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Metabolomics for Plant Improvement: Status and Prospects

Rakesh Kumar, Abhishek Bohra, Arun K. Pandey and 2 more

Frontiers in Plant Science · 2017 · Review

doi:10.3389/fpls.2017.01302

Abstract

Post-genomics era has witnessed the development of cutting-edge technologies that have offered cost-efficient and high-throughput ways for molecular characterization of the function of a cell or organism. Large-scale metabolite profiling assays have allowed researchers to access the global data sets of metabolites and the corresponding metabolic pathways in an unprecedented way. Recent efforts in metabolomics have been directed to improve the quality along with a major focus on yield related traits. Importantly, an integration of metabolomics with other approaches such as quantitative genetics, transcriptomics and genetic modification has established its immense relevance to plant improvement. An effective combination of these modern approaches guides researchers to pinpoint the functional gene(s) and the characterization of massive metabolites, in order to prioritize the candidate genes for downstream analyses and ultimately, offering trait specific markers to improve commercially important traits. This in turn will improve the ability of a plant breeder by allowing him to make more informed decisions. Given this, the present review captures the significant leads gained in the past decade in the field of plant metabolomics accompanied by a brief discussion on the current contribution and the future scope of metabolomics to accelerate plant improvement.

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From PubMed Central, U.S. National Library of Medicine, as current on Oct 22, 2026. Paragraph numbers are ours, so an answer can point at one.

Introduction

1Recent years have witnessed huge developments in different ‘Omics’ fields, namely genomics, transcriptomics, epigenomics, proteomics, metabolomics and phenomics. The information generated by these ‘Omics’ approaches has enhanced precision and speed to the ongoing breeding programs in developing climate smart and nutrition rich germplasm, which is key for ensuring food security. In recent times, the role of phenomics-based breeding has become evident in improving the crop’s performance, and similarly, genomics has made notable contribution in achieving higher genetic gains. Nevertheless, the diverse omics platforms have great potential in improving the current understanding of important traits, enabling us to develop new strategies for plant improvement. Among omics approaches, the metabolomics is the most complex and has received inadequate attention in crop science, particularly for trait mapping and plant selections.

2Metabolites are indispensable component of plant metabolism owing to their influence on plant biomass and architecture. In recent years, metabolomics has established itself as one of the major breakthroughs in science, paving the way for accurate metabolite profiling in microbes, plants and animals. Metabolomics has the ability to detect a vast array of metabolites from a single extract, thus allowing speedy and precise analysis of metabolites. In other words, metabolomics offers a comprehensive view of cellular metabolites like small organic compounds, which participate in different cellular events, thus representing the absolute physiological state of a cell. In view of the rapidly advancing metabolomics, the metabolite investigation of mutants and transgenic lines holds potential to understand the metabolic networks and to pinpoint the underlying candidate gene(s). Also, the metabolomics helps to resolve gene‘s’ function: how a particular gene impacts upon the metabolic pathway, and uncovers different layers of regulation and interception between linked pathways, which otherwise is difficult to achieve by conventional assays like microarray. An integrated approach accommodating inferences from genomics, transcriptomics, proteomics, and metabolomics will allow researchers for cataloging and prioritizing the genes to improve important traits in crop species. Further, above-mentioned omics studies have been further extended to explore the associated regulatory steps such as epigenetic regulation, post-transcriptional and post-translation modification. To this end, the interactome network studies aiming to reveal molecular interactions between biomolecules (nucleic acid, proteins, amino acids, carbohydrates, lipids, etc.) deepen our knowledge about the genotype–phenotype relationship.

3Metabolomics is being increasingly used in many crop species irrespective of the availability of transgenic system. The metabolomics has the potential to facilitate selection of superior traits and improvement of breeding materials. In conjunction with the advances in metabolomics, the availability of whole genome sequence, genome-wide genetic variants and cost-effective genotyping assays opens exciting opportunity to effectively integrate metabolomics in crop breeding programs.

4The methods and tools employed in metabolomics study, including the mass spectrometry (MS) and nuclear magnetic resonance (NMR) spectroscopy have witnessed substantial improvement. The currently available metabolomics platforms have the capacity to allow large-scale metabolite surveys covering both known as well as unknown metabolites. The deluge of such data, however, makes annotation of metabolites a considerable challenge. In this context, the ever growing strength of bioinformatics tools coupled with the establishment of metabolomics databases such as the one for model plant Arabidopsis1, and others for various plant species2 have greater implications for metabolite annotation. A considerable amount of data have resulted from metabolic surveys, which might support plant improvement schemes focusing on the traits of agricultural importance such as yield and stress tolerance. Further, rapid generation of genome scale data by sequencing of DNA and RNA, and by MS quantification of proteins and metabolites necessitates integration of these information in order to devise a holistic way of improving traits of interests. Although, most of the current studies are coming in well-established model organisms, such studies may be of common occurrence in other plant species as well. Scientific community currently faces a herculean challenge of dealing with massive multi-omics data for conducting systems-level analyses. In such scenario, improved statistical and bioinformatics tools will be required to analyze these data sets together for better consolidation, which can eventually be translated for improving plant performance. In this review, we briefly describe about the latest investigations on plant metabolites and the application of metabolomics including metabolic engineering for plant improvement.

Analytical Tools for Metabolomic Studies

5The modern metabolomics platforms involve generation of metabolome data using two important techniques, namely NMR and MS (Figure 1). The NMR based metabolite detection relies upon the utilization of magnetic properties of nuclei of atoms under magnetic field. The NMR is a non-destructive method extensively used to identify metabolites with smaller molecular weight (<50 kDa) for diverse applications like metabolite fingerprinting, profiling, metabolic flux and extracting the atomic structural information of compound present in the biological samples. However, the poor sensitivity of this technique owing to a limited coverage of low-abundance biomarkers poses a major limitation that in turn restricts its extensive use. Unlike NMR, greater sensitivity of MS allows researchers to attain a wide coverage of metabolome data. This led researchers to identify novel metabolic biomarker, and molecules that can facilitate the reconstruction of metabolic pathways and networks. Recently, MS has achieved greater accuracy with the advances in the ionization methods such as atmospheric pressure chemical ionization (APCI), electrospray ionization (ESI) and MALDI-TOF. For enhancing the throughput, MS is usually combined with chromatography techniques such as gas chromatography (GC), liquid chromatography (LC), capillary electrophoresis (CE), fourier transform ion-cyclotron resonance (FT-ICR) and field asymmetric waveform ion mobility spectrometry (FAIMS). Notwithstanding the low sensitivity and large sample requirement of NMR, its capacity of identifying physical properties of ligands, binding sites on protein, uncovering structures of protein ligand complexes and direct binding of target protein retains its use over MS.

6The GC-MS platform is widely used for non-targeted analysis. GC-MS approach involves derivatization of samples which makes the compounds volatile; however, this leaves underivatized compounds (except hydrocarbon) unnoticed during analysis. Introduction of GC X GC-TOF-MS has notably improved the separation of co-eluting peaks (deconvoluted peak) and also facilitated higher sample throughput. LC-MS mostly uses ESI and APCI; it has been widely used for targeted and non-targeted approach to detect both primary and secondary metabolites of higher mass i.e., <1500 Da. Additionally, the combination of UPLC with QTOF-MS has increased the peak resolution, mass accuracy and rapid identification of hundreds of metabolites in a short span of time. In addition to these platforms, CE-MS provides high-resolution separation of different groups of analytes (charged, neutral, polar and hydrophobic) in both targeted and untargeted metabolomics studies. FT-ICR-MS driven by high-resolution mass analysis facilitates detection of large-scale metabolite species with high accuracy, which could also be combined with separation techniques in order to resolve “very complex matrices” and to tackle other issues including ion separation. Additionally, FAIMS or differential mobility spectrometry (DMS) an ion mobility based electrophoretic technique coupled with MS. The FAIMS technology was used for the detection of biological samples like volatile compounds formed during bacterial growth.

7Exhaustive data set generated from above high throughput tools are processed through data processing platforms like MET-COFEA, Met-Align, ChromaTOF, MET-XAlign, etc.,. This basically includes baseline correction, alignment, separation of co-eluting peaks (deconvolution), normalization, etc. (Figure 1) prior to identification of compounds. Metabolome databases like METLIN, NIST, GOLM etc., can be used for identification of metabolites. Further, the identified metabolites data are subject to statistical analysis such as correlation map, principal component analysis (PCA), partial least squares (PLS), K-means clustering, boxplot, heatmap, reconstructing metabolic pathways etc., by using web tool and softwares such as MetaboAnalyst, Cytoscape, Statistical analysis tool etc.,. These analyses are useful to monitor and identify metabolic markers associated with several agronomic traits.

Metabolomics for Improvement of Fruits

8Metabolomics studies have provided greater insights in fruit biology specially related to ripening and quality. Tomato (Solanum lycopersicum) is a rich source of carotenoids, anti-oxidants and flavonoids. Metabolite segregation pattern of 50 tomato cultivars showed close agreement with segregation of fruit’s size. Metabolome is useful to dissect the ripening event by plotting a correlation with fruit transcriptome. Metabolome can be used to elucidate diverse and differential biochemical pathways exist in the fruits of tomato ILs and Ecotypes, and the ancestral species through genome wide metabolic survey.

9Apple (Malus spp.) contains beneficial nutrients in the peel and flesh, including antioxidants that reduce the risk of chronic diseases such as asthma, cancer, cardiovascular disease, and diabetes. The metabolite contents of the apple fruits are used to differentiate commercially important cultivars. For example, the cultivar ‘Golden Delicious’ contains a high load of myo-inositol, sugars and succinic acid; whereas, the cultivars ‘Red Delicious’ and ‘Fuji’ show relatively higher abundance of triterpene/sterols, flavonoids, phenolic acids, stearic acid, anthocyanins, and carbohydrates. The fruit peel extract of ‘Fuji’ contained high levels of carbohydrate including glucose and sorbitol, and was significantly differentiated from ‘Red Delicious’ and ‘Granny Smith’ which contain high levels of unsaturated fatty acids (oleic and linoleic acid). Spatial distribution of sugars and organic acids between fruit layers has been elucidated in a recent study on metabolic profiling of apple fruit. The browning of apple fruits during storage renders them unmarketable, thus exerting an adverse impact on the apple industry. The metabolomics study on stored apple fruits showed a difference in the level of primary metabolites with different time duration. The increased levels of mannose and xylose during post-harvest indicated a breakdown of cell wall hemicellulose, which enhances fruit senescence. The study by established a relation between metabolic regulation during post-harvest storage and cellular respiration and stress.

10In recent years, the Kiwifruit (Actinidia Lindl. spp.) has gained popularity in international markets due to its distinct appearance and the health benefiting nutrients such as vitamin C and fiber. A total of 51 metabolites were detected during kiwifruit development and ripening. The content of soluble sugars and ascorbate significantly changes during ripening, which eventually determines the fruit quality and taste. Hence, the quality and flavor of Kiwifruit can be improved by targeting the metabolites that can render consumer acceptance. In Kiwifruit, application of synthetic cytokinin N-(2-chloro-4-pyridyl)-N′-phenylurea significantly increases fruit size, and affects the ripening processes by altering the accumulation pattern of metabolites such as amino acids, sugars, organic acids etc.,.

11The quality and taste of orange (Citrus spp.) fruit depend on the composition of metabolites such as organic acids, sugars, vitamins, flavonoids, and carotenoids. The metabolomics study of orange bud mutant ‘Hong Anliu’ (accumulates higher levels of lycopene and sweeter than wild type) led to the identification of 130 metabolites that include acids, sugars, flavonoids, alkaloids, limonoids, coumarins, amino acids, and plant hormones. The flavor and the taste of ‘Hong Anliu’ sweet orange was determined by the higher levels of soluble sugars and lower levels of organic acids along with differential levels of flavonoids at ripe stage.

12The infection of Candidatus Liberibacter asiaticus, causal agent of Citrus Huanglongbing disease, deteriorates juice quality. The infection leads to severe decrease in glucose, fructose, sucrose and amino acids such as alanine, arginine, isoleucine, leucine, proline, threonine, and valine; whereas, it enhances the levels of citrate and phenylalanine. Heat treatment of fruit is widely used as a means to avoid fruit infection during post-harvest storage, which is well supported by metabolomics study. In a study, the heat treatment significantly decreased the content of organic acids and amino acid; however, it promoted the accumulation of metabolites such as 2-keto-D-gluconic acid, tetradecanoic acid, oleic acid, ornithine, succinic acid, myo-inositol, glucose, fructose, sucrose, and turanose, which reduces the risk of post-harvest infection. Recently, ABA is reported to serve as a regulator of citrus cuticular wax biosynthesis during fruit development.

13In grape (Vitis vinifera), the fruit setting relies upon the abundance of metabolites, and is regulated by the reprograming of hormones and sugar metabolism pathways. The effect of geographical distribution on grape metabolite content is well documented. The grapes grown in the regions perceiving high sun light-low rainfall show enhanced content of sugars and amino acids, Na and Ca, along with low levels of organic acids, suggesting the role of extrinsic factors on grape fruit qualities. The metabolite abundance in grapes berry that is reported to be stage specific and cultivar dependent, regulates the ripening processes. Stilbenes are the major polyphenols present in the grapes that determine the quality of drinking wine. The MS analysis of grapes allowed the detection of several bioactive stilbenes like ampelopsin H, caraphenol, isohopeaphenol, trans-resveratrol, Z- and E-astringin, piceatanno, Z- and E-piceid, B pallidol and pallidol-3-O-glucoside and parthenocissin A. The study focused on the polyphenolics content of the grape identified upto 450 compounds including anthocyanin, glycoside aroma precursors, flavanols and procyanidins, flavones and flavanones, phenolic acids and stilbenes. Particularly, this study allowed identification of several 100 compounds, which were used to build a new database of putative compounds (Grape Metabolomics).

14Pear (Pyrus communis), a member of Rosaceae, is grown worldwide for its unique ‘melting’ texture. Japan is one of the largest producers of pears. The metabolomics analysis of pear fruit confirmed differential accumulation of ∼250 metabolites during fruit development and ripening. Ripening of pear fruit manifested accumulation of sugars (e.g., sucrose), sulphur-containing amino acids, phytohormone such as ABA and brassinosteroids. This study reported detection of 15 phytohormones including abscisic acid, auxin, brassinosteroids, gibberellins, jasmonic acid and salicylic acid. The blooming stage shows a substantial increase of the metabolites (amino acids and organic acids), which further decreases during fruit development.

15Like pears, strawberry (Fragaria × ananassa) is rich in secondary metabolites such as flavonoids. The process of gain and loss of strawberry fruit flavors during evolution and domestication was illustrated by. The cultivated species of strawberry predominantly contain terpenoids such as monoterpene linalool and the sesquiterpene nerolidol. Whereas, the wild species were rich in the olefinic monoterpenes and myrtenyl acetate. Surprisingly, these were absent in the cultivated species. The untargeted (GC-MS) and targeted (HPLC) based studies of strawberry fruits were employed at seven different stages of fruit development. The metabolic study revealed a shift in the metabolite content during fruit development and ripening. The strawberry ripening involved rise of free amino acid content, with change in sugar content, including substantial changes in other major metabolic pathways such as ester biosynthesis, shikimate, and tricarboxylic acid.

16The effect of biotic stress and the fungicide (to avoid biotic stress) on strawberry quality was evaluated by quantitative estimation of primary and secondary metabolites accumulated in the infected and non-infected fruits. The Colletotrichum nymphaeae infection induces accumulation of sugars and reduces the organic acid content. The infected fruits displayed altered content of metabolites such as ellagic acid derivatives, flanonols, flavan-3-ols, oligomeric procyanidins and total phenolics. Recent work by revealed an increase in the polyphenol levels in white-fruited species of strawberry as a result of infection from fungal pathogens viz. Botrytis cinerea and Colletotrichum acutatum.

Metabolomics for Improvement of Legume Crops

17Forage and grain legumes contribute 27% of the world gross primary crop. The grain legumes alone cater 33% of required human dietary protein, contribute to food security and environmental sustainability. Notwithstanding the extensively investigated model legumes, metabolomics studies in other legumes remain limited. Concerning model legume, investigation of the effect of rhizobial node factor (Nod) in Medicago revealed a decrease in oxylipins. In another study, metabolic profiling of salt tolerant Lotus species uncovered a series of changes involving metabolic adjustments of shoot constituent for survival.

18Stress conditions such as salinity and anoxia result in an accumulation of alanine, and its biosynthesis co-substrates such as glutamate and GABA, and succinate in soybean. Differential expression was also obtained for genes involved in nitrogen fixation and fermentation in root. Interestingly, a negative correlation was observed for the amino acid derived from glycolysis and the TCA cycle during water logging, and several TCA cycle enzymes were induced upon exposure to water logging. Likewise, an attempt to elucidate the metabolic changes associated with flooding stress in soybean led authors to identify a set of 81 mitochondria associated metabolites, thus suggesting a boost in concentrations of metabolites involved in respiration and glycolysis such as, amino acids, NAD and NADH coupled with the depletion of free ATP. Under drought and salinity conditions, metabolite phenotyping of four different Mediterranean accessions of lentil suggested a decrease in intermediates of the TCA cycle and glycolytic pathway. Importantly, this study yielded metabolite markers for specific stress; such as threonate, asparagine/ornithine and alanine/homoserine for NaCl, drought and salinity, respectively. Another study that aimed to assess the impact of water deficiency on Lupinus albus demonstrated plant stem serving as a storage organ for sugars and amino acids. Importantly, tolerant plant accumulated significantly higher level of metabolites such as asparagine, proline, sucrose and glucose in the stem stelar region. The authors proposed reorganization of nitrogen and carbon metabolism pathways in plants in order to tolerate salinity stress. In soybean, consistent increase in pinitol (sugar alcohol, osmoprotectant) was reported in the tolerant plant at both normal and drought-stressed conditions. Similarly, accumulation of sucrose, free amino acids and soluble proteins was observed in tolerant soybean in response to water stress.

Metabolomics for Improvement of Cereal Crops

19Cereals remain the prime source of nutrition worldwide owing to their grains rich in vitamins, minerals, carbohydrates and fats. Cereals have been widely studied in order to quantity variation in metabolites and their association with sequence variation. In rice, different research groups have harnessed the potential of metabolomics in order to explore the metabolites diversity between different varieties and natural variants. Similarly, metabolomics studies in maize have allowed researchers to differentiate and subsequently select the superior genotypes with enhanced nutritional composition. Recently, metabolomic approach has been utilized to survey chemical diversity between different maize and rice variety and its natural variants. In maize, drought stress is reported to be regulated by amino acid metabolism. Photorespiration is tightly regulated under drought as the two amino acids involved in this pathway, glycine and serine are rendered up-regulated. Further, accumulation of glycine and myo-inositol was reported to relate with grain size of maize under drought, implicating these metabolites as potential markers for identifying drought tolerant maize. Similar work in rice demonstrated drastic induction of certain compounds in tolerant plants such as allantoin, galactaric acid, glucose, gluconic acid, glucopyranoside and salicylic acid, which could be considered as metabolite markers to address drought stress in rice. As demonstrated in sorghum by, the plant’s ability to acquire and reorganize its metabolic status in order to cope with drought shows considerable variation within species. Under drought condition, sorghum variety having a greater tolerance to drought (Samsorg 17) accumulated sugars and sugar alcohols in comparison with less drought tolerant variety (Samsorg 40) that accumulated free amino acids. Marked abundance of soluble sugars with amino acids was also observed in the roots of tolerant barley plants under salinity stress. Like drought, chilling stress is also known to induce accumulation of amino acids and carbohydrates. For example, chilling stress caused substantial changes in metabolic profiles of rice varieties viz. Nipponbare (Japonica) and 19-11 (Indica). The chilling tolerance of Nipponbare involved metabolic adjustment to activate antioxidation pathway by modulating key metabolites such as γ-glutamylisoleucine, γ-glutamylglutamine, 5-oxoproline, glycine, glutamate, adenine dinucleotide and putrescine. Further, chilling stress activates glycolytic pathway, however, normal activity is resumed during recovery phase. In both wheat and barley, cold stress expedites the amino acid pool and induces the GABA-shunt genes to promote conversion of glutamate to GABA. It is well established that cereal grains accumulate flavones/flavone-glycosides, which protects plants from various stresses. For example, rice produces plenty of flavone-glycosides to protect it from abiotic stress and herbivores. However, examination of herbivore-induced defense system in maize showed an increase in azealic acid, N-hydroxycinnamoyl tyramines, phospholipids, tryptophan, and 1,3-benzoxazin-4-ones. Accumulation of resistance related metabolites is also reported during plant–pathogen interaction. For instance, a tolerant variety of wheat can accumulate a wide range of metabolites conferring tolerance such as coumaroylputrescine and coumaroylagmatine during fusarium head blight. Further, evaluation of these hydroxycinnamic acid amide compounds and their placement on metabolic pathways has led to the identification of an important gene agmatine coumaroyl transferase (ACT).

Impact of High CO2 Stress on the Metabolome and its Attributes Toward Quality and Yield

20According to a report of the intergovernmental panel on climate change (IPCC), anthropogenic activity, deforestation and combustion of fossil fuel could boost CO2 level upto 700 ppm by 21003. The CO2 uptake and water availability are directly connected to photosynthesis and plant growth, and CO2 sequestration by plants helps in maintaining terrestrial ecosystems. A recent study by has shown the impacts of elevated atmospheric CO2 on plant growth rate, biomass and leaf area. Terrestrial plants and phytoplankton significantly utilize increased atmospheric CO2 to increase their biomass. However, enhanced CO2 levels might promote grass species in the long term, which is an encouraging finding concerning food crops such as cereal. Sustaining crop performance in the face of growing CO2 levels remains a key challenge of 21st century agriculture. Therefore, studies are required to understand the metabolic composition and the relevant alterations on metabolome due to high CO2 stress.

Effect on Quantity

21Fruit, grain and tuber are the ultimate sink organs of the plant. The growth of these sink organs is directly depends on the partitioning of photosynthate from source organ to sink. The sink organs store variety of metabolites which depends on species, source strength, composition of allocated photosynthate and plant requirement. To date several reports have been published that have focused on the correlation of high CO2 with yield (harvesting sink organ) in commercial crop species. For instance, high CO2 was reported to cause a significant increase in productivity due to the increased level of photosynthesis in rice, wheat and soybean. More recent studies in wheat and rice validated stimulation of yield under greater amount of atmospheric CO2. Though, the increase in soybean was quite consistent, it was not as significant and high as reported in the case of rice and wheat. Coupling enrichment of CO2 with drought stress in barley to examine yield loss rescue ability of elevated CO2 suggested that modern barley cultivar could perform better under climate change. Similar result was obtained earlier in potato in which enriched CO2 farming led a 54% increase of tuber yield. Likewise, enhanced CO2 level registered higher yield in cotton, however, it was lower than the yield obtained under elevated temperature.

Effect on Quality

22Obtaining crop produce with high quality also remains a global concern, especially at a time when a substantial proportion of the population worldwide is affected with nutrition related disorders. Though enhanced yield was witnessed as a result of elevated CO2, will this be able to meet the demand concerning nutritional quality and food security as most of these studies are being conducted in cereals that are rich in carbohydrate. Also, though elevated CO2 in atmosphere increases yield, it affects the C/N ration in C3 and C4 plants by altering nitrate assimilation. For instance, as shown by, wheat grown in the elevated CO2 open field condition manifests slower nitrate metabolism. The reduced nitrogen in cereal results from increased levels of carbohydrates. Metabolomics studies of wheat grown under CO2 enriched atmosphere have shown a substandard accumulation of amino acids, and a significant increase in fructose, fructan and lipidic content in grains. In soybean leaves, ureide (derived from urea) and total amino acid levels were increased at the early season, but, later it resumed to initial level. Similarly, a combination of temperature and elevated CO2 efficiently decreases the levels of amino acids in root of Chinese cabbage. In the strawberry fruit, elevated CO2 and high temperature increase the sugar and sweetness index along with a reduction in the antioxidant and nitrogen content. CO2 enrichment has also shown encouraging results in other crops, such as increase of vitamin A and C in tomato, and vitamin C in orange fruit. Taken together, it becomes evident that crop grown in elevated CO2 obtains higher yield to a certain extent; however, this may drastically affect the nutritional content, especially nitrogenous amino acids.

23Elevated CO2 was reported to exert a huge impact on mustard seed oil quality due to an increase in starch and oil content of seed at the expense of protein. The excess of carbohydrate affects the lipid composition of mustard seed, thus causing an increase in the concentration of oleic acid, and a simultaneous decrease in the content of linolenic acid and nervonic acid. The CO2 enrichment is reported to reduce the erucic acid (undesired factor) while improving mustard seed quality. In groundnut, elevated CO2 directed storage of high-quality oil in seeds of two varieties JL 24 and ICGV 91114 corroborated with the results reported in mustard. Similarly, sunflower seed showed a decrease in amino acids, proteins and minerals at high CO2 concentration, however, oil load with health-benefiting unsaturated acids was increased.

Effect of Biotic and Abiotic Stress on Plant Lipidome

24Lipids are an important constituent of cell membrane enclosing organelles and suborganelles, in which various biochemical reactions occur. Modern lipidomics has facilitated profiling of lipids to understand lipid dynamics and biosynthesis on exposure to a range of stresses.

25Plants adjust their lipid structure according to varying environmental conditions. For instance, cold tolerant plants increase the levels of desaturated glycerolipids to maintenance membrane fluidity. Freezing plants up to a sublethal temperature can induce the level of lysophospholipids, phosphatidic acid, and phosphatidylglycerol. In contrast, tolerance to heat stress involves an increase in saturated glycerolipids. Recently, MS based analysis revealed remodeling of lipids, antioxidants and galactolipids in tomato plant during high temperature stress. A combined glycerolipidomic and transcriptomics study provided insight on lipid remodeling, and regulatory genes involved in lipid biosynthesis and heat stress management. Most strikingly, high temperature can induce dramatic increase of lipid antioxidant such as α-tocopherol and plastoquinone/-ol, and saturation of membrane lipids like galactolipids and phosphatidyl ethanolamine.

26Hypoxia represents another important type of abiotic stress that plant faces due to excessive watering or flood and leads to limited O2 availability and increased salinity for a submerged plant. According to, plant cell synthesizes and accumulates unsaturated ceramides, a class of sphingolipids under hypoxia. More recently, root lipidic content of two barley genotypes was examined to understand the mechanism underlying their tolerance to salinity stress. Phosphorus availability during stress is known to directly affect the membrane lipid texture. For instance, Arabidopsis grown in phosphorus-deficient condition can induce replacement of phospholipids with non-phosphorus SQDG class lipids (galactolipids). These galactolipids are mostly associated with plastic thylakoid membrane, and phosphorus deprivation causes its enrichment in the roots extraplastidic membrane for survival.

27Compared to abiotic stress, lipidomics studies of biotic stress are scanty. During biotic stress, lipid peroxidation occurs due to formation of reactive oxygen species (ROS), ultimately leading to program cell death (PCD). A recent report suggests inositol phosphorylceramide synthase as instrumental to coordinate the PCD, a mechanism acquired by plants for its self-defense to limit biotrophic pathogens. Lipid peroxidation results in formation of jasmonate and oxylipins, which are signaling molecules during plant immune response. Recently, nearly 100 membrane-associated lipids were quantified in response to methyljasmonate and cerium, suggesting increase of lysophosphatidylcholine, phosphatidic acid and phosphatidylcholine associated with PCD. Plant–pathogen interaction also impacts upon plant cuticle that serves as a first physical barrier limiting pathogen invasion along with protecting plants from other physical damages. The cuticle layered over epidermal cells, is mainly composed of wax and cutin. The cutin is mainly composed of hydroxylated C16 and C18. The permeability of cuticle relies upon its composition, which can restrict the invasion of fungal pathogens such as Botrytis cinerea. The role of cuticle in relation to plant defense against pathogen invasion is well described in the recent articles.

Epigenetic Modifications and Plant Metabolites

28Epigenetic modification refers to DNA methylation and histone modification, which in turn alters the gene expression in a heritable fashion without causing any change in the underlying DNA sequence. For example, deformity of the flower in the toadflax (Linaria vulgaris) mutant was created due to extensive methylation and suppression of cyc-like gene that controls flower symmetry. Research during the last decade has led to a significant gain in the knowledge related to epigenetic influence on metabolism, however, most of the studies were confined to animal system. The reason may be less availability of epigenetic mutants in the plants. In plant breeding, the epialleles can serve as a novel source of trait variation.

29In Arabidopsis, disruption of MSH1 caused altered plant growth phenotypes due to hypermethylation of chromosome segments. Hypomethylation of RAV6 promoter in rice Epi-rav6 mutant resulted altered leaf size and grain size, via modulating brassinosteroid (BR) homeostasis. In maize, the IPA mutation affects the biosynthesis and accumulation of phytic acid in the seed, which influences germination along with affecting plant growth and responses to various environmental conditions. The maize epigenetic mutation lpa1-241 leads to drastic reduction of phytic acid and higher level of free inorganic phosphate in seeds. Similarly, epigenetic regulation of maize booster1, Pericarp color1, purple plant1 and red1 genes impacting upon anthocyanin and flavonoid biosynthesis is well documented. In tomato, whole genome bisulphite sequencing of fruit revealed methylation of 1% of the total genomic region. Further, it was demonstrated that epigenetic modification is not static during tomato fruit development and ripening, instead methylation of the promoter region significantly decreases for ripening specific genes such as ripening inhibitor (RIN) and colorless non-ripening (CNR). In fact, DNA methylation regulates fruit phenotype by altering wide range of primary and secondary metabolites in tomato. For example, methylation of SBP-box promoter of epigenetic mutant Cnr results in severe decline of ethylene and carotenoids, thus affecting fruit shelf life. Additionally, the interaction of CNR with RIN affects the expression of ripening related gene. The rin mutant exhibits reduced levels of carotenoids, downregulation of ethylene, amino acids, organic acids and sugars. A recent study in tomato has demonstrated that methylation in the promoter region of the gene 2-methyl-6-phytylquinol methyltransferase (VTE3) affects biosynthesis and accumulation of γ- and α-tocopherols. VTE3 underlies VTE quantitative trait locus (QTL) that is responsible for the modulation of important metabolic QTL. Domestication of allotetraploid cotton has resulted 12 million differentially methylated cytosines, which includes more than 500 genes contributing to agronomyic traits including seed dormancy and flowering time.

Correlation Analyses of Transcriptomics and Metabolomics

30Researchers increasingly focus on correlating metabolome with genomic segments to discover genetic determinants of regulatory pathways to improve compositional quality of crops species. Metabolome study in Arabidopsis has enriched the understanding of the metabolism and biosynthesis of glucosinolate, oil biosynthesis and oligosaccharides in seed. Recent advances have revealed an association of genetic variants with metabolites that could be used for metabolic engineering across various plant species such as Arabidopsis, broccoli, maize, mustard, potato, rice, sesame, tomato, and wheat. For example, study of Arabidopsis ecotypes Landsberg erecta from Cape Verdi Islands revealed a strong correlation of fatty acid desaturase 3 with the unsaturated fatty acid content (linoleic and linolenic acids) in seeds. The flavonoid biosynthesis in Arabidopsis is regulated by gene flavonol 7-O-rhamnosyltransferase, its transcripts accumulate with the flavonoid abundance in floral buds. Another study revealed induction of eight novel anthocyanins out of 1800 metabolites in an overexpression line of MYB transcription factor encoding PAP1 gene. These approaches in tomato and populus enabled gathering in-depth knowledge about the flavonoid biosynthetic pathway. Concerning the flavonoid metabolism pathway, a strong correlation between transcripts and metabolites was inferred in potato through combining transcriptomics and metabolomics approaches. The study captured interaction between 22 metabolites and 119 transcripts, which strongly regulate the anthocyanin content of light-red Hongyoung and dark-purple Jayoung potatoes. Analysis of 210 recombinant inbred lines (RILs) derived from Bay × Sha facilitated detection of more than 400 QTLs for 243 metabolites. Total 11 QTL clusters were obtained, of which five overlapped with expression QTLs reported in earlier studies. Importantly, epistatic interactions were noted in eight QTL clusters. In a similar fashion, genetic interactions explained the metabolic variation in maize. Two RIL populations (B73/By804 and Zong3/Yu87-1) were phenotyped for 155 metabolites and detected > 800 QTLs from both populations, majority of which had smaller effect sizes. This work provided deeper insights on flavonoid pathway, highlighting the significance of the p locus. Notably, 32 QTLs were cross validated between the two populations, whereas 57 associations detected in the genomic regions that overlapped with the QTLs detected earlier in genome-wide association studies (GWAS) performed by. In rice, 2,800 metabolite QTLs (mQTLs) were detected for 900 metabolites showing strong association with 24 candidate genes involved in various metabolic biosynthetic pathways, including O-glycosyl flavonols. Recently, metabolic profiling of leaf and fruits of five wild relatives of tomato (S. chmielewskii, S. habrochaites, S. neorickii, S. pennellii, and S. pimpinellifolium) showed a wide range of metabolome variability that are important for stress response, and also contribute to nutritional richness. Another study that combined transcriptomics and metabolomics of tomato fruits revealed a strong correlation between the ripening-induced transcripts and metabolites specific to the Krebs cycle and sugars. A more recent study consolidating profiling patterns of transcripts, proteins, and metabolites of ripening defective mutants non-ripening (NOR), never-ripe (Nr) and ripening-inhibitor (RIN) suggested shifts in the primary metabolites that eventually reduced metabolic activities during ripening. Metabolite QTLs analysis based on metabolic profiling of 76 introgression lines (ILs) of tomato has uncovered a strong regulation of seed metabolism during fruit development. Recently, a tomato Eco-TILLING population showed wide variation in the folate content in the fruits. Additionally, the genome-wide metabolomic survey of ILs and the ancestral species Solanum pennellii led to identification of important compounds such as Vit-E etc. and importantly, this analysis assigned nearly 2,000 compounds to the tomato genome. Interestingly, the segments introgressed from S. pennellii (Chromosomes 3, 6, 8, and 12) into ILs were reported to alter isoprenoids and tocopherols content at the fruit level and the study led authors to associate the differential expression of metabolites with photosynthesis and photorespiration. Similarly, metabolic profiling of aneuploid wheat highlighted the genes regulating variation in the branched chain amino acids and accumulation of trehalose in mature grain.

31Further, the use of metabolic information in genome wide predictions, as demonstrated by in hybrid maize, opens up novel opportunities to considerably enhance genetic gains. Similarly, modern techniques such as the epigenome wide association studies (EWAS) employed recently in human may also be extended to plants to better capitalize on the potential of trait-associations like “methylome-metabotype association” for accelerating plant improvement. Additionally, recent interactome network studies, which focus on molecular interactions between biomolecules (nucleic acid, proteins, amino acids, carbohydrates, lipids, etc.) provide deeper insights on correlation between genotype and phenotype.

Combining Proteome Analysis with Metabolite Profiling

32In addition to genomics, proteomics in combination with other modern high throughput approaches such as genomics and transcriptomics has contributed to revolutionize the omics era, and has paved the way to decipher the complex molecular mechanism underlying various commercial traits. For instance, the effect of pollutant ozone (O3) was studied in rice because it damages cellular tissue by creating ROS, thus altering photosynthetic ability that severely reflects in yield loss. It was reported that exposure of O3 to rice leaves significantly induced oligopeptidase-B and proteasome subunit alpha type1, which are involved in the 20S proteasome alpha subunit that mediate ATP dependent protein degradation. Further, O3 exposure induced accumulation of stress and metabolism related proteins such as glutathione peroxidase, aconitate hydratase, fumarylacetoacetase hydrolase, dehydrogenase P protein, and thiamine biosynthetic protein. These protein modulations in O3 exposed leaves were concomitant with dramatically increased levels of free amino acids, nucleotides and glutathione. A combined proteomics and metabolomics approach in response to temperature induced stress in Arabidopsis revealed several important markers. Cold or heat stress induces production of osmolytes (metabolic markers) proline, glutamine, raffinose and galacinol. In Arabidopsis, these metabolites were identified along with protein markers chloroplastidic glyceraldehyde-3-phosphate dehydrogenase (GAPDH), cytosolic GAPDH, chloroplast chaperonin, cyclophilins, protein 78, COR6.6 and several RNA binding proteins. Heavy metals are potential threat to crop productivity, accumulation of these elements causes developmental and physiological changes. For example, cadmium (Cd) accumulation retards plant growth and causes chlorosis. Such investigation has involved several plant species such as Arabidopsis, mustard, soybean, flax, Medicago, rice, pea, tomato, and spinach to understand the cellular responses to Cd stress. Cadmium induced toxicity in rice drastically affects the expression of RuBisCO, Calvin’s cycle and kreb’s cycle enzymes, which leads to attenuation of carbohydrate and amino acid metabolism. Further, the use of these platforms has been extended to understand biotic stress. Study of chickpea roots infected by Fusarium oxysporum suggested efficient and increased carbon and nitrogen metabolism, accumulation of phytoalexins, and lignification coupled with enhanced accumulation of proteins related to pathogenesis. Similarly, a system biology approach to understand the response of microbial symbioses on the pea plant metabolism under Didymella pinodes infection reports systemic resistance via adjustment of proteome and metabolome. The rhizobia associated resistant plants showed induction of amino acid, TCA, and secondary metabolism, including the pisatin, and proteins associated with pisatin biosynthesis. Coupling metabolomics with other omics tool has enabled researchers to acquire deeper knowledge of molecular events involved in important biological process required for plant sustainability (Figure 2). As a result, metabolomics has been exploited in several plant species to better understand the biological phenomena including plant development and stress response (Table 1).

Examples of Plant Improvement Through Metabolic Engineering

33Metabolites are the ultimate downstream factors that regulate and decide the cell fate; hence the content of metabolite directly affects organ physiology and often signifies the quality of fruits. The improvement of gene annotation is important to validate the gene function. In fact, it facilitates the use of these genes in the field of crop sciences to improve the quality and yield. This section describes significant leads achieved in the field of crop species through metabolic engineering.

Altering Photosynthate Levels to Change Fruit Dimensions

34Fruit development and weight are significantly correlated with the metabolic composition of fruit. The development of fruit represents substantial change of organic acid (predominantly citrate and malate) and sugars that determines the final quality of the ripe fruits. Unlike leaves, fruits act as a sink and its development depends on the translocation of photo-assimilates of leaves than that of own photosynthesis products. The impact of phloem translocate on fruit development and size was evident by concomitant increased growth for both flower and fruits with increased levels of photo-assimilate by reducing the number of flowers or fruits per truss. For example, the incubation of tomato plant in the dark significantly reduces fruit size and shape due to repression of cell cycle genes of fruit which severely affects the cell number and cell size.

35In order to investigate the correlation between sugar content and fruit size, the hexokinase 1 (AtHXK1) of Arabidopsis was over expressed in tomato plant. The overexpression line showed reduced fruit size due to reduction of cell expansion concomitant with reduced photosynthate. Additionally, transgenic fruits exhibited reduced respiratory rates accompanied by reducing ATP levels. The load of sucrose known to involve in the early stage of fruit development, import of sucrose in fruits is much needed in young fruits that influence fruit set and development. The establishment of relations between glycolysis, sucrose metabolism and organic acid biosynthesis was profound from the transgenic plants expressing malate dehydrogenase (mMDH) in tomato. The enhanced fruit dry mass of RNAi-mMDH plants was concomitant with enhanced photosynthetic ability, which improved carbon assimilation. The silencing of mMDH promoted the accumulation of redox stabilizing compounds such as l-galactono-1,4-lactone precursor of ascorbic acid. The silencing of l-galactono-1,4-lactone dehydrogenase (Gal-LDH) substantially affecting cell size that resulted in smaller fruits. Additionally, silencing of the key enzyme of ascorbate biosynthesis GDP-D-mannose 3,5-epimerase (GME) results defect in cell expansion and biosynthesis of cell wall non-cellulosic components. This finding suggests the direct influence of ascorbate in the process of channeling energy during respiration and photosynthesis, and fruit metabolite levels during tomato fruit development.

Exploring MYB Transcription Factors to Improve Fruit Quality

36In eukaryotes, MYB family transcription factors represent huge family, which controls diverse function such as development, metabolism, and stress related response. Sequencing of the Arabidopsis genome leads to the discovery of the several MYB transcription factors which are mostly characterized to R2R3-MYB family. In fruit anthocyanin biosynthesis regulated by R2R3-MYB transcription factor family. The red color of apple skin requires accumulation of anthocyanin, which is controlled by the expression of anthocyanin biosynthetic gene expression. MYB transcription factor MdMYBA and MdMYB10 positively regulates anthocyanin content in apple fruits by binding to the promoter region of anthocyanin biosynthesis genes. Interestingly, low temperature and UV-B exposure, enhance the expression of MYB, which enhances anthocyanin accumulation. Expression of MdMYBA under 35S promoter in tobacco results remarkable increase in the anthocyanin content of flowers. MdMYB10 share homology to PAP protein and overexpression of MdMYB10 in apple up-regulate anthocyanin in the whole part of regenerated transgenic plants, including the transformed callus. In Arabidopsis overexpression of MdMYB results elevated level of anthocyanin only in seeds, but not in the leaves. Like tobacco, Arabidopsis also lacks bHLH which interact with MYB to enhance the anthocyanin accumulation. In addition to bHLH, MYB also interacts with WD-repeat proteins and regulates anthocyanin biosynthesis through “MBW” complex, which is formed of MYB, basic helix-loop-helix (bHLH) TFs and WD-repeat proteins.

37In strawberry, overexpression of FaMYB10 resulted elevated levels of anthocyanin in the leaves, flowers, fruits, and roots. Recent studies suggest hormonal regulation of MYB expression: during ripening auxin negatively, but ABA positively regulates the expression of FaMYB10 in strawberry receptacles. In contrast to strawberry, overexpression of FaMYB1 in tobacco suppressed the accumulation of anthocyanin and flavonol by repression of tobacco homolog. MYB regulates the flavonoid levels in capsicum, Chinese bayberry and grape by up-regulating flavonoid biosynthetic genes encoding chalcone synthase (CHS), chalcone isomerase, flavanone 3-hydroxylase (F3H), flavonoid 30-hydroxylase (F30H), dihydroflavonol 4-reductase (DFR), anthocyanidin synthase (ANS) and UDP glucose: flavonoid 3-O-glucosyltransferase (UFGT). In grapes, VvMYBA1 and VvMYBA2 regulates the anthocyanin content of berries, for instance, inactivation of VvMYBA2 due to mutation in conserved domain results in white berries.

38Normally the fruits of cultivated tomatoes do not accumulate high levels of anthocyanin in the peel or flesh. However, the peel of tomatoes wild relative S. chilense relatively accumulate high levels of anthocyanin under control of MYB family transcription factor anyhocynin1 (ANT1). showed overexpression of S. chilense ANT1 and ANT2 in tomato cultivar exceptionally increased the levels of flavonoids in the cotyledon, leaves, floral organ and fruit peel. Additionally, the accumulation of flavonoid such as naringenin chalcone in the tomato fruit peel is controlled by SLMYB12, downregulation of it results colourless peel phenotype in yellow mutant, which was rescued by overexpression of MYB12. In tomato, the green shoulder at the top end is very common in wild type, but this phenotype lacks in uniform ripening (u) mutant. The U gene encodes for protein GOLDEN2-LIKE (GLK); a transcription factor, GARP subfamily of the MYB super family. Interestingly, overexpression of either SLGLK1 or SLGLK2 in both u and U background Ailsa Craig mimicked hp fruit phenotype such as enhanced chloroplast and high carotenoids.

Improving Fruit Shelf Life

39The initial evidence of ethylene in ripening led researchers to target genes such as ACS and ACO, which were involved in ethylene biosynthesis. The antisense ACS and ACO transgenic plants produce non-climacteric tomato fruits which ripen in presence of external ethylene. Similar results were obtained in other agronomic crops transgenic like melon and papaya. Later metabolite SAM and ACC, precursors of ethylene biosynthesis was targeted to achieve delayed ripening. SAM methyltransferases regulates the levels of SAM, which methylate homocysteine to methionine. SAM hydroxylase breaks SAM to methyl thioadenosine and homoserine instead of S-adenosyl-L-homocysteine thus resulting in low level of SAM. demonstrated the expression of the SAM hydroxylase in tomatoes fruit results reduced levels of ethylene and delayed ripening. On the other hand, the expression of prokaryotic ACC deaminase in tomato plant effectively decreases the available cellular ACC, which facilitates ethylene formation. The bacterial ACC deaminase protein is able to reverse the breakdown of ACC into α-ketobutyric acid and ammonia. Transgene expression of ACC deaminase enzyme in tomato resulted reduced ethylene levels that delayed ripening and enhanced post-harvest life. In apple, disruption of MdACS3 gene using a transposon-tagging technique confers prolonged shelf life of fruits.

40Respiration has huge impact on fruit shelf life. To elucidate the role of respiration on fruit texture and post-harvest sustainability, the levels of Krebs cycle intermediates were manipulated in tomato. The recent report of revealed that malate and fumarate plays significant role in the post-harvest transpirational water loss. The upregulation of both malate and fumarate in the transgenic of tomato antisense Malate dehydrogenase (MDH) resulted enhanced post-harvest shelf life due to decreased amount of post-harvest transpirational water loss.

Improving Quality

41The growth and development of plant is facilitated by hormones. The function of phytohormones in the tissue and organ differentiation was evident from the hybrids in Arabidopsis (C24/Col), where increased IAA level enhanced leaf cell numbers and reduced salicylic acid (SA) level promoted size of photosynthetic cells. The overexpression of Brassica gene shoot meristemless (STM) in Arabidopsis reduced the level of abscisic acid (ABA) and cytokinins, caused an enhanced growth of SAM and the ectopic meristem, which eventually reflected as lobed leaves, and increased number of reproductive organs such as flowers and siliques.

42A recent work suggests cross talk between hormones during growth and development. In tomato, inhibition of AUXIN RESPONSE FACTOR 7 (SlARF7) can produce seedless parthenocarpic fruits. Similarly, suppression of ARF4 and GH3 genes, combined with high ethylene production in AP2a suppressed transgenic lines suggest ethylene mediated response of auxin. Interestingly, non-climacteric fruits, such as grape and citrus are much more dependent on the ABA.

43In tomato, suppression of ABA biosynthetic gene 9-cis-epoxycarotenoid dioxygenase1 (NCED1) results non-climacteric pattern of ripening due to low levels of ethylene. In fact, ABA negatively regulates carotenoid levels in fruits. For example, ABA deficiency in hp3, flc and sit mutants of tomato causes over-pigmentation in fruits. Similar phenotype was evident in SlNCED1 silenced transgenic tomato fruits, which accumulates high levels of lycopene and β-carotene. In banana, ABA in coordination with ethylene promotes cell wall hydrolysis and fruit softening, whereas in grapes ABA promotes fruit colouration and softening. In non-climacteric fruits such as strawberry and grapes, ABA influences the flavonoid content, but in the ethylene dependent manner, because application of 1-methylcyclopropene (MCP, an ethylene inhibitor) delays anthocyanin accumulation. The role of ABA in flavonoid biosynthesis was confirmed through the rescue of colourless phenotype in NCED silenced strawberry fruits after exogenous ABA treatment. Likewise, methyl jasmonate enhances anthocyanin accumulation in the strawberry fruit peel by up-regulating phenyl-propanoid pathway related genes (CHS, DFR, UFGT, PAL1, C4H, CHI and F3H). In addition, MeJA and SA are also known to be involved in fruit softening. Recent work of provides direct evidences for the role of jasmonate in carotenoid biosynthesis. The jasmonate deficiency in the tomato mutants def1 (defective in the octadecanoid synthesis pathway) and spr2 (suppressor of pro-systemin-mediated responses2) reduces the lycopene content due to downregulation of carotenogenesis.

Response to Stress

44Mass spectrometry based plant metabolomics has geared up the evaluation of metabolite responses to stress. For instance, ABA is recognized as the stress response hormone that signals shoot for anti-transpirant activities such as reduction of leaf size and stomatal closure during water deficit condition and facilitates deeper root growth by altering root architecture under scarcity of water and nitrogen deficiency. ABA mediated drought tolerance in plants involves modulation of root aquaporins, and enhanced cell turgor pressure management by affecting the biosynthesis of antioxidant enzymes and soluble solutes. The over expressing NCED1 gene in tomato leading to stomatal closure during water deficiency confers tolerance against drought. However, the increased stomatal closure in the NCED1 over expressing transgenic line affects the overall carbon assimilation, which exerts a dramatic influence on the number of seeds. Therefore, the repercussions of the ABA-induced drought resistant in plant includes reduced crop yield, sterile pollen and seed dormancy (due to elevated levels of ABA). As a remedy, use of drought inducible gene (ABA3/LOS5, in rice) and promoter (era1, in canola) increases the ABA level along with the crop yield.

45The growth hormone cytokinin (CK), acting antagonistically to the senescence hormone ABA, and promotes proliferation and differentiation of cell or tissue, thus preventing premature senescence. Agronomic trait stay green (enhanced the photosynthetic activity) in drought tolerant genotypes allows accumulation of higher levels of CK in tissue and xylem sap. This CK accumulation promotes normal grain filling and limits premature leaf senescence. Researches have used the CK biosynthetic gene isopentenyl transferase (ipt) for improving crop performance under drought stress. To date, ipt gene has been tested in many crop species such as rice, pea, tobacco and cassava for high yield under reduced irrigation. The grain productivity in barley and rice was reported to improve under limited water supply through enhancing CK content by attenuation of cytokinin oxidase gene.

46Brassinosteroids (BRs) are new class of phytohormones that regulate a wide range of bio-physiological activities such as plant growth, root development, flowering and reproduction, seed germination, and biotic and abiotic responses. Arabidopsis was widely used to study the genotype to phenotype correlation in the BRs biosynthetic or signaling mutants. For example, the BRs mutants exhibit hypersensitivity to the seed germination inhibition exerted by the ABA, and the exogenous application of BRs rescues the low seed germination phenotype in gibberellin (GA) mutant. Overexpression of hydroxysteroid dehydrogenase1 (HSD1, encodes a putative enzyme in BRs synthesis) gene in Arabidopsis resulted reduced seed dormancy compared to wild type. Similarly, in Arabidopsis overexpression of DWARF4 (DWF4) gene rescued the ABA seed inhibition phenotype. Interestingly, the overexpression of DRAWF4/CYP90B1 gene in crop plants such as rice registered a positive response with respect to agronomical traits. The overexpression DRAWF4/CYP90B1 transgenic rice showed increased CO2 uptake and enhanced photosynthetic efficiency, which increased the seed yield. The CYP85A2 (encodes BRs biosynthetic enzymes) mutant confirmed the role of BRs in reproduction. The cyp85a2 mutant exhibited phenotype similar to Arabidopsis mutant seuss because it lacks proper development of reproductive organs like ovule. Furthermore, the downregulation of BRs in the maize nana plant1 and dwarf brassinosteroid-dependent1 (brd1) mutants result minimized male flowers. Recently, disruption of squalene synthase (SQS) gene in rice by RNA-interference reduced the overall sterol content, including BRs, which reduced the stomatal conductance to provide drought tolerance during vegetative and reproductive stages. Apart from abiotic stress, BRs provides resistance against a broad range of diseases in potato, rape seed, rice, tomato and tobacco. For example, the elevated levels of BRs in Brassica juncea improves the resistance against potent fungal pathogen Botrytis cinerea.

475-hydroxy tryptamine (serotonin) acts as neurotransmitter in animal system. Moreover, in plants, serotonin assumed as intermediate between tryptamine and IAA during auxin biosynthesis, but still more work and evidence is required to approve this hypothesis. Recently, the role of serotonin in senescence was demonstrated in rice leaf tissue. During senescence, leaf tissue synthesizes and accumulates high levels of serotonin to maintain cellular integrity. Additionally, inhibition of serotonin biosynthesis causes early senescence of leaf. Hence, serotonin could be used as a potential marker for senescence.

Enhancing the Level of Provitamin A

48The deficiency of vitamin A causes night blindness, which can further result in complete blindness. Interestingly, β-carotene acts as pro-vitamin A, and it was targeted to reduce the deficiency of vitamin A. Considering rice as one of the major staple food especially in the Asian region; the supplementation of vitamin A via β-carotene was initiated by enrichment of rice endosperm to produce golden rice. This approach involved, upregulation of carotenoid biosynthetic pathways in rice endosperm, which includes transgene expression of phytoene synthase (psy, from daffodil and maize) and phytoene desaturase (crt1, from Erwinia uridovora) under endosperm specific Glutelin (Gt1). This resulted in an increase of up to 27 fold (37 μg/g) in the β-carotene levels in golden rice. Interestingly, transgene overexpression of three bacterial carotenoids biosynthetic genes CrtB, CrtI, and CrtY, encoding phytoene synthase, phytoene desaturase, and lycopene β-cyclase, respectively, resulted ∼40 fold increase of the β-carotene and ∼100–200 fold increase for total carotenoid. Till date, several attempts have been made toward enrichment of β-carotene in important staple crop food species such as cassava, maize, potato and sweet potato.

Enhancing the Level of Folates

49Folates belongs to the class of vitamin B, act as Co-factors for C1-metabolism (one-carbon transfer reactions) such as amino acid metabolism, nucleotide biosynthesis and the methylation cycle. Deficiency of folate in human causes birth defect, increases cardiovascular disease and megaloblastic anemia. Plants are capable of biosynthesizing folate in mitochondria and plastids from pterins. Pterins are synthesized from guanosine-50- triphosphate (GTP) and p-aminobenzoate (PABA). The overexpression of folate biosynthetic gene GTP-cyclohydrolase 1 (GTPCH1) in transgenic tomato enhanced the pterins content of ripe fruits, which resulted two-fold increase in the folate content. Recently, a transgenic lettuce expressing synthetic codon-optimized gene GTPCH1 was generated, which had showed 2.1–8.5 fold higher levels of folate compared to non-transgenic plant. However, previous attempts suggest 100 times increased folate content in the overexpression transgenic rice, which contains two transgenes from Arabidopsis, GTPCH1 and aminodeoxychorismate synthase (ADCS). generated an elite inbred of transgenic Maize, in which, the kernel endosperm contained double amount of folate, six fold of ascorbate and 169 fold of β-carotene. Interestingly, they used four genes from different sources; PSY1 from maize under glutenin promoter and CRT1 from Pantoea ananatis, GTPCH1 from Escherichia coli and dehydroascorbate reductase (DHAR) from rice under barley D-hordein promoter. Notably, the above mentioned leads are crop/genotype dependent, because transgenic lines of potato and Arabidopsis failed to accumulate higher levels of folate. Hence, a better understanding of folate pathway is required, which could be useful and applicable to enhance the folates content in wide range of plant species.

Altering the Levels of Flavonoids

50Flavonoids play an important role in the maintenance of fruit quality. It represents a huge family of secondary metabolites that consists of more than 6000 compounds. The peel of fleshy fruits like grape and strawberry accumulates flavonoids such as anthocyanin, catechin, epicatechin, quercetin, kaempferol, myricetin, and isorhamnetin., ectopically expressed the Del/Ros1gene (from snapdragon plant) in tomato under fruit specific E8 promoter. As a result, the fruits of Del/Ros1 tomato transgenic lines accumulated substantial amount of anthocyanin (lycopene is the major secondary metabolite in cultivated tomatoes) due to the increased expression of anthocyanin biosynthetic genes. Recently, the genetically engineered purple tomato was investigated to demonstrate the impact of anthocyanin (antioxidant) on prolonging fruit shelf life and resistance against fungal infection.

Altering Flavor and Aroma

51The flavor and aroma of fruit are important and it influences the customer choices. Over the past decades, most of the research on fruit and vegetable crop species was mainly focused on the yield and resistance. Genome wide association mapping and metabolite assisted quantitative trait loci analysis has helped to fish out useful genes that confers aroma of rice grain. The recent advancement in the field of metabolomics and the available metabolic network databases has fascinated researcher to focus on flavor and aroma. Breeding has long served toward improvement of flavor; however, it was dedicated more toward a balance between sugar: organic acid ratio and the post-harvest management. Recent studies on flavor and aroma include metabolic engineered tomato. The heterologous expression of Clarkia breweri plant S-linalool synthase (LIS) gene in tomato resulted accumulation of S-linalool and 8-hydroxylinalool at the ripe stage of fruit. In addition to S-linalool, the transgenic exhibited increased levels of geranial, limonene, myrcene, and β-ocimene, and a decrease in nor-isoprenes. Similarly, the metabolic analysis of fruits from the overexpression lines of tomato alpha-Zingiberene synthase (ZIS, encodes for sesquiterpene synthase) transgenic showed higher levels of alpha-zingiberene and other sesquiterpenes, such as 7-epi-sesquithujene, alpha-bergamotene, beta-bisabolene and beta-curcumene, whereas control fruit showed absence of sesquiterpenes. studied the aroma in transgenic cucumber. The GC/MS based study of transgenic cucumber expressing transgene preprothaumatin II gene under 35S promoter showed enhanced production of (E, Z)-2,6-nonadienal.

52Fragrance of flowers is known to play multiple roles including attraction of pollinators and the interaction between plant and their surroundings. The ornamental plants like lisianthus (Eustoma grandiflorum) produces beautiful flowers, but these lacks floral scent. Transformation of lisianthus with benzyl alcohol acetyltransferase (BEAT; obtained from Clarkia breweri) under constitutive CaMV 35S promoter generated substrate dependent transgenic which produced 5–7 times higher levels of benzyl acetate (aromatic compound) when treated with benzyl alcohol. Interestingly, the recent report displayed the role of the aroma profile in stress tolerance. For example, omega-3 fatty acid desaturases FAD3 and FAD7 genes (involves in the conversion of C18:2 to C18:3, a precursor for hexanals and its derivatives) were over expressed in tomato to achieve cold stress tolerance. The overexpression transgenic tomato exhibited increased levels of 18:3/18:2 and (Z)-hex-3-enal/hexanal ratio with enhanced cold stress tolerance. Similarly, ectopic expression of aroma biosynthetic transgenes, such as strawberry linalool/nerolidol synthase (FaNES1) in Arabidopsis and potato, maize terpene synthase (TPS10) gene in potato, and patchoulol synthase (PTS) coupled with FPP synthase in tobacco was used to improve defense management from plant pest.

Metabolomics to Cater Biofuel Demand

53Burgeoning petroleum demand worldwide motivates researchers to explore renewable and alternative sources, such as biodiesel. In the current omics era, a refined understanding of biochemical pathways is being used to genetically improve biodiesel crop species, including jatropha, soybean, mustard, pongamia, algae, etc. The oil composition of the plant determines its quality. Currently, agronomical suitable jatropha (Jatropha curcas) is extensively grown as an alternative source of energy. The oil content of jatropha seed is rich in polyunsaturated fatty acid mainly linoleic acid, which is vulnerable to oxidation and has negative impact on the quality. Silencing of fatty acid desaturase (FAD2s) in jatropha by Qu and colleagues significantly lowered the level of linoleic acid, while increasing the oleic acid content by 78%. To improve the yield and oil quality of jatropha under water deficient condition, three transgenics were raised by overexpressing genes GSMT and DMT (encodes enzyme catalyzes glycine betaine catalyses), PPAT (encodes an enzyme that catalyzes CoA biosynthetic pathway) and NF-YBI (encodes transcription factor NF-Y subunit). A range of candidate genes have been identified and characterized so far in jatropha, which are either involved in the metabolism of fatty acid or contribute to improve the seed oil content during stress. These genes include PIP2 encoding aquaporin protein, betaine aldehyde dehydrogenase, Δ6-fatty acid desaturase, ω6-fatty acid desaturase, ω3-fatty acid desaturase, diacylglycerol acyltransferase and long chain acyl coenzyme A synthetase. Similar to jatropha, castor is another excellent source of biodiesel because of its transesterified oil, which is soluble in alcohol without heating. Castor yield was improved by overexpressing the Cry1Ab gene, which provides resistance against feeders. A non-transgenic method targeting induced local lesions in genomes (TILLING) was also used to increase the quality of caster seed oil by knocking out the gene that encodes ricin (alkaloid inhibits protein synthesis)4. The use of seed oil as biodiesel has been extended to many plant species such as coconut, cotton, mustard, pongamia, sunflower, etc..

54Photosynthetic water micro algae are also a rich source of oils that are mainly composed of unsaturated fatty acids. The simple cellular structure of these microorganisms, and their only dependency on CO2, water and the sunlight for their rapid growth renders algal derived biodiesel more accessible than that obtained from higher plants. Attempts aiming at genetic manipulation of algae were undertaken to increase the oil content. The overexpression of DGAT (gene from the fatty acid biosynthetic pathway) in Chlamydomonas reinhardtii, however, produced unintended result, i.e., no increase for total fatty acid content.

55Biofuels are also obtained through fermentation of sugars yielding alcohol such as ethanol and butanol. In sugarcane, the load of sucrose, trehalulose and isomaltulose was obtained by overexpressing trehalulose synthase and sucrose isomerase. Similarly, xylanases from bacterial and fungal source was expressed in crop plants such as barley, potato, rice, sunflower, and tobacco. Xylanases degrade β-1,4-xylan to pentose sugar, which can easily be fermented to alcohols. In addition, several other hydrolases (endo-Glucanases, cellobiohydrolases, β-glucosidases, glycosyl hydrolase etc.) were overexpressed to improve the biofuel availability from plants.

Metabolomics: An Integral Part of Knowledge-Based Plant Breeding

56The last decade has witnessed tremendous advancements in technologies followed by their deployment in understanding different facets of biology to understand the complex biology of desired traits. Knowledge-based plant breeding (KPB) utilizes all the meaningful information inferred from analysis of the large-scale data pertaining to genome, epigenome, transcriptome, metabolome, and proteome that collectively lead to a particular phenotype. The data generated from these ‘Omics’ approaches enable better understanding of the systems biology of the trait, so far mostly contributed by systems genetics and genomics, and to some extent transcriptomics. The other ‘Omics’ approaches, including metabolomics and proteomics have also started contributing toward generating important information, which can become an integral component of KPB, thereby strengthening the approach further for achieving higher genetic gain.

57Technological advancement has contributed to improve the efficiency of plant breeding techniques via precise selection of desired plants. An easy access to the different ‘Omics’ platforms will cause a paradigm shift in breeding process by facilitating plant selections based on the genome-scale information generated at different levels of biological processes. The plant breeders will gradually embrace these developments, which in turn will help them to make informed decisions.

Concluding Remarks and Future Perspectives

58Advances in plant metabolomics in recent time has allowed the precise selection of desirable traits along with offering opportunities to undertake metabolic engineered plants. The shift of technology from single metabolite analysis to high throughput assays generating footprints of a variety of metabolites in one go has paved the way for discovery/construction of better models for metabolite networks, and the identification of robust biomarkers. In the last decade, the implementation of metabolomics in conjunction with other omics technologies has not only uncovered a plethora of known as well as novel metabolites, but also allowed to determine their specific contribution toward improving key plant attributes such as quality, yield, shelf life, etc. To this end, high throughput genotyping/sequencing platforms based on NGS technology has been a tremendous support as a cost-effective and high-throughput means to elucidate the architecture of metabolic traits. The newly created avenues such as GWAS, GS and EWAS that allow efficient integration of metabolite profiling could provide a great impetus to metabolomics assisted breeding. We anticipate that the integration of metabolomics and the other omics tools greatly improves the ability of a plant breeder in order to design and develop agronomically superior plants, thus enabling rapid development of high-performing crop genotypes that adequately meet the challenges of 21st century agriculture.

Author Contributions

59RK, AB, MKP, and AK designed the article. RK and AK wrote the article. AB, AP, RK, and MKP corrected the article and finally all authors read and approved the final article.

Conflict of Interest Statement

60The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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