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Contribution of Post-Anthesis Growthand Manganese Dynamics to DifferentialGrain Yield in Different Wheat SpeciesArun Shankara, Upkar S. Sadanaa & Nirmal K. Sekhona

a Department of Soil Science, Punjab Agricultural University,Ludhiana, IndiaAccepted author version posted online: 28 Feb 2014.Publishedonline: 27 Jun 2014.

To cite this article: Arun Shankar, Upkar S. Sadana & Nirmal K. Sekhon (2014) Contribution of Post-Anthesis Growth and Manganese Dynamics to Differential Grain Yield in Different Wheat Species,Journal of Plant Nutrition, 37:11, 1770-1781, DOI: 10.1080/01904167.2014.889151

To link to this article: http://dx.doi.org/10.1080/01904167.2014.889151

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Journal of Plant Nutrition, 37:1770–1781, 2014Copyright C© Taylor & Francis Group, LLCISSN: 0190-4167 print / 1532-4087 onlineDOI: 10.1080/01904167.2014.889151

CONTRIBUTION OF POST-ANTHESIS GROWTH AND MANGANESE

DYNAMICS TO DIFFERENTIAL GRAIN YIELD IN DIFFERENT

WHEAT SPECIES

Arun Shankar, Upkar S. Sadana,

and Nirmal K. Sekhon

Department of Soil Science, Punjab Agricultural University, Ludhiana, India

� Manganese (Mn) deficiency has become a serious nutritional problem for wheat grown in alka-line coarse textured soil. The study aimed to investigate post-anthesis Mn partitioning in differentwheat species. Cultivars of bread wheat (‘PBW509’, ‘DBW17’, ‘PBW550’ and ‘PBW636’); durumwheat (‘PDW291’) and triticale (‘TL2908’) were grown in 6.5 L pots with two treatments of Mn(0 and 50 mg Mn kg−1 soil) in screen house and harvested at anthesis, 18- days post-anthesis, andmaturity to record Mn uptake. Durum cv. ‘PDW291’ retained highest proportion of Mn in its vege-tative parts under Mn deficiency resulting into lowest partitioning to the grain and had the lowestgrain yield. All bread wheat cv. facilitated superior Mn partitioning to the grain, lesser retentionin vegetative organs and higher Mn utilization efficiency, than triticale and durum wheat species.Cultivars producing higher yield on Mn deficit soils are viable alternative to foliar application ofMn.

Keywords: manganese efficiency, Mn dynamics, Mn partitioning, wheat cultivars

INTRODUCTION

Wheat is highly susceptible to manganese (Mn) deficiency (Lucas andKnezek, 1972; Krahmer and Sattelmacher, 2001). A lot of attention has beenmade to study the mechanism of tolerance to low Mn status in terms ofroot geometry (Sadana et al., 2002); uptake kinetics (Pedas et al., 2005;Sadana et al., 2005); chemical mobilization (Gherardi and Rengel, 2004;Fang et al., 2008); superior internal utilization (Jiang and Ireland, 2005);seed Mn content (Khabaz-Saberi et al., 2000); rhizosphere microorganisms(Huang et al., 1994; Posta et al., 1994; Nogueira et al., 2007), and post-anthesis Mn dynamics (Pearson and Rengel, 1994). However, exhaustive

Received 17 November 2011; accepted 29 April 2012.Address correspondence to A. Shankar, Department of Soil Science, Punjab Agricultural University,

Ludhiana-141004, India. E-mail: [email protected]

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Manganese Partitioning in Different Wheat Species 1771

study on differential Mn dynamics in wheat during the generative phase andits impact on plant growth is still lacking. Keeping this lacuna in mind, thepostanthesis Mn dynamics in six wheat cultivars from three wheat species(triticale, bread, and durum wheat) and its impact on plant growth wereinvestigated. The current paper represents the first exclusive study on post-anthesis Mn dynamics and its impact on plant growth in bread, durum, andtriticale wheat species.

To understand plant Mn dynamics, we need to focus on the behavior ofMn in terms of its mobility within different organs leading to its better distri-bution and partitioning in plant. The uptake and/ or mobility of Mn withinshoot and to the grain are mainly affected by Mn application and growthstages (Pearson and Rengel, 1994); sucrose status and humidity (Pearsonet al., 1996); heat stress which generally increases Mn uptake (Dias et al.,2009), and plant genotypes (Hocking et al., 1977). Manganese accumulatesin plant organs where intensive chemical reactions take place and whichare in active vegetation. Manganese is primarily present as a divalent ionin equilibrium with unstable organic acid complexes in xylem sap and itmoves freely in the transpiration stream and, when supplied in adequateamounts, accumulates in roots, stems, and leaves in a pattern traditionallydescribed as phloem immobile. However, phloem sap of plants may alsocontain high concentrations of Mn and supply adequate amounts to devel-oping seeds (Loneragan, 1988). Phloem mobility of Mn is very low and itcan reach glumes directly via xylem in mature wheat plants or can be firsttransferred from xylem to phloem and then reach the glumes via phloem inyoung plants (Riesen and Feller, 2005) though the extent of Mn mobility inphloem varies with plant species (Epstein, 1971).

Good reproductive phase mobilization of Mn to barley grains at harveststage with an increased spike Mn concentration (along with flag leaf) accom-panied by decreased Mn concentration in the other plant parts includingolder leaves has been reported recently by Birsin et al. (2010). Manganesemoves readily from roots, stems, and petioles to developing sinks, includingseeds in lupin (Hannam et al., 1985). Under Mn deficiency, Mn content ofstem, peduncle and flag leaf decreases and that of glumes increases towardsmaturity (Pearson and Rengel, 1994). Sharp decline of mineral nutrientcontent from vegetative organs during reproductive growth stage occurs be-cause nutrient uptake generally decreases, mainly as a result of decreasingcarbohydrate supply to the roots (Marschner, 1995). So the literature sug-gests evidences of Mn mobilization as well as Mn being relatively immobile.The present study aimed to investigate the post-anthesis growth and Mndynamics in different plant parts of three wheat species during the repro-ductive phase. It was expected that cultivars producing higher yield shouldfacilitate superior Mn partitioning to grain and lesser retention of Mn in thevegetative parts especially under Mn deficiency.

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1772 A. Shankar et al.

TABLE 1 Physico-chemical characteristics of the used soil for pot experiment

Physico-chemical characteristics Amount

Particle density (g cm−3) Prihar and Sandhu (1968) 2.64Bulk density (g cm−3) (Blake and Hartge, 1986) 1.53Saturation percentage 24Sand (%) 85Silt (%) 6Clay (%) 9Textural class Loamy sandpH (1:2 soil water) 8.3EC (dS m−1) (1:2 supernatant) 0.35CaCO3 (%) 0.60Organic Carbon (g kg−1 soil) (Walkley and Black, 1932) 6.0Extractable NPK (mg kg−1 soil)

N(Subbiah and Asija, 1956) 60P (Olsen et al., 1954) 15K(Merwin and Peech, 1951) 126

DTPA- extractable micronutrients (mg kg−1 soil) (Lindsay and Norwell, 1978)Zn 1.9Fe 6.2Mn 1.54Cu 0.35

MATERIALS AND METHODS

Six cultivars of three wheat species bread wheat (‘PBW 509’, ‘DBW17’, ‘PBW 550’, and ‘PBW 636’); durum wheat (‘PDW 291’), and triticale(‘TL2908’) were grown with two treatments of Mn (0 and 50 mg Mn kg−1

soil) in pot culture experiment (volume of used pots was 6500 cc) in a screenhouse under natural sunlight at Punjab Agricultural University, Ludhiana(30◦56 N, 75◦32 E and 247 m above mean sea level). Surface soil (0−15 cm)was collected from Mn-deficient field from village Batha Dhuha near Lud-hiana, Punjab, India. The physico-chemical characteristics of the soil aregiven in the Table 1. A basal dose of 125 mg N kg−1 soil through Urea[CO(NH2)2] and 13 mg P kg−1 soil through potassium dihydrogen phos-phate (KH2PO4) was applied. 50 mg Mn kg−1 soil treatment was given toensure growth differences compared to Mn unfertilized pots (Sadana et al.,2002, 2005). Seeds were sown in polythene lined plastic pots containing 9 kgsoil during winter and final harvest was done in the following summer. Tenseeds of both cultivars were sown and later thinned to five plants per pot.Soil moisture was maintained at field capacity. Growth conditions were keptsimilar.

Initial soil solution Mn concentration (CLi) was measured by inductivelycoupled argon plasma atomic emission spectrophotometer. Soil solution wascollected by displacement technique of Adams (1974) at soil water content

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Manganese Partitioning in Different Wheat Species 1773

equivalent to 60 per cent of the maximum water holding capacity of thesoil. The treated soil was incubated for 24 hours before the collection of soilsolution samples. Plants were grown with nine replicates (three replicatesfor three harvest stages i.e. harvested at anthesis, 18-days post-anthesis andat grain maturity.

Plants harvested at anthesis were separated into lower leaves (includingall leaves and their leaf sheaths), stem, flag leaf (including the leaf sheath),peduncle, and spikes. Plants harvested at 18- days post-anthesis were sepa-rated into lower leaves (including all leaves and their leaf sheaths), stem,flag leaf (including the leaf sheath), peduncle, and spikes. For maturitythe plants harvested were separated into lower leaves (including all leavesand their leaf sheaths), stem, flag leaf (including the leaf sheath), pedun-cle, chaff and grains. Samples were washed with distilled water and driedat 70◦C to a constant weight to record dry weight. The dried samples wereground in a stainless steel willey mill, digested in diacid mixture [nitricacid (HNO3) and perchloric acid (HClO4) in 3:1 ratio] and aqueous ex-tracts were prepared. These extracts were analyzed for Mn concentrationusing Atomic Absorption Spectrophotometery (Varian Spectra AA 20 plus;Varian Medical Systems, Palo Alto, CA, USA) and to calculate uptake [con-centration (mg plant−1) x dry matter (mg plant−1) x .001]. Manganesepartitioning of individual organs was calculated as the percent uptake ofthese organs. Statistical procedure of a completely randomized design in-volving factorial treatment combinations was used for analysis of variance(ANOVA).

RESULTS

In the zero Mn treatment, CLi was 2.0 ×10−10 mol cm−3, which increasedto 3.2 ×10−10 mol cm−3 with application of 50 mg Mn kg−1 soil. Althoughthe amount of Mn applied seems large, the corresponding increase the soilsolution Mn concentration is comparatively lower and researchers can easilystudy the Mn dynamics at various growth stages. All the cultivars producedlower shoot dry matter yield under Mn deficiency and recorded reducedgrain yield at maturity (Tables 2, 3, 4). Wheat cultivars ‘PBW 550’ and ‘PBW509’ recorded highest grain weight under Mn deficiency and sufficiency,respectively. Under Mn deficiency, highest retention of dry matter in vege-tative organs was observed for cultivar ‘PDW 291’. In Mn deficient plants, atanthesis (Table 2), the spike weight relative to whole plant dry weight was30.8%, 28.2, 23.1, 18.8, 18.7, and 14.8% recorded for wheat cultivars ‘PBW550’, ‘DBW 17’, ‘PBW 509’, ‘PBW 636’, ‘TL 2908’, and ‘PDW 291’, respec-tively. At 18 days post-anthesis (Table 3), it raised to 42.5%, 40.6, 36.9, 34.2,33.2, and 19.4% for cultivars ‘PBW 550’, ‘PBW 509’, ‘PBW 636’, ‘DBW 17’,‘TL2908’, and ‘PDW 291’, respectively.

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TABLE 2 Dry matter yield (g pot−1) of six wheat cultivars at anthesis as influenced by Mn application

0 mg Mn kg−1 soil 50 mg Mn kg−1 soil

CultivarLowerleaves Stem

Flagleaf Peduncle Spike Total

Lowerleaves Stem

Flagleaf Peduncle Spike Total

PBW509

2.18 1.10 1.27 0.80 1.62 6.97 3.00 3.13 2.57 1.88 7.50 18.08

DBW 17 1.11 1.10 0.77 0.43 1.33 4.74 3.00 2.70 1.90 1.30 6.20 15.10PDW

2912.00 1.50 1.07 0.60 0.90 6.07 4.80 4.20 2.77 0.86 2.30 14.93

PBW550

2.20 1.70 1.53 0.90 2.84 9.17 3.53 3.13 2.67 2.07 4.90 16.30

TL 2908 2.71 1.80 0.93 0.68 1.40 7.52 5.07 4.33 2.60 1.80 4.07 17.87PBW

6362.24 1.41 1.11 0.4 1.20 6.36 4.20 3.40 1.60 1.37 2.50 13.07

CD(5%)

Mn application = 0.05, cultivars = 0.08, Mn application x cultivars = 0.12

At maturity (Table 4), the relative grain yield corresponding to its max-imum yield was 76.6%, 65.9, 62.7, 56.4, 54.1, and 30.5% for cultivars ‘PBW550’, ‘TL2908’, ‘DBW 17’, ‘PBW 636’, ‘PBW 509’, and ‘PDW 291’, respec-tively. The grain weight relative to chaff ranged from 1.23 (‘TL 2908’) to1.64 (‘DBW 17’) under Mn deficiency and from 1.29 (‘TL 2908’) to 1.77(‘DBW 17’) in Mn applied plants. Wheat cultivar ‘TL 2908’ recorded highernon-grain dry matter yield and lower grain weight relative to chaff in bothtreatments. Under Mn deficiency, maximum weight of lower leaves, stemand peduncle in both cultivars was attained at 18 days post-anthesis.

TABLE 3 Dry matter yield (g pot−1) of six wheat cultivars at 18- days post anthesis as influenced by Mnapplication

0 mg Mn kg−1 soil 50 mg Mn kg−1 soil

CultivarLowerleaves Stem

Flagleaf Peduncle Spike Total

Lowerleaves Stem

Flagleaf Peduncle Spike Total

PBW509

4.01 1.90 2.10 1.47 6.50 15.98 4.67 4.10 3.03 2.13 14.77 28.7

DBW 17 2.70 2.00 1.60 0.93 3.76 10.99 3.00 4.30 2.47 1.63 12.40 23.8PDW

2913.27 2.60 2.30 1.40 2.33 11.90 6.23 4.43 3.20 2.27 9.60 25.73

PBW550

3.20 2.33 2.13 1.50 6.80 15.96 4.50 3.03 2.70 2.17 11.87 24.27

TL 2908 4.73 4.07 2.77 1.90 6.64 20.11 5.40 4.77 2.87 2.1 10.37 25.51PBW

6363.73 2.27 2.00 1.57 5.53 15.1 4.47 3.30 2.80 2.07 9.03 21.67

CD(5%)

Mn application = 0.08, cultivars = 0.14, Mn application x cultivars = 0.20

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TA

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TABLE 5 Manganese uptake (µg pot−1) of six wheat cultivars at anthesis as influenced by Mnapplication

0 mg Mn kg−1 soil 50 mg Mn kg−1 soil

CultivarLowerleaves Stem

Flagleaf Peduncle Spike Total

Lowerleaves Stem

Flagleaf Peduncle Spike Total

PBW509

17.7 4.1 6.5 2.9 7.2 38.4 56.7 22.7 40.5 16.0 78.2 214

DBW 17 9.2 3.9 3.5 1.3 8.1 26 64.1 17.2 31.6 11.2 94.7 219PDW

29110.4 3.2 1.6 1.4 1.8 18.4 107 37.3 53.3 15.7 37.4 251

PBW550

16.6 5.7 7.3 2.6 10.6 42.8 93.3 25.3 49.2 33.6 98.8 300

TL 2908 25.8 6.8 5.0 3.4 7.5 48.5 97.7 24.3 30.4 18.9 61.2 232PBW

63621.0 6.2 5.8 0.76 5.0 38.8 103 38.9 32.5 18.7 39.8 233

CD(5%)

Mn application = 0.8, cultivars = 1.3, Mn application x cultivars = 1.9

Total uptake increased for all cultivars throughout the experiment forboth treatments. At anthesis (Table 5), lower leaves were the largest pool ofMn for each cultivar in Mn deficient plants. Spike uptake ranged from 1.8to 10.6 µg for cultivar ‘PDW 291’ to ‘PBW 550’, respectively. Wheat cultivars‘DBW 17’ and ‘PBW 550’ accumulated higher proportion of total uptakein the spike (31.2% and 24.8%, respectively). Wheat cultivar ‘PDW 291’retained highest proportion in its lower leaves (56.5%) and lowest in spikes(9.8%). At 18 days post-anthesis (Table 6), under Mn deficiency conditions,cultivar ‘PDW 291’ retained highest proportion of Mn in the lower leaves

TABLE 6 Manganese uptake (µg pot−1) of six wheat cultivars at 18 days post-anthesis as influenced byMn application

0 mg Mn kg−1 soil 50 mg Mn kg−1 soil

CultivarLowerleaves Stem

Flagleaf Peduncle Spike Total

Lowerleaves Stem

Flagleaf Peduncle Spike Total

PBW509

37.5 9.3 19.3 5.4 54.2 126 67.7 17.2 18.2 7.4 245 356

DBW 17 17.8 5.8 18.6 3.1 31.0 76 51.8 23.2 27.4 9.4 212 324PDW291

25 12.8 9.9 6.4 11.8 66 117 21.6 25.6 22.0 207 393

PBW550

21.8 8.1 13.4 5.6 61.8 111 111 13.8 27.4 10.3 319 482

TL 2908 28.9 16.9 13.3 8.4 58.1 126 84.8 28.0 24.7 10.6 277 425PBW636

34.0 8.0 11.6 6.4 43.1 103 96.3 18.6 43.0 11.7 223 393

CD(5%)

Mn application = 1.6, cultivars = 2.7, Mn application x cultivars = 3.8

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Manganese Partitioning in Different Wheat Species 1777

(38%). Manganese partitioning in stem and peduncle was also higher in thiscultivar. All the cultivars recorded increased Mn uptake in the spikes. Spikesbecame the largest pool of Mn in all cultivars (except ‘PDW 291’ under Mndeficiency) for the both treatments. Under Mn deficiency, Mn partitioningin the spike was 56% of total Mn uptake for cultivar ‘PBW 550’ and only18% for ‘PDW 291’. At maturity (Table 7), highest grain Mn partitioningof 51% was recorded for ‘PBW 550’ and only 16% for cultivar ‘PDW 291’.All the Mn treated cultivars recorded reduction of Mn uptake in stem andpeduncle compared to anthesis. With time, cultivar ‘PBW 550’ recorded thelowest uptake in lower leaves, flag leaf, and peduncle altogether under Mndeficiency, and cultivar ‘DBW 17’ recorded lesser retention in lower leavescompared to ‘PBW 509’. Considering chaff partitioning, cultivar ‘TL 2908’recorded highest retention in chaff among cultivars for both treatments.

DISCUSSION

At anthesis, lower leaves were the largest pool of Mn in all the culti-vars under Mn deficiency (Table 5). This can be explained by binding ofMn+2 to the xylem walls in case of acute Mn deficiency in them (Pearsonet al., 1999). However in Mn applied plants, spikes became the largest poolof Mn for cultivars ‘PBW 509’, ‘DBW 17’, and ‘PBW 550’, suggesting theirhigher translocation ability of Mn to spikes. It was also true for these threecultivars under Mn deficiency as proportion retained in spikes was compara-tively higher in them. Compared to other cultivars, proportionate retentionin lower leaves was highest in ‘PDW 291’ at 18- days post-anthesis onwardsin both Mn treatments which can be explained by higher internal require-ment in durum cultivar (Sadana et al., 2002), ultimately resulting in poorpartitioning of Mn to its spike. In Mn treated plants, loss of Mn from flagleaf at 18- days post-anthesis can be explained by its closer proximity tospikes.

At maturity, under deficiency there was mobilization of Mn from pe-duncle, flag leaf (except ‘PBW 636’) and lower leaves and stem (except‘PDW 291’), for all the cultivars. However, the magnitude of mobilizationwas higher in cultivar ‘PBW 550’ leading to higher partitioning to grain.On the other hand, partitioning in the lower leaves, stem and pedunclewas higher in cultivar ‘PDW 291’ towards maturity (Table 7) in both Mntreatments leading to inferior partitioning to the grain. Loss of Mn fromstem and peduncle was observed for Mn treated plants also compared toanthesis. The same trend has been observed by Pearson and Rengel (1994).All the Mn treated cultivars at maturity recorded accumulation of Mn inlower leaves and flag leaf compared to 18 days post-anthesis which can beexplained possibly by negative feedback regulation to save the grains fromreaching toxic levels (Pearson et al., 1999). In contrast to Mn, Zn seems to

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TA

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Man

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27.8

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77.2

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20.0

28.8

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149

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14.3

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66.4

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118

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Manganese Partitioning in Different Wheat Species 1779

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

TL 2908 PDW 291 PBW 509 PBW 636 PBW 550 DBW 17

10Χ

Mn

u�liz

a�on

effi

cien

cy (g

μg-

1)

Wheat cul�vars

FIGURE 1 Manganese utilization efficiency of six wheat cultivars calculated for maturity stage.

be more mobile (Marschner, 1995). In wheat, good transport of Zn fromstem and leaves to developing grains (Pearson et al., 1996), as well as fromolder leaves to younger leaves (Page and Feller, 2005) has been recorded,indicating its superior phloem transport than Mn.

The Mn utilization efficiency [(grain weight)(total Mn content)−1] atmaturity is a measure of the efficiency with which Mn is converted into grains.Durum and triticale species were found to be less Mn efficient than breadwheat cultivars on this basis (Figure 1) depicting higher internal requirementfor durum and triticale wheat species.

CONCLUSIONS

The findings suggest that bread wheat cultivars are more Mn efficientthan triticale and durum wheat cultivar based on differential Mn partitioningto grain resulting from higher mobilization from vegetative organs coupledwith higher Mn utilization efficiency. Identification of cultivars/species pro-moting superior Mn partioning to grain resulting in higher production onMn deficit soils can provide viable alternative to soil or foliar application ofMn. Moreover, by application of breeding techniques we can transfer theseMn efficiency traits to other cultivars.

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1780 A. Shankar et al.

FUNDING

The financial assistance by the Indian Council of Agricultural Research,New Delhi through its Junior Research Fellowship to the first author is greatlyacknowledged.

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