If. Hal Review 2019
If. Hal Review 2019
If. Hal Review 2019
To cite this article: Neelma Munir, Zainul Abideen & Nadia Sharif (2019): Development of
halophytes as energy feedstock by applying genetic manipulations, Frontiers in Life Science, DOI:
10.1080/21553769.2019.1595745
Article views: 94
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 affects 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 effi- 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
million hectares of irrigated land (Munns and Tester 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
are present; though the cost is higher especially for termed as second generation biofuel feedstocks plant
poor developing countries in the world. It will cre- productivity changes are still held to baseline levels.
ate the transporting cost to transfer huge amounts of These second generation feedstocks for biofuel still
desalinated seawater in to the plant (Hinrichsen and can pop up the land compactions against food 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, for all the food curse issues may the plants which
somewhere down in the inside of a landmass, or at cannot compete to use the cultivated lands for their
elevated rise. Tragically, that incorporates a portion of survival. Those plants which can grow and complete
the areas with greatest water issues. Another poten- their life events on marginal soil, saline soil and other
tial issue with desalination is the creation of salt water, then the prime agricultural lands. On the basis of these
which can be a noteworthy reason for marine contami- 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
has been a serious issue of experience malnutrition 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 huge numbers of halophytes can possibly be changed
FRONTIERS IN LIFE SCIENCE 3
into valuable ‘new crops’, after extensive a domestica- Table 1. Ligno-cellulosic contents of halophytic biomass (% dry
tion procedure. They are already salt resistant plants – weight).
which is the most essential and the most difficult qual- Species Cellulose Hemicellulose Lignin
ity to introduce and manipulate- it ought to be moder- Grass halophytesa
1 Aeluropus lagopoides 26.67 29.33 7.67
ately simple to practice particular breeding programs 2 Cenchrus ciliaris 22.67 23.17 7
to quickly enhance the required agronomic attributes 3 Chloris baraeta 25.33 23 8.33
4 D. bipinnata 26.67 24.68 6.67
of the most encouraging halophytic taxa. For spe- 5 D. annulatum 19 24.33 7
cific development conditions, it might be important 6 Eleusine indica 22 29.67 7
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 (time span of usability, market 13 Urochondra setulosa 25.33 25 6.33
accessibility, consistency of the item in size, shad- 14 Typha domingensis 26.33 38.67 4.67
ing, taste, and so forth), and to modify general farm- Non grass halophytesa
1 A. javanica 15.67 13.33 6.33
ing techniques to specific crops (Baram and Bourrier 2 A. indicum 11.33 13 7
2011). Individuals of halophytes have been collected 3 Calotropis procera 12.33 11 5
4 Ipomea pescaprea 12.67 17 5.33
from nature for hundreds of years. Sometimes they 5 Salsola imbricata 9 18.33 2.67
are pickled or cooked, or their leaves are regularly 6 Salvadora persica 22 13.33 7
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 Speciesb
as sustenance of these species will make them all the 1 Panicum virgatum 45 31.4 12
more effectively worthy by the overall population, with 2 Popolar 40 23 20
3 Cynodon dactylon 25 35.7 6.4
the goal that they are fitting possibility to be tamed a Abideen et al. (2011).
and changed into verdant vegetable products for saline b Karp and Shield (2008), Reshamwala et al. (1995).
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
(EC approximately 3 dS/m−1 ) to different salinity lev- of halophytes to enhance bioethanol production
els or with brine (EC approximately 7–10 dS/m−1 ),
produced 52 and 26 t/ha, respectively, of organic It is essential to outline the most suitable approach to
biomass. Tamarix was selected as a biofuel plants convert plant complex polysaccharides into the sug-
for its higher cellulose and low hemicellulose and ars and their conversion to ethanol by fermentation
polyphenol contents, properties particularly suitable for biofuel production. If cell wall degrading enzymes
for bioethanol production, because the species of yeast (hemicellulase and cellulase) production can be induced
commonly used for fermentation prefer C6 − sugars inside the growing cell through bioengineering of the
to C5 − sugars (Calvin 1980; Santi et al. 2015). The crop, then the reliance on microbial bioreactors for
FRONTIERS IN LIFE SCIENCE 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
Allenrolfea occidentialis 14 193.44 121.36 47.21
initial step. Tissue culture specifies the strategies and
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
Atriplex rosea 12.9 194.05 115.5 49.33 of cells in controlled and axenic environment. Cell
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
H. mucronatum 22.7 202.95 124.63 45.15 fertile plants, that depends on the expression of devel-
Haloxylon stocksii 23.3 203.27 121.71 45.77 opmental genes is the basic principle of tissue cul-
Kochia scoparia 9.7 200.56 138.69 42.31
Kosteletzkya virginica 17.54 205.99 113.14 47.37 turing. The last are typically heritable, in light of the
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
Salicornia brachiata 22.4 129.89 29.7 81.67 tations of plant growth regulators are needed to be
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
Suaeda aralocaspica 29.92 198.7 146.59 40.82
culture as a baseline for genetic transformation, this is
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 offers another method for acquiring particular
could be efficient (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, plant species, availability of utilizable carbon,
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-
above describe procedure may not suffer the advance- ing S. bigelovii (Lee et al. 1992), Leymus chinensis T,
ment procedure of plants, but will increase extrac- Suaeda maritima has been explored recently. There are
tion of important saccharides which is critical for the many halophytes that show potential in biofuel pro-
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) and soy bean
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) genes required in TAG assembly. A 40% increase in
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
lipid content 6% (384 mg g−1 and 408 mg g−1 dry needed for TAG formation is catalyzed by the G3 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. In lipid finding was further strengthening by studies on the
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; Jako et al. 2001; Taylor et al. 2002; Lardiza- synthesis of unsaturated fatty acids protect photosyn-
bal et al. 2008) reported significant increase in plant 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.
Genetic manipulation in halophytes for the biofuel 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; Zhang et al. 2005), total absolute unsaturated FAs content was (20–42%)
which infers that the drought and salt 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; Mikami and 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
sorts of halophytes were noticed which increment their 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 fluidity, 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 fluid- the total FAs comprised 4–64%. In vegetative organs
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) to enhance 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 changes in fatty acid composition interestingly 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) focused on mulation in these plants (Zhai et al. 2017). Another
sulfolipids role and salt resistance mechanisms of future option would be to dissolve lignocellulose mate-
halophytes including Sesuvium portulacastrum, Aster rial from halophytes in saline ionic liquids, which
tripolium L., members of Compositae and L., Aizoa are well established as alternative and ‘green’ sol-
ceae families, and glycophyte A. thaliana (L.) Heynh, vents to be used in the pre-treatment of the walls
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
quinovosyldiacyl glycerol. The presence of 16:0/18:3 recommended that biofuel production be increased up
and 18:3/18:3 molecules was confirmed through sul- to 10–20 EJ a year by 2050 (Searle and Malins 2015)
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). In a conclusion from the above studies 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. They exposed these halophytes to
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 CO2 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
(GL) and phospholipids (PL) reduced more in M. Disclosure statement
crystallinum as compared to S. portulacastrum at 200 No potential conflict of interest was reported by the authors.
μM cadmium concentration. Additionally there was
no noteworthy changes in the aggregate unsaturated References
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