. 11. The PEW Charitable Trusts. Application of Biotechnology for Functional Foods. 2007, (http://www.pewtrusts.org/en/research-and-analysis/reports/0001/01/01/application-ofbiotechnolgy -for-functional-foods/) (08/20/2014)

544 545 546 547 548 549 550

12. Beyer, P.; Al-Babili, S.; Ye, X; Lucca, P.; Schaub, P.; Welsch, R.; Potrykus, I. Golden Rice: Introducing the β-carotene biosynthesis pathway into rice endosperm by genetic engineering to defeat vitamin A deficiency. J. Nutr. 2002, 132, 506S–510S.

551 552 553 554 555 556 557 558 559

14. The Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 2000, 408(14), 796–815.

560 561 562 563 564 565 566 567 568 569 570 571 572 573 574 575 576 577

17. Valdes, A.; Ibanez, C.; Simό, C.; García-Cañas, V. Recent transcriptomics advances and emerging applications in food science. Trends Anal. Chem. 2013, 52, 142–154.

13. An Overview of the Human Genome Project, http://www.genome.gov/12011238, (Accessed: 19 September 2014).

15. International Rice Genome Sequencing Project.The map-based sequence of the rice genome. Nature 2005, 436(11), 793–800. 16. GenBank Overview, http://www.ncbi.nlm.nih.gov/genbank/, (Accessed: 23 September 2014)

18. Roberts, K.M. Proteomics and a future generation of plant molecular biologists. Plant Mol. Biol. 2002, 48, 143-154. 19. Cilindre, C.;Jegou, S.; Hovasse, A.; Schaeffer, C.; Castro, A.J.; Clement, C.; Van Dorsselaer, A.; Jeandet, P.; Marchal, R. Proteomic approach to identify champagne wine proteins as modified by Botrytis cinerea infection. J. Proteome Res. 2008, 7, 11991208. 20. Agrawal, G.K.; Pedreschi, R.; Barkla, B.J.; Bindschedler, L.V.; Cramer, R.; Sarkar, A.; Renaut, J.; Job, D.; Rakwal, R. Translational plant proteomics: A perspective. J. Proteomics 2012, 75, 4588-4601. 21. Aliferis, K.; Chrysayi-Tokousbalides, M. Metabolomics in pesticide research and development: review and future perspectives. Metabolomics 2011, 7(1), 35–53.


Page 24 of 32

Page 25 of 32

578 579 580 581 582 583 584 585 586 587 588 589 590 591 592 593 594 595 596 597 598 599 600 601 602 603 604 605 606 607 608 609 610 611 612 613 614 615 616 617 618


22. Dixon, R.; Gang, D.; Charlton, A.; Fiehn, O.; Kuiper, H.; Reynolds, T.; Tjeerdema, R.; Jeffery, E.; German, J.B.; Ridley, W.; Seiber, J. Applications of Metabolomics in Agriculture. J. Agric. Food Chem. 2006, 54, 8984–8994. 23. Teng, Q. Structural Biology: Practical NMR Applications; Springer: New York, NY, 2013. 24. Valdes, A.; Simo, C.; et al. Foodomics strategies for the analysis of transgenic foods. Trends Anal. Chem. 2013, 52, 2–15. 25. Wang, X.; Wang, S.; Cai, Z. The latest development and applications of massspectrometry in food-safety and quality analysis. Trends Anal. Chem. 2013, 52, 170–185. 26. Shi, Y.; Jiang, L.; Kang, R.; Yu, Z. Dynamic changes in proteins during apple (Malus x domestica) fruit ripening and storage. Hortic. Res. 2014, 1. 27. Wang, J.; Kliks, M.M.; Qu, W.; Jun, S.; Shi, G.; Li, Q.X. Rapid determination of the geographical origin of honey based on protein fingerprinting and barcoding using MALDI TOF MS. J. Agr. Food Chem. 2009, 57, (21), 10081-10087. 28. Mamone, G.; Picariello, G.; Caira, S.; Addeo, F.; Ferranti, P. Analysis of food proteins and peptides by mass spectrometry-based techniques. J. Chromatogr. A 2009, 1216, 7130-7142. 29. James, C. 2014, Global Status of Commercialized Biotech/GM Crops: 2014. ISAAA Brief No. 49. ISAAA: Ithaca, NY. 30. Bass, C.; Puinean, A.M.; Zimmer, C.T.; Denholm, I.; Field, L.M.; Foster, S.P.; Gutbrod, O.; Nauen, R.; Slater, R.; Williamson, M.S. The evolution of insecticide resistance in the peach potato aphid, myzus persicae. Insect Biochem. Mol. Biol. 2014, 51, 41-51. 31. Langridge, W. Edible vaccines. Sci. Am. 2000, 9, 66–71. 32. Giritch,A.; Marillonnet, S.; Engler, C.; Van eldik, G.; Botterman, J.; Klimyuk, V.; Gleba, Y. Rapid high-yield expression of full-size IgG antibodies in plants coinfected with noncompeting viral vectors. Proc. Natl. Acad. Sci. USA 2006, 103(40), 14701-14706. 33. Lai, H.; Engle, M.; Fuchs, A.; Keller, T.; Johnson, S.; Gorlatov, S.; Diamond, M.D.; Chen, Q. Monoclonal antibody produced in plants efficiently treats West Nile virus infection in mice. Proc. Natl. Acad. Sci. USA 2010, 107(6), 2419-2424.



619 620 621 622 623 624 625 626 627 628 629 630 631 632 633 634 635 636 637 638 639 640 641 642 643 644 645 646 647 648 649 650 651 652 653 654 655 656 657 658 659 660 661 662

34. Both, L.; van Dolleweerd, C.; Wright, E.; Banyard, A.C.; Bulmer-Thomas, B.; Selden, D.; Altmann, F.; Fooks, A. R.; Ma, J.K.-C. Production, characterization, and antigen specificity of recombinant 62-71-3, a candidate monoclonal antibody for rabies prophylaxis in humans. FASEB J. 2013, 27, 1-11. 35. Drake, P.M.W.; Barbi, T.; Drever, M.R.; van Dolleweerd, C.J.; Porter, A.J.R.; Ma, J.K.C. Generation of transgenic plants expressing antibodies to the environmental pollutant microcystin-LR. FASEB J. 2010, 24, 882-890. 36. Corbett, P. PBI Bulletin 2002, Issue 1. Diversification of Canadian oilseeds. Part 1: adding value to oil – soybean oil products: composition, quality and stability. (http://www.pbi.nrc.ca/en/bulletin/2002issue1/page3.htm) (8/20/2014) 37. Liu Q.; Singh,S.; Green, A. High-oleic and high-stearic cottonseed oils: Nutritionally improved cooking oils developed using gene silencing. J. Am. Coll. Nutr. 2002, 21, 205S211S. 38. Sharma, A.K. and Sharma, M.K. Plants as bioreactors: recent developments and emerging opportunities. Biotechnol. Adv. 2009, 27, 811-832 39. Pan, P., Van Emon, J.M. Application in Pesticide Analysis: Liquid Chromatography – A Review of the State of the Science for Biomarker Discovery and Identification. In High Performance Liquid Chromatography in Pesticide Residue Analysis; CRC Press Taylor & Francis Group LLC: New York, NY, 2015, 449-468. 40. Eaglesham, A.; Hardy, R.W.F. NABC Report 21: Adapting Agriculture to Climate Changes. National Agricultural Biotechnology Council, 2009. (http://nabc.cals.cornell.edu/pubs/pubs_reports.cfm#nabc21) (8/23/2014) 41. Johnson, T.S.; Eswaran, N.; Sujatha, M. Molecular approaches for improvement of Jatropha curcas Linn. as a sustainable energy crop. Plant Cell. Rep. 2011, 30, 15731591. 42. National Research Council. Biobased Industrial Products. National Academies Press. Washington, DC. 2000. 43. The Whitehouse. National Bioeconomy Blueprint. www.whitehouse.gov/national_bioeconomy_blueprint_april_2012.pdf (8/19/2014) 44. Biodesic 2011 Bioeconomy Update. http://www.biodesic.com/library/Biodesic_2011_Bioeconomy_Update.pdf (8/20/2014) 45. Monitoring Global Population Trends, http://www.un.org/en/development/desa/population/, (Accessed: 13 March 2015) 26 ACS Paragon Plus Environment

Page 26 of 32

Page 27 of 32

663 664 665 666 667 668 669 670 671 672 673


46. ACS Climate Science Toolkit, http://www.acs.org/content/acs/en/climatescience.html, (Accessed: 3 June 2015) 47. National Research Council. Advancing the Science of Climate Change. National Academies Press. Washington, DC. 2010 48. Fedoroff, N.V.; Battisti, R.N.; Beachy, R.N.; Cooper, J.M.; Fischhoff, D.A.; Hodges, C.N.; Knauf, V.C.; Labell, D.; Mazur, B.J.; Molden, D.; Reynolds, M.P.; Ronald, P.C.; Rosegrant, M.W.; Sanchez, P.A.; Vonshak, A.; Zhu, J.-K. Radically rethinking agriculture for the 21st century. Science 2010, 327, 833-834.

674 675 676 677 678

49. Qi, S-W; Li, Q.X. Proteomics in Pesticide Toxicology. In Hayes’ Handbook of Pesticide Toxicology; Academic Press: New York, NY; Vol. 1, pp. 603-626.

679 680 681 682 683

51. National Science and Technology Council. National Plant Genome Initiative Five-Year Plan: 2014-2018 (http://www.whitehouse.gov/sites/default/files/microsites/ostp/NSTC/npgi_fiveyear_plan_5-2014.pdf) (8/19/2014)

684 685 686 687 688 689 690 691 692 693 694 695 696 697 698 699 700 701 702 703 704

52. Library of Congress. Restrictions on Genetically Modified Organisms. http://www.loc.gov/law/help/restrictions-on-gmos/usa.php (8/19/2014)

50. Genome Portal, http://genome.jgi.doe.gov/genome -projects/, (Accessed 30 January 2015)

53. Privalle, L.; Gillikin, N.; Wandelt, C. Bringing a transgenic crop to market: Where compositional analysis fits. J. Agric. Food Chem. 2013, 61, 8260–8266. 54. Brune, P.; Culler, A.; Ridley, W.; Walker, K. Safety of GM crops: Compositional analysis. J. Agric. Food Chem. 2013, 61, 8243–8247. 55. Hoekenga, O.; Srinivasan, J.; Barry, G. Bartholomaeus, A. Compositional analysis of genetically modified (GM) crops: Key issues and future needs. J. Agric. Food Chem. 2013, 61, 8248–8253. 56. Herman, R.; Price, W. Unintended compositional changes in genetically modified (GM) crops: 20 years of research. J. Agric. Food Chem. 2013, 61(48), 11695–11701. 57. Mehrotra, S.; Goyal, V. Evaluation of designer crops for biosafety – A Scientist’s Perspective. Gene 2013, 515, 241-248. 58. Jameel, S. Genetically decaffeinated coffee. J. Biosci. 2003, 28, 529–531



705

Figure Captions

706

Figure 1. Omics research has expanded into several disciplines.

707

Figure 2. The interrelationships of omic disciplines.

708 709 710

Figure 3. A simplified description for making a trans-genic plant. In agriculture, the bacteria Argobacterium tumefaciens is often used as a vector to deliver genes into plants. The bacteria are parasites with the natural ability to transfer their genes into plants.

711 712 713 714 715 716 717 718 719 720 721 722 723 724 725 726 727 728 729 730 28 ACS Paragon Plus Environment

Page 28 of 32

Page 29 of 32


Excotoxicogenomics

Foodomics

Transcriptomics

Proteomics

Omics

Agricultural economics

Genomics Metabolomics

Figure 1



Page 30 of 32

Interrelationships of Omic Disciplines Genomics

Transcriptomics

Proteomics

Metabolomics

DNA

RNA

Proteins

Metabolites

Figure 2


Page 31 of 32




Table of Contents Graphic


Page 32 of 32

The Omics Revolution in Agricultural Research - ACS Publications

Recommend Documents