Transgenic and knockout plant assays available in the literature related to (poly)phosphoinositides and inositol (poly)phosphates. Relevant information: EC number of the enzyme coded by the studied gene, plant donor species, the genetically modified organisms (transformants), the modulation of the studied gene, the analyzed stress condition, the impact on plant tolerance and physiology (additional details, please see the legends).
Abstract
Among the multifunctional molecules that participate in processes of plant tolerance/resistance to stresses, inositol (Ins) and its derivatives (phosphorylated, methylated, oxygenated, and Raffinose Family Oligosaccharides) have attracted the attention of researchers. These compounds represent versatile and dynamic signaling molecules and osmolytes in all eukaryotes. Due to the impacts related to Ins and its derivatives in a plant cell, assays have been conducted to understand how these biomolecules affect plant physiology. Thus, overexpression or knockout of Ins-related genes has been shown as interesting strategies for generating more efficient plants capable of growing under stress conditions. In this chapter, studies using molecular tools are presented, and the impacts of their results are discussed based on the plant stress tolerance/resistance. Furthermore, an informative panel is provided with transcriptional modulation of genes related to Ins and its derivatives expressed in plants under stress. There is a gap involving about two dozen enzymes associated with the synthesis of Ins-related compounds that have not been adequately studied, and they represent an area of high biotechnological potential.
Keywords
- Transgeny
- tolerance
- resistance
- biotechnology
1. Introduction
To survive and integrate in the niche in which they germinate, plants constantly regulate their internal environment to external fluctuations encompassing soil, climate, and biological interactions. Thus, along its evolutionary processes, plants were selected through the need of molecular mechanisms for physiological adjustments to inadequate conditions for development, resulting from adverse conditions. In this way, plants have a diverse and active cellular machinery at different stratified levels, covering perception, signaling, transcriptional control of key metabolic pathways and synthesis of molecules responsive to stresses [1].
Among the molecules functioning in more than one of the aforementioned levels, inositol (Ins; C6H12O6) is a biomolecule of great interest. It is a cyclic carbohydrate (polyalcohol) that anchors in each of the six carbons forming the ring, a hydroxyl group. Along with their derivatives, Ins has multiple effects on plant metabolism. They act from the production of secondary messengers to the synthesis of osmolytes and antioxidants (more details in the reviews of [2, 3]). Phosphorylated Ins-derivatives [(poly)phosphoinositides and inositol (poly)phosphates] are versatile and dynamic signaling molecules in all eukaryotes, particularly in plants [4]. These two classes of compounds [highlighted in red and orange respectively, in Figure 1] are interdependent. While (poly)phosphoinositides are used in the synthesis of inositol (poly)phosphates through the action of phospholipases; the breaking of inositol (poly)phosphates produces inositol, which is a substrate for the synthesis of (poly)phosphoinositides. Moreover, according to Ins metabolism, shown in Figure 1, another branch realizes the synthesis of methylated derivatives (highlighted in green). These compounds act as important osmoregulators during periods of unfavorable conditions [5]. Additionally, oxygenated Ins-derivatives are observed (highlighted in yellow in Figure 1), which are involved in increasing plant tolerance to stresses by decreasing oxidative damage [6]. Still associated with Ins is the metabolism of the Raffinose Family Oligosaccharides (RFOs) [7]. In this biosynthetic pathway, the galactinol synthase (GolS; EC 2.4.1.123) uses myo-inositol and UDP-galactose to produce galactinol, which serve as galactose donors for subsequent synthesis of RFO members ([8, 9]; highlighted in red in Figure 2). Recent reports indicate that RFOs may assist in the reactive oxygen species (ROS) cleaning process. In periods of stress, ROS accumulation favors the physiological imbalance of plants [10].
Due to the impacts related to the Ins and its derivatives in a plant cell, assays have been conducted to understand how these biomolecules affect the physiology of plants. Thus, overexpression or knockout of genes present in these pathways has been shown as interesting strategy for generating more efficient plants capable of growing under abiotic stress conditions. In this chapter, studies using molecular genetic tools will be presented, which affect the above-mentioned metabolic pathways and the studied organisms.
2. The use of Ins and phosphorylated Ins-derivatives in plant cells under stress
Although there are several articles addressing the involvement of Ins and its derivatives in plant stress responses, so far no report has described the overall transcriptional orchestration of these components covering the metabolic pathways related to them. Information is available only in particular assays covering few genes and their expression modulations, some individual gene knockout analyses or a specific GMO (genetically modified organism) assay. In most cases, Ins and its phosphorylated derivatives have positive impact in plant tolerance/resistance to several stresses, promoting a biotechnological interest in these compounds.
Among the Ins-derivatives, those that are phosphorylated [(poly)phosphoinositides (highlighted in red in Figure 1) and inositol (poly)phosphates (highlighted in orange)] are the most discussed in the literature. This fact reflects the importance of these compounds in plant physiology in signaling activities. An example is a work developed by Hunt et al. [11] with transgenic tobacco plants (
Mills et al. [12] provide more details on this ABA-mediated stomatal regulation in transgenic plants obtained by Hunt et al. [11]. A three-day assay under drought and in dark-adapted conditions, to reopen the stomata in response to light, was carried out. The results showed that transgenic plants with reduced PI-PLC as compared to control plants (with the empty vector without the transgene insert) have a greater increase in stomatal conductance. Thus, there is a strengthening of the role of inhibition due to PI-PLC in ABA-mediated stomatal opening. Further analysis indicated tobacco PI-PLC acting on the inhibition of stomatal opening by ABA, but not in promoting ABA-induced stomatal closure.
There are also reports of the involvement of Ins-derivatives in ABA-independent mechanisms during periods of drought. Perera et al. [13] obtained
In a similar assay, Khodakovskaya et al. [14] reported physiological consequences in transgenic lines of
The involvement of InsP3 in other stress tolerance processes, beyond drought, has also been demonstrated. Alimohammadi et al. [15] obtained transgenic tomato plants (
The biotechnological potential through the manipulation of compounds shown in Ins-related metabolic pathways may also be seen in the work of Ahmad et al. [17]. These authors performed a comprehensive analysis of
Kusuda et al. [18] went beyond the study of transformed lines overexpressing enzymes from the Ins-related pathways. They analyzed the differences among wild type and transformants lines in regard to salt tolerance in 3.5 days in medium with concentrations up to 250 mM NaCl. They also sought for differences by mining the metabolomes (the fourth leaf tissue harvested at 0, 6, and 12 h after NaCl stress induction) of the studied plants. To this end, a rice cultivar (
Ins metabolism and phosphorylated Ins-derivatives are also associated with response to biotic stresses in plants. This fact shows the plurality of actions of these compounds. Murphy et al. [19] report evidence in this direction. They obtained transgenic potato [
Recently, Meng et al. [20] found that
Reports presented in Table 1 also show the broad roles of Ins and its phosphorylated derivatives in plant cells. From the wide spectrum of analyzed genes, a range of effects on plants at different levels was observed. These effects have shown associations with hormone signaling pathways, such as ABA [12], influences in photosystems [21, 22], with reactive oxygen species (ROS; [23]), with relative water content, with osmotic adjustment [24], among others (Table 1).
3. Methylated Ins-derivatives in plant cell and the biotechnological use to increase stress tolerance
Some plants use Ins as precursor of compatible solutes such as D-ononitol and D-pinitol, which act as osmoprotectants (small molecules that act as osmolytes and help organisms survive in extreme osmotic stress [35]). In halophyte ice plant (
|
|
|
|
|
|
|
|
5.5.1.4 |
|
|
Overexp. | HS | Raise | [25] | a. |
5.5.1.4 |
|
|
Overexp. | HS | Raise | [21] | b. |
5.5.1.4 |
|
|
Overexp. | HS | Raise | [22] | c. |
3.1.3.25 |
|
|
Overexp. | HS, P, PEG, and HT | Raise | [26] | d. |
2.7.1.140; 2.7.1.151 |
|
|
Overexp. | HS and OS | Raise | [27] | e. |
2.7.1.140; 2.7.1.151 |
|
|
Overexp. | HS, D, and OS | Raise | [28] | f. |
3.1.4.11 |
|
|
Overexp. | D | Raise | [29] | g. |
2.7.1.159; 2.7.1.134 |
|
|
Overexp. | HS | Decrease | [24] | h. |
3.1.3.57 |
|
|
Knockout | HS, F, and D | Decrease | [30] | i. |
2.7.1.137 |
|
|
Knockout | HS | Decrease | [31] | j. |
2.7.1.67 |
|
|
Overexp. | HS and ABA | Raise | [23] | l. |
2.7.8.11 |
|
|
Overexp. | D | Raise | [32] | m. |
3.1.3.8 |
|
|
Overexp. | HS and OSM | Raise | [33] | n. |
2.7.1.149 |
|
|
Overexp. | HS, D, and ABA | ** | [34] | − |
Sheveleva et al. [39] were one of the first to report the biotechnological potential of methylated Ins-derivatives. In their work, the authors superexpressed O-methyltransferase (IMT1; EC 2.1.1.40; Figure 1) of
Recently, Zhu et al. [41] used a similar strategy as the one developed by Sheveleva et al. [39] to express in
4. Oxygenated Ins-derivatives in plant cell and the plant strategy to tackle stress
So far, the myo-inositol oxygenase (MIOX; EC 1.13.99.1; Figure 1) is the only enzyme known by the oxidation of Ins [42]. Its importance in plants stood out from the statement in the Ins metabolism as a precursor in Ascorbic Acid (AsA) biosynthesis in Arabidopsis. In this sense, Lorence et al. [43] observed the expression of a myo-inositol oxygenase (miox4) increasing the content of AsA in leaves (approximately two- to threefold). By that, they anticipated a potential use of the gene by genetic engineering, enhancing levels of this important antioxidant in plants. Further analysis indicated that D-GlcUA (Figure 1), a derivative from MIOX reaction (EC 1.13.99.1, Figure 1), plays a negligible role for AsA biosynthesis [44]. However, MIOX can control the metabolite level of myo-inositol in plants [44].
Nevertheless, the metabolic consequences of MIOX action are still unclear. In order to contribute with information from gene regulation and catalytic activity of this enzyme, Duan et al. [6] performed a functional characterization in rice (
Moreover, Alford et al. [45] reported MIOX enzymes responding to growing conditions of
5. Raffinose Family Oligosaccharides (RFOs) and plant strategy to address stresses
RFOs are a class of compatible solutes coming from Ins metabolism ramifications. As mentioned before, the enzyme GolS (EC 2.4.1.123, highlighted in red in Figure 2) connects the metabolism of these compounds, producing galactinol (highlighted in red in Figure 2), which serves as galactose donor for further synthesis of RFO members [8, 9]. To date, structural genomics data and global transcriptome analysis concerning RFOs are only available for corn [46]. For this crop, the authors have performed a genomic identification of genes associated with raffinose metabolism, together with an expression analysis using data-mining from GEO (http://www.ncbi.nlm.nih.gov/geo) and PLEXdb databases (http://www.plexdb.org). Additionally some transgenic lines overexpressing specifics gene isoforms related to RFO pathway, under particular growth conditions, are available for some species. These studies showed a positive impact in some crops.
Taji et al. [47], for example, analyzed the expression of seven genes encoding GoIS in
In
Latter, Pennycooke et al. [50] studied the expression of α-galactosidase gene (EC 3.1.2.22 highlighted in red in Figure 2) from petunia (Petunia x hibrida "Mitchell"), monitoring acclimated plants to low temperatures (4°C) and in response to increasing temperature (25°C). Transcripts induction were observed after one hour of desacclimation occurring together with an increase in enzymatic activity and decreased raffinose content, suggesting that the rise in temperature can regulate the RFO catabolism of certain members, through gene regulation that encoding α-galactosidase.
Thus, the diversity of functions performed by compounds presenting in the Ins metabolism was shown in the described works. Also, studies of distinct isoforms showed positive correlations with plant responses to various abiotic stresses. In this way, the identification of new transcripts, as well as the understanding of its regulation (spatial and temporal) in plants under unfavorable conditions for the development may lead to the discovery of new genes with biotechnological potential.
According to the Kyoto Encyclopedia of Genes and Genomes (KEGG) Pathway database (http://www.genome.jp/kegg/pathway.html), which provides diagrams of various metabolic processes, at least 45 enzymes are associated with the metabolic pathways described here. Of these enzymes, 21 (highlighted in green boxes in Figures 3A and 3B) have been studied in previous works addressing the transcriptional expression of their genes or effects on plants under stress. Therefore, there are at least 24 enzymes (in red boxes in Figures 3A and 3B) that have not been targets of these analyses, with significant potential for further research in biotechnology.
6. Ins and its derivatives in humans: Antinutrients versus disease prevention
Once Ins and its derivatives are present in vegetables and these are part of the daily diet of large populations around the world, it is essential to analyze their potential effects on consumers. The Ins and related metabolites play a heterogeneous physiological role, depending on the concerned organism, plant or animal (including human). In plants, as already mentioned, such compounds help regulate plant homeostasis during periods of stress. In animals (including humans), their influence has very diverse physiological repercussions. Initially, they were only seen as harmful agents because some representatives when present in certain plants could act as antinutritional factors, thereby reducing the bioavailability of important nutrients and the nutritional value of the food. According to Kokhar and Apenten [51], this effect is present a result of a selected adaptive mechanism due to a "chemical warfare" between higher plants and herbivorous pests.
Among the various Ins-derivatives, phytic acid (1-D-myo-inositol-P6; Figure 1) is the most studied, concerning the impacts on human and animal health. Its unique structure provides the ability to chelate cations such as iron, zinc, potassium, magnesium, and copper, forming insoluble salts denominated phytate. These salts adversely affect animal’s ability to absorb and digest nutrients [52, 53]. Phytates can form complexes with proteins, changing their structures and their enzymatic activities and characteristics of solubility and proteolytic digestibility [54]. However, there are reports that show positive aspects in phytates consumption. The presence of these in the diet of patients with diabetes has positive effects in reducing the level of blood glucose due to decreased starch digestion rate and slowing of gastric evacuation [55]. There are also reports of activity against HIV replication, kidney stones prevention, reduction of cholesterol and triglycerides levels, as well as assistance in prevention of heart diseases (for review see [54]). Studies also indicate that both Ins [56] and phytic acid [56, 57] have anticancer properties. With regard to RFOs, besides the fact that they are potential antinutritional factors, there are indications that they may act as important immunostimulants in animals (including humans). Also, RFOs’ involvement is suggested in universal mechanisms of oxidative balance in several taxa [58].
7. Concluding remarks and perspectives
Experimentally, mutants and transgenic analyses are being successfully carried out to uncover the various roles played by Ins-related compounds. It is known today that some phosphorylated derivatives of inositol are connected with a large number of signaling procedures which are regulated by both abiotic and biotic stress. Methylated and oxygenated Ins-derivatives, including RFOs, have also proven to be active agents in the process of plant acclimatization to unfavorable conditions, involved in a number of functions. However, there is a gap to be filled. About two dozen enzymes associated with the synthesis of these compounds have not been adequately studied and they represent an area of high biotechnological potential.
Acknowledgments
The authors thank CNPq (National Council of Technological and Scientific Development – process number 454112/2014-9) for financial support. JRCFN thanks to CAPES (InterSis Network – Biocomp Project) for the fellowship granted. EAK thanks to CNPq for the fellowship granted.
References
- 1.
Bartels D, Souer E. Molecular Responses of Higher Plants to Dehydration. In: Hirt H, Shinozaki K, editors. Plant Responses to Abiotic Stress . 1st edn. Springer; 2004. p. 9–38. DOI: 10.1007/978-3-540-39402-0_2 - 2.
Loewus, FA, Murthy PPN. Myo-Inositol Metabolism in Plants. Plant Sci . 2000; 150: 1–19. DOI: doi:10.1016/S0168-9452(99)00150-8 - 3.
Majumder AL, Biswas BB. Biology of Inositols and Phosphoinositides: Subcellular Biochemistry . 2nd edn. Springer; 2006. DOI: 10.1007/0-387-27600-9 - 4.
Munnik T, Vermeer JEM. Osmotic Stress-Induced Phosphoinositide and Inositol Phosphate Signalling in Plants. Plant Cell Environ . 2010;33:655–669. DOI: 10.1111/j.1365-3040.2009.02097.x - 5.
Flowers TJ, Colmer TD. Salinity Tolerance in Halophytes. New Phytol . 2008;179:945–963. doi: 10.1111/j.1469-8137.2008.02531.x - 6.
Duan J, Zhang M, Zhang H, Xiong H, Liu P, Ali J, Li J, Li Z. OsMIOX, a Myo-Inositol Oxygenase Gene, Improves Drought Tolerance through Scavenging of Reactive Oxygen Species in Rice (Oryza Sativa L.). Plant Sci . 2012;196:143–151. DOI: 10.1016/j.plantsci.2012.08.003 - 7.
Keller F, Pharr DM. Metabolism of Carbohydrates in Sinks and Sources: Galactosyl-Sucrose Oligosaccharides. In: Zamski E, Schaffer AA, editors. Photoassimilate Distribution in Plants and Crops . 1st edn. New York: Marcel Dekker; 1996. p. 115–184. - 8.
Liu JJJ, Krenz DC, Galvez AF, De Lumen BO. Galactinol Synthase (GS): Increased Enzyme Activity and Levels of mRNA due to Cold and Desiccation. Plant Sci . 1998;134:11–20. DOI: 10.1016/S0168-9452(98)00042-9 - 9.
Sprenger N, Keller F. Allocation of Raffinose Family Oligosaccharides to Transport and Storage Pools in Ajuga Reptans: The Roles of Two Distinct Galactinol Synthases. Plant J . 2000;21:249–258. DOI: 10.1046/j.1365-313X.2000.00671.x - 10.
Elsayed A I, Rafudeen MS, Golldack D. Physiological Aspects of Raffinose Family Oligosaccharides in Plants: Protection against Abiotic Stress. Plant Biol . 2014;16:1–8. DOI: 10.1111/plb.12053 - 11.
Hunt L, Mills LN, Pical C, Leckie CP, Aitken FL, Kopka J, Mueller-Roeber B, McAinsh MR, Hetherington AM, Gray JE. Phospholipase C Is Required for the Control of Stomatal Aperture by ABA. Plant J . 2003;34:47–55. DOI: 10.1046/j.1365-313X.2003.01698.x - 12.
Mills LN, Hunt L, Leckie CP, Aitken FL, Wentworth M, McAinsh MR, Gray JE, Hetherington AM. The Effects of Manipulating Phospholipase C on Guard Cell ABA-Signalling. J Exp Bot . 2004;55:199–204. DOI: 10.1093/jxb/erh027 - 13.
Perera IY, Hung C-Y, Moore CD, Stevenson-Paulik J, Boss WF. Transgenic Arabidopsis Plants Expressing the Type 1 Inositol 5-Phosphatase Exhibit Increased Drought Tolerance and Altered Abscisic Acid Signaling. Plant Cell . 2008;20:2876–2893. DOI: 10.1105/tpc.108.061374 - 14.
Khodakovskaya M, Sword C, Wu Q, Perera IY, Boss WF, Brown CS, Sederoff WH. Increasing Inositol (1,4,5)-Trisphosphate Metabolism Affects Drought Tolerance, Carbohydrate Metabolism and Phosphate-Sensitive Biomass Increases in Tomato. Plant Biotechnol J . 2010;8:170–183. DOI: 10.1111/j.1467-7652.2009.00472.x - 15.
Alimohammadi M, De Silva K, Ballu C, Ali N, Khodakovskaya MV. Reduction of Inositol (1,4,5)-Trisphosphate Affects the Overall Phosphoinositol Pathway and Leads to Modifications in Light Signalling and Secondary Metabolism in Tomato Plants. J Exp Bot . 2012;63:825–835. DOI: 10.1093/jxb/err306 - 16.
Alimohammadi M, Lahiani MH, Khodakovskaya MV. Genetic Reduction of Inositol Triphosphate (InsP3) Increases Tolerance of Tomato Plants to Oxidative Stress. Planta . 2015;242:123–135. DOI: 10.1007/s00425-015-2289-1 - 17.
Ahmad A, Niwa Y, Goto S, Kobayashi K, Shimizu M, Ito S, Usui Y, Nakayama T, Kobayashi H. Genome-Wide Screening of Salt Tolerant Genes by Activation-Tagging Using Dedifferentiated Calli of Arabidopsis and Its Application to Finding Gene for Myo-Inositol-1-P-Synthase. PLoS One . 2015;10: e0115502. DOI: 10.1371/journal.pone.0115502 - 18.
Kusuda H, Koga W, Kusano M, Oikawa A, Saito K, Hirai MY, Yoshida KT. Ectopic Expression of Myo-Inositol 3-Phosphate Synthase Induces a Wide Range of Metabolic Changes and Confers Salt Tolerance in Rice. Plant Sci . 2015;232:49–56. DOI: 10.1016/j.plantsci.2014.12.009 - 19.
Murphy, AM, Otto, B, Brearley, Ca, Carr, JP, Hanke, D.E. A Role for Inositol Hexakisphosphate in the Maintenance of Basal Resistance to Plant Pathogens. Plant J . 2008;56:638–652. DOI: 10.1111/j.1365-313X.2008.03629.x - 20.
Meng PH, Raynaud C, Tcherkez G, Blanchet S, Massoud K, Domenichini S, Henry Y, Soubigou-Taconnat L, Lelarge-Trouverie C, Saindrenan P, Renou JP, Bergounioux C. Crosstalks between Myo-Inositol Metabolism, Programmed Cell Death and Basal Immunity in Arabidopsis. PLoS One . 2009;4. DOI: 10.1371/journal.pone.0007364 - 21.
Majee M, Maitra S, Dastidar KG, Pattnaik S, Chatterjee A, Hait NC, Das KP, Majumder AL. A Novel Salt-Tolerant L-Myo-Inositol-1-Phosphate Synthase from Porteresia Coarctata (Roxb.) Tateoka, a Halophytic Wild Rice. Molecular Cloning, Bacterial Overexpression, Characterization, and Functional Introgression into Tobacco-Conferring Salt Tolerance Phenotype. J Biol Chem . 2004;279:28539–28552. DOI: 10.1074/jbc.M310138200 - 22.
Joshi R, Ramanarao MV, Baisakh N. Arabidopsis Plants Constitutively Overexpressing a Myo-Inositol 1-Phosphate Synthase Gene (SaINO1) from the Halophyte Smooth Cordgrass Exhibits Enhanced Level of Tolerance to Salt Stress. Plant Physiol Biochem . 2013;65:61–66. DOI: http://dx.doi.org/10.1016/j.plaphy.2013.01.009 - 23.
Akhter S, Uddin MN, Jeong IS, Kim DW, Liu X-M, Bahk JD. Role of Arabidopsis AtPI4Kγ3, a Type II Phosphoinositide 4-Kinase, in Abiotic Stress Responses and Floral Transition. Plant Biotechnol J . 2015:1–16. DOI: 10.1111/pbi.12376 - 24.
Niu X, Chen Q, Wang X. OsITL1 Gene Encoding an Inositol 1,3,4-Trisphosphate 5/6-Kinase is a Negative Regulator of Osmotic Stress Signaling. Biotechnol Lett . 2008;30:1687–1692. DOI: 10.1007/s10529-008-9730-5 - 25.
Das-Chatterjee A, Goswami L, Maitra S, Dastidar KG, Ray S, Majumder AL. Introgression of a Novel Salt-Tolerant L-Myo-Inositol 1-Phosphate Synthase from Porteresia Coarctata (Roxb.) Tateoka (PcINO1) Confers Salt Tolerance to Evolutionary Diverse Organisms. FEBS Lett . 2006;580:3980–3988. DOI: 10.1016/j.febslet.2006.06.033 - 26.
Saxena SC, Salvi P, Kaur H, Verma P, Petla BP, Rao V, Kamble N, Majee M. Differentially Expressed Myo-Inositol Monophosphatase Gene (CaIMP) in Chickpea (Cicer Arietinum L.) Encodes a Lithium-Sensitive Phosphatase Enzyme with Broad Substrate Specificity and Improves Seed Germination and Seedling Growth under Abiotic Stresses. J Exp Bot . 2013;64:5623–5639. DOI: 10.1093/jxb/ert336 - 27.
Yang L, Tang R, Zhu J, Liu H, Mueller-Roeber B, Xia H, Zhang H. Enhancement of Stress Tolerance in Transgenic Tobacco Plants Constitutively Expressing AtIpk2, an Inositol Polyphosphate 6-/3-Kinase from Arabidopsis Thaliana. Plant Mol Biol . 2008;66:329–343. DOI: 10.1007/s11103-007-9267-3 - 28.
Zhu JQ, Zhang JT, Tang RJ, Lv QD, Wang QQ, Yang L, Zhang HX. Molecular Characterization of ThIPK2, an Inositol Polyphosphate Kinase Gene Homolog from Thellungiella Halophila, and its Heterologous Expression to Improve Abiotic Stress Tolerance in Brassica Napus. Physiol Plant . 2009;136: 407–425. DOI: 10.1111/j.1399-3054.2009.01235.x - 29.
Wang C-R, Yang A-F, Yue G-D, Gao Q, Yin H-Y, Zhang J-R. Enhanced Expression of Phospholipase C 1 (ZmPLC1) Improves Drought Tolerance in Transgenic Maize. Planta . 2008;227:1127–1140. DOI: 10.1007/s00425-007-0686-9 - 30.
Xiong L, Lee B, Ishitani M, Lee H, Zhang C, Zhu J. FIERY1 Encoding an Inositol Polyphosphate 1-Phosphatase Is a Negative Regulator of Abscisic Acid and Stress Signaling in Arabidopsis. Gene Dev . 2001;15:1971–1984. DOI: 10.1101/gad.891901.netic - 31.
Leshem Y, Seri L, Levine A. Induction of Phosphatidylinositol 3-Kinase-Mediated Endocytosis by Salt Stress Leads to Intracellular Production of Reactive Oxygen Species and Salt Tolerance. Plant J . 2007;51:185–197. DOI: 10.1111/j.1365-313X.2007.03134.x - 32.
Liu X, Zhai S, Zhao, Y, Sun B, Liu C, Yang A, Zhang J. Overexpression of the Phosphatidylinositol Synthase Gene (ZmPIS) Conferring Drought Stress Tolerance by Altering Membrane Lipid Composition and Increasing ABA Synthesis in Maize. Plant Cell Environ . 2013;36:1037–1055. DOI: 10.1111/pce.12040 - 33.
Zhang W, Gruszewski HA, Chevone BI, Nessler CL. An Arabidopsis Purple Acid Phosphatase with Phytase Activity Increases Foliar Ascorbate. Plant Physiol . 2008;146:431–440. DOI: 10.1104/pp.107.109934 - 34.
Mikami K, Katagiri T, Iuchi S. A Gene Encoding Phosphatidylinositol-4-Phosphate 5-Kinase is Induced by Water Stress and Abscisic Acid in Arabidopsis Thaliana. Plant J . 1998;15:563–568. DOI: 10.1046/j.1365-313X.1998.00227.x - 35.
Lang F. Mechanisms and significance of cell volume regulation. J Am Coll Nutr . 2007;26(5 Suppl):613S–623S. DOI: 10.2174/1389202911314030001 - 36.
Taji T, Takahashi S, Shinozaki K. Inositols and Their Metabolites in Abiotic and Biotic Stress Responses. In: Majumder AL, Biswas, BB, editors. Spring;2006. p. 239–264. DOI: 10.1007/0-387-27600-9_10 - 37.
Rammesmayer G, Pichorner H, Adams P, Jensen RG and Bohnert HJ. Characterization of IMT1, Myo-Inositol O-Methyltransferese, from Mesembryanthemum Crystallium. Arch Biochem Biophys . 1995;322:183–188. DOI: doi:10.1006/abbi.1995.1450 - 38.
Vernon DM, Bohnert HJ. Increased Expression of a Myo-Inositol Methyl Transferase in Mesembryanthemum Crystallinum is Part of a Stress Response Distinct from Crassulacean Acid Metabolism Induction. Plant Physiol . 1992;99:1695–1698. DOI: 10.1104/pp.99.4.1695 - 39.
Sheveleva E, Chmara W, Bohnert HJ, Jensen RC. Increased Salt and Drought Tolerance by D-Ononitol Production in Transgenic Nicotiana Tabacum L. Plant Physiol . 1997;115:1211–1219. DOI: http://dx.doi.org/10.1104/pp.115.3.1211 - 40.
Sengupta S, Patra B, Ray S, Majumder AL. Inositol Methyl Tranferase from a Halophytic Wild Rice, Porteresia Coarctata Roxb. (Tateoka): Regulation of Pinitol Synthesis under Abiotic Stress. Plant Cell Environ . 2008;31:1442–1459. DOI: 10.1111/j.1365-3040.2008.01850.x - 41.
Zhu B, Peng RH, Xiong AS, Xu J, Fu XY, Zhao W, Jin XF, Meng XR, Gao JJ, Cai R, Yao QH. Transformation with a Gene for Myo-Inositol O-Methyltransferase Enhances the Cold Tolerance of Arabidopsis Thaliana. Biol Plant . 2012;56:135–139. DOI: 10.1007/s10535-012-0029-y - 42.
Arner RJ, Prabhu KS, Thompson JT, Hildenbrandt GR, Liken AD, Reddy CC. Myo-Inositol Oxygenase: Molecular Cloning and Expression of a Unique Enzyme That Oxidizes Myo-Inositol and D-Chiro-Inositol. Biochem J . 2001;360:313–320. 10.1042/0264-6021:3600313 - 43.
Lorence A, Chevone BI, Mendes P, Nessler CL. Myo-Inositol Oxygenase Offers a Possible Entry Point into Plant Ascorbate Biosynthesis. Am Soc Plant Biol . 2004;134: 1–338. DOI: 10.1104/pp.103.033936.sapiens - 44.
Endres S, Tenhaken R. Myoinositol Oxygenase Controls the Level of Myoinositol in Arabidopsis, but Does Not Increase Ascorbic Acid. Plant Physiol . 2009;149:1042–1049. DOI: 10.1104/pp.108.130948 - 45.
Alford SR, Rangarajan P, Williams P, Gillaspy GE. Myo-Inositol Oxygenase Is Required for Responses to Low Energy Conditions in Arabidopsis Thaliana. Front Plant Sci . 2012;3:1–11. DOI: 10.3389/fpls.2012.00069 - 46.
Zhou ML, Zhang Q, Zhou M, Sun ZM, Zhu XM, Shao JR, Tang YX, Wu YM. Genome-Wide Identification of Genes Involved in Raffinose Metabolism in Maize. Glycobiology . 2012;22:1775–1785. DOI: 10.1093/glycob/cws121 - 47.
Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K. Important Roles of Drought and ColdInducible Genes for Galactinol Synthase in Stress Tolerance in Arabidopsis Thaliana. Plant J . 2002;29:417–426. DOI: 10.1046/j.0960-7412.2001.01227.x - 48.
dos Santos TB, Budzinski IGF, Marur CJ, Petkowicz CLO, Pereira LFP, Vieira LGE. Expression of Three Galactinol Synthase Isoforms in Coffea Arabica L. and Accumulation of Raffinose and Stachyose in Response to Abiotic Stresses. Plant Physiol Biochem . 2011;49:441–448. DOI: 10.1016/j.plaphy.2011.01.023 - 49.
Nishizawa-Yokoi A, Yoshida E, Yabuta Y, Shigeoka S. Analysis of the Regulation of Target Genes by an Arabidopsis Heat Shock Transcription Factor, HsfA2. Biosci Biotechnol Biochem . 2009;73:890–895. DOI: 10.1271/bbb.80809 - 50.
Pennycooke JC, Vepachedu R, Stushnoff C, Jones ML. Expression of an Α-Galactosidase Gene in Petunia Is Upregulated during Low-Temperature Deacclimation. JASHS . 2004;129:491–496. - 51.
Khokhar S, Apenten, RKO. Antinutritional Factors in Food Legumes and Effects of Processing. In: Squires VR, editor. The Role of Food, Agriculture, Forestry and Fisheries in Human Nutrition . 1st edn. EOLSS; 2003. p. 82–116. - 52.
Raboy V, Young KA, Dorsch JA, Cook A. Genetics and Breeding of Seed Phosphorus and Phytic Acid. J Plant Physiol . 2001;158:489–497. DOI: 10.1078/0176-1617-00361 - 53.
Raboy V. Seeds for a Better Future: “Low Phytate” Grains Help to Overcome Malnutrition and Reduce Pollution. Trends Plant Sci . 2001;6:458–462. DOI: 10.1016/S1360-1385(01)02104-5 - 54.
Kumar V, Sinha AK, Makkar HPS, Becker K. Dietary Roles of Phytate and Phytase in Human Nutrition: A Review. Food Chem . 2010;120:945–959. DOI: 10.1016/j.foodchem.2009.11.052 - 55.
Thompson LU. Potential Health Benefits and Problems Associated with Antinutrients in Foods. Food Res Int . 1993;26:131–149. DOI: 10.1016/0963-9969(93)90069-U - 56.
Vuverick I, Shamsuddin AM. Cancer Inhibition by Inositol Hexaphosphate (IP6) and Inositol: From Laboratory to Clinic. J Nutr . 2003;133:3830–3836. - 57.
Shamsuddin AM. Anti-Cancer Function of Phytic Acid. Int J Food Sci Technol . 2002;37:769–782. DOI: 10.1046/j.1365-2621.2002.00620.x - 58.
Van den Ende W. Multifunctional Fructans and Raffinose Family Oligosaccharides. Front. Plant Sci. 2013;4:247. DOI: 10.3389/fpls.2013.00247