Application of Micronutrients in Rice-Wheat Cropping System of South Asia

2019-11-12 13:20FaisalNadeemMuhammadFarooq
Rice Science 2019年6期

Faisal Nadeem, Muhammad Farooq,

Review

Application of Micronutrients in Rice-Wheat Cropping System of South Asia

Faisal Nadeem1, Muhammad Farooq1,2

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Rice-wheat cropping system (RWCS) is one of the most important cropping systems in South Asia. However, sustainability of this system is under threat owing to several factors, of which deficiency of micronutrients particularly zinc (Zn), boron (B) and manganese (Mn) is one of the major problems. Continuous rotation of rice and wheat, imbalanced fertilizer use and little/no use of micronutrient-enriched fertilizers induce deficiencies of Zn, B and Mn in the RWCS of South Asia. Here we review that (i) imbalanced fertilizer use and organic matter depletion deteriorate soil structure resulting in low efficiency of applied macro- and micro-nutrients in RWCS. (ii) The micronutrients (Zn, B and Mn) are essentially involved in metabolism of rice and wheat plants, including chlorophyll synthesis, photosynthesis, enzyme activation and membrane integrity. (iii)Availability and uptake of Zn, B and Mn from rhizosphere depend on the physico-chemical soil properties (which differ under aerobic and anaerobic conditions) including soil pH, soil organic matter, soil moisture and interaction of these micronutrients with other nutrients. (iv) Plant ability to uptake and utilize the nutrients is affectedby several plant factors such as root architecture, root hairs, transport kinetics parameter and root exudates. (v) Crop management and application of these microelements can help correct the micronutrients deficiency and enhance their grain concentration.

micronutrient deficiency; rice-wheat cropping system; agronomic approach

Rice-wheat cropping system (RWCS) is one of the most important crop production systems in South Asia, which occupies 12.3, 2.2, 0.8 and 0.5 million-hectare area in India, Pakistan, Bangladesh and Nepal, respectively. However, the sustainability and productivity of this cropping system is under threat due to deteriorating soil health and micronutrient deficiency,and resulting in less grain yield and poor quality (Kumar et al, 2016).

Adoption of inadequate agricultural practices together with intensive cultivation leads to deficiency of micronutrients in fertile regions of Indo-Gangetic Plains (IGP), India(Nayyar, 2003). Injudicious fertilizer management nitrogen (N), phosphorus (P), potassium (K), less use of organic fertilizers and manures, poor on-farm residue management and intensive cropping create negative nutrients balance and deficiency of micronutrients. Among these, deficiency of zinc (Zn) is predominant after P and N, particularly in the high pH soil irrigated with poor quality water, whereas iron (Fe), boron (B), manganese (Mn) and molybdenum (Mo) deficiencies have also been reported in RWCS (Nayyar, 2003). Zn deficiency has been noticed as the major limiting factor. Many of the soils in rice and wheat growing regions are prone to Zn, B, Mn, Fe, Mo and copper (Cu) deficiencies (Rashid, 2005). Zn, B and Mn deficiencies are thus becoming an increasing problem in RWCS of the IGP, India (Nayyar, 2003).

Micronutrients are as important as macronutrients and involved in vital metabolic events in the plants. Deficiency of even a single essential micronutrientmay disturb the plant developmental cascades and cause substantial reduction in crop yield (Tripathi et al, 2015). The intensity of micronutrient deficiency is determined by several factors, including soil characteristics and the crop types. Thus, deficiency of micronutrients in RWCS of IGP is worse due to the size of its available pools in the soil rather than its total contents which is further affected by poor agricultural practices (Nayyar et al, 2001). Several other factors including soil texture, clay contents, microbial activity, soil organic matter, nutrients interaction in soil and redox potential also affect the micronutrients availability to the crop plants (Kumar et al, 2016).

Growth and yield improvement in cereals with Zn, B and Mn applications have been reported (Rehman et al, 2016; Ullah et al, 2018). However, there is no comprehensive review on Zn, B and Mn applications in RWCS of South Asia, the dynamics and transformations in soils, and options to overcome Zn, B and Mn deficiencies in RWCS. In this review, we discussed:(1) Micronutrient deficiency issues experienced by the RWCS of South Asia with emphasis on Zn, B and Mn;(2) Roles of Zn, B and Mn in plant biology, factors affecting their availability in RWCS and their soil dynamics; (3)Agronomic approaches to manage micronutrient deficiency, as well as their utilization in RWCS and grain biofortification.

Zinc, boron andmanganese deficiencies and their symptoms in RWCS

RWCS has fundamental importance for the increasing food security and livelihood of people around the globe, particularly in South Asian. However, various factors threaten its sustainability, of which Zn, B and Mn deficiencies are of high concern. Moreover, adoption of RWCS on coarse textured soils of IGP also causes deficiencies of Fe and Cu that limit productivities of rice and wheat (Nayyar et al, 2001). However, Cu deficiency is not widespread (less than 3%) in IGP based on soil analysis (Nayyar et al, 2001). Hence, critical limits used for soil Cu need to be re-caliberated. Whereas, Fe deficiency in IGP may due to inherent low Fe content of soil and inadequate degree of reduction of Fe oxides under flooding conditions. Fe deficiency is considered as the second most important micronutrient deficiency after Zn in IGP, India (Nayyar et al, 2001).

Zinc

In northern India, deficiency of Zn was first reported in rice crop grown on calcareous soil(Yoshida and Tanaka, 1969), and now become the most widespread micronutrient disorder (Quijano-Guerta et al, 2002). About 50% area under cereal cultivation isZn deficient. Lowland rice (puddled-transplanted) are the most affected by Zn deficiency because of low soil redox potential (Rose et al, 2013). Most of rice in RWCS is sown under flooded conditions with Zn insufficiency due to high pH (reduced conditions), bicarbonate and soil P contents. In rice, Zn deficiency symptoms appear in 2–3 weeks after transplantation. These symptoms include streaks and brown blotches on developed leaves which fuse and cover older leaves. Under severe deficiency, plant grows stuntedly and may die.

However, high soil pH and chemisorption cause Zn deficiency in wheat crop as well (Alloway, 2009). In wheat, first symptom of Zn deficiency appears on the middle-aged leaves (Ozkutlu et al, 2006). Under severe deficiency, whitish brown patches and necrotic lesions are observed on the leaf blades leading to collapse in middle-aged leaves (Cakmak and Braun, 2001).

Boron

Boron deficiency often occurs in soil with low organic matter and coarse texture that is more prone to leaching (Nayyar et al, 2001). B deficiency is considered as an important yield-limiting factor in calcareous soil of IGP, which severely affects the growth of flooded rice (Rashid et al, 2004). Under flooded conditions, B deficiency mainly expresses in response to high leaching losses, high B adsorptive capacity of soil particles and low soil organic matter content (Saleem et al, 2011). In rice, B deficiency causes delay in flowering, induces flower bud abortion and causes panicle sterility (Rehman et al, 2018b).

B deficiency substantially induces the grain yield of wheat by 8.5%–16.0% due to sterility (Rerkasem and Jamjod, 2004; Iqbal et al, 2017). In young wheat seedling, B deficiency causes longitudinal splitting of emerging leaves near to the midrib position, and induces the development of saw-tooth effect on the margins of younger leaves that depicts irregular cellular development (Rehman et al, 2018b). Furthermore, B deficiency may restrict root growthand cause degeneration of terminal spikelets, resulting in the ‘rat-tail’ like symptoms (Marschner, 1995).

Manganese

Continuous practice of rice-wheat sequence in IGP leads to deficiency of Mn in soil. Mndeficiency appears to be the most prominent in wheat grown in rice-wheat rotation (Lu et al, 2004). In IGP, traditionally, rice is cultivated with flooding, which causes downward movement of Mn in soil layer and results in decreased Mn concentration (Lu et al, 1990). Loss of Mn through leaching during rice cultivation is the primary reason for inducing Mn deficiency in following wheat crop (Takkar et al, 1986). In rice, Mn deficiency results in chlorotic interveinal areas on the developing leaves that may expand into streaks under its severe deficiency (Tanaka and Navasero, 1966). In wheat, Mn deficiency induces patchy areas with yellowing of upper leaves, whitish or colorless spots and slight stripping of particularly new leaves. Under severe deficiency, striping and light grey flacking appear at the base of newly emerged leaves and expand onto entire leaves.

Roles of zinc, boron, manganese in plant biology

Reproductive growth

Micronutrients including Zn, B and Mn are very important for better reproductive growth and development of crop plants. Plants require continuous supply of mineral elements to produce flower and viable seed. Microelement insufficiency affects flowering, floral development, anthesis, fertilization and grain formation (Pandey, 2010), and leads to delayed maturity resulting large reduction in yield and grain quality. Zn deficiency alters the function and structure of stigma and pollen grains, affects pollen viability, and disturbs the fertilization in plants (Nautiyal et al, 2011).

Boron insufficiency in plant damages flower and grain formation, resulting in yield losses. Plant sexual reproductionphase is highly sensitive to B deficiency than vegetative phase (Rehman et al, 2018b). B deficiency induces anther, stigma and ovary aberrations, and results in poor pollen tube development (Pandey, 2010). In wheat, critical stages of reproductive growth including anther, pollen and ovule development are more sensitive to B deficiency,which causes irreversible decrease in floret sterility (Jiang and Miles, 1993).Pollination, seed-setting rate, grain formation and panicle sterility are also affected by B element, because B is involved in carbohydrate metabolism in pollen tube walls that is central to pollen tube(Rehman et al, 2018b). Under B deficiency, pollen tube may burst because naturally B concentration is low in pollen grains compared with stigma and ovary (Rehman et al, 2018b).

Manganese requirement seems to be high for reproductive segments and functions than vegetative phase as its deficiency affects floral and flowering development in plants (Pandey, 2010). Mn deficiency impedes plant ability to produce pollen, and reduces pollen viability and pollen grain size, resulting in inferior pollen tube growth (Sharma, 1992). Moreover, under Mn deficiency, alterations of anther enzymes and reductions of their efficacies affect development of reproductive tissues (Pandey, 2010).

Photosynthesis

Micronutrients have crucial role in various plant metabolic processes and have direct role in photosynthesis. Zn is involved in carbohydrate metabolism through its vital role in photosynthesis and sugar transformation (Römheld and Marschner, 1991). Zn deficiency is correlated with disruption of normal enzymatic activities. Under Zn nutritional stress, efficiency of carbonic anhydrase (CA)that is principal enzyme in photosynthesis is decreased, resulting in reduced photosynthesis (Römheld and Marschner, 1991).

Boron deficiency does not directly obstruct photosynthesis process in plants. However, B insufficiency causes reduction in leaf constituents (e.g., chlorophyll) and photosynthetic area that inhibit photosynthesis (Wang et al, 2007). Moreover, B deficiency disrupts chloroplasts development and decreases their amount, leading to poor photosynthesis (Rehman et al, 2018b).

Manganeseis of importance for photosynthesis through its catalytic nature for light induced breakdown of water molecule in photosystem II (PSII)and RuBP carboxylase reaction (Marschner, 1986, 1995). It is integral component of oxygen evolving complex (OEC) associated with PSII as Mn ions bound with amino acid residue of proteins PSII reaction center (Pandey, 2010). Thus, under Mn deficiency, efficiency of OEC associated with PSII reduces causes decline in photosynthesis. Mn also acts as co-factor of enzyme Mn2+dependent superoxide dismutase and various enzymes of tricarboxylic cycle in shikimic acid pathway leading to biosynthesis of aromatic amino acids (Marschner, 1995).

Membrane function

Zinc plays a key role in upholding the membrane integrity in plants. It helps in maintaining the membrane structure and integrity and ion transport as observed in cell membrane of wheat (Broadley et al, 2007). Membrane leakages have been noticed in roots of plant experiencing Zn deficiency (Broadley et al, 2007). Zn plays an important role in protecting proteins, membrane lipids, DNA and various cell components due to its ability to bind with SH- containing compounds (Cakmak, 2000) and being constituent of Cu-Zn superoxide dismutase (Cakmak and Marschner, 1988).

Boron is an essential element which can affect the structural integrity of membrane and transport across the membrane, involving in activations of enzymes and other plasma membrane proteins (Brown et al, 2002). Moreover, insufficiency of B reduces Fe-reductase and proton pumping ATPase functioning (Obermeyer et al, 1996), alters the membrane potential, and hampers functioning of phospholipid bound oxidoreductase (Schon et al, 1990). Changing in B amount induces abrupt changes in cell membrane that indicates its essentiality for plant cell membrane (Obermeyer et al, 1996).

Protein synthesis

Zinc is one of the important microelements for various plant proteins because it helps to preserve their structural orientation and integrity (Broadley et al, 2007). Zn deficiency impairs the biosynthesis of proteins (Marschner, 2012). Furthermore, Zn nutrition affects the functioning of nitrate reductase (NR), and glutamine synthetase (GS) in wheat flag leaves (Crawford, 1995). Activities of enzymes such as NR and GR in flag leaves regulate the total protein contents and some protein components of flour (Zhao et al, 2013). Contents ofgrain protein and concentrations of gliadins, albumins, globulins and glutenins increase with Zn fertilization.

Numerous physiological segments including synthesis of proteins and nucleic acid metabolism are affected by B. B regulates the AtBor1-1 (transporter) that functions as post translational modification of plasmalemma associated proteins (Takano et al, 2005). Fluxes of energy distribution coupled with minimization of thylakoid arrangement were interfered with Mn deposition. Moreover,synthesis of proteins governed by Mn is also affected by Mn accumulation (Lindon and Teixeira, 2000).

Factors affecting micronutrients availability in RWCS

Availability, movement and uptake of micronutrients including Zn, B and Mn from soil to plant roots are affected by different soil physical and chemical properties (Fig. 1).

Soil pH

Soil pH is the most critical factor influencing the availability of nutrients to crop plants. As soil pH increases, the solubility and availability of Zn decrease, because Zn2+activity is proportional to square of proton (H+) activity in soil (Kiekens, 1995). Meanwhile, adsorptive ability of soil particles increases,because pH-dependent negative charges cause precipitation with Fe-oxides and formation of hydrolysed (Alloway, 2009). Zn deficiency is more common in high pH soils, and therefore, in rice, it is called as ‘alkali disease’. In RWCS, fields remain under submerged conditions during most of growing seasons of rice, and soil undergoes different changes such as increase in pH of acidic soils whereas decrease in alkaline soils (Xu et al, 2003),which reduces the Zn concentration in soil solution due to more solubility of phosphorus (P), precipitation of Zn(OH)2(Sajwan and Lindsay, 1986), conversion of soluble Zn to insoluble ZnS, and formation of ZnCO3in calcareous soils(Johnson-Beebout et al, 2009).

High pH of soil solution reduces the bioavailability of B, because there is a direct relationship between soluble B level and soil solution pH (Niaz et al, 2007). Rise in soil pH from 3 to 9 increases the adsorption of B with soil particles (Keren and Bingham, 1985), however, with further increase in pH from 10.0 to 11.5, B adsorption starts decreasing (Goldberg and Glaubig, 1986). According to Keren and Bingham (1985),there are two reasons. Firstly, B(OH)3is dominant when pH is below 7, and low affinity of this substance for clay particles decreases the adsorption of B by soil particles. Secondly, with increase in pH, amount of B(OH)4becomes predominant that has strong affinity for clay particles and increases the concentration of adsorbed B.

With decrease in soil pH, the availability of Mn in cationic form (e.g., Mn2+) in soil solution increases. Mn2+is released into soil solution at pH 5.5 due to solubilization of Mn oxides (Rengel, 2000). However, availability of Mn decreases with increase in pH value (Kumar et al, 2016), because higher pH promotes adsorption of Mn2+with soil particles and makes it unavailable for plants (Fageria et al, 2002). At pH 8, chemical auto oxidation of Mn2+takes place and other forms such as MnO2, Mn2O7, Mn3O4and Mn2O3that are unavailable to plant prevails were produced (Humphries et al, 2007).

Fig. 1. Uptake mechanism of zinc, boron and manganese from soil to plant.

Plant uptakes Zn as Zn2+, B as B(OH)3and Mn as Mn2+from soil solution. Uptake of these micronutrients is influenced by soil physio-chemical properties such as soil pH, organic matter, soil moisture, soil temperature and soil micro biota. Phytosiderophores secreted by plant roots, microbes and organic molecule increase the mobility of Zn and Mn to plant. Plant uptakes Zn via ZIP transporters, B movement occur through BOR transporter facilitated by NIP5;1 channels, and Mn via membrane transporters IRT1, NRAMP1 and YS1, YSL6 through symplastic (cell to cell) and apoplastic pathway (movement via extra-cellular spaces). (I) Using these transporters, Zn, B and Mn enter into epidermis and then cortex. (II) To enter the xylem, Zn, B, Mn must pass through casparian strip. ZIP transporter, NIP5;1 and YSL2 have role in the mobilization of these nutrients from cortex to endodermis and then pericycle. (III) Casparian strip present in endodermis obstruct the uptake of nutrients directly from root apoplast. (IV) Xylem loading of Zn, B and Mn takes place via HMA pumps, BOR1 and ZIP2, respectively. (V) ZIP, YSL and YS/YSL transporters have role in movement and translocation of Zn and B from xylem to phloem. (VI) B accumulation in leaf occurs through transpirational pull. Symplastic movement depict solute movement from cell to cell, whereas, apoplastic refers to movement through extracellular spaces.

Organic matter (OM)

Decrease in microelement availability due to OM is attributed to formation of complex with lignin, humic acid and insoluble compounds. Whereas availability increases are due to mineralization and solubilization, as well as action of low molecular weight ligands (e.g. amino acid), resulting in mobilization of micronutrients (Mortvedt, 2000).

Fractionation and solubility of Zn are strongly regulated by soil adsorption and desorption reactions governed by OM content in soil (Alloway, 2009). In flooded rice, high OM content and Mg:Ca ratio greatly affect Zn solubility and uptake (Neue and Lantin, 1994). Soil under submerged conditions has low available Zn concentration.Moreover, addition of OM accelerates this condition (Haldar and Mandal, 1979). High P, Mn and Fe concentrations and application of OM coupled with microbiological immobilization substantially reduce Zn availability. Zn and P solubility and availability decrease in alkaline soils with high OM content due to their adsorption with carbonate and Fe hydroxides (Kirk and Bajita, 1995).

Soil OM content can affect B uptake by plants. Some studies have indicated strong relationship between organic carbon content and B (Goldberg et al, 2000; Arora and Chahal, 2010). Further, positive correlation exists between B adsorption maxima and soil OM content, because OM has more ability to adsorb B than other soil particles or clay minerals (Yermiyahu et al, 1988). Application of composted OM in soil results in increase in B adsorption (Van et al, 2005). Humus is a good source that possess high B concentration, but chemical reactions occur between B and di-hydroxy organic substances, indicating that B is bound with ‘diols’ of OM or those compounds and is gradually released in the process of microbiological breakdown of OM in soil (Parks and White, 1952).

Addition of OM into soil has reducing potential that results in marked and rapid increase in exchangeable Mn (Andrade et al, 2002). Low OM content in soil is considered as an important reason of Mn deficiency (Kielbaso and Ottman, 1976). Contrarily, in field crops, high OM content may cause Mn deficiency in soil (Rengel, 2000) and restrict its availability and uptake due to formation of organic Mn-complexes (McBride, 1982), and vice versa has been observed with low OM content in soil (Shuman, 1979).

Soil moisture and temperature

Environmental factors including soil moisture content and temperature influence the availability and acquisition of micronutrients (Moraghan and Mascagni, 1991). Zn deficiency is common in rainfed areas having low available water (Cakmak et al, 1996). Crops grown in these areas experience severe Zn deficiency due to low moisture availability that restricts Zn movement in soil.Moreover, low moisture negatively affects root growth, ultimately resulting in poor Zn uptake (Marschner, 2012). At low soil temperature, Zn deficiency may be due to decrease in solubility of native soil Zn (Deb et al, 2009). Changes in soil Zn availability with variation in soil temperatureare attributed to low rate of mineralization (release of Zn by OM decomposition)(Moraghan and Mascagni, 1991). Moreover, low OM decomposition under low soil temperature limits root growth and decreases uptake of Zn by plants (Alloway, 2008). However, at high soil temperature, Zn uptake and concentration in soil increase (Kumar et al, 2016). Availability and translocation of Zn at low temperature reduce due to poor root growth and planmycorrhizal colonization (Moraghan and Mascagni, 1991).

Mineralization of OM is affected by soil moisture content,which eventually affects B availability (Gupta, 1979). Under low soil moisture and dry weather, B deficiency appears more serious, because water deficiency decreases B mobility in soil solution, increases the length of diffusion path and reduces the B liberation from organic complexes (Tisdale et al, 1985), leading to poor root B uptake. Increase in root zone temperature may increase soil B adsorption because high soil temperature causes soil dryness, and soil water content is directly associated with B availability/deficiency (Goldberg, 1997). Gupta (1979) stated that reduced B uptake is observed at low soil temperature. In addition, microbial activity decreases at low soil temperature that may increase the plant demand for B.

Soil moisture content and temperature influence Mn solubility and also cause its deficiency (Hebbern et al, 2005). Under aerobic conditions (having less moisture),Mn2+oxidation starts resulting in precipitation of oxides of Mn3+and Mn4+, which are not easily taken up by plants. For instance, in rice, submerged conditions reduce the O2diffusion in soil and decrease the substance containing Mn, ultimately resulting in Mn deficiency. Low soil temperature affects Mn solubility in soil solution, and indirectly affects root uptake of Mn (Moraghan and Mascagni, 1991). Temperature influence on Mn availability seems complex. For example, microbial activity in soil is also governed by soil temperature, resulting in mobilization and immobilization of Mn in soil (Marschner, 1988).

Soil salinity and interaction of micronutrients with other elements

Micronutrients availability and uptake are affected by their interaction with other nutrients. Interaction with other nutrient elements also depends on soil physio-chemical properties (Malvi, 2011). Positive interaction exists between N application and Zn (Lakshmanan et al, 2005). Furthermore, with high N application/concentration, increases in abundance of Zn transporters and Zn chelating nitrogenous compounds are observed (Kutman et al, 2010).In wheat, more N fertilization enhances uptake and translocation of Zn by 300% in roots and shoots (Erenoglu et al, 2011), resulting in higher Zn accumulation in grain (Kutman et al, 2011).Zhang et al (2012) found negative association between Zn and P. Molar ratio of P and Zn expands with more P fertilization that adversely affects Zn bioavailability. Negative interaction between P and Zn also depends on mycorrhizal infection (Ova et al, 2015).There is a positive relationship between K and Zn because Zn decreases the leakage of K and amides by maintaining the membrane integrity (Cakmak and Marschner, 1988).

Zn being a cation reacts with nearly all soil anions and other mineral elements (Lakshmanan et al, 2005). At the interface of root, the availability of Zn reduces due to strong interaction between salt cations and Zn (Tinker and Lauchli, 1984). The soils receiving irrigation water that has high sodium levels are prone to Zn leaching (Alloway, 2008) as the exchange sites are occupied by Na+in saline-sodic soils. If soils are contaminated with cadmium, the uptake of Zn also decreases due to the formation of highly soluble CdCl2(Khoshgoftar et al, 2004).

Various functions of B are associated with the presence of other elements including N, P, K and Ca in plants. The presence of N, P, Ca, K, Mg, Zn and Al may interrupt the plant to take up B. In the presence of Zn, increase in B accumulation occurs. Therefore, Zn application significantly reduces B toxicity by inhibiting its uptake. Negative interaction exists between B and N (Chapman and Vanselow, 1955). B interaction with P is not clear as compared to N because borate resembles with phosphate in its physiological and biochemical actions (Gupta, 1979). Similarly, with P, borates are essential constituents of esters and make polyhydroxyl compounds with organic complexes. Under B deficiency, symptoms of P deficiency become more severe(Bergmann, 1992). Indirect influence of K on B availability has been observed due to its effect on Ca absorption. Nevertheless, excessive application of B increases K and B concentration in rice (Kumar et al, 1981). B adsorption with soil particles is not parallel to some other soil anions such as NO3-, PO43-, SO42-and Cl-(Bingham and Page, 1971). The soil pH turns acidic due to the presence of phosphate group by the use of Ca(H2PO4),which decreasesB uptake due to fixation (Bingham and Garber, 1960). Availability of B reduces in acidic soil with addition of lime that causes formation of insoluble Ca-metaborate.

Mn has positive interaction with N. Uptake of Mn in rice increases with application of N fertilizers e.g., urea(Hao et al, 2007), because nitrate has ability to enhance the Mn availability (Yadava and Malik, 2016). Application of N fertilizers as nitrate (NO3-) increases rhizospheric pH, while ammonium ions (NH4+) results in higher uptake of Mn (Yadava and Malik, 2016). Mn uptake also increases by chloride and sulfate ions associated with K, whereas carbonate content causes decrease in Mn availability, and sulfate ion acts as reducing agent that increases Mn uptake (Cheng and Ouellette, 1970).

Micronutrients dynamics/transformation in soil in RWCS

Zn concentration in soil largely depends on different factors including parent material, atmospheric deposition, farmyard application, industrial waste, and synthetic fertilizers. It is also existing in different chemical forms with different rate of solubility (Marschner, 1995). In RWCS, Zn deficiency in flooded rice occurs due to several reasons such as high soil pH, bicarbonate concentration and soil P (Alloway, 2009),whereas high soil pH and chemisorption resulting in Zn deficiency in wheat. Flooding induces different physical, chemical and biochemical changes in soil such as pH fluctuation that decreases Zn concentration in soil solution (Xu et al, 2003). Declining Zn concentration is associated with increased P availability and Zn(OH)2precipitation due to high pH and transformation of Zn to insoluble franklinite (ZnFe2O4) and zinc sulfide (ZnS) in acidic soil whereas ZnCO3in alkaline soils (Sajwan and Lindsay, 1986). Low redox potential in flooded field decreases Zn availability to plants due to its conversion in ZnS, high OM and bicarbonate content, and high Mg and Ca ratio (Neue and Lantin, 1994).

In RWCS, most of lowland rice is cultivated on alkaline soils having low soil OM content and higher leaching losses (Rashid et al, 2007; Saleem et al, 2011). Standing water in paddy fields leads to B deficiency (Saleem et al, 2011). Undissociated boric acid and borate anions freely move in water and are quickly leached from upper soil layer. In flooded soils, B availability decreases due to its high mobility rate which causes its leaching. At high pH, B availability reduces due to its fixation with soil particles (Goldberg, 1997). Substantial increase up to 185.7% in exchangeable soil Mn content at 0–20 cm depth has been observed in continuous wheat cropping system as compared to fallow soil (Wang et al, 2016). Application of synthetic fertilizers may increase the exchangeable and carbonate bounded Mn in soil. Whereas carbonate bounded Mn acts as direct source of available Mn followed by OM bound and exchangeable Mn (Wang et al, 2016). Mn associated with OM and exchangeable Mn is more easily taken up by plants (Wei et al, 2008).

Agronomic approaches to managing micronutrient in RWCS

Soil application

Micronutrients application through soil is the most convenient and effective method and has multiple benefits. It is a quite effective method to correct the deficiencies of Zn (Rehman et al, 2018a), B (Rehman et al, 2015, 2018b) and Mn (Ullah et al, 2018). Moreover, soil applied Zn fertilizers causes significant increase in grain yield, improvement in crop growth along with increase in grain Zn concentration (Table 1)(Khan et al, 2003). Under water deficient conditions, plants have shown a high tendency to Zn concentration, therefore, under these conditions, Zn application through soil did not enhance its concentration in grain (Gomez-Coronado et al, 2016). Maqsood et al (2009) reported increase in grain Zn concentration (51.7%–69.9%) with soil Zn fertilization as 6 mg/kg.

Table 1. Effects of Zn nutrition on grain yield of rice and wheat crop.

Soil B application rates for various crops range from 0.25 to 3.00 kg/hm2depending on soil types, crop requirement and application methods (Gupta, 1979). There is a narrow range between B deficiency and toxicity. Cereals including rice are B sensitive and show toxicity symptoms when grown on calcareous soils containing high level of inherent B (Singh et al, 1990). Therefore, great care is warranted in applying a safe B dosage and uniform field broadcast of B fertilizer. In transplanted rice, 0.75 kg/hm2B applied via broadcasting in calcareous soils overcomes its deficiency. Moreover, it had a beneficial residual effect for three subsequent crops grown in the same field (Rashid et al, 2007).

Foliar application

Foliar application of nutrients seems helpful compared to soil amendments for efficient use of nutrients and curing the visual deficiency problems in a short time (Fageria et al, 2009). Soil deficiency problems are minimized by the micronutrient application through foliar spray as compared to soil application (Modaihsh, 1997). Foliage applied Zn and Mn enhances the grain yield of field crops including wheat, barley and rice (Ullah et al, 2018). Foliar fertilization with micronutrientsis proved to be an effective strategy to remove the deficiency when soil application is not beneficial (Cakmak, 2008). Under field conditions, application of Zn through foliar method improvesZn concentration in edible parts (Cakmak, 2008). B can also be applied as foliage particularly under water deficient conditions to overcome B deficiency (Mortvedt, 2000) as it can translocate easily into plants due to formation of organic substance (e.g., mannitol, sorbitol)(Brown and Shelp, 1997).

Organic fertilizers

Organic sources help in maintenance of Zn pool and its availability in RWCS compared with inorganic ZnSO4(Kumar and Yadav, 1995). Manures are good sources of plant nutrient and can change soil chemical, physical and biological properties, thus improvingthe availability of micronutrients. Integrated nutrient management (i.e. combination of organic and inorganic sources) significantly improves soil OM, soil physical conditions and hence micronutrient contents (Rehman et al, 2018a, b). Mobilization of Zn in calcareous soils is improved through N supply by manures and decreasing soil pH by the application of organic acids (Marschner, 1995). Application of organic manure adds OM in soil and may decrease the requirement of Zn fertilizers. Upon decomposition of crop residue, organic acid is releases that helps improving the availability of Zn (Dwivedi and Srivastva, 2014). Heterotrophic bacterial biomass is increased by the application of organic fertilizers, which encourages other mineral nutrients and secondary productivity to improve primary productivity (Qin et al, 1995). Application of manure affects the accumulation of B in soil by adding organic matter (Marschner, 1995). Addition of farmyard manure enhances the availability of applied and native B by reducing B fixation with soil particles and increasing desorption of applied B into soil (Marzadori et al, 1991).

Seed priming

Seed priming is pre-sowing hydration technique that allows seeds to perform their pre-germination activities without radical protrusion (Bradford, 1986). Primed seeds have more potential to give uniform stand establishment than dry seeds (Farooq et al, 2006). Seed priming improves the growth and productivity of crop as observed in an experiment conducted in South Asia (Harris et al, 2007). Nutri-primed seeds show better growth and improved yield of both rice and wheat (Rehman et al, 2012a). Seed Zn concentration is increased by nutrient (Zn) seed priming before sowing and results in better germination and uniform seedling (Harris et al, 2007). Harris et al (2018) reported that seed priming with 0.05% Zn solution increases the grain Zn concentration and yield by 29% and 19%, respectively.Seed priming with B content of 0.001% or 0.1% improves the stand establishment of rice crop.However, priming with B content of 0.5% hampers the germination (Rehman et al, 2012a). Seed priming with B solution improved the yield contributing parameters of wheat as compared to control (Table 2, Iqbal et al, 2012).By increasing priming solution concentration (up to 0.2% MnSO4), for 12 h, linear increase in grain yield and grain Mn content were noted (Khalid and Malik, 1982). In wheat, priming with MnSO4has also increased the yield and Mn concentration in grain (Marcar and Graham, 1986).

Seed coating

Seed coating refers to the application of finely ground powder of nutrients together with inert sticky material (e.g., arabic gum). Seed coating affects the soil or seed at soil-seed interface which may influence the availability of coated and soil applied nutrients (Farooq et al, 2012). However, several factors including coated micronutrient, nutrient:seed ratio, soil moisture, soil type,soil fertility and material used for coating alter the efficiency of micronutrients applied through seed coating (Halmer, 2008). Application of Zn through seed coating has great potential in crop advancement as it improves the yield of various field crops. Zinc seed coating in wheat crop enhanced the germination, seedling growth, Zn concentration in tissue than non-coated seeds (Rehman and Farooq, 2016).Seed coating of rice with B (1.0, 1.5, 2.0, 2.5 and 3.0 g/kg) results in better uniform germination and tillering (Rehman et al, 2012b) by improving water relation and assimilate partitioning, resulting in B enrichment in rice grain (Rehman and Farooq, 2013). Coating wheat seeds with Mn improved the grain and straw yield, grain Mn concentration and Mn uptake ratio (Table 3)(Ullah et al, 2018).

Table 2. Effects of B nutrition on the grain yield and grain B concentration of rice and wheat crop.

Tillage

Carbon sequestration, soil chemical properties and distribution of soil nutrients are much affected by soil tillage practices (West and Post, 2002; Houx et al, 2011). Soil tillage increases crop yield by improving soil physical conditions (aeration and porosity) and conservation of soil moisture for plants, and also increases uptake of nutrients in roots by releasing microbes from soil micro-flora pool (Wang and Dalal, 2006). Soil organic residues accumulate in conservation tillage system improves water holding capacity, increasesmoisture in soil and decreases soil temperature (Aziz et al, 2013; Motschenbacher et al, 2014). These features may be helpful to make easy and frequent availability of soil micronutrients which is not possible in soilswith regularly tilled. However, little information is available regarding the micronutrients supply under no tillage cultivation and surface liming. Bhaduri and Purakayastha (2011) inferred that conservation tillage system with organic nutrient sources can improve soil quality as it improves Zn availability in rice.

Residual effect of soil applied micronutrients

Micronutrient application in soil to improve the growth and yield of crop may have residual effect that reduces the requirement of fertilizers for the following crops (Table 4). In two-year field study, application of B fertilizers (2 kg/hm2) in B deficient soil (0.29 mg/kg) results in beneficial residual B that helps to improve yield of rice and wheat (Khan et al, 2011). B fertilization (1 kg/hm2) shows residual effect (Yang et al, 2000).For instance, rice (puddled transplanted) grown in calcareous soil only uptakes 1.7%–3.4% [plant basis] of applied B (Rashid et al, 2007). Kumar and Singh (2018) studied residual effect of micronutrients including Zn and B and reported a significant residual effect of Zn and B fertilizers on the yield of both rice and wheat. In field experiment, following rice-wheat rotation, different Zn fertilizers (ZnSO4∙7H2O, EDTA-chelated Zn and ZnO) were applied to investigate its residual effect on subsequent wheat crop, and EDTA-chelated Zn givesthe maximum residual effect with respect to grain Zn concentration, grain and straw yield (Table 4) due to its less soil retention and greater transport of Zn to plant roots (Maftoun and Karimian, 1989; Singh and Shivay, 2013). Amanullah and Inamullah (2016) applied Zn (0–15 kg/hm2) to rice crop under RWCS and found that grain yield of subsequent wheat crop is significantly improved by Zn residual effect. However, beneficial and magnitude of residual effect of micronutrients are governed by various soil properties, soil absorption or adsorption and leaching (Shorrocks, 1997).

Biofortification with micronutrients

Approximately 25 nutrients are needed by human to maintain proper health, and the major portion is taken up by plant sources. People of both developed and developing countries are suffering from mineral defieicncies. In addition, about one third of population around the globe are more affected due to consumption of food with less nutrients (Stein, 2010). Malnutrition is now considered as widespread problem globally. Various nutrient deficiencies have been observed in human diet, and among those, deficiency of micronutrients is of high concern (Stein, 2010). It is estimated that about two billions of population is facing threat of Zn deficieny worldwide (Khalid et al, 2014). Bifortification is an efficient and cost effective approach to produce nutreint enriched food and to bring million from malnourishment to micronutrients sufficieny (Bouis et al, 2011). Genetic and agronomic biofortification are two important tools to improve nutrient status in cereals (Cakmak, 2008). However, several factors including interaction between environment and genotype, poor genetic diversity among cultivars, yield and consumer resistance are major issue in success of genetic biofortification (Cakmak, 2008). In contrary, agronomic biofortication is considered as a rapid solution to increase micro- nutrient concentration in food crops (Rehman et al, 2018a).

Table 3. Effects of Mn nutrition on the grain yield and grain Mn concentration of rice and wheat crop.

Table 4. Influence of residual Zn and B on the grain yield of rice and wheat crop under rice-wheat cropping system.

Foliar application of Zn in rice improves grain Zn content compared with soil application that has disadvantage of soil fixation and high application rates (Fang et al, 2008). Zn-phytate interaction is a major factor determining bioavailability of Zn when applied through different methods. Therefore, soil applied Zn by using adequate quantity helps in improving the grain yield, whereas application of Zn as foliage at the booting stage increases Zn concentration (Hussain et al, 2012) and its bioavailability in wheat grain. In rice, agronomic biofortification is unpredictable because rice is generally grown under flooded condition and certain chemical changes in soil properties affect the uptake of Zn by crop (Impa and Johnson-Beebout, 2012). In wheat, embryo and aleurone layer contain more Zn concentration, however, bioavailability of Zn is much important than its higher concentration in grain (Cakmak et al, 2010). Furthermore, Zn application at the grain filling phase enhancesZn content in endosperm, and minimum phytate is present in seed fraction at the stage (Cakmak, 2012).

Conclusion and future research thrusts

Micronutrient deficiency such as Zn, B and Mn is a widespread problem affecting the performance and productivity of RWCS in South Asian region. Moreover, several other sustainability issues, nutrient imbalance and farmers’ reluctance to use micronutrient-enriched fertilizers accelerate this problem. The prodigious significance of Zn, B and Mn in plant metabolism is unavoidable, because plant relies primarily on these micronutrients,and these elements have profound effects on array of plant physiological and biochemical activities such as cell wall integrity, chlorophyll synthesis, protein synthesis and photo- synthesis. However, various soil physio-chemical and biological properties and plant factors affect the availability, uptake and utilization of Zn, B and Mn. Moreover, deficiency of micronutrients is considered as a major index of malnourishment in growing population of developing countries in South Asian. Deficiency of micronutrients can be corrected by agronomic management practices that also help to improve grain biofortication.

Micronutrients (Zn, B and Mn) dynamics and transformation vary under different production systems. Thus, in future research, nutrient dynamics and transformation in conservation tillage system may be explored for better understanding of their availability to crops. Crop residue is also a source of nutrients, therefore, Zn and B release patterns together with retention of previous crop residues on the uptake of these nutrients should be evaluated. Nutrient transformations, with and without residue retention, may be evaluated at different soil moisture regimes and wetting and drying cycles. To enhance micronutrient concentration in edible part of rice and wheat, integration of agronomic and genetic strategies to increase mineral transport to phloem fed tissues should be studied. Geological survey should also be conducted to identify Zn, B and Mn deficient pocket existing in RWCS of IGP.

Ahmad R, Irshad M. 2011. Effect of boron application time on yield of wheat, rice and cotton crop in Pakistan.,30:50–57.

Ali S, Shah A, Arif M, Miraj G, Ali I, Sajjad M, Farhatollah, Yasir Khan M, Moula Khan M. 2009. Enhancement of wheat grain yield components through foliar application of zinc and boron.,25:15–19.

Alloway BJ. 2009. Soil factors associated with zinc deficiency in crops and humans.,31(5):537–548.

Amanullah, Inamullah. 2016. Residual phosphorus and zinc influence wheat productivity under rice-wheat cropping system.,5:255.

Andrade E, Miyazawa M, Pavan MA, de Oliveira EL. 2002. Effect of organic matter on manganese solubility.,45(1):17–20.

Arora S, Chahal DS. 2010. Effect of soil properties on boron adsorption and release in arid and semi-arid benchmark soils.,41:2532–2544.

Aziz I, Mahmood T, Islam KR. 2013. Effect of long term no-till and conventional tillage practices on soil quality.,131:28–35.

Bhaduri D, Purakayastha TJ. 2011. Soil available Zn: A potent soil quality indicator in a rice-wheat system. 3rd International Zinc Symposium. October 10–14, 2011. Hyderabad, India: 10–14.

Bingham FT, Garber MJ. 1960. Solubility and availability of micronutrients in relation to phosphorus fertilization.,24:209–213.

Bingham FT, Page AL. 1971. Specific character of B adsorption by an amorphous.,35(6):892–893.

Biswas A, Mukhopadhyay D, Biswas A. 2015. Effect of soil zinc and boron on the yield and uptake of wheat in an acid soil of West Bengal, India.,6(4):203–217.

Bouis HE, Hotz C, McClafferty B, Meenakshi JV, Pfeiffer WH. 2011. Biofortification: A new tool to reduce micronutrient malnutrition.,32:S31–S40.

Bradford KJ. 1986. Manipulation of seed water relations via osmotic priming to improve germination under stress conditions.,21:1105–1112.

Broadley MR, White P J, Hammond J P, Zelko I, Lux A. 2007. Zinc in plants.,173(4):677–702.

Brown PH, Shelp BJ. 1997. Boron mobility in plants.,193:85–101.

Brown PH, Bellaloui N, Wimmer MA, Bassil ES, Ruiz J, Hu H, Pfeffer H, Dannel F, Römheld V. 2002. Boron in plant biology.,4:211–229.

Cakmak I, Marschner H. 1988. Increase in membrane permeability and exudation in roots of Zn deficient plants.,132(3):356–361.

Cakmak I, Yilmaz A, Kalayci M, Ekiz H, Torun B, Erenoglu B, Braun HJ. 1996. Zinc deficiency as a critical problem in wheat production in Central Anatolia.,180(2):165–172.

Cakmak I. 2000. Possible roles of zinc in protecting plant cells from damage by reactive oxygen species.,146(2):185–205.

Cakmak I, Braun HJ. 2001. Genotypic variation for zinc efficiency.: Reynolds MP, Ortiz-Monasterio I, McNab A. Application of Physiology in Wheat Breeding. Mexico: CIMMYT: 183–199.

Cakmak I. 2008. Enrichment of cereal grains with zinc: Agronomic or genetic biofortification?,302:1–17.

Cakmak I, Kalayci M, Kaya Y, Torun AA, Aydin N, Wang Y, Arisoy Z, Erdem H, Yazici A, Gokmen O, Ozturk L, Horst WJ. 2010. Biofortification and localization of zinc in wheat grain.,58:9092–9102.

Cakmak I. 2012. Harvest plus zinc fertilizer project: Harvest zinc.,96:17–19.

Chapman HD, Vaselow AP. 1955. Boron deficiency and excess, 40:31–34.

Cheng BT, Ouellette GJ. 1970. Effect of various nitrogen fertilizers on manganese and iron availability as measured by incubation and sand culture studies.,50(2):163–170.

Crawford NM. 1995. Nitrate: Nutrient and signal for plant growth.,7(7):859–868.

Deb DL, Sakal R, Datta SP. 2009. Fundamentals of Soil Science: Indian Society of Soil Science. New Delhi: Cambridge Printing Works: 728.

Debnath C, Kader MA, Islam N. 2012. Effect of nitrogen and boron on the performance of wheat.,7:105–110.

Dwivedi R, Srivastva PC. 2014. Effect of zinc sulphate application and the cyclic incorporation of cereal straw on yields, the tissue concentration and uptake of Zn by crops and availability of Zn in soil under rice-wheat rotation.,3:53.

Erenoglu EB, Kutman UB, Ceylan Y, Yildiz B, Cakmak I. 2011. Improved nitrogen nutrition enhances root uptake, root-to-shoot translocation and remobilization of zinc (65Zn) in wheat.,189(2):438–448.

Fageria NK, Baligar VC, Clark RB. 2002. Micronutrients in crop production.,77:185–268.

Fageria NK, Filho MPB, Moreira A, Gulmaraes CM. 2009. Foliar fertilization of crop plants.,32:1044–1064.

Fakir OA, Rahman MA, Jahiruddin M. 2016. Effects of foliar application of boron (B) on the grain set and yield of wheat (L.).,12(2):1–8.

Fang Y, Wang L, Xin Z H, Zhao L Y, An X X, Hu Q H. 2008. Effect of foliar application of zinc, selenium, and iron fertilizers on nutrients concentration and yield of rice grain in China.,56(6):2079–2084.

Farooq M, Basra SMA, Wahid A. 2006. Priming of field-sown rice seed enhances germination, seedling establishment, allometry and yield.,49:285–294.

Farooq M, Wahid A, Siddique KHM. 2012. Micronutrients application through seed treatments.,12(1):125–142.

Farooq M, Ullah A, Rehman A, Nawaz A, Nadeem A, Wakeel A, Nadeem F, Siddique KHM. 2018. Application of zinc improves the productivity and biofortification of fine grain aromatic rice grown in dry seeded and puddled transplanted production systems.,216:53–62.

Goldberg S, Glaubig RA. 1986. Boron adsorption on California soils.,50(5):1173–1176.

Goldberg S. 1997. Reactions of boron with soils.,193:35–48.

Goldberg S, Lesch SM, Suarez DL. 2000. Predicting boron adsorption by soils using chemical parameters in the constant capacitance model.,64:1356–1363.

Gomez-Coronado F, Poblaciones M J, Almeida A S, Cakmak I. 2016. Zinc (Zn) concentration of bread wheat grown under Mediterranean conditions as affected by genotype and soil/foliar Zn application., 401: 331–346.

Gupta UC. 1979. Boron nutrition of crops.,31:273–307.

Haldar M, Mandal LN. 1979. Influence of soil moisture regimes and organic matter application on the extractable Zn and Cu content in rice soils.,53:203–213.

Halmer P. 2008. Seed technology and seed enhancement.,771:17–26.

Hao HL, Wei YZ, Yang XE, Feng Y, Wu CY. 2007. Effects of different nitrogen fertilizer levels on Fe, Mn, Cu and Zn concentrations in shoot and grain quality in rice ().,14(4):289–294.

Harris D, Rashid A, Miraj G, Arif M, Shah H. 2007. ‘On-farm’ seed priming with zinc sulphate solution-A cost-effective way to increase the maize yields of resource-poor farmers.,102:119–127.

Harris D, Rashid A, Miraj G, Arif M, Yunas M. 2008. ‘On-farm’ seed priming with zinc in chickpea and wheat in Pakistan.,306:3–10.

Hebbern CA, Pedas P, Schjoerring JK, Knudsen L, Husted S. 2005. Genotypic differences in manganese efficiency: A field trial with winter barley (L.).,272:233–244.

Houx JH, Wiebold WJ, Fritschi FB. 2011. Long-term tillage and crop rotation determines the mineral nutrient distributions of some elements in a Vertic Epiaqualf.,112:27–35.

Humphries J, Stangoulis J, Graham R. 2007. Manganese.: Barker A, Pilbeam D. Handbook of Plant Nutrition. USA: Taylor and Francis: 351–366.

Hussain M, Khan MA, Khan MB, Farooq M, Farooq S. 2012. Boron application improves growth, yield and net economic return of rice.,19:259–262.

Impa SM, Johnson-Beebout SE. 2012. Mitigating zinc deficiency and achieving high grain Zn in rice through integration of soil chemistry and plant physiology research.,361:3–41.

Iqbal S, Farooq M, Nawaz A, Rehman AU, Rehman A. 2012. Optimizing boron seed priming treatments for improving the germination and early seedling growth of wheat.,8:57–61.

Iqbal S, Farooq M, Cheema SA, Afzal I. 2017. Boron seed priming improves the seedling emergence, growth, grain yield and grain biofortification of bread wheat.,19:177–182.

Jiang Y, Miles PW. 1993. Generation of H2O2during enzymic oxidation of catechin.,33:29–34.

Johnson SE, Lauren JG, Welch RM, Duxbury JM. 2005. A comparison of the effects of micronutrient seed priming and soil fertilization on the mineral nutrition of chickpea (), lentil (), rice () and wheat () in Nepal.,41:427–448.

Johnson-Beebout SE, Lauren JG, Duxbury JM. 2009. Immobilization of zinc fertilizer in flooded soils monitored by adapted DTPA soil test.,40:1842–1861.

Keren R, Bingham FT. 1985. Boron in water, soil and plants.,1:229–276.

Khalid BY, Malik NSA. 1982. Presowing soaking of wheat seeds in copper and manganese solutions.,13:981–986.

Khalid N, Ahmed A, Bhatti MS, Randhawa MA, Ahmad A, Rafaqat R. 2014. A question mark on zinc deficiency in 185 million people in Pakistan-possible way out.,54(9):1222–1240.

Khan MU, Qasim M, Jamil M. 2002. Response of rice to zinc fertilizer in calcareous soils of D.I. Khan.,1:1–2.

Khan MU, Qasim M, Subhan M, Jamil M, Ahmad RD. 2003. Response of rice to different methods of Zn application in calcaerous soils.,3:524–529.

Khan R, Gurmani AH, Gurmani AR, Zia MS. 2006. Effect of boron on rice yield under wheat rice system.,8:805–808.

Khan RU, Gurmani AR, Khan MS, Din J U, Gurmani AH. 2011. Residual, direct and cumulative effect of boron application on wheat and rice yield under rice-wheat system.,27(2):219–223.

Khoshgoftar AH, Shariatmadari H, Karimian N, Kalbasi M, van der Zee SEATM, Parke DR. 2004. Salinity and zinc application effects on phytoavailability of cadmium and zinc.,68:1885–1889.

Kiekens L. 1995. Zinc.: Alloway BJ. Heavy Metals in Soils. London, UK: Blackie Academic: 284–305.

Kielbaso JJ, Ottman K. 1976. Manganese deficiency-contributory to maple decline?, 1:27–32.

Kirk GJD, Bajita JB. 1995. Root-induced iron oxidation, pH changes and zinc solubilization in the rhizosphere of lowland rice.,131(1):129–137.

Korzeniowska J. 2008. Response of ten winter wheat cultivars to boron foliar application in a temperate climate (South-West Poland).,6(2):471–476.

Kumar A, Yadav DS. 1995. Use of organic manures and fertilizer in rice wheat cropping system and for sustainability.,65:703–707.

Kumar A. 2013. Effect of zinc, iron and manganese levels on growth, yield and quality of rice (L.) [Ph.D. Thesis]. Varanasi, Uttar Pradesh, India. Banaras Hindu University.

Kumar A, Choudhary AK, Pooniya V, Suri VK, Singh U. 2016. Soil factors associated with micronutrient acquisition in crops-biofortification perspective.: Singh U, Praharaj CS, Singh SS, Singh NP. Biofortification of Food Crops. New Delhi: Springer: 159–176.

Kumar A, Singh AP. 2018. Direct and residual effect of zinc and boron on growth parameters of rice and wheat grown in sequence in red and alluvial soils of eastern Uttar Pradesh., 6:587–592.

Kumar S, Arora BR, Hundal HS. 1981. Potassium-boron synergism in the nutrition of rice (L.).,29:563–564.

Kutman UB, Yildiz B, Oztruk L, Cakmal I. 2010. Biofortification of durum wheat with zinc through soil and foliar application of nitrogen.,87(1):1–9.

Kutman UB, Yildiz B, Cakmak I. 2011. Improved nitrogen status enhances zinc and iron concentrations both in the whole grain and the endosperm fraction of wheat.,53(1):118–125.

Lakshmanan R, Prasad Dr R, Jain MC. 2005. Yield and uptake of micronutrients by rice as influenced by duration of variety and nitrogen utilization.,51:1–14.

Lindon FC, Teixeira MG. 2000. Oxy-radicals production and control in the chloroplast of Mn-treated rice.,152(1):7–15.

Lu SH, Xu YX, Hu SN. 1990. Features of manganese of paddy soil conditions of manganese deficiency on wheat.,3:87–91.

Lu S H, Liu X J, Li L, Zhang F S, Zeng X Z, Tang C X. 2004. Effect of manganese spatial distribution in the soil profile on wheat growth in rice-wheat rotation.,261:39–46.

Maftoun M, Karimian N. 1989. Relative efficiency of two zinc sources for maize in two calcareous soils from an arid area of Iran.,9:771–775.

Malvi UR. 2011. Interaction of micronutrients with major nutrients with special reference to potassium.,24(1):106–109.

Maqsood MA, Rahmatullah, Kanwal S, Aziz T, Ashraf M. 2009. Evaluation of Zn distribution among grain and straw of twelve indigenous wheat (L.) genotypes.,41(1):225–231.

Marcar NE, Graham RD. 1986. Effect of seed manganese content on the growth of wheat () under manganese deficiency.,96(2):165–173.

Marschner H. 1986. Mineral Nutrition of Higher Plants. London, UK: Academic Press: 195–340.

Marschner H. 1988. Mechanisms of manganese acquisition by roots from soils.: Graham RD, Hannam RJ, Uren NC. Manganese in Soils and Plants. Kluwer, Dordrecht: 191–204.

Marschner H. 1995. Manganese.: Mineral Nutrition of Higher Plants. 2nd edition. London, UK: Academic Press: 324–333.

Marschner H. 2012. Mineral Nutrition of Higher Plants. 3rd edn. London, UK: Academic Press.

Martin WE, McLean JG, Quick J. 1965. Effect of temperature on the occurrence of phosphorus-induced zinc deficiency.,29(4):411–413.

Marzadori C, Antisari LV, Ciavatta C, Sequi P. 1991. Soil organic matter influence on adsorption and desorption of boron.,55(6):1582–1585.

McBride MB. 1982. Electron spin resonance investigation of Mn2+complexation in natural and synthetic organics.,46:1137–1143.

Modaihsh AS. 1997. Foliar application of chelated and non-chelated metals for supplying micronutrients to wheat grown on calcareous soil.,33:237–245.

Moraghan JT, Mascagni HJ. 1991. Environmental and soil factors affecting micronutrient deficiencies and toxicities.,2:371–425.

Mortvedt JJ. 2000. Bioavailability of micronutrients.: Kamprath EJ. Soil Fertility and Plant Nutrition. Boca Raton, FL: CRC Press: D71–D86.

Motschenbacher JM, Brye KR, Anders MM, Gbur EE. 2014. Long-term rice rotation, tillage, and fertility effects on near-surface chemical properties in a silt-loam soil.,100(1):77–94.

Nautiyal N, Yadav S, Singh D. 2011. Improvement in reproductive development, seed yield, and quality in wheat by zinc application to a soil deficient in zinc,42:2039–2045.

Nayyar VK, Sadana US, Takkar TN. 1985. Methods and rates of application of Mn and its critical levels for wheat following rice on coarse textured soils.,8(2):173–178.

Nayyar VK, Arora CL, Kataki PK. 2001. Management of soil micronutrient deficiencies in the rice-wheat cropping system.,4(1):87–131.

Nayyar VK. 2003. Soil micronutrient deficiencies in the rice-wheat cropping system.: Addressing Resource Conservation Issues in Rice-Wheat Systems of South Asia: A Resource Book: 157–162.

Nazir MS, Jabbar A, Mahmood K, Ghaffar A, Nawaz S. 2000. Morphochemical traits of wheat as influenced by presowing seed steeping in solution of different micronutrients.,2:6–9.

Neue HU, Lantin RS. 1994. Micronutrient toxicities and deficiencies in rice.: Yeo A R, Flowers T J. Soil Mineral Stresses: Approaches to Crop Improvement. Berlin, Germany: Springer: 175–200.

Niaz A, Ranjha AM, Rahmatullah, Hannan A, Waqas M. 2007. Boron status of soils as affected by different soil characteristics- pH, CaCO3, organic matter and clay contents.,44(3):428–435.

Obermeyer G, Kriechbaumer R, Strasser D, Maschessning A, Bentrup FW. 1996. Boric acid stimulates the plasma membrane H+-ATPase of ungerminated lily pollen grains.,98(2):281–290.

Ova EA, Kutman UB, Ozturk L, Cakmak I. 2015. High phosphorus supply reduced zinc concentration of wheat in native soil but not in autoclaved soil or nutrient solution.,393:147–162.

Ozkutlu F, Torun B, Cakmak I. 2006. Effect of zinc humate on growth of soybean and wheat in zinc-deficient calcareous soil.,37:2769–2778.

Pahlavan-Rad MR, Pessarakli M. 2009. Response of wheat plants to zinc, iron, and manganese applications and uptake and concentration of zinc, iron, and manganese in wheat grains.,40:1322–1332.

Pandey N. 2010. Role of micronutrients in reproductive physiology of plants.,4:1–13.

Parks WL, White JL. 1952. Boron retention by clays and humus systems saturated with various cations.,16:298–300.

Prasad B, Sharma MM, Sinha SK. 2002. Evaluating Zn fertilizer requirements on typichaplaquent in the rice-wheat cropping system.,19:39–49.

Qin J, Culver DA, Yu N. 1995. Effect of organic fertilizer on heterotrophs and autotrophs: Implications for water quality management.,26:911–920.

Quijano-Guerta C, Kirk GJD, Portugal AM, Bartolome VI, McLaren GC. 2002. Tolerance of rice germplasm to zinc deficiency.,76:123–130.

Rao PR, Subrhamanyam D, Sailaja B, Singh RP, Ravichandran V, Rao G V S, Swain P, Sharma SG, Saha S, Nadaradjan S, Reddy PJ R, Shukla A, Dey D P, Ravichandran S, Voleti S R. 2013. Influence of boron on spikelet fertility under varied soil conditions in rice genotypes.,36:390–400.

Rashid A, Yasin M, Ashraf M. 2004. Boron deficiency in calcareous soil reduces rice yield and impairs grain quality.. 29:58–60.

Rashid A. 2005. Establishment and management of micronutrient deficiencies in soils of Pakistan: A review.,24:1–22.

Rashid A, Yasin M, Ali MA, Ahmad Z, Ullah R. 2007. An alarming boron deficiency in calcareous rice soils of Pakistan: Boron use improves yield and cooking quality.: Xu F. Advances in Plant and Animal Boron Nutrition. Dordrecht, the Netherlands: Springer: 103–116.

Rehman A, Farooq M, Nawaz A, Iqbal S, Rehman A. 2012a. Optimizing the boron seed coating treatments for improving the germination and early seedling growth of fine grain rice.,14(3):453–456.

Rehman A, Farooq M, Cheema ZA, Wahid A. 2012b. Seed priming with boron improves growth and yield of fine grain aromatic rice.,68(2):189–201.

Rehman A, Farooq M. 2013. Boron application through seed coating improves the water relations, panicle fertility, kernel yield, and biofortification of fine grain aromatic rice.,35(2):411–418.

Rehman A, Farooq M, Nawaz A, Ahmad R. 2014a. Influence of boron nutrition on the rice productivity, kernel quality and biofortification in different production systems.,169:123–131.

Rehman A, Farooq M, Cheema ZA, Nawaz A, Wahid A. 2014b. Foliage applied boron improves the panicle fertility, yield and biofortification of fine grain aromatic rice.,14(3): 723–733.

Rehman A, Farooq M, Nawaz A, Rehman A, Iqbal S. 2015. Soil application of boron improves the tillering, leaf elongation, panicle fertility, yield and its grain enrichment in fine-grain aromatic rice.,38:338–354.

Rehman A, Farooq M. 2016. Zinc seed coating improves the growth, grain yield and grain biofortification of bread wheat.,38:238.

Rehman A, Farooq M, Nawaz A, Ahmad R. 2016. Improving the performance of short duration basmati rice in water-saving production systems by boron nutrition.,168(1):19–28.

Rehman A, Farooq M, Ozturk L, Asif M, Siddique KHM. 2018a. Zinc nutrition in wheat-based cropping systems.,422:283–315.

Rehman A, Farooq M, Rashid A, Nadeem F, Stuerz S, Asch F, Bell RW, Siddique KHM. 2018b. Boron nutrition of rice in different production systems: A review.,38: 25.

Rengel Z. 2000. Uptake and transport of manganese in plants.: Sigel A, Sigel H. Metal Ions in Biology Systems. New York, USA: Marcel Dekke: 57–87.

Rerkasem B, Jamjod S. 2004. Boron deficiency in wheat: A review.,89:173–186.

Romheld V, Marschner H. 1991. Genotypical differences among gramineae species in release of phytosiderophores and uptake of iron phytosiderophores.,123(2):147–153.

Rose TJ, Impa SM, Rose MT, Pariasca-Tanaka J, Mori A, Heuer S, Johnson-Beebout SE, Wissuwa M. 2013. Enhancing phosphorus and zinc acquisition efficiency in rice: A critical review of root traits and their potential utility in rice breeding.,112(2):331–345.

Sajwan KS, Lindsay WL. 1986. Effects of redox redox (rē`dŏks): See oxidation and reduction and zinc deficiency in paddy rice.,50:1264–1269.

Saleem M, Khanif YM, Ishak YMF, Samsuri AW. 2011. Solubility and leaching of boron from borax and colemanite in flooded acidic soils.,42:293–300.

Saleem M, Khanif YM, Fauziah CI, Samsuri AW, Hafeez B. 2013. Efficacy of crushed ore colemanite as boron fertilizer for rice grown under calcareous soil conditions.,50:37–42.

Schon MK, Novacky A, Blevins DG. 1990. Boron induces hyperpolarization of sunflower root cell membranes and increases membrane permeability to K+.,93(2):566–571.

Sharma PN. 1992. Pollen fertility in manganese deficient wheat.,69(1):21–24.

Shivay YS, Kumar D, Prasad R. 2008. Effect of zinc-enriched urea on productivity, zinc uptake and efficiency of an aromatic rice- wheat cropping system.,81(3):229–243.

Shorrocks VM. 1997. The occurrence and correction of boron deficiency.,193:121–148.

Shuman LM. 1979. Zinc, manganese, and copper in soil fractions.,127(1):10–17.

Singh A, Shivay YS. 2013. Residual effect of summer green manure crops and Zn fertilization on quality and Zn concentration of durum wheat (Desf.) under a Basmati rice-durum wheat cropping system.,29:271–287.

Singh BP, Singh A, Singh BN. 1990. Response of rice (L.) to zinc sulfate under mid-altitude conditions of Meghalaya.,60:70–71.

Slaton NA, Wilson CE Jr, Ntamatungiro S, Norman RJ, Boothe DL. 2001. Evaluation of zinc seed treatments for rice.,93:152–157.

Slaton NA, Gbur EE Jr, Wilson CE Jr, Norman RJ. 2005a. Rice response to granular zinc sources varying in water soluble zinc.,69:443–452.

Slaton NA, Norman RJ, Wilson CE Jr. 2005b. Effect of Zn source and application time on Zn uptake and grain yield of flood irrigated rice.,92:272–278.

Stein AJ. 2010. Global impacts of human mineral malnutrition.,335:133–154.

Sultana S, Naser HM, Shil NC, Akhter S, Begum RA. 2016. Effect of foliar application of zinc on yield of wheat grown by avoiding irrigation at different growth stages.,41(2):323–334.

Swarup A. 1981. Effect of iron and manganese application on the availability of micronutrients to rice in sodic soil.,60(3):481–485.

Takano J, Miwa K, Yuan L X, von Wiren N, Fujiwara T. 2005. Endocytosis and degradation of BOR1, a boron transporter of, regulated by boron availability.,102:12276–12281.

Takkar PN, Nayyar VK, Sadana US. 1986. Response of wheat on coarse textured soils to mode and time of manganese application.,22(2):149–152.

Tanaka A, Navasero SA. 1996. Interaction between iron and manganese in the rice plant.,12:29–33.

Tariq M, Hameed S, Malik KA, Hafeez FY. 2007. Plant root associated bacteria for zinc immobilization in rice.,39(1):245–253.

Tinker PB, Lauchli A. 1984. Advances in Plant Nutrition. San Diego, CA: Academic Publishers.

Tisdale SL, Nelson WL Beaton JD. 1985. Soil Fertility and Fertilizers. New York, USA: Macmillan Publishing Company.

Tripathi DK, Singh S, Singh S, Mishra S, Chauhan DK, Dubey NK. 2015. Micronutrients and their diverse role in agricultural crops: Advances and future prospective.,37:139.

Ullah A, Farooq M, Rehman A, Arshad MS, Shoukat H, Nadeem A, Nawaz A, Wakeel A, Nadeem F. 2018. Manganese nutrition improves the productivity and grain biofortification of bread wheat in alkaline calcareous soil.,54:744–754.

Van TK, Kang Y, Sakurai K. 2005. Boron fixation and its release in soils and bark compost.,51(1):69–74.

Wang S Z, Wei X R, Hao M D. 2016. Dynamics and availability of different pools of manganese in semiarid soils as affected by cropping system and fertilization.,26(3):351–361.

Wang WJ, Dalal RC. 2006. Carbon inventory for a cereal cropping system under contrasting tillage nitrogen fertilizer and stubble management practices.,91:68–74.

Wang Y, Shi L, Cao X, Xu F. 2007. Plant boron nutrition and boron fertilization in China.: Xu F, Goldbach HE, Brown PH, Bell RW, Fujiwara T, Hunt CD, Goldberg S, Shi L. Advances in Plant and Animal Boron Nutrition. Netherlands: Springer: 93–101.

Wang Z M, Liu Q, Pan F, Yuan L X, Yin X B. 2015. Effects of increasing rates of zinc fertilization on phytic acid and phytic acid/zinc molar ratio in zinc bio-fortified wheat.,184:58–64.

Wei XR, Shao MA, Zhang XC, Gao J L. 2008. Fraction distribution and availability of soil manganese as affected by landforms in the Loessial Gully Region.,14:439–444.

West TO, Post WM. 2002. Soil organic carbon sequestration by tillage and crop rotation: A global data analysis.,66:1930–1946.

Xu R K, Zhao A, Li Q M, Kong X L, Ji G L. 2003. Acidity regime of the red soils in a subtropical region of southern China under field conditions.,115:75–84.

Yadava N, Malik RS. 2016. Effect of nitrate and manganese application on manganese pools in soil and its uptake in wheat (L.).,10:97–103.

Yang X, Yu YG, Yang Y, Bell RW, Ye ZQ. 2000. Residual effectiveness of boron fertilizer for oilseed rape in intensively cropped rice-based rotations.,57(2):171–181.

Yermiyahu U, Keren R, Chen Y. 1988. Boron sorption on composted organic matter.,52:1309–1313.

Yoshida S, Tanaka A. 1969. Zinc deficiency of the rice plant in calcareous soils.,15:75–80.

Zayed BA, Salem AKM, El Sharkawy HM. 2011. Effect of different micronutrient treatments on rice (L.) growth and yield under saline soil conditions.,7(2):179–184.

Zeidan MS, Mohamed MF, Hamouda HA. 2010. Effect of foliar fertilization of Fe, Mn and Zn on wheat yield and quality in low sandy soils fertility.,6(6):696–699.

Zhang YQ, Deng Y, Chen RY, Cui ZL, Chen XP, Yost R, Zhang FS, Zou CQ. 2012. The reduction in zinc concentration of wheat grain upon increased phosphorus-fertilization and its mitigation by foliar Zn application.,361:143–152.

Zhao P, Yang F, Sui FQ, Wang QY. 2013. The effects of zinc and nitrogen on wheat nitrogen using, yield and grain protein content.,18:28–33. (in Chinese with English abstract)

Zoz T, Steiner F, Fey R, Castagnara DD, Seidel EP. 2012. Response of wheat to foliar application of zinc,42(5):784–787.

1 August 2018;

8 February 2019

Muhammad FAROOQ (farooqcp@gmail.com)

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http://dx.doi.org/10.1016/j.rsci.2019.02.002

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