Molybdenum potential vital role in plants metabolism for optimizing the growth and development

Molybdenum potential vital role in plants metabolism for optimizing the growth and development Muhammad Shoaib Rana1,2, Parashuram Bhantana1-3, Muhammad Imran4, Muhammad Hamzah Saleem5, Mohamed G Moussa1,2, Zaid Khan5, Imran Khan1, Mufi d Alam6, Muhammad Abbas7,8, Rana Binyamin9, Javaria Afzal1,2, Muhamad Syaifudin1,2, Intisar Ud Din1,2, Muhammad Younas1,2, Ilyas Ahmad10, Md Ashrafuzzaman Shah1,2 and Chengxiao Hu1,2* 1Key Laboratory of Arable Land Conservation (Middle and Lower Reaches of Yangtze River), Ministry of Agriculture, Micro-elements Research Center, College of Resource and Environment, Huazhong Agricultural University, Wuhan 430070, China


Introduction
Molybdenum (Mo) is very important and an essential micronutri ent for plants, animals and bacteria [1][2][3]. A lot of soils in the world suffer due to the defi ciency of microelements such as Mo [4,5]. Mo is defi cient in more than 44.7 million hectares of land and B is defi cient in 33.3 million hectares in China [6]. Consequently, the defi ciency of Mo and B of soil is an extensive agricultural problem that induces quality and yield losses in various crop spe cies worldwide [6,7]. Mo-defi cient plants show poor growth [8] and less contents of chlorophyll and ascorbic acid [9].
It is seen that itself Mo not so much biologically active but mostly occurs as a vital part of a complex organic pterin that is also being called molybdenum co-factor (Moco). Including plants, prokaryotes and animals, Moco being found to binds with molybdoenzyme in the most of the biological systems [10]. A lot of different phenotypes starts to develop when under the insuffi ciency of molybdenum plant are being grown.
Due to the reduction of molybdoenzyme activity maximum of these phenotypes are associated. Enzymes most of them include that are involving in prime N-assimilation like the nitrogenase (nitrogen-fi xing enzyme), Nitrate Reductase (NR) and those that are present in legumes nodules bacteroids. In plants together with xanthine dehydrogenase/oxidase some other additional molybdoenzyme also has been recognized that have very important role in the ureide biosynthesis and purine catabolism. It can be seen that in the legumes, during the biosynthesis of ABA the conversion of sulfi te to sulfate may be carried by the sulfi te oxidase and Aldehyde Oxidase (AO), that is very signifi cant in amino acid metabolism that contains sulfur [10]. Current review articles about the molybdenum in plants, prokaryotes and animals have shown the wide-ranging literature on formation and regulation of Moco and its activity with molybdenum-dependent apoenzymes [10][11][12]. In the lower order eukaryotes and prokaryotes, the system about the molybdate transport is characterized very well and designed at biochemical, genetics and physiological levels [13]. In the plant development aldehyde oxidase (AO; EC1.2.3.1) that is plant molybdoenzyme, has a very important role in relation to the development of plant and stresses in the environment [14][15][16]. Xanthine dehydrogenase and molybdenum-hydroxylases aldehyde oxidase in plants have distinctive reactive oxygen species signatures that are tempted by the abscisic acid and drought. Biosynthesis of phytohormones is catalyzed by the AO multigene family members in the preceding step, such as ABA and IAA by converting abscisic aldehyde and indoleacetoaldehyde to their respective phytohormones [12].
IAA being the vital member of auxins that are plant hormones has a major crucial role in a lot of activities of plants comprising abscission, root initiation, phototropism, fruit development, gravitropism and apical dominance [12]. The involvement of IAA to stress as in salinity and defi ciency of water in plants has also been suggested. In response to environmental stress ABA also plays a very crucial and important role in plants [17].
As molybdenum is vital constitute in the nutrition of plants, this review will inspect the transport of Mo within and into the plants and will also explore the crucial and comprehensive nutrition of Mo in plant growth and development.

Impact of Mo insuffi ciency on Growth
Molybdenum insuffi ciency resembles nitrogen defi ciency, as in the plant metabolism the most signifi cant role of Mo is the reduction of nitrate. Plants facing the Mo insuffi ciency, the leaves start to become pale, restricted in growth, fl ower development and formation may also be affected and eventually wither. The most typical visual defi ciency impact in dicotyledons is the severe abnormality in size. These are caused by the inadequate discrepancy of the vascular bundles at initial development stages of leaf and the necrosis in tissue [18].
There is a direct relationship between the molybdenum bioavailability in the soil and the molybdenum contents in soil. The molybdenum availability will be low if a soil having the lower soil pH [18] and the plant that is facing the Mo less availability shows the lesions and leaves different morphology was 1 st time explained by Arnon and Stout, [19] and then in a comprehensive way by Hewitt's group [20].
Mo insuffi ciency could also be due to a mutation in the Mo-specifi c uptake system [21,22]. In the MOT1, the knockout mutants in mitochondrial transport revealed that there is very minute change in the growth pattern [23]. As is being seen that though, in plant cells there are numerous Mo transporters,

Abstract
Molybdenum importance for appropriate plant functioning and growth is inconsistent by the most of the plants in respect to the total quantity that is obligatory for them. Molybdenum is a micronutrient that is directly involved in the metabolic functions of nitrogen in the plant. The transition metal molybdenum, in molybdate form, is essential for plants as a number of enzymes use it to catalyze most important reactions in the nitrogen acclimatization, the synthesis of the phytohormone, degradation of the purine and the detoxifi cation of the sulfi te. There are more than known 50 different enzymes that need Mo, whether direct or indirect impacts on plant growth and development, primarily phytohormones and the N-metabolism involving processes. On the other hand, in the synthesis of ABA uniquely Moco is involved, there on the level of ABA Moco effect is highly vital and ultimately by the response in the stress and the stomatal control, it has a very important role in the rate of transpiration and water relations. The practices that are involved in the fertilization of Mo optimization in crops, has a very important scope in discovering and improving these practices where the legumes are fi xing the N or NO 3 is primarily source of available N. The defi ciency of Mo and to enhance the molybdoenzymes activity, it may be very effective and vital important to use the spray of Mo as foliar application through the soil. The most recent understanding that from the soil how the plant gets access Mo or how they redistribute it is not still clear. However in the system f prokaryotes, it has been found that in plants it has likewise physiological Mo transport phenotypes. So, the mechanism of transport of Mo in the prokaryotes is needed as well as the reconsideration of anion transport mechanism that is in plants, will provide a help to solve that how this is accumulated. In this review, the discussion covers about the vital importance of Mo to enhance the productivity for optimizing the yield concentrating on metabolism, uptake, transport, storage, Mo cofactors, application, focusing on some other recent constrains in the recent situation of agriculture, where the yield and development in agriculture may be aided by increasing the Mo nutrition.

Molybdenum in soils
Mo generally exists in highly soluble form, and is rare in the soils building it liable to leaching. Though, usually consider that in the acidic soils the molybdenum is attached to mineral surface, it may avoid the leaching, but it may also and colloids molybdate is adsorbed in related way to these two anions. This adsorption is very closely dependent on the soil pH [29]. It increases as the pH falls but at the neutrality it is very low. On acid soil availability of Mo for the plants is the poorest and can be upgraded by foliar application, seed priming, seed coating pelleting and with liming, in case soil is not characteristically lacking in molybdenum [18].

Molybdenum adsorption in soils
The pH dependency of Mo adsorption on the soil resembled the one found for clay and oxides minerals. pH is a very dominant factor in the availability of nutrients [30][31][32]. It controls many processes occurring in the soil system [33][34][35]. Absorption demonstrated a peak in the range of pH 3-4, and then declined with the increasing pH above 4. With temperature, there is an little increase in the adsorption of Mo on surface of soil [36].
Carroll, et al. [37], to examine the transport of Mo in soil with and without biosolid amendment employed the miscible-  To study the mechanism of Mo adsorption with iron oxides, , are formed in conditions, anoxic (i.e., DO < 1 mg l −1 ) [46].
This conversion of goethite could be due to the reduction facilitated by the activities of microbial [47]. Impact in the acidic soil is due to the strong adsorption in relation between the pH and molybdenum that can not be ignored. Some other soil properties may also effect on the availability of Mo. A detail of factors that infl uence the availability, leaching and adsorption process are shown in Figure 2.

Oxidation and redox behavior of Mo species
Molybdenum resembles tungsten and vanadium, in its chemical properties, the Group 5 th fi rst number, rather than Cr.
Molybdenum, chemically is tremendously versatile, forming compounds in array of the freely interconvertible states of oxidation. Molybdenum shows all the oxidation states from 2− to 6+ in its compounds, among which the lowest oxidation states, ranges from 2 − -1 + , found in the complexes with the ligands acceptor, primarily cyclopentadiene, C-monoxide and related compounds, P, nitric oxide and Ar-donor ligands.
Molybdenum the short oxidation states (2− to 2+) are unlikely be to arise in enzymatic processes or encountered in biological systems. In its oxidation states the Mo in its oxidation 3+ to   Generally, the transmission of an oxygen atom to is catalyzed by all the Mo-enzyme or to from a substrate (Hille, 2002). Each reaction, by transfer of two electrons either oxidation or reduction, is also characterized by this, which

Mo crucial role in biological nitrogen fi xation
Specifi cally for plants, Mo is a micronutrient that with nitrogen-fi xing bacteria form root nodules, however trace amounts of Mo are also used in a protein involved with nitrogen metabolism and uptake plants that do not form nodules [67]. Its signifi cance to the N 2 fi xation is vibrant, given that Mo in 'FeMoCo' cofactor is at heart of the nitrogen reduction process -at least for the most of the nitrogenases.
Two atoms of molybdenum contained by the Mo-Fe protein and has two distinct types of oxidation-reduction centers: four Fe-S centers and two iron-molybdenum cofactors called

Molybdenum uptake, storage and transport into the cells
By the sulfate transporters or related systems, it is being proposed that molybdate distribution and import are facilitated [75]. In contrast to the homeostasis of bacterial molybdate, the transport of Mo in eukaryotes is less understood. Protein MOT1that belongs to the family that is large sulfate carrier and that was revealed to transport molybdate by the ultrahigh affi nity across the cellular membranes [23,76,77]. In the plasma membrane surprisingly, it was not found to reside.
Confl icting reports localized it to the mitochondrial envelope or to endomembrane system [23,77]. As in the cytosol, into the Moco-backbone the insertion of Mo occurs both suggested the subcellular locations are questionable. Another molybdate transporter of sulfate transporter family, in addition to MOT1, it is being described the vacuole provide functional evidence for MOT2 that is confi ned to the tonoplast and as an important molybdate store [21,22], and low content of Mo in the leaves while in seed by the accumulation of Mo contents, the plants that are defi cient in MOT2 are characterized. Still for Mo cellular importer is missing, but it is being expected that this task is carried not only in animals but also in autotrophs by the additional transporters. It can be assumed, in addition to a high-affi nity system, non-specifi cally molybdate can also move in the cell by sulfate uptake system that has been revealed for a sulfate transporter [78][79][80].
In the wildtype and MOT2 mutant leaves, however, it is found total molybdenum contents with the levels of Moco were to correlate, which indicates molybdate at cellular levels, Moco synthesis is adjusted by the plant.

Seed coating, treatment and pelleting with Molybdenum:
Numerous studies have shown the effi cacy of the Mo seed coating [81,82]. Seeds were treated by the Mo (80 g/ha) causing in improved comparative grain yield, chlorophyll index, seed weight and pod number. It shows the better results when soybean seeds with ferrous sulfate 500 mg/kg and ammonium molybdate 250 mg/kg were pelleted were highly effective for the improvement of dry matter production, yield, plant height, growth rate and area index of leaves [81,82]. Similarly in fi eld experiments, to increase yield of soybean and cowpea on acidic soils, benefi ts from the Mo applied together with the rock phosphate or alone, were greater or comparable than liming evaluating the effectiveness of a number of pelleting materials [83]. Though, from Mo seed-coating, several reports indicating no toxicity or improvement. Burton and Curley [84] reported that bacterial survival, N fi xation and nodulation were strappingly suppressed when seed with sodium molybdate was pelleted. By inoculant and Mo nearly inoculated bacteria 99% died just after seed treatment in four days. As groundnuts kernel yield is increased due to seed dressing nearly more than 300 kg ha -1 in Senegal by applying 28 g ammonium molybdate/ ha ( [85]. In Sierra Leone on groundnuts grown on an upland soil seed pelleting with 0.2, 0.4 and 0.8 g inoculation with rhizobia plus sodium molybdate/100 g seed was tested. Where sodium molybdate was applied at 0.2 g/100 g was applied to seeds, by this it is seen an increased protein content by 4.21%, DM yield by 17.2% , 14.0% grain yield and N uptake 38.5% [86]. Rhodes and Nangju [83]  Some other researchers also observed on bradyrhizobium, salts suppressive effects used as molybdenum sources [88,89].
But there is also reports present that indicates in improving crop performance Mo seed coating is effective, from the bacterial strains used for inoculation, it may have toxic effects.
So, before using Mo seed coating, it must be evaluated the seed coating effi cacy of Mo with bacterial strains.

Seed priming with molybdate
Numerous studies pointed out that for Mo application, seed treatment is a more effective method than soil application. For instance, in eastern India 48 trials conducted, mean yield was increased by 17%-22% by application of Mo as compared to the control where Mo was not applied and when it is applied to soil the increase was 20%-25% ( [90,91]. Similarly, over the no application control, Mo through the seed treatment (4 g kg-1 seed) application was more economical and effective for increasing the yield by 15.79%; 10.53% with1.5 kg/ha the soil application [92]. 0.1 or 1% sodium molybdate solution, priming of Trifolium subterraneum L. (Subterranean clover) seeds in improving yield and growth was as alike effective as through the soil application, in soil that is defi cient in Mo. Donald and Spencer [90] reported that in grains high N and Mo content resulted in the seed priming than soil application as the application levels increases for the maximum yield. Mohandas [93] reported that improved nitrogen fi xation, dry matter accumulation, yield and nodulation was seen when common bean seeds primed in sodium molybdate. It has been reported that a yield increase of compared with Mo soil application 27% by seed priming in a pot study on chickpea, with Mo for 8 h at 0.5 g/L solution of sodium molybdite, while in the fi eld experiment, increase in the yield of chickpea from the same treatment was 20% [94,95]. In Bangladesh, over untreated control yield an increase was 37%-90% and was up to 50% more than the water-soaked control in trials at farmers' fi elds at different locations [96]. By adding rhizobium in the priming solution, the effi cacy with Mo seed priming could be enhanced. Similarly, in Vigna radiata L. (Green gram), priming with the rhizobia and sodium molybdate ominously enhance the nutrient uptake, nodulation, crop yield, nitrogen fi xation and growth of the plant. In fulfi lling the Mo requirements of various crops, the Mo application by the priming of seed is highly economical and more effective as compared to the soil application, however with rhizobia its amalgamation needs to be the more investigated and modifi ed. Pattanayak, et al. [97], indicated that fertilizer application effi ciency is also increased by combining the seed treatments that indicate the better use of the resources. Even though in the priming media incorporation of rhizobial strains was synergistic, the protocol should be modifi ed for micronutrient requirements and individual crops Table 4.

Foliar application
Katyal and Randhawa [99] indicated that a spray solution may be comprised of 0.1%-0.3% of soluble Mo. With the increasing soil pH, the Mo availability increases, and acid soils that have a pH <5.2, Mo available amount to plants is very low, i.e., 0.10 mg/kg-0.25 mg/kg [18]. Since in the phloem and xylem Mo is highly mobile, and this Mo by seed treatment can be provided or may be by the foliar application as the crops require it in low amounts. Foliar sprays of Mo are more effective often than the applications to soils, principally for the acidic soils, and if it is applied at early stages of plant development it may be of supreme effectiveness [100]. Foliar spray effectiveness depends on nutrient its translocation into the plant and uptake rate by the leaves [101]. Mo applied by leaf spray, the leaves rapidly absorb it. Campo and Hungria [102] found that to the soybean nodules translocation of the calengo, et al. [105] reported that in common bean defi ciency of Mo results in low effi ciency of N assimilation of plants. Lombin, et al. (1985) [106] considered the effect of molybdenum i.e,30 g ammonium molybdate/ha, in 1971, 1972 wet and dry year respectively, sprayed on groundnut three weeks after sowing at the Samaru, northern Nigeria Table 5.
It has been found that Mo in the dry year is more likely to increase kernel yields of the groundnut short-season varieties.
The groundnuts kernel yield by 200 kg ha -1 increased by the foliar application of Mo [107]. After 10 days emergence100

Soil application
There are many crops, that need Mo fertilizers [111]. High nitrogen application and under the low pH conditions with the Mo, oilseed rape should be fertilized. The Mo uptake by oilseed rape can also be decreased by the sulfur application [112]. On very acidic soils in Australia, some research conceded out that indicated that when fertilization of Mo applied it was possible to attain higher yields of wheat.In the seed material the actual Mo concentration shows the increment in yield. Better the yield; lower the Mo content in seeds, stimulating Mo fertilization effects [111]. Mo rates between 35 and 140 g/ha had a noteworthy effect. Towards seed molybdenum increasing concentration in common bean has been examined by applying the Mo rates at high level, between 90 and 720 g/ha, applied to leaves [115].

Conclusion
Our considerate of the function and the biological role of the molybdenum is progressing rapidly. Moco as it occurs in CNX mutants the complete loss of it is lethal and when they are grown in the soil leads to the death of plants. However in the cell culture, when grown on the media these mutants could be retained alive with the reduced N as N-source. As well as Moco biosynthesis proteins the crystallization of further molybdenum enzymes is under way. Though Moco on ABA levels have an important effect in the plant cells, Moco is also uniquely takes part in ABA synthesis and as a result a role in transpiration rates and water relations through in the stressrelated responses and stomatal control. In crops the practices which optimize the fertilization of Mo have signifi cant scope in exploring where the predominant available N source is No 3 -

Future prospects
For NR there is a lot of physiological data, but not for SO, AO and XDH and there are, yet, a number of open questions.  The coming years perhaps into these will bring deep insight into innovative molybdenum aspects within the physiological and metabolic network of cells. In the fi eld of molybdenum enzymes future research is likely to focus on detailed mechanistic of the functions of cofactors, the cofactor biosynthesis and cofactor allocation in specifi c enzymes.