ALL LIFE 2020, VOL. 13, NO. 1, 1–10 https://doi.org/10.1080/21553769.2019.1595745 PERSPECTIVES Development of halophytes as energy feedstock by applying genetic manipulations a b c Neelma Munir , Zainul Abideen and Nadia Sharif a b Department of Biotechnology, Lahore College for Women University, Lahore, Pakistan; Institute of Sustainable Halophyte Utilization, University of Karachi, Karachi, Pakistan; Department of Biotechnology, Women University, Mardan, Pakistan ABSTRACT ARTICLE HISTORY Received 19 April 2018 Decreasing arable land and fresh water resources, and increasing soil salinization and production of Accepted 6 March 2019 energy from food crops pose a threat to plant productivity and caused several environmental prob- lems. Using plant species which can grow on saline degraded soils for energy production can be a KEYWORDS sustainable approach because they do not compete for the agricultural lands and availability of fresh Bioenergy; desalination; water. These plants can be cultivated with seawater without compromising their biomass for com- drought; genetic mercializing purposes such as lignocellulosic content and seed yields and could strongly benefit as manipulation; halophytes; energy plants. Optimizing biomass production and its economic conversion to the end product are, lignocellulose; salinity however, of paramount importance. The biomass of halophytes can be improved through studying unexplored aspects of these plants related to genetic manipulations. Here, we recommended current advances and highlight the key genetic approaches required in halophytes for biofuel production. Genetic approaches might lead to desired alterations in the composition of halophytic lignocellulosic biomass, including higher quantity of cellulose and hemicelluloses and lower lignin. In summary, the genetic manipulations in halophytes might lead to improvement in biomass compositions hence can be used as a feedstock for the production of biofuel on nutrient poor degraded soils. Abbreviations energy resources are necessary to improve energy effi- ciency and to drop energy demand by oeff ring more EIA Energy Information Agency opportunity for daily energy consumption. IPCC Intergovernmental Panel on Climate Change Creeping energy crisis Shortage of fresh water Theworld isexperiencingtheenergycrisisbecause of Fresh water provisions are running lower throughout consumption of the limited fossil fuel assets (Amaro the world and this water emergency would worsen et al. 2012). The utilization of fossil fuel as a primary asthepopulationisincreasing. Most oftheworld’s energy source is currently perceived to be unsustain- Availability of fresh water is limited because they are able in light of exhausting assets and environmental mainly located in the polar icecaps and underground pollution (Khan et al. 2009). According to Energy stream frameworks which could only supply through Information Agency (EIA), the world energy require- wells and springs. In addition, irregular precipitation, ments are expected to be raised 60% more than today periodic rise in temperature and change in land cli- till 2030. If this trend continues then the world overall mate interactions also presented imbalance in water fossil oilstoreswillbedepletedinlessthan45years availability. Global climate models predict many dry (Ahmad et al. 2011) that might cause a shortage of periods in future that might experience greater water energy supply for economic activity. Thusly to unravel stress as these regions become warmer and drier (Ward these essential issues the advancements in renewable et al. 2016). Uneven rain timing, decreased access CONTACT Neelma Munir email@example.com © 2019 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 2 N. MUNIR ET AL. to water supplies, winds and low relative humidity that are grown and processed for bioenergy will have caused innate dry periods over a extended duration huge impact on food supply and demand system. This in many countries that aeff cts millions of people of is particularly fact that the cultivation of these dedi- the world (Sun et al. 2006;Grainger 2013). The grow- cated food crops for the purpose of bioenergy rather ing aridity and freshwater demands build a serious than food purposes only. The utilization of prime need to link scientific research with optimal water agricultural lands which was patents to feed the peo- management that will assist to allocate water more e-ffi ples in previous decades sharply boasting the food ciently in extremes water scarce areas. (Salinas et al. prices up to the limit which can harm life of common 2016). One solution is to use saline water in sub- people (Colombo and Onorati 2013). Growing food tropical habitats for agricultural purposes instead of crops for bioenergy instead of those for food prod- fresh water. Use of saline water impairs more than 45 ucts really invented the huge contention between food millionhectaresofirrigatedland(MunnsandTester and fuel. In order to represent and provides relax- 2008). Fresh water can be generated by using largely ation to extensive utilization for food-based feedstock available saline water through the process of desalina- crops to biofuel raises emerging technology that con- tion. Numerous nuclear powered desalination plants vert non-edible grasses and forest products. These are termed as second generation biofuel feedstocks plant are present; though the cost is higher especially for productivity changes are still held to baseline levels. poor developing countries in the world. It will cre- ate the transporting cost to transfer huge amounts of These second generation feedstocks for biofuel still desalinated seawater in to the plant (Hinrichsen and canpop up thelandcompactionsagainstfood crops Tacio 2002). Zhoua and Tolb (2005) estimated that can harm food prices and food security (Flora et al. the cost of desalination is equal to the cost required 2012). to transport it over 1600 km or raise the water up to Now the whole world is searching for more sustain- 2000 km. Somewhat high and far places have higher able and environmental friendly crops for the biofuels desalination costs while other places cost is higher otherwise the image of fuels production from plants due to transport rather than desalination. Desalinated can get bad views in the world regarding environmen- water might be an answer for some water-push dis- tal and food shortage issues. The compatible solution tricts, however not designed for spots that are poorer, forall thefood curseissuesmaytheplantswhich somewhere down in the inside of a landmass, or at cannot competetouse thecultivatedlandsfortheir elevated rise. Tragically, that incorporates a portion of survival. Those plants which can grow and complete the areas with greatest water issues. Another poten- theirlifeeventsonmarginalsoil, saline soilandother tial issue with desalination is the creation of salt water, then the prime agricultural lands. On the basis of these whichcanbeanoteworthyreasonformarinecontami- plants, we may solve dilemma of food vs fuel. nation when drained once again into the sea at elevated temperature (Zhou and Tol 2005). Limitation of water Halophytic crops for a saline agriculture and or presence of salty water both can decrease biomass bioenergy of economic important and might cause shortage in food supply. A consistent supply of reliable feedstock regarding quantity and quality of plant biomass is required for the monetary viability of the biofuel industry. The Food security plants specific to saline environments and can survive Lack of affordable nutrition by conventional channels and complete their life cycles, no less than, 200 mM hasbeenaseriousissueofexperiencemalnutrition NaCl are called halophytes (Grigore et al. 2014). How- and starvation on daily basis especially in third world ever, many can develop at salt concentration signifi- countries. Many scientists recommended that energy cantly higher than that of seawater (Rabie and Alma- made from edible plants for transport is not appropri- dini 2005). Salt resistance plants cover around 0.25% of ate (Nouairi et al. 2006). angiosperm species that represent approximately 600 Food crops such as sugarcane, wheat, maize and taxa of plants consist of genera and families (Fita et al. corn are the most efficient energy crops in current 2015). Halophytes are highlighted as wild plants but scenario (Cherubini et al. 2009). These edible crops hugenumbersofhalophytescan possiblybechanged ALL LIFE 3 Table 1. Ligno-cellulosic contents of halophytic biomass (% dry into valuable ‘new crops’, after extensive a domestica- weight). tion procedure. They are already salt resistant plants – Species Cellulose Hemicellulose Lignin which is the most essential and the most difficult qual- Grass halophytes ity to introduce and manipulate- it ought to be moder- 1 Aeluropus lagopoides 26.67 29.33 7.67 atelysimpletopracticeparticularbreedingprograms 2 Cenchrus ciliaris 22.67 23.17 7 3 Chloris baraeta 25.33 23 8.33 to quickly enhance the required agronomic attributes 4 D. bipinnata 26.67 24.68 6.67 of the most encouraging halophytic taxa. For spe- 5 D. annulatum 19 24.33 7 6 Eleusine indica 22 29.67 7 cific development conditions, it might be important 7 H. mucronatum 37 28.67 5 to choose the best genotypes, by killing or possibly 8 Lasiurus scindicus 24.67 29.67 6 9 Panicum turgidum 28 27.97 6 decreasing the substance of dangerous mixes or hostile 10 Paspalum paspaloides 20.33 32 2.33 to supplements, by expanding yields, or by enhancing 11 P. karka 26 29 10.33 12 S. ioclados 15.33 30.67 2 showcasing attributes (timespanofusability,market 13 Urochondra setulosa 25.33 25 6.33 14 Typha domingensis 26.33 38.67 4.67 accessibility, consistency of the item in size, shad- Non grass halophytes ing,taste, andsoforth), andtomodifygeneralfarm- 1 A. javanica 15.67 13.33 6.33 ing techniques to specific crops (Baram and Bourrier 2 A. indicum 11.33 13 7 3 Calotropis procera 12.33 11 5 2011). Individuals of halophytes have been collected 4 Ipomea pescaprea 12.67 17 5.33 from nature for hundreds of years. Sometimes they 5 Salsola imbricata 9 18.33 2.67 6 Salvadora persica 22 13.33 7 arepickledorcooked,ortheirleavesareregularly 7 Suaeda fruticosa 8.67 21 4.67 eaten as raw vegetables and salad, or sold in local mar- 8 Sueda monoica 10.67 11.33 2.33 9 Tamarix indica 12.17 24.67 3.33 kets (Nyankanga et al. 2012). The conventional use Conventional Species as sustenance of these species will make them all the 1 Panicum virgatum 45 31.4 12 2 Popolar 40 23 20 more effectively worthy by the overall population, with 3 Cynodon dactylon 25 35.7 6.4 thegoalthattheyarefitting possibilitytobetamed Abideen et al. (2011). and changed into verdant vegetable products for saline Karp and Shield (2008), Reshamwala et al. (1995). agribusiness. Halophytes are exceptionally nutritious alongside eatable trademark; for the most part they are rich in basic supplements – minerals, vitamins, amino of S. salsa oil can be processed to fatty acid methyl acids, as well as unsaturated fats, protein and antiox- esters (Piloto-Rodríguez et al. 2014). Substantial scale idants (Fita et al. 2015). These plants can grow under advancement and modern production of halophytes seawater and many of them are cultivated and domes- could be received as another agribusiness alternative ticated as vegetable crops due to their salt resistance by using reasonable areas along coastal areas. There ability. For instance Salicornia and Sarcocornia are two is a requirement for the efficient investigation of halo- suitable halophytes attracted due to their utilization in phytes to screen out high value industrial species and food purposes (Fita et al. 2015). Numerous halophytes their rearing for desirable plant attributes Many halo- can be potential oilseed plant to their chemical com- phytic species including Phragmites karka, Halopyrum position (Abideen et al. 2015). For instance, Salicornia mucronatum, Panicum antidotale and Desmostachya bigelovii is fascinating because of its seed production, bipinnata has been reported for promising lignocellu- approximately two tons per hectare every year, which losic content (Table 1)(Pantaetal. 2014). are similar to those of oilseed harvests of conventional Halophytes are reported as a sustainable source of species such as soybean. The chemical composition of bioethanol production in many studies. The produc- thesehalophytesare acceptable interm oftheirseed tion of ethanol from plant biomass depends on cellu- total protein (30%), oil contents (30%), and the oil con- lose, hemicelluose and lignin content of a potential fast tains of these plants composed of a high percentage growing species. Presence of higher lignin (30–40%) of polyunsaturated fatty acids (70% of linoleic acid) in energy feedstock ensure resistant to their sequen- so that it can be considered as promising edible oil. tial conversion from dry biomass to fermentable Chenopodium quinoa also need to be focused regard- sugars and in to ethanol. It was reported earlier ing food nutrient (Ladeiro 2012). Seeds of S. salsa studies that vfi e promising plants such as Phrag- can be used as a raw material to produce fatty acid mites karka, Panicum antidotale, Desmostchya bipin- methyl esters from their high oil contents, about 97% nata, Halophyrum mucronatum and Typha domengesis 4 N. MUNIR ET AL. Figure 1. Some halophytes that can be a potential candidate for biofuel production. (Figure 1) showed exceptionally optimal ratios of cel- variation in lignocellulosic contents and oil yields may lulose, hemicellouse and lignin and in some cases be due to the harvesting stage, different plant species, better than our food crops. There are also some cultivation time, climate change, ripening stage of plant species those showed lower cellulose and hemi- plant, and/or extraction method of chemical analysis. cellulose content such as Dichanthium annulatum, Considerable genetic variability exists among halo- Sporobolus ioclados, Aerva javanica and Arthrocne- phytic genotypes (Llanes et al. 2011) and genotypes of mum indicum (Tables 1 and 2). A recent study some populations may perform better in suboptimal assessed Juncus maritimus a salt marsh plant that conditions (Maron et al. 2004). Now a day’s mod- can be used for producing lignocellulosic biomass, ern genetic manipulation tools are also in operation because its total carbohydrate content can reach up to enhance biomass of salt and the drought resistance to 73%, with cellulose and hemicellulose represent- plants to produce higher biomass which can be useful ing approximately 41% and 31%, respectively, of the for bioenergy. lignocellulose biomass (Smichi et al. 2016). Tamarix aphylla plants were irrigated from domestic sewage Genetic manipulation of biosynthetic pathways −1 (EC approximately 3 dS/m ) to different salinity lev- of halophytes to enhance bioethanol production −1 els or with brine (EC approximately 7–10 dS/m ), It is essential to outline the most suitable approach to produced 52 and 26 t/ha, respectively, of organic convert plant complex polysaccharides into the sug- biomass. Tamarix wasselectedasabiofuelplants ars and their conversion to ethanol by fermentation forits higher celluloseand lowhemicelluloseand for biofuel production. If cell wall degrading enzymes polyphenol contents, properties particularly suitable (hemicellulase and cellulase) production can be induced for bioethanol production, because the species of yeast inside the growing cell through bioengineering of the commonly used for fermentation prefer C6 − sugars crop, then the reliance on microbial bioreactors for to C5 − sugars (Calvin 1980;Santi et al. 2015). The ALL LIFE 5 Table 2. Oil content, Saponiﬁcation number (SN) Iodine value (IV) suitable genes to modify synthesis of sugars, lignin and Cetane number (CN) of fatty acid methylesters of some halophytes lipids in plants.. seeds oils. Finding an operative method for tissue culturing Name of species Oil content % SN IV CN and transformation of water hyacinth cultivars is the Alhagi marorum 21.9 202.31 97.31 51.38 initial step. Tissue culture specifies the strategies and Allenrolfea occidentialis 14 193.44 121.36 47.21 Arthrocnemum macrostachyum 25 205.66 115.5 46.86 procedures accessible for cultivating a huge number Atriplex bunge 15.8 194.89 75.29 57.35 of cells in controlled and axenic environment. Cell Atriplex rosea 12.9 194.05 115.5 49.33 Cressa cretica 23.3 203.5 114.27 47.41 totipotency that is to regenerate intact generally as Halogeton glomeratus 24.7 199.82 103.47 50.31 fertile plants, that depends on the expression of devel- H. mucronatum 22.7 202.95 124.63 45.15 Haloxylon stocksii 23.3 203.27 121.71 45.77 opmental genesisthe basicprinciple of tissuecul- Kochia scoparia 9.7 200.56 138.69 42.31 turing. The last are typically heritable, in light of the Kosteletzkya virginica 17.54 205.99 113.14 47.37 Sacrobatus vermiculatus 17.5 199.22 139.84 42.23 tissue culture conditions. Hence, numerous permu- S. bigelovii 29.7 200.86 154.32 38.78 tations of plant growth regulators are needed to be Salicornia brachiata 22.4 129.89 29.7 81.67 S. europaea 30 202.55 155.96 38.19 evaluated for plant organogenesis and regeneration Salicornia fruticosa 25.98 204.38 93.68 51.96 Sarcocornia ambigua 13 187.19 106.66 51.49 (Hassanein and Soltan 2000). In order to use the tissue Suaeda fruticosa 25.98 204.38 93.68 51.96 cultureasabaseline forgenetictransformation,thisis Suaeda aralocaspica 29.92 198.7 146.59 40.82 Suaeda salsa 25.99 171.1 133.9 48.1 a crucial pre-requisite. In biolistic gene delivery and Sueda torreyana 25.25 202.02 154.77 38.49 Agrobacterium tumefaciens-mediation tissue culturing Source: Abideen et al. (2015). techniques this is a key component needed (Bhatia et al. 2004). Mass multiplication of plants and micro- propagation is a major application of tissue cultur- enzymes will be reduced and the production costs ing. It oer ff s another method for acquiring particular couldbeecffi ient(Balan 2014). Cost optimization can pathogen free plants from meristem culture, heredi- be accomplished by engineering of lignin biosyn- tary control, and the generation of haploid plants. In thetic pathway in plants. These measures can substan- the propagation of various plant species the Micro- tially reduce the cost of pretreatments but the plants propagation has been applied broadly. The compo- those already have lower lignin may be more cost nents that are responsible for the success of a tissue effective in hydrolysis of biomass. The yield of cellu- culture system includes composition of the growth losic biofuel can be enhance by up regulation of cellu- media,plantspecies,availabilityofutilizablecarbon, lose biosynthesis pathway enzymes to support higher growth regulators, the axenic culture conditions and polysaccharide production (Bita and Gerats 2013). It callus induction response. Some additional factors are is reported earlier that adaptable polymerization is carbon source, trace elements, plant growth regulators, possible in plants and mono-lignins can be substi- inorganic salts and organic compounds (Bhattacharya tuted by polyphenols (Wymelenberg et al. 2006). These and Kumar 2010). Tissue culture of halophytes includ- ing S. bigelovii (Lee et al. 1992), Leymus chinensis T, above describe procedure may not suffer the advance- Suaeda maritima hasbeenexploredrecently.Thereare ment procedure of plants, but will increase extrac- many halophytes that show potential in biofuel pro- tion of important saccharides which is critical for the energy production from the plants. Similar approach duction but still needs careful studies to improve their can be applied to water hyacinth and many other yield by genetic transformation. bioenergy feedstocks which is composed of lower lignin content and might enhance extraction of sac- Genetic transformation can enhance oil content charides (Lukuyu et al. 2014). Vanden Wymelenberg of halophyte et al. (2006) revealed a substantial number of genes involved in breakdown of lignin from the fungus Knockout and overexpression strategies have been Phanerochaetechrysosporium genome. Accordingly, applied lately to clarify the genes role in lipid synthesis expression of such genes in water hyacinth may also and accumulation in order to enhance the Arabidop- reduce the cost of biofuel. The utilization of transgenes sis thaliana, rapeseed (Brassica napus)andsoybean could support already existing breeding methods to (Glycine max), plants lipid contents. These above enhance biofuel production through accessibility of described studies might improve quality and quantity 6 N. MUNIR ET AL. triacylglycerols of seed oil and other plant organs. biosynthesis the ACCase levels are a restricting stride Ohlrogge and Jaworski (1997) that seed might be pre- for the most part in cells that ordinarily don’t store programmed to produce the particulate amount of a lot of lipid (Figure 2). Another endeavor to expand fatty acids (Ohlrogge and Jaworski 1997); substan- the lipid production involving unsaturated fat amal- tial efforts have been made to make the expression of gamation through 3-ketoacyl-acyl-transporter protein pathways of fatty acid synthesizing enzymes. synthase III (KASIII) was made but was not much The initial step in synthesis of fatty acid in many effective (Dehesh et al. 2001). Many fascinating results organisms is catalyzed by acetyl-CoA carboxylase have been performed through the overexpression of (ACCase) is the exchange of acetyl-coenzyme A (CoA) genesrequiredinTAG assembly.A40% increasein to malonyl-CoA. Nevertheless, significant efforts were lipid content was achieved through the overexpres- made to enhance lipid content in a range of sys- sion of cytosolic yeast, glycerol-3-phosphate dehydro- tems by utilizing ACCase overexpression which seems genase (G3PDH), in the seeds of B. napus (Vigeolas somehow disappointing. Insignificant increase in seed et al. 2007). Synthesis of glycerol-3-phosphate which is −1 −1 lipid content 6% (384 mg g and 408 mg g dry needed for TAG formation is catalyzed by the G PDH. weight for wild-type and transgenic ACCase rapeseed Overall seed oil production thus is also dependent lines, respectively) was noted by the overexpression of somewhat on genes involved in TAG assembly. This ACCase in the oleaginous seeds of B. napus.Inlipid finding was further strengthening by studies on the Figure 2. Mechanism pathways for drought tolerance in B. napus. ALL LIFE 7 correlation of TAG assembly genes overexpression additional un-saturated fatty acids. It is also pragmatic and increase in seed oil content. Studies (Jain et al. that at lower temperature and light intensity favors the 2000;Jakoetal. 2001;Tayloretal. 2002; Lardiza- synthesis of unsaturated fatty acids protect photosyn- bal et al. 2008)reportedsignificantincreaseinplant thesis apparatus by reducing the photoinhibition and lipid productivity by overexpressing the TAG assembly photodamage of PSII and PSI (Sui et al. 2007). Plant genes (lysophosphatidic acid acyltransferase, glycerol- seedlings of Solanum tuberosum L. was transformed 3-phosphate acyltransferase or diacylglycerol acyl- with the desA encoding gene 12 acyl-lipid desaturase transferase). Due to the fact that enzymes seem to in to another organism cyanobacterium Synechocys- be good candidates for overexpression strategies to tissp. PCC 6803. In this situation sequence of genes increase storage lipid contents, an attempt has also was translationally fuzed with the sequence of the been made to use directed evolution for increasing the reporter gene encoding to thermostable lichenase to efficiency of DAGAT enzymes (Siloto et al. 2009). analyze the efficiency of this gene expression in plant . Geneticmanipulationinhalophytesfor thebiofuel Interestingly the lichenase retained the thermostability productivity can be introduced for two purposes (a) and its activity within the hybrid protein observed by to increase lipids contents (b) to improve oil quality. the comparison of hybrid and native gene expression Recently researchers have observed that high levels of however another enzyme named as desaturase started NaCl enhance membrane lipids’ unsaturated fatty inserting the double bond in fatty acid chains to amend acid in halophytes. α-linolenic acid 18:3 is the main their composition in membrane lipids. (Maali-Amiri fatty acid enhance under NaCl stress in halophytes. et al. 2007). The shoots enclosed higher linoleic acid Stress resistance ability of transgenic tobacco plant (39–73%) and linolenic acid (12–41%) in most trans- at water deficit and salinity was improved through x- formed plants. In comparison to wild-type plants, the 3 desaturases (Sui and Han 2014;Zhanget al. 2005), total absolute unsaturated FAs content was (20–42%) whichinfersthatthe droughtandsalt resistance of higher in transformants. When severely cooled to plant is dependent on the unsaturated fatty acids −7°C wild-type plants increased their membrane lipid (Berberich et al. 1998;Mikamiand Murata 2003). substantially by 25% whereas in under such condi- This concept was further strengthen by the lower tions the membrane lipid peroxidation rate was not of the x-3 and x-6 desaturase activity in Synechocys- increased in transformed plants. The reason for the tis mutants (Allakhverdiev et al. 2001). In another higher resistance to lower temperatures and the study an increased tolerance to low temperature and oxidative injury could have induced by hypothermia salt stress was observed when x-6 desaturase sun- (Maali-Amiri et al. 2007). flower gene were transformed in yeast cells. Three Gas–liquid chromatography (GLC) technique was sortsofhalophyteswerenoticedwhichincrementtheir used for the oil compositions (qualitative and quanti- resilience to salt stress through expanding or keep- tative) of esterified fatty acids (FAs) in the total fat con- ing up their unsaturated fats composition. Possible tent of halophytic plants such as Salicornia europaea, clarification about role of higher unsaturated fatty Artemisia lerchiana and Suaedaaltissima collected in acid is linked with the membrane (Na+ or K+)ion their natural environments. GLC results showed that channels and Na+/H+ antiporter frameworks stabil- the vegetative tissues of these halophytes contained ity under stress situations. Higher quantity of unsat- 16 very-long-chain FAs among total 24 FA species. urated fatty acids robust the membrane uidi fl ty, and Around four very-long-chain FAs groups were C20, triggers the activity of Na+/H+ antiporter and H+- C21, C22, and C23, each including saturated, mono-, ATPase to protect the photosynthesis apparatus and and di-unsaturated components; C24 and C25 FAs ultimately increase carboxylation efficiency. It was also were also present. The concentration of VLCFAs in reported that with the change in membrane u fl id- the total FAs comprised4–64%.Invegetativeorgans ity can activate certain membrane bound enzymes of higher plants not subjected to genetic transforma- which can alter physiological responses of plants under tion, such a high VLCFA content was found for the suboptimal conditions (Zhang et al. 2012). Accord- first time. Saturated and even-numbered components ing to Sui and Han (Sui and Han 2014)toenhance predominated among the VLCFAs, and the roots membrane fluidity for the ion compartments, it’s prob- exceeded several fold the above-ground organs in the able that euhalophytes for example, S. salsa required total VLCFA content. Possible pathways of VLCFA 8 N. MUNIR ET AL. biosynthesis in plants, VLCFA content in the vegeta- (C18:3) was observed in M. crystallinum leaves. These tive tissues, and the physiological role of membrane changesinfatty acid compositioninterestingly block lipid FA composition in the plant salt metabolism are the sugar transport to leaves and conversion path- discussed (Ivanova et al. 2009). ways but resulted in higher oil production and accu- The study by Ramani et al. (2004)focusedon mulation in these plants (Zhai et al. 2017). Another sulfolipids role and salt resistance mechanisms of futureoption wouldbetodissolvelignocellulosemate- halophytes including Sesuvium portulacastrum, Aster rial from halophytes in saline ionic liquids, which tripolium L., members of Compositae and L., Aizoa arewellestablished as alternativeand ‘green’sol- ceae families, and glycophyte A. thaliana (L.) Heynh, ventstobeusedinthepre-treatmentofthewalls Brassicaceae. The sulfolipid contents of Sesuvium and of plant cells prior to enzymatic hydrolysis (Gunny Aster increased significantly at 517 mM or 864 mM et al. 2014). Lignocellulosic biomass from halophytes salt stress conditions. At up to 100 mM NaCl changes for ethanol production proved advantageous both in in sulfolipid contents were not observed in Arabidop- term of high net productivity and low maintenance sis. Whereas with an increase in NaCl concentra- costs (Fooladvand and Fazelinasab 2014). Consider- tion of Aster modified the fatty acid profile of sulfo- ing the advantages of second-generation biofuels, it is recommended that biofuel production be increased up quinovosyldiacyl glycerol. The presence of 16:0/18:3 to 10–20 EJ a year by 2050 (Searle and Malins 2015) and 18:3/18:3 molecules was confirmed through sul- folipids quantification performed by LC-MS from and the share of biofuels in the transport sector be Aster and Sesuvium. increased from 3% to 8% worldwide between 2013 and The sulfolipid content improved substantially in the 2035. presence of NaCl in Crithmum maritimum halophyte. Plants treated with salinity were similar in fatty acid Conclusions composition of sulfolipids, except for linolenic acids Halophytes have a strong potential of biofuel pro- and linoleic composition. duction as there are multiple feedstocks which could There was a significant decline in sulfolipids con- be exploited industrially at lower cost. Exploration of tent under NaCl-treated plants in the unsaturated fatty halophytes to produce biofuel can reduce the depen- acid (C18:3) composition as compared to the con- dence on conventional fuels in the world and can trol plants, whereas the percentage of unsaturated discover some environmental benefits. However, bio- fatty acids (C18:2) increase analogously (Ben Hamed fuel productions from some halophytes stocks need et al. 2005).Inaconclusionfromthe abovestudies it special attention to improve their biomass for higher is found that the sulfolipds are an important aspect yields by using genetic manipulations. A suitable com- of strategy in salt tolerance of halophytes. Nouairi position of lignocellulosic biomass (higher cellulose et al. (2006) carried out the experiments on young and hemi cellulose but lower lignin content) induce small-sized hydroponically grown S. portulacastrum through genetic manipulations manifest the poten- and aseptically germinated seeds of Mesembryanthe- tial of halophytes as a compatible biofuel candidate to mum crystallinum.Theyexposed thesehalophytesto existing edible feedstock. These plant not only avoids 0, 50, 100 and 200 μM of cadmium concentration competition with water and land meant for production for four weeks. The effect of cadmium on fatty acid of edible crops because of its ability to grow in soils composition and leaf lipid contents of S. portulacas- with salinity but will also help in CO sequestration trum and M. crystallinum were studied recently. It was and reclaiming degraded lands. found that the total lipids (TL) contents as well as lipid fractions such as neutral lipids (NL) galactolipids Disclosure statement (GL) and phospholipids (PL) reduced more in M. No potential conflict of interest was reported by the authors. crystallinum as compared to S. portulacastrum at 200 μM cadmium concentration. Additionally there was no noteworthy changes in the aggregate unsaturated References fat composition of S. portulacastrum leaves. How- AbideenZ,AnsariR,KhanMA. 2011. Halophytes: potential ever, an increase in the di-unsaturated fatty acid source of ligno-cellulosic biomass for ethanol production. (C18:2) and decrease of the tri-unsaturated fatty acid Biomass Bioenergy. 35(5):1818–1822. ALL LIFE 9 Abideen Z, Qasim M, Rizvi RF, Gul B, Ansari R, Khan MA. Ortíz S., editors. Integrating agriculture, conservation and 2015. Oilseed halophytes: a potential source of biodiesel ecotourism: societal influences. Issues in agroecology – using saline degraded lands. Biofuels. 6(5–6):241–248. present status and future prospectus. Dordrecht: Springer; Ahmad AL, Yasin NHM, Derek CJC, Lim JK. 2011. Microal- p. 163–225. gae as a sustainable energy source for biodiesel production: Fooladvand Z, Fazelinasab B. 2014. Evaluate the potential halo- a review. Renew Sust Energ Rev. 15(1):584–593. phyte plants to produce biofuels. Eur J Biotechnol Biosci. Allakhverdiev SI, Kinoshita M, Inaba M, Suzuki I, Murata N. 2:1–3. 2001. Unsaturated fatty acids in membrane lipids protect the Grainger A. 2013. Controlling tropical deforestation. London: photosynthetic machinery against salt-induced damage in Routledge/CRC Press. synechococcus. Plant Physiol. 125(4):1842–1853. Grigore MN, Ivanescu L, Toma C. 2014. Halophytes: An inte- Amaro HM, Macedo ÂC, Malcata FX. 2012. Microalgae: grative anatomical study. New York, NY: Springer. an alternative as sustainable source of biofuels? Energy. Gunny AA, Arbain D, Edwin Gumba R, Jong BC, Jamal P. 2014. 44(1):158–166. Potential halophilic cellulases for in situ enzymatic sacchari- Balan V. 2014. Current challenges in commercially produc- fication of ionic liquids pretreated lignocelluloses. Bioresour ing biofuels from lignocellulosic biomass, ISRN. Biotechnol. Technol. 155:177–181. 2014:31. HassaneinA,SoltanD. 2000. Solanum nigrum is a model sys- Baram M., Bourrier M. 2011. Governing risk in GM agricul- tem in plant tissue and protoplast cultures. Biol Plantarum. ture:Anintroduction. In:Baram M.,BourrierM.,editors. 43(4):501–509. Governing risk in GM agriculture. New York: Cambridge Hinrichsen D, Tacio H. 2002. The coming freshwater crisis is University Press; p. 1–12. already here, the linkages between population and water. Ben Hamed K, Ben Youssef N, Ranieri A, Zarrouk M, Abdelly Washington (DC): Woodrow Wilson International Center C. 2005. Changes in content and fatty acid profiles of total for Scholars, 1–26. lipids and sulfolipids in the halophyte Crithmum maritimum Ivanova T, Myasoedov N, Pchelkin V, Tsydendambaev V, under salt stress. J Plant Physiol. 162(5):599–602. Vereshchagin A. 2009. Increased content of very-long-chain BerberichT,HaradaM,SugawaraK,KodamaH,Iba K,Kusano fatty acids in the lipids of halophyte vegetative organs, Rus- T. 1998. Two maize genes encoding omega-3 fatty acid desat- sian. J Plant Physiol. 56(6):787–794. urase and their differential expression to temperature. Plant Jain RK, Coeff y M, Lai K, Kumar A, MacKenzie SL. 2000. Mol Biol. 36(2):297–306. Enhancement of seed oil content by expression of glycerol- Bhatia P, Ashwath N, Senaratna T, Midmore D. 2004. Tissue 3-phosphate acyltransferase genes. Biochem Soc T. 28(6): culture studies of tomato (Lycopersicon esculentum). Plant 958–961. Cell Tissue Organ Cul. 78(1):1–21. Jako C, Kumar A, Wei Y, Zou J, Barton DL, Giblin EM, Cov- Bhattacharya A, Kumar P. 2010. Water hyacinth as a poten- ello PS, Taylor DC. 2001. Seed-specific over-expression of an tial biofuel crop. Electron J Environ Agric Food Chem. Arabidopsis cDNA encoding a diacylglycerol acyltransferase 9(1):112–122. enhances seed oil content and seed weight. Plant Physiol. Bita C, Gerats T. 2013. Plant tolerance to high temperature in 126(2):861–874. a changing environment: scientific fundamentals and pro- Karp A, Shield I. 2008. Bioenergy from plants and the sustain- duction of heat stress-tolerant crops. Front Plant Sci. 4: able yield challenge. New Phytolog. 179(1):15–32. 273. Khan SA, Rashmi, Hussain MZ, Prasad S, Banerjee UC. 2009. Calvin M. 1980. Hydrocarbons from plants: analytical methods Prospects of biodiesel production from microalgae in India. and observations. Naturwissenschaften. 67(11):525–533. Renew Sust Energ Rev. 13(9):2361–2372. Cherubini F, Bird ND, Cowie A, Jungmeier G, Schlamadinger Ladeiro B. 2012. Saline agriculture in the 21st century: using B, Woess-Gallasch S. 2009.Energy- andgreenhousegas- salt contaminated resources to cope food requirements. J based LCA of biofuel and bioenergy systems: key issues, Botany. 2012:1–7. ranges and recommendations. Resour Conserv Recycl. Lardizabal K, Effertz R, Levering C, Mai J, Pedroso MC, Jury T, 53(8):434–447. Aasen E, Gruys K, Bennett K. 2008.ExpressionofUmbelop- Colombo L, Onorati A. 2013. Food. Riots and rights. London sisramannianaDGAT2Ainseedincreasesoilin soybean. (UK): IIED. Plant Physiol. 148(1):89–96. Dehesh K,TaiH,EdwardsP,ByrneJ,JaworskiJG. 2001.Over- Lee CW, Glenn EP, O’Leary JW. 1992.Invitropropaga- expression of 3-ketoacyl-acyl-carrier protein synthase IIIs tion of Salicornia bigelovii by shoot-tip cultures. Hort Sci. in plants reduces the rate of lipid synthesis. Plant Physiol. 27(5):472–472. 125(2):1103–1114. Llanes A, Bonercarrere V, Capdevielle F, Vidal S, Luna V. 2011. Fita A, Rodríguez-Burruezo A, Boscaiu M, Prohens J, Vicente Genetic diversity in a natural population of the halophytic O. 2015. Breeding and domesticating crops adapted to legume Prosopis strombulifera revealed by AFLP finger- drought and salinity: a new paradigm for increasing food printing. B Soc Argent Bot. 46(3–4):305–312. production. Front Plant Sci. 6:978. Lukuyu B, Okike I, Duncan AJ, Beveridge M, Blummel M. Flora CB, Bain C, Call C. 2012. Sustainability standards and 2014. Use of cassava in livestock and aquaculture feeding their implications for agroecology. In: Campbell W., López programs. ILRI Discussion Paper 25. Nairobi, Kenya: ILRI. 10 N. MUNIR ET AL. Maali-Amiri R, Goldenkova-Pavlova IV, Yur’eva NO, Pchelkin Siloto RM, Truksa M, Brownfield D, Good AG, Weselake RJ. VP, Tsydendambaev VD, Vereshchagin AG, Deryabin AN, 2009. Directed evolution of acyl-CoA:diacylglycerol acyl- Trunova TI, Los DA, Nosov AM. 2007.Lipid fattyacid transferase: development and characterization of Brassica composition of potato plants transformed with the 12- napusDGAT1 mutagenizedlibraries.Plant PhysiolBioch. desaturase gene from cyanobacterium, Russian. J Plant Phys- 47(6):456–461. iol. 54(5):600–606. Smichi N, Messaoudi Y, Moujahed N, Gargouri M. 2016. Maron JL, Vilà M, Bommarco R, Elmendorf S, Beardsley P. Ethanol production from halophyte Juncus maritimus using 2004. Rapid evolution of an invasive plant. Ecol Monogr. freezing and thawing biomass pretreatment. Renew Energ. 74(2):261–280. 85:1357–1361. Mikami K, Murata N. 2003. Membrane u fl idity and the percep- Sui N, Han G. 2014.Increases ofunsaturatedfattyacidsin tion of environmental signals in cyanobacteria and plants. membrane lipids protects photosystem II from photoinhi- Prog Lipid Res. 42(6):527–543. bition under salinity in different halophytes. J Agricul Sci. Munns R, Tester M. 2008. Mechanisms of salinity tolerance. 6(12):251. Annu Rev Plant Biol. 59:651–681. SuiN,LiM,ZhaoS-J,LiF,LiangH,Meng Q-W. 2007.Over- NouairiI,GhnayaT,Youssef NB,Zarrouk M,GhorbelMH. expression of glycerol-3-phosphate acyltransferase gene 2006. Changes in content and fatty acid profiles of total lipids improves chilling tolerance in tomato. Planta. 226(5):1097– of two halophytes: Sesuvium portulacastrum and Mesem- 1108. bryanthemum crystallinum under cadmium stress. J Plant Sun Y, Solomon S, Dai A, Portmann RW. 2006.Howoftendoes Physiol. 163(11):1198–1202. it rain? J Climate. 19(6):916–934. Nyankanga RO, Onwonga RN, Wekesa FS, Nakimbugwe D, Taylor DC,Katavic V,ZouJ,MacKenzie SL,KellerWA,An Masinde D, Mugisha J. 2012. Effect of inorganic and organic J, Friesen W, Barton DL, Pedersen KK, Giblin EM. 2002. fertilizers on the performance and profitability of grain ama- Field testing of transgenic rapeseed cv. Hero transformed ranth (Amaranthus caudatus L.) in Western Kenya. J Agricul with a yeast sn-2 acyltransferase results in increased oil con- Sci. 4(1):223. tent, erucic acid content and seed yield. Molecul Breed. Ohlrogge JB, Jaworski JG. 1997. Regulation of fatty acid syn- 8(4):317–322. thesis annual review of plant physiology and plant molec- Vigeolas H, Waldeck P, Zank T, Geigenberger P. 2007.Increas- ular biology. Annu Rev Plant Physiol Plant Mol Biol. 48: ing seed oil content in oil-seed rape (Brassica napus L.) by 109–136. over-expression of a yeast glycerol-3-phosphate dehydroge- PantaS,Flowers T,LaneP,DoyleR,HarosG, ShabalaS. 2014. nase under the control of a seed-specific promoter. Plant Halophyte agriculture: success stories. Environ Exper Bot. Biotechnol J. 5(3):431–441. 107(Supplement C):71–83. Ward RD, Friess DA, Day RH, MacKenzie RA. 2016.Impacts of Piloto-Rodríguez R, Melo EA, Goyos-Pérez L, Verhelst S. 2014. climate change on mangrove ecosystems: a region by region Conversion of by-products from the vegetable oil industry overview. Ecosyst Health Sustainabil. 2(4):e01211. into biodiesel and its use in internal combustion engines: a WymelenbergAV,Minges P,SabatG,MartinezD,Aerts A, review. Braz J Chem Eng. 31(2):287–301. Salamov A, Grigoriev I, Shapiro H, Putnam N, Belinky Rabie G, Almadini A. 2005. Role of bioinoculants in devel- P. 2006. Computational analysis of the Phanerochaete opment of salt-tolerance of Vicia faba plants under salinity chrysosporium v2.0 genome database and mass spectrom- stress. Afr J Biotechnol. 4(3):210. etry identification of peptides in ligninolytic cultures reveal Ramani B, Zorn H, Papenbrock J. 2004. Quantification and fatty complex mixtures of secreted proteins. Fungal Genet Biol. acidprofilesofsulfolipidsintwohalophytesandaglycophyte 43(5):343–356. grown under different salt concentrations. Z Naturforsch C. Zhai Z, Liu H, Xu C, Shanklin J. 2017.Sugar potentiation of 59(11–12):835–842. fatty acid and triacylglycerol accumulation. Plant Physiol. Reshamwala S,Shawky BT,DaleBE. 1995. Ethanol produc- 175(2):696–707. tion from enzymatic hydrolysates of AFEX-treated coastal Zhang M, Barg R, Yin M, Gueta-Dahan Y, Leikin-Frenkel A, bermudagrass and switchgrass. Appl Biochem Biotechnol. Salts Y, Shabtai S, Ben-Hayyim G. 2005.Modulated fatty 51–52(1):43–55. acid desaturation via overexpression of two distinct ω-3 Salinas CX, Gironás J, Pinto M. 2016.Water security as achal- desaturases differentially alters tolerance to various abi- lenge for the sustainability of La Serena-Coquimbo conurba- otic stresses in transgenic tobacco cells and plants. Plant J. tion in northern Chile: global perspectives and adaptation. 44(3):361–371. Mitig Adapt Strat Gl. 21(8):1235–1246. ZhangJ,LiuH, SunJ,LiB,Zhu Q,Chen S,ZhangH. 2012.Ara- Santi G, Muzzini VG, Galli E, Proietti S, Moscatello S, Bat- bidopsis fatty acid desaturase FAD2 is required for salt tol- tistelli A. 2015.Mycelialgrowthand enzymaticactivities erance during seed germination and early seedling growth. of white-rot fungi on anaerobic digestates from industrial PloS One. 7(1):e30355. biogas plants. Environ Engin Manag J. 14(7):1713–1719. Zhou Y, Tol RSJ. 2005.Evaluatingthe costsofdesali- Searle S, Malins C. 2015. A reassessment of global bioenergy nation and water transport. Water Resour Res. 41(3). potential in 2050. GCB Bioen. 7(2):328–336. doi:10.1029/2004WR003749.
Frontiers in Life Science
– Taylor & Francis
Published: Jan 1, 2020
Keywords: Bioenergy; desalination; drought; genetic manipulation; halophytes; lignocellulose; salinity