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Boron Seed Priming Improves the Seedling Emergence, Growth, Grain Yield and Grain Biofortification of Bread Wheat.

Byline: Saba Iqbal, Muhammad Farooq, Sardar Alam Cheema and Irfan Afzal

Abstract

Boron (B) deficiency is quite prevalent in wheat growing regions of Indo-Gangetic Plains. This study, consisted of three experiments, was conducted to evaluate the effect of B seed priming on the productivity and grain biofortification of bread wheat. In first experiment, wheat seeds were primed with 1, 0.5, 0.1, 0.05 and 0.01 M B solutions of boric acid (H3BO3) and borax (Na2B4O7.10H2O) while dry seeds and hydropriming were taken as control. Seed priming with 0.05 M B and 0.01 M B were better than other treatments of both B sources in improving germination and early seedling growth. In second experiment, wheat seeds primed with 0.01 and 0.05 M B solutions of both sources of B were sown in sand filled small pots.

Seed priming with 0.01 M B solution of borax was better than other treatments in improving the germination and seedling growth. In third experiment, wheat seeds primed with 0.01 and 0.05 M B solution of borax only were sown. Seed priming with 0.01 M B solution increased the grain yield by 64% over control; however, increase in grain B contents was 27%. In conclusion, wheat seeds may be primed with 0.01 M B using borax to improve the grain yield and grain B contents in wheat.

Keywords: Biofortification; Boron; Seed priming; Yield

Introduction

For proper growth and development of plants, supply of specific nutrients is necessary at appropriate time and in readily available form. To achieve higher yield, proper crop nutrition including both micro and macronutrients is essential (Arif et al., 2006). For vascular plants, B is considered as an essential micronutrient. Deficiency of B affects vegetative as well as reproductive growth in plants thus causing cell expansion inhibition, death of meristematic cells and reduction in plant fertility (Marchner, 1995). Immediate B deficiency symptoms in plants include inhibition of root growth (Dell and Huang, 1997) and cessation of leaf elongation (Huang et al., 1996). However, all of physiological process are not equally affected by B deficiency in plants.

Boron is an important micronutrient that regulates various physiological processes in life cycle of vascular plants such as cell wall development, metabolism of carbohydrates and RNA (Herrera-Rodriguez et al., 2010). Moreover, it also modulates the pollen tube growth and germination, integrity of plasma membrane, floret fertility, anther development and seed development as well (Oosterhuis, 2001). In wheat, floret sterility is one of the major causes of low grain yield (Anantawiroon et al., 1997).

Floret sterility is caused by a combination of factors including abiotic stresses such as drought and heat (Saini and Aspinall, 1982), and inadequate supply of B during reproductive phase of plant life cycle (Rerkasem, 1995, Khan et al., 2016). Plant has poorley developed anthers and pollens as it prone to B deficiency (Cheng and Rerkasem, 1993). Therefore the sterility induced by inadequate supply of B is of major concern in B deficient soils (Rashid et al., 1997; Shorrocks, 1997). In wheat, due to sterility, grain setting is impaired, which results in more number of open spikelets with less number of grains (Rerkasem et al., 1993). Deficiency of B may result in failure of grain setting without affecting its vegetative growth (Rerkasem and Loneragan, 1994). Hence, the amount of B which is sufficient for normal vegetative growth in wheat can cause improper development of anthers and pollens during reproductive growth (Rerkasem et al., 1997).

This deficiency can be cured by sufficient exogenous supply of B during reproductive growth of plant. Boron requirement for reproductive growth is more than vegetative growth as in leaves B concentration is 2 mg kg-1 dry matter which is about five times <the B concentration in anther tissues (Rerkasem et al., 1997).

Micronutrients may be delivered as soil application, foliar sprays and/or seed treatment. Each method helps in providing the required amount of nutrient to the crop and also enrich the seeds of progeny crop obtained from micronutrient treated crop (Johnson et al., 2005). These both goals can be achieved by foliar application of micronutrients to the plants (Savithri et al., 1999). However, this method requires additional application cost. For soil application of micronutrients, high quality fertilizers are not available and it is not easy to spread the small quantity of fertilizer evenly on the soil surface (Savithri et al., 1999). Seed priming provides an effective and easy alternative for micronutrient application (Savithri et al., 1999; Johnson et al., 2005). Small amount of nutrient is required for seed priming hence can be an economical approach as compared with other methods.

In rice for instance, seed priming with 0.001% B solution has been found an effective and pragmatic way of B application that improved yield related traits consequently better yield and grain B enrichment (Rehman et al., 2012). In another study, B application methods (soil, foliar and seed priming) were compared and B seed priming proved economically the most viable option in improving rice yield (Rehman et al., 2014).

However, to the best of our knowledge no study has been conducted to optimize the source as well as concentration of B for wheat seed priming. Therefore, this study was conducted to optimize levels and source of B for seed priming, and to monitor its potential in improving germination, seedling growth, grain yield and grain B contents of wheat.

Materials and Methods

This study was carried out in the Allelopathy Laboratory and Greenhouse, University of Agriculture, Faisalabad, Pakistan during 2012-2013. Seeds of wheat cultivars Faisalabad-2008 and Lasani-2008 were obtained from the Wheat Research Institute, Ayub Agriculture Research Institute, Faisalabad, Pakistan.

Experiments 1

For the 1st experiment, 50 g seeds of each wheat cultivars were soaked in aerated solution of 1.0, 0.5, 0.1, 0.05 and 0.01 M B [boric acid (H3BO3), B = 17% (MERCK, Purity = 99.5%) and borax (Na2B4O7), B = 11% (MERCK, Purity = 98%)] or water (hydropriming) for 12 h at 25 +- 2degC and then dried back to their original weight. Aeration was provided with simple aquarium pump. Dry seeds and hydropriming were taken as control. Seeds were sown on November 16, 2012 in petri plates arranged according to three factor factorial completely randomized design with four replications. Ten seeds were sown in each petri plate (90 mm x 15 mm) between two layers of moist filter paper. Petri plates were placed at 25 +- 2degC throughout the experiment. After attaining the constant germination count, four seedlings were maintained in each petri plate. Seedlings were harvested on November 28, 2012.

Experiments 2

Seeds were primed with two best performing treatments from 1st experiment (0.01 and 0.05 M B solutions of both B sources) and water (hydropriming) for 12 h. Dry seeds and hydropriming were taken as control. Seeds of both wheat cultivars were primed with B by above mentioned procedure. Ten seeds of each treatment were sown manually in each sand filled pot on November 30, 2012. Pots were arranged by completely randomized design in factorial arrangement with four replications. After attaining the constant count, five seedlings of uniform size were maintained in each pot. Plants were harvested on December 20, 2012.

Experiments 3

Seeds were primed with best performing treatments and source (0.01 and 0.05 M B solutions of borax) and water (hydropriming) for 12 h. Seeds of both wheat cultivars were primed with B by above mentioned procedure while dry seeds and hydropriming were taken as control. Twenty seeds of each treatment were sown manually in each pot (45x 30 cm) filled (15 kg soil each) with sandy loam soil (having pH= 8.20. EC= 0.33 dS m-1 and B= 0.56 mg L-1) on December 26, 2012. Pots were arranged according to completely randomized design in factorial arrangement with four replications. After attaining the constant count, ten seedlings of uniform size were maintained in each pot. Plants were harvested manually on April 24, 2013.

Observations

Seeds were scored as germinated when radicles reached 2 mm in length. The germination count was taken according to Association of Official Seed Analysts (AOSA, 1990) until a constant count was achieved. Mean germination/emergence time was calculated according to formula given by Ellis and Robert (1981). For final germination percentage (FGP), number of seeds germinated at constant were expressed in percentage. For final emergence count (FEC), number of seedling emerged at constant were expressed in percentage. Seedling length was measured with the help of a ruler. Seedlings were oven-dried at 70degC for 48 h to determine seedling dry weight by using weighing balance (USA, OHAUS, TS400S).

Five spikes were selected at random from each pot, and number of spikelets and grains in each spike were counted. The plants were harvested, and for grain yield, spikes were threshed manually and grains were weighed on a weighing balance. For 100-grain weight, a sub sample of 100 grains taken from each pot was weighed on weighing balance. For grain B contents, dry ashing of grain samples was done (Chapman and Pratt, 1961) and B was measured by azomethine-H method in the digested samples (Bingham, 1982). Data collected on all parameters were analyzed statistically by Statistical software Statistix 8.1.

Least significance difference (LSD) test at 5% probability level was applied to compare the treatment means.

Results

Experiment 1

Seed priming treatments and B sources significantly (p[?]0.05) affected mean germination time (MGT), final germination percentage (FGP), seedling length and seedling dry weight, however cultivars did not differ significantly for these traits (Table 1). Interaction of cultivars with B sources and treatments was also not significant (p[?]0.05) for these traits (Table 1) and was significant between B sources and treatments (Table 1). Likely, interaction among cultivars, B sources and treatments was also not significant (p[?]0.05) for each of emergence and seedling traits (Table 1). Less MGT and FGP was recorded in seeds primed with 1.00 and 0.50 M B solution of boric acid than rest of the treatments (Table 2). Seed priming with 0.01 M B solution of borax produced longer seedlings than control (Table 2). Similarly, maximum seedling dry weight was recorded in seed priming with 0.01 M B solution of borax and boric acid as well (Table 2).

Experiment 2

Seed priming treatments significantly (p[?]0.05) affected mean emergence time (MET), final emergence percentage (FEP), seedling length and seedling dry weight while wheat cultivars differed significantly (p[?]0.05) for FEP and seedling dry weight only (Table 3). Moreover, B sources also differed significantly (P[?]0.05) for seedling length and seedling dry weight (Table 3). However, interaction between cultivars and B sources was not significant (p[?]0.05) for MET, FEP, seedling length and seedling dry weight (Table 3). Interaction between cultivars and seed priming treatments was only significant (p[?]0.05) for seedling dry weight (Table 3). Likely, interaction between B sources and seed priming treatments and among cultivars, B sources and seed priming treatments was also non-significant (p[?]0.05) (Table 3). Seed priming with 0.01 M B solution and hydropriming took less time to mean emergence and had more FEP than control (Table 4).

However, between cultivars, more FEP was recorded in cv. Faisalabad-2008 than cv. Lasani-2008 (Table 4). More seedling length was recorded in seed priming with 0.01 M B solution and hydropriming (Table 4), however borax gave more seedling length than boric acid (Table 4). While maximum seedling dry weight was recorded in cv. Faisalabad-2008 seeds primed with 0.01 M B solution (Table 4).

Experiment 3

Seed priming with B significantly (p[?]0.05) affected MET, FEP, spikelets per spike, grains per spike, 100-grains weight, grain yield and grain B contents; while wheat cultivars differed significantly (P[?]0.05) for 100-grains weight and grain yield (Table 5). Interaction between cultivars and seed priming treatments was non-significant (p[?]0.05) for MET, FEP, spikelets per spike, 100-grains weight, grain yield and grain B contents (Table 5). Less MET was taken by seeds primed with 0.01 M B solution (Table 6). All treatments showed similar FEP except for seeds primed with 0.05 M B solution however maximum FEP was recorded in hydroprimed seeds while lowest in 0.05 M B solution (Table 6). Maximum spikelets per spike and grains per spike were recorded in seeds primed with 0.01 M B solution (Table 6). Maximum 100-grains weight was recorded in seeds primed with 0.01 M B solution and hydropriming (Table 6).

More grain yield was recorded in seeds primed with 0.01 M B solution (Table 6). However, maximum grain B contents were recorded in seeds primed with 0.05 M B solution (Table 6).

Discussion

Seed priming with B, especially at low concentration, has potential to boost germination rate and seedling growth of wheat. Metabolic processes involved in early phases of germination are stimulated by seed priming thus seedlings produced from primed seeds with B emerged earlier and produced healthy seedlings (Tables 4, 6). Seed priming activates the hydrolytic enzymes and improve the physiology of embryos thus germination take place in less time (Bam et al., 2006). Moreover, B facilitates the remobilization of seed nutrients stores during seed germination (Bonilla et al., 2004). Boron affects the seed germination by controlling dormancy same as gibberellic acid (Cresswell and Nelson, 1972). In addition to that it also modulates the germination metabolism and translocation of sugars from endosperm to the developing embryo (Cresswell and Nelson, 1972).

As only small amount of B is required to regulate the meristematic growth (Khan et al., 2006), any excessive amount becomes toxic impeding the normal growth (Bonilla et al., 2004). Therefore, germination and seedling growth was improved by seed priming with 0.01 M B solution, whereas it was suppressed by 1 M B solution (Tables 2 and 4). Toxic B concentration leads to different physiological effect during life cycle of vascular plants. Moreover, percentage of germinated seed is reduced under high concentration of B (Banuelos et al., 1999) through inhibition of polyphenol oxidase activity in embryos and endosperm during germination process (Olcer and Kocacaliskam, 2007).

Early start of germination in seeds primed with 0.01 M B solution of borax gave rise to longer seedlings. Boron is required for elongation of cell wall (Martin-Rejano et al., 2011) by providing mechanical support (O'Neill et al., 2004) to newly synthesized polysaccharides due to its involvement in crosslinking of these polysaccharides (Kobayashi et al., 1996).

Table 1: Analysis of variance for influence of seed priming with boron on germination and seedling growth of wheat cultivars

SOV###DF###MGT###FGP###SL###SDW

Cultivars (C)###1###0.11 ns###22.3 ns###4.38 ns###2.43 ns

Boron sources (B)###1###6.92**###12643.80**###627.58**###63.75**

Treatments (T)###6###2.93**###12782.70**###1226.94**###574.18**

CxB###1###0.96 ns###72.30 ns###3.98 ns###2.43 ns

CxT###6###0.38 ns###49.40 ns###10.93 ns###3.77 ns

BxT###6###3.81**###4691.70**###204.34**###22.00**

CxBxT###6###0.47 ns###45.20 ns###6.05 ns###0.86 ns

Error###84###0.25###55.1###24.59###5.70

Total###111

Table 2: Influence of seed priming with boron on germination and seedling growth of wheat cultivars

Treatments###Mean germination time (days) Final germination percentage (%)###Seedling length (cm)###Seedling dry weight (mg)

###Boric acid Borax###Mean###Boric acid###Borax###Mean###Boric acid###Borax###Mean###Boric acid###Borax###Mean

Control###2.78a###2.78a###2.78###98.75a###98.75a###98.75###30.27abc###30.27abc###30.27###18.62bc###18.62bc###18.62

HP###2.55a###2.55a###2.55###100.00a###100.00a###100.00###29.26a-d###29.26a-d###29.26###19.75b###19.75b###19.75

1.00 M###0.38c###2.79a###1.58###2.50e###70.00d###36.25###2.56f###19.25e###10.90###4.75f###10.54e###7.64

0.50 M###1.50b###2.76a###2.13###7.50e###82.50c###45.00###6.12f###19.60e###12.86###6.88f###10.15e###8.51

0.10 M###2.79a###2.67a###2.73###91.25b###95.00ab###93.13###25.01d###26.13cd###25.57###15.50d###16.75cd###16.12

0.05 M###2.67a###2.62a###2.64###98.75a###100.00a###99.38###27.22cd###28.14bcd###27.68###20.25b###19.12b###19.69

0.01 M###2.57a###2.55a###2.56###98.75a###100.00a###99.38###32.58ab###33.50a###33.04###22.75a###24.12a###23.44

Mean###2.67###2.18###71.07###92.32###21.86###26.59###15.50###17.00

Table 3: Analysis of variance for influence of seed priming with boron on seedling emergence and growth of wheat cultivars

SOV###DF###MET###FEP###SL###SDW

Cultivars (C)###1###0.56 ns###85.33*###5.98 ns###99.19**

Boron sources (B)###1###0.13 ns###9.19 ns###14.43*###9.19*

Treatments (T)###3###5.91**###196.50**###74.78**###22.02**

CxB###1###0.74 ns###1.69 ns###0.01 ns###0.52 ns

CxT###3###0.57 ns###10.28 ns###2.42 ns###5.08*

BxT###3###0.26 ns###7.08 ns###5.31 ns###4.19 ns

CxBxT###3###0.04 ns###0.91 ns###0.47 ns###4.19 ns

Error###32###0.45###10.66###2.64###1.44

Total###47

Table 4: Influence of seed priming with boron on seedling emergence and growth of wheat cultivars

Treatments###Mean emergence time (days)###Final emergence percentage (%)###Seedling length (cm)###Seedling dry weight (mg)

###FSD-2008###LS-2008###Mean FSD-2008###LS-2008###Mean###Boric acid###Borax###Mean###FSD-2008###LS-2008###Mean

Control###6.74###6.45###6.59A 93.33###90.00###91.67B###28.10###28.10###28.10B 13.67cd###12.67d###13.17

HP###4.88###5.42###5.15B 99.50###99.00###99.25A###32.50###32.50###32.50A 17.00ab###13.33cd###15.17

0.01 M###5.04###5.66###5.35B 98.67###96.67###97.67A###32.17###33.87###33.02A 18.33a###14.50c###16.42

0.05 M###6.29###6.29###6.29A 93.83###89.00###91.42B###27.52###30.22###28.87B 16.00b###13.00d###14.50

Mean###5.74###5.95###96.33A###93.67B###30.07B###31.17A###16.25###13.38

Deficiency of B also down regulates several enzymes, which are required for loosening of cell wall to facilitate the process of cell elongation (Cosgrove, 1999; Camacho-Cristobal et al., 2008). Furthermore, longer seedlings resulted in more seedling dry weight in seed priming with 0.01 M B solution of borax. However, higher concentrations of B beyond 0.05 M B were more toxic in case of boric acid as compared to borax. Similarly, early seedling growth and germination was improved in rice by seed priming with 0.001% B solution while higher concentration of B (0.5% B solution) proved to be toxic (Rehman et al., 2012).

Table 5: Analysis of variance for influence of seed priming with boron on stand establishment, yield related traits, grain yield and grain boron contents of wheat cultivars

SOV###DF###MET###FEP###SPS###GPS###GW###GY###GBC

Cultivars (C)###1###0.03ns###225.78 ns###1.56 ns###9.74 ns###0.59**###3.06**###0.74 ns

Treatments (T)###3###2.71**###675.78**###6.71**###41.96**###0.49**###15.48**###0.57**

CxT###3###0.31 ns###19.53 ns###0.69 ns###4.30 ns###0.13 ns###0.12 ns###0.08 ns

Error###24###1.34###84.63###0.51###3.17###0.05###0.14###0.09

Total###31

Table 6: influence of seed priming with boron on stand establishment, yield related traits, grain yield and grain boron contents of wheat cultivars

Treatments###MET###FEP###SPS###GPS###GW###GY###GBC

Control###13.00c###87.50a###16.38c###40.84c###3.94b###3.00c###1.33c

Hydropriming###12.68c###89.38a###17.51b###43.77b###4.34a###3.79b###1.34c

Seed priming (0.01 M)###13.49b###85.62a###18.56a###46.39a###4.50a###4.92a###1.70b

Seed priming (0.05 M)###14.01a###69.38b###17.19b###42.98c###4.10b###3.62b###1.84a

Improvement in germination and seedling growth by lower concentration of B priming solution (Tables 2, 4 and 6) enabled plants to grow better and produce more yield (Tables 2, 4 and 6). Deficiency of B reduces the grain setting in wheat owing to abnormality in pollen development and stigma function (Rerkasem et al., 1993); whereas B application regulates the grain setting in cereals (Rehman et al., 2012). Deficiency of B also impairs viability of pollen grains (Huang et al., 2000). Pollen tube may also burst in the absence of B owing to the role of B in structure of cell wall of pollen tube (Brown et al., 2002). Boron deficiency also inhibits cell expansion (Hu and Brown 1994). Thus, fertilization may not occur, which resulted in failure in grain setting and consequently low grain set in B deficient plants. As B is required for seed setting thus greater yield in B priming might be the result of more grain setting (Dear and Lipsett, 1987; Noppakoonwong et al., 1997).

Boron is also involved in translocation of assimilates from source to sink during grain development (Reddy et al., 2003). Seed priming in 0.01 M B solution also increased the 100-grains weight in wheat. Boron-induced increase in assimilate supply (Reddy et al., 2003) seems the main reason of this improvement in grain size. Significant increase in yield contributing traits by B priming (0.01 M) resulted in substantial increase in grain yield. It might also be due to role of B in enhancing the translocation of photo-assimilates from vegetative to reproductive parts (Reddy et al., 2003), which might increase the grain yield in wheat.

Seed priming with B, 0.05 and 0.01 M B solutions, resulted in increase in grain B contents of wheat cultivars. Boron is mainly transported to the seed by xylem and to some extent by phloem (Brown and Shelp, 1997). In this study, the increase in grain B contents (Table 6) was due to its better availability to plants and translocation to the developing grain (Dvorak et al., 2003). Principal mechanism of B transport from soil to plant is diffusion which governs by concentration gradient but under limited supply of B, other mechanisms of B transport are necessary which can transport B against concentration gradient (Dannel et al., 2000). In Arabidopsis, a B transporter is observed to be upregulated under limited supply of B, which can transport B from soil to roots against concentration gradient (Takano et al., 2002).

However, this transporter of B only up-regulates in plants under limited B supply and adequate or luxuriant supply of B may result in degradation of this protein thus the up-regulation of this transporter is necessary to maintain the adequate supply of B during variable growing conditions (Takano et al., 2005). In this study, the improvement in growth and yield (Tables 2, 4 and 6) at lower concentration of B solution (0.01 M B) might be due to up-regulation of B transporter which further enhance the supply of B to plant thus improved its performance. Seed priming with B at low concentration resulted in seedlings with longer shoots and roots and consequently able to acquire nutrients including B from more area and depth of soil. Thus seeds produced by these plants had more B contents as compared with control also reported earlier for rice (Rehman et al., 2012).

Conclusion

Wheat seeds may be primed with 0.01 M B using borax to improve the germination, early seedling growth, yield and grain B contents of wheat.

Acknowledgments

Financial support from Higher Education Commission of Pakistan to conduct this research is highly acknowledged.

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Author:Iqbal, Saba; Farooq, Muhammad; Cheema, Sardar Alam; Afzal, Irfan
Publication:International Journal of Agriculture and Biology
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Date:Feb 28, 2017
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