Zinc Biofortified Wheat Cultivar Lessens Grain Cadmium Accumulation under Cadmium Contaminated Conditions

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1 INTERNATIONAL JOURNAL OF AGRICULTURE & BIOLOGY ISSN Print: ; ISSN Online: /201x/ DOI: /IJAB/ Full Length Article Zinc Biofortified Whet Cultivr Lessens Grin Cdmium Accumultion under Cdmium Contminted Conditions Muhmmd Ishfq 1, Aysh Kirn 2*, Arif Khliq 1, Srdr Alm Cheem 3, Ibrhim A. Alridh 4, Noki Hirotsu 5,6 nd Abdul Wkeel 1* 1 Institute of Soil nd Environmentl Sciences, University of Agriculture, Fislbd-38040, Pkistn 2 Deprtment of Botny, University of Agriculture, Fislbd-38040, Pkistn 3 Deprtment of Agronomy, University of Agriculture, Fislbd-38040, Pkistn 4 Deprtment of Botny nd Microbiology, College of Science, King Sud University, Riydh 2455, Sudi Arbi 5 Fculty of Life Sciences, Toyo University, Gunm Jpn 6 Centre for Crop Helth, University of Southern Queenslnd, Toowoomb, QLD 4350, Austrli * For correspondence: bdul.wkeel@uf.edu.pk; ysh.kirn@uf.edu.pk Abstrct Zinc (Zn) efficient whet genotypes hve been developed to enhnce grin Zn concentrtion to combt the Zn mlnutrition in humns. However, such biofortified genotypes/cultivrs my lso tke up the toxic metls from hevy-metls contminted soils due to similrities with Zn uptke nd trnsport mechnisms in plnts. This study ws designed to explore uptke of ubiquitous toxic metl i.e., cdmium (Cd) by Zn-efficient (Zincol-2016) nd ws compred with Zn-inefficient (Fislbd-2008) whet cultivr. Both whet cultivrs were sown in pots till mturity in Zn nd Cd mended soil. Growth nd yield response, nd dissemintion of Cd nd Zn, in roots, shoot nd grins were observed. Significnt differences in Zn nd Cd concentrtion in root, shoot nd grin were found mong both cultivrs in response of Zn nd Cd ppliction. Zincol-2016 ws more efficient cultivr for Zn uptke compred to the Fislbd Cd uptke ws incresed by both cultivrs nd suppressed plnt growth in Cd contminted soil. However, Zn ppliction in Cd contminted soil significntly diminished the Cd uptke nd vice vers. Interestingly, Cd concentrtion ws higher in root of Zincol-2016 s compred to Fislbd-2008; similr ws the cse in shoot of both cultivrs, while it ws lower in grin of Zincol In conclusion, Zn efficient cultivr not only produces high Zn grins but lso hs bility to contin Cd in root nd shoot reducing its ccumultion in grins. Furthermore, Zn fertiliztion in Cd contminted soils cn decrese Cd uptke by plnts nd my be used s n meliorting strtegy to grow whet in Cd contminted soils Friends Science Publishers Keywords: Biofortifiction; Cdmium; Hevy metl; Triticum estivum; Zinc Introduction Zinc (Zn) plys substntil prt in photosynthesis, ctlytic nd structurl ctivities, protein synthesis, bio-membrne stbility, energy trnsfer rections nd DNA repliction in plnts (Allowy, 2004; Hjibolnd nd Amirzd, 2010). It lso improves the concentrtion of ntioxidnt enzymes nd chlorophyll contents in plnt tissues. Furthermore, it encompsses s cofctor for the stimultion of more thn 300 enzymes nd plys vitl role in wter uptke nd trnsport decresing the ntgonistic effect of slt nd het stresses (McCll et l., 2000; Ksim, 2007; Sbrti et l., 2011). Zn is lso essentilly required by humns nd pproximtely 17.3% people world-wide suffer from Zn deficiency (Wessells nd Brown, 2012). Zn deficiency in soils correltes with humn Zn deficiency (Joy et l., 2017) nd numerous fctors hve been reported for Zn deficiencies in soils including high cly content, high ph nd soil clcreousness (Ashrf et l., 2008). Different pproches, for exmple Zn supplementtion, food fortifiction nd dietry diversifiction, re dopted to improve Zn deficiency in humns. However, these re prcticlly nd economiclly less fesible in the developing countries (Bouis et l., 2000). Therefore, Zn biofortified cultivrs of cerels were developed by HrvestPlus to fulfill the Zn scrcity in the food (Andersson et l., 2017), by incresing its Zn uptke efficiency under Zn deficient soil conditions. Hevy-metls pollution in soil is prevlent globl issue (Tndy et l., 2006) nd hs been elevted s foremost environmentl issue over the lst few decdes due to metls trnsloction in the food chin is injurious to nimls nd long with humn helth. The biovilbility of hevy metls in soils rely on their concentrtion in soil solution which in order is relint on numerous soil processes To cite this pper: Ishfq, M., A. Kirn, A. Khliq, S.A. Cheem, I.A. Alridh, N. Hirotsu nd A. Wkeel, 201x. Zinc biofortified whet cultivr lessens grin cdmium ccumultion under cdmium contminted conditions. Int. J. Agric. Biol. 00:

2 Ishfq et l. / Int. J. Agric. Biol., Vol. 00, No. 0, 201x such s specific dsorption, ction exchnge complextion nd precipittion s well s the uptke efficiency of crop plnts (Bst et l., 2005; Crrillo González et l., 2006). It is pprehended tht cultivrs efficient for Zn uptke my enhnce the cdmium (Cd) uptke s well in contminted soils. Cdmium is toxic metl pollutnt nd cuse considerble toxicity to plnts t even t low concentrtion. It is lso deliberted s highly detrimentl to humn, s once it ccumultes in the body remins there for longer period of time. Compounds of Cd re comprtively more soluble thn mny other metls. Therefore, it cn certinly become the prt of food chin when existing in griculturl soils (Simmons et l., 2003). Zn nd Cd interct with ech other in the soil, during uptke by plnt from roots nd its trnsloction to upper edible portion becuse of similr geochemicl properties (Ds et l., 1997). Oxidtive dmge due to Cd is esed by Zn, which decreses membrne nd metbolic dmges by decresing uptke trnsloction of Cd to edible prts (Srwr et l., 2010). Although ionic rdii of Cd nd Zn re dissimilr, they hve equivlent electro-negtivities (Abdel-Sbour et l., 1988); therefore their ntgonistic effect cn be perceived. Zn efficient crop plnts my lso be efficient for Cd nd cn ccumulte it in edible prts cusing toxicity to the consumers (Adrino, 2001). As Zn competes with Cd for plnt uptke, therefore it ws hypothesized tht Zn efficient cultivr my lso tke up Cd efficiently in Cd contminted soils. The objectives of proposed study were to explore i) Cd uptke nd leding to its ccumultion in grins by Zn efficient whet cultivr in Cd contminted soils ii) ppliction of Zn fertilizer in Cd contminted soils reduce the Cd uptke by plnts. Mterils nd Methods Experimentl Detils nd Tretments This study ws conducted in plstic pots (ech contining 4.5 kg soil) in green-house t Institute of Soil nd Environmentl Sciences, University of Agriculture, Fislbd-38040, Pkistn in winter seson. Bsic nlysis of soil for EC e, ph, texture, Zn nd Cd concentrtion is presented in Tble 1. The tretments comprised of control (soil without Zn or Cd ppliction), Zn mended soil (10 mg kg -1 soil), Cd mended soil (10 mg kg -1 soil), Zn plus Cd mended soil (10 mg kg -1 soil ech). Source of Zn, nd Cd were zinc sulfte hepthydrte (ZnSO 4. 7H 2O) nd cdmium chloride dihydrte (CdCl 2. 2H 2O), respectively. Whet (Triticum estivum L.) cultivrs Zincol-2016 (Zn efficient) nd Fislbd-2008 (Zn inefficient) were used s test mteril. All the tretments were rrnged ccording to completely rndomized fctoril design with replicted four times. The seeds of Fislbd-2008 were obtined from Ayub Agriculture Reserch Institute (AARI), Fislbd, Pkistn nd Zincol-2016 from HrvestPlus Islmbd, Pkistn. Tble 1: Physicochemicl chrcteristics of the soil used in the experiment Prmeter Unit Vlue ph EC e ds m Snd, Silt, Cly b % 53, 24, 23 Texturl clss c --- Sndy Lom Zn d mg kg Cd d mg kg Mesured in 1:1 soil to wter b. Hydrometer method (Pge et l., 1982) c. USDA clssifiction d. AB-DTPA extrctble (Soltnpour nd Workmn, 1979) Crop Husbndry nd Hrvesting Recommended dose of nutrients N, P 2O 5 nd K 2O t the rte of 115, 80 nd 60 kg h -1 were pplied s ure, triple super phosphte nd sulphte of potsh, respectively. Recommended dose of fertilizers were pplied t the time of sowing s well s soil ws contminted t the sme time. Crop ws irrigted ccording to its wter requirement t 60% of wter holding cpcity of soil. In ech pot (contining 4.5 kg soil) primrily eight seeds were sown on 22 November 2015 nd four plnts were hrvested from ech pot fter two months of sowing (before the booting stge). Remining four plnts were hrvested t mturity. Plnt growth ttributes i.e. plnt height, shoot nd root fresh nd dry weight were considered from first hrvesting while yield prmeters i.e. spike length, grin yield s well s Zn nd Cd from root, shoot nd grin were determined from second hrvesting. Hrvest index (HI) ws clculted ccording to following formul: Hrvest Index (%) = Determintion of Zn nd Cd Grin yield Biologicl yield 100 To determine Zn nd Cd concentrtion in the root, shoot nd grin, fine ground root, shoot nd grin mteril ws digested in di-cid mixture (HNO 3:HClO 4 t 2:1) t 250±5 C. Dense white fumes of perchloric cid ppered in the tubes, nd digestion continued for 30 min more. Then fter smples were diluted with distilled wter up to 25 ml volume nd filtered using Whtmn 42 filter pper. Zn nd Cd concentrtions were determined using the tomic bsorption spectrophotometer (Hitchi Polrized Zeemn AAS, Z-8200, Jpn). Sttisticl Anlysis The dt collected were nlysed by sttisticl technique (Steel et l., 1997) by using Sttistix 8.1 (Anlyticl Softwre, Tllhssee, USA). Two wy nlysis of vrince (ANOVA) followed by LSD test ws used t P 0.05 for the comprison of both whet vrieties s well s tretments vrition.

3 Results Cdmium Uptke by Zinc Efficient nd Inefficient Whet Cultivrs / Int. J. Agric. Biol., Vol. 00, No. 0, 201x Tble 2: Effect of Zn nd Cd ppliction on growth nd yield of whet cultivrs Zincol-2016 (Zn efficient) nd Fislbd (Zn inefficient). Vlues re men ± stndrd error Whet cultivr Tretments Plnt height(cm) Totl biomss(g pot -1 ) Spike length(cm) Grin yield(g pot -1 ) Hrvest Index(%) Grin Zn (%) Grin Cd (%) Fislbd Plnt Growth nd Yield Control 39.9 ± 0.7d 9.57±0.4cd 5.74± ± ± ± ±4.50 Zn 41.7±0.8cd 9.97±0.3d 6.43± ±0.2cd 23.08±0.96b 36.65± ±3.35 Cd 44.4± ±0.2d 5.38±0.31c 2.23±0.5d 19.50±3.15b 34.41±4.27c 38.85±4.83 Zn+Cd 44.0±0.8d 9.47±0.7cd 6.69± ±0.2cd 23.92±0.66b 41.39± ±1.23 Zincol-2016 Control 44.6± ± ±0.53b 4.10±0.3b 28.07± ± ±1.54b Zn 51.7± ± ± ± ± ± ±2.20c Cd 46.4±1.5b 10.6±0.9d 6.06± ±0.2cd 22.86±0.81b 41.68± ±1.92 Zn+Cd 47.1±0.9 b 11.3±0.2b 6.33± ±0.3b 26.87± ±1.47b 40.21±1.67 LSD vlues: plnt height, totl biomss, spike length, grin yield, hrvest index, grin Zn (%) nd grin Cd (%) s 4.23, 1.5, 4.23, 0.95, 5.22, 7.56 nd 8.80 respectively Plnt growth nd yield were ffected significntly in both whet cultivrs in response to vrious tretments. Plnt height ws significntly (P 0.05) incresed by ppliction of Zn in Zincol-2016 but not in Fislbd Totl biomss (shoot + root + grin) ws significntly decresed under Cd contmintion in both cultivrs; however ppliction of Zn under Cd contmintion improved the totl biomss. Zinc fertiliztion in non-contminted soil incresed the totl biomss production in Zincol-2016 but not in Fislbd Spike length ws not ffected by Zn or Cd tretment, however Fislbd-2008 showed shorter spike length s compred to Zincol-2016 (Tble 2). Significnt (P 0.05) decrese in grin yield ws observed due to Cd contmintion, while Zn ppliction improved the grin yield more in Zincol-2016 s compred to Zn-inefficient Fislbd Similrly hrvest index ws significntly decresed under Cd contmintion s compre to control tretment; however ppliction of Zn under Cd contmintion improved it more in Zincol-2016 s compred to control cultivr (Tble 2). Zinc Concentrtion in Root, Shoot nd Grin Plnt smples of root, shoot nd grins were nlysed seprtely to determine the Zn distribution in different plnt prts. Incresed in Zn concentrtion ws bout 12-21% in root, shoot nd grin of Zincol-2016 s well s Fislbd-2008 under Zn mended soil compred to control (Fig. 1A, B nd C). However, Zn concentrtion in root, shoot nd grin of Zincol-2016 were higher compred to Fislbd-2008 under Zn tretment. In the presence of Cd, decrese in the Zn concentrtion in root, shoot nd grin of Zincol-2016 nd Fislbd-2008 ws observed (Fig. 1A, B nd C). However, Zn ppliction under Cd contminted soil conditions significntly (P 0.05) improved Zn concentrtion in root (~26 nd 25%), shoot (~30 nd 28%) nd grin (~28 nd 26%) of Zincol-2016 nd Fislbd-2008 respectively, compred to Cd contminted soil. Fig. 1: Zn concentrtion in root (A), shoot (B) nd grin (C) of whet cultivrs Zincol-2016 nd Fislbd Tretments re; control, Zn (10 mg kg -1 soil) ppliction, Cd (10 mg kg -1 soil) mendment, nd Zn plus Cd (10 mg kg -1 soil ech) ppliction together. Grph show the men vlues nd error brs indicte ± stndrd devitions; dissimilr letters bove brs represent significnt (p 0.05) vrition ccording to LSD (root, shoot nd grin s 2.73, 3.85 nd 3.86, respectively) Cdmium Concentrtion in Root, Shoot nd Grin Cdmium concentrtion ws higher (P 0.05) in root, shoot nd grin of both whet cultivrs, however its ccmmultion in root ws more in Zincol-2016 (~39 µg kg -1 dry mtter),

4 Cd concentrtion in grin (µg kg -1 ) Cd comcentrtion in shoot (µg kg -1 ) Cd concentrtion in root (µg kg -1 ) Ishfq et l. / Int. J. Agric. Biol., Vol. 00, No. 0, 201x while ws the highest in grins of Fislbd-2008 (~49 µg kg -1 dry mtter), wheres in shoot both cultivrs showed similr concentrtion (~37 µg kg -1 dry mtter) (Fig. 2A, B nd C). Zincol-2016 exhibited significntly lower Cd concentrtion in whet grin s compred to Fislbd-2008 in Cd contminted soils. Interesingly, ppliction of Zn fertilizer to Cd contminted soil shrply decresed Cd cncentrtion in root (~21 nd 23%), shoot (~14 nd 33%) nd grin (~24 nd 16%) of Zincol-2016 nd Fislbd-2008, respectively (Fig. 2A nd B). Discussion Micronutrient mlnutrition is criticl issue world-wide nd Zn is mong the most limiting micronutrients ffecting humn helth in vrious prts of world. Development of biofortified cultivrs with high Zn concentrtion is the results of esteemed efforts of reserchers (Andersson et l., 2017). Results of present study lso reveled higher grin Zn ccumultion in Zincol-2016 thn Fislbd Plnt biomss production incresed in both whet cultivrs due to Zn fertiliztion, however better growth of Zincol-2016 ws observed in control where crop plnts hd to rely on ntive Zn concentrtion, which cn be ttributed to bility of this Zn efficient vriety to cquire more Zn (Fig. 1A, B nd C) from Zn deficient soils (Tble 1). As mny enzymtic rections re directly relted to Zn vilbility in the plnts (Tiz nd Zeiger, 2002), therefore sufficient Zn concentrtion is very criticl for optimum crop growth. In Pkistni soils, it hs lredy been reported tht Zn pplictions significntly incresed the plnt biomss (Iqbl nd Aslm, 1999), which my be due to fvourble vritions in root morphology nd physiology (Linemn et l., 1989). Furthermore, Zn fertiliztion significntly improves plnt growth in noncontminted clcreous soils due to lesser biovilbility of indigenous Zn content (Khttk et l., 2015). Reltively better response of Zincol-2016 to Zn ppliction my lso be owing to its better Zn utiliztion cpbility. Zincol-2016 showed higher Zn concentrtions in the root (35 mg kg -1 ), shoot (36 mg kg -1 ) nd grin (39 mg kg -1 ) compred to Fislbd-2008 showing more Zn ccumultion in grins (Fig. 1). This suggests tht Zincol hs better Zn trnsloction mechnisms to grins which re very crucil trit for biofortified cerels. Zinc nd Cd distribution index shows similr Zn prtitioning percentge in both cultivrs, nevertheless Cd distribution in grin is different in both cultivrs. In Fislbd-2008 Zn ppliction enhnced the Cd prtitioning in grin, while in Zincol-2016 the story ws reverse. Moreover, ppliction of Zn lso decresed the Cd portioning in grin (Tble 2). Not only in grin, Zn concentrtion in root nd shoot ws significntly improved with Zn ppliction in both whet cultivrs due to better vilbility of Zn for plnt (Joy et l., 2015). Higher Zn concentrtions in shoots is useful s niml fodder nd source of Zn for better niml helth (Fig. 1B) cd c b b c Zincol-2016 cd e Fig. 2: Cd concentrtion in shoot (A), spike (B) nd grin (C) of whet cultivrs Zincol-2016 nd Fislbd Tretments re; control, Zn (10 mg kg -1 soil) ppliction, Cd (10 mg kg -1 soil) mendment, nd Zn plus Cd (10 mg kg -1 soil ech) ppliction together. Grph show the men vlues nd error brs indicte ± stndrd devitions; dissimilr letters bove brs represent significnt (p 0.05) vrition ccording to LSD (root, shoot nd grin s 3.32, 4.88 nd 4.45 respectively) Such rise in Zn concentrtion in whet shoot by Zn fertiliztion nd its beneficil effect on niml helth hs lredy been reported (Kerm et l., 2013). Hence, Zincol hs potentil to be used s Zn biofortified cultivr for both humn nd nimls. In both cultivrs, the growth nd plnt biomss were decresed when grown with Cd, while these reductions were cncelled when grown with Zn nd Cd both. Reduction in plnt growth nd biomss production is usully deliberted s preliminry indiction of Cd toxicity on Cd contminted soil (Chen et l., 2017). Cd toxicity symptom my pper t plnt vegettive or reproductive growth phses. However, numerous plnts my ccumulte substntil concentrtion of Cd without displying remrkble visul toxicity symptoms nd yield loss, which cn led to Cd entry into e d b Fislbd-2008 Control Zn Cd Zn+Cd b c d d cd b

5 Cdmium Uptke by Zinc Efficient nd Inefficient Whet Cultivrs / Int. J. Agric. Biol., Vol. 00, No. 0, 201x food chin. Interestingly, Zn ppliction significntly reduced the Cd toxicity nd concentrtion in both cultivrs, lthough more in Zincol-2016, might be due to the suppressive influence of Zn for Cd uptke (Dlir et l., 2017; Venktchlm et l., 2017) s plnt tke up both Zn nd Cd using sme trnsport membrne proteins (Moustks et l., 2011). Zincol-2016 seems more cpble to reduce Cd concentrtion in grin in response to Zn fertiliztion, which ws not expected s per hypothesis mde for this study. Nevertheless, Zincol-2016 hd more Cd concentrtion in roots, while similr in shoot (Fig. 2A nd B). As bove mentioned, it is considered tht uptke nd trnsport of Zn nd Cd by plnts re similr (Grnt et l., 1998); however, Zincol-2016 showed different pttern of trnsporttion between Zn nd Cd from root to grin. Zincol-2016 my hve selective mechnism to ccumulte Cd in the roots nd very less trnsloction into the grins during ccumultion of Zn into the grins. This trit is beneficil to grow in Cd contminted soils with the pprehension of Cd entry into the food chin. Therefore, our hypothesis tht Zn efficient vriety lso tke up Cd efficiently is prtilly true becuse Cd concentrtion only in root ws higher in Zincol-2016, while lower in grins. Genetic vrition exists in mny crops for uptke nd ccumultion of Cd (Tvrez et l., 2015) nd Zn (Yilmz et l., 2017). Further genetic nd moleculr mechnisms of Zn nd Cd selection should be elucidted to design high Zn ccumultor without ccumultion Cd in grin, nd Zincol-2016 will be useful mteril to nlyse this. Conclusion Zincol-2016 is Zn biofortified whet cultivr, which ccumultes preferbly high Zn in grins nd it cn lso be recommended in Cd contminted soils, becuse it kept very low concentrtion of Cd in grins. Furthermore, Zn fertiliztion cn decrese Cd uptke more efficiently in Zincol-2016 under Cd contminted soil conditions. Acknowledgements The uthors cknowledge Qdir Bloch (lte) from HrvestPlus for Zincol-2016 seed nd Ayub Agriculture Reserch Institute (AARI) for providing Fislbd-2008 seed. References Abdel-Sbour, M., J. Mortvedt nd J. Kelsoe, Cdmium-zinc interctions in plnts nd extrctble cdmium nd zinc frctions in soil. Soil Sci., 145: Adrino, D.C., Arsenic. In: Trce Elements in Terrestril Environments, pp: Springer Allowy, B.J., Zinc in Soils nd Crop Nutrition. Interntionl Zinc Assocition Brussels Andersson, M.S., A. Sltzmn, P. Virk nd W. Pfeiffer, Progress updte: Crop development of biofortified stple food crops under hrvestplus. Afr. J. Food Agric. Nutr. Dev., 17: Ashrf, M., A. Rnjh, M. Yseen, N. Ahmd nd A. Hnnn, Zinc dsorption behvior of different textured clcreous soils using freundlich nd lngmuir models. Pk. J. Agric. Sci., 45: 6 10 Bst, N., J. Ryn nd R. 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6 Ishfq et l. / Int. J. Agric. Biol., Vol. 00, No. 0, 201x Steel, R.G., J.H. Torrie nd D.A. Dickey, Principles nd Procedures of Sttistics: A Biologicl Approch, pp: McGrw-Hill, Book Co. Inc., New York, USA Tiz, L. nd E. Zeiger, Plnt Physiology, 3 rd nd 5 th edition. The Benjmin Cummings Publishing Compny, Redwood City- Cliforni, USA Tndy, S., R. Schulin nd B. Nowck, The influence of edds on the uptke of hevy metls in hydroponiclly grown sunflowers. Chemosphere, 62: Tvrez, M., A. Mcri nd R.P. Snkrn, Cdmium nd zinc prtitioning nd ccumultion during grin filling in two ner isogenic lines of durum whet. Plnt Physiol. Biochem., 97: Venktchlm, P., M. Jyrj, R. Mnikndn, N. Geeth, E.R. Rene, N. Shrm nd S. Shi, Zinc oxide nnoprticles (ZnONPs) llevite hevy metl-induced toxicity in leucen leucocephl seedlings: A physiochemicl nlysis. Plnt Physiol. Biochem., 110: Wessells, K.R. nd K.H. Brown, Estimting the globl prevlence of zinc deficiency: Results bsed on zinc vilbility in ntionl food supplies nd the prevlence of stunting. PloS One, 7: e50568 Yilmz, O., G.A. Kzr, I. Ckmk nd L. Ozturk, Differences in grin zinc re not correlted with root uptke nd grin trnsloction of zinc in wild emmer nd durum whet genotypes. Plnt Soil, 411: (Received 30 June 2018; Accepted 11 August 2018)