Iodine biofortification in tomato

Transcription

1 480 DOI: /jpln J. Plnt Nutr. Soil Sci. 2011, 174, Iodine iofortifiction in tomto Mrtin Lndini 1, Silvi Gonzli 1, nd Pierdomenico Pert 1 * 1 PlntL, Scuol Superiore Snt Ann, Vi Mriscoglio 34, 56124, Pis, Itly Astrct Iodine is n essentil element in the humn diet, nd iodine deficiency is significnt helth prolem. No ttempts to increse iodine content in plnt-derived food (iofortifiction) hve so fr een prticulrly effective. We studied iodine uptke in tomto (Solnum lycopersicum L.) to evlute whether it is possile to increse the iodine concentrtion in its fruits. Iodine trnsloction nd storge inside tomto tissues were studied using rdioctive iodine. Potssium iodide ws lso supplied t different concentrtions to tomto plnts to evlute the resulting iodide concentrtion oth in the vegettive tissues nd the fruits. The results indicte tht iodine ws tken up etter when supplied to the roots using hydroponiclly grown plnts. However, considerle mount of iodine ws lso stored fter lef tretment, suggesting tht iodine trnsport through phloem lso occurred. We found tht tomto plnts cn tolerte high levels of iodine, stored oth in the vegettive tissues nd fruits t concentrtions tht re more thn sufficient for the humn diet. We conclude tht tomto is n excellent crop for iodine-iofortifiction progrms. Key words: iofortifiction / iodine deficiency / phytotoxicity / Solnum lycopersicum Accepted Mrch 14, Introduction Iodine is n essentil element for humn physiology (Andersson et l., 2005), eing involved in the synthesis of thyroid hormones. The recommended dietry llownce (RDA) for dults mounts to 150 lg iodine per dy (Perce et l., 2004). Chronic iodine deficiency, clled hypothyroidism, cn trigger goiter, growth impirment, reproductive filure, hering loss, cretinism, nd severl kinds of rin dmge (Andersson et l., 2005; Delnge, 2000; Dillon nd Milliez, 2000; Hddow et l., 1999). Although iodine deficiency cn e treted, it is still pulic helth prolem for lmost 35% of the world s popultion (Perce et l., 2004; Winger et l., 2008), nd the popultion t risk is more thn one illion (Winger et l., 2008; World Helth Orgniztion, 2004). Iodized slt is the most common pproch for dietry iodine supplementtion (Andersson et l., 2005; Delnge nd Lecomte, 2000). However, since iodine supplementtion my cuse prolems during food processing, it is difficult to control its loss during trnsport, storge, nd food cooking (Winger et l., 2008). Therefore, enhncing iodine content in vegetles represents cost-effective wy to control its deficiency, since iodine in food is redily ioville (up to 99%) nd ssimilted (Di et l., 2004; Weng et l., 2009; White nd Brodley, 2009). Despite its importnce for humn nutrition, iodine relevnce hs not yet een estlished for plnts. Vegetles cn ccumulte iodine, nd incresing iodine ppliction to the soil results in enhncing iodine ccumultion in plnts (Di et l., 2004; Whitehed, 1973; Zhu et l., 2003), s it ws demonstrted for pkchoi, celery, pepper, rdish (Hong et l., 2008), cge (Weng et l., 2008), nd spinch (Zhu et l., 2003). However, results re lrgely ffected y the iodine concentrtion nd the chemicl form supplied (Blsco et l., 2008; Di et l., 2004; Mckowik nd Grossl, 1999) nd y the growth sustrte used (Weng et l., 2008c). Iodide, rther thn iodte, hs the gretest iovilility for plnts (Umly nd Poel, 1971; Whitehed, 1973), nd very low concentrtions of iodine, regrdless to the form, re eneficil to severl crops (Borst-Puwels, 1961). In tomto plnts, very low mount of iodide cn stimulte the tngentil growth nd, to some extent, improve the yield (Lehr et l., 1958). However, t higher concentrtions, iodine cn e toxic, leding to lef dmges, stunted growth, nd deth (Lehr et l., 1958). Once inside the plnt, xylem flux of iodine seems to e lrgely predominnt (Lewis nd Powers, 1941; Shinong et l., 2001; Weng et l., 2008c, 2009; Whitehed, 1973), ut, generlly, the sored iodine is not uniformly distriuted mong plnt tissues, rnking s follows: root > lef > stem (Weng et l., 2008). Finlly, further spect, which needs explntion, is whether iodine uptke could e ffected y other nutrients. A negtive correltion etween nitrte nd hlogens hs een speculted for rdish, lettuce, nd cge (Roord vn Eysing nd Spn, 1985; Shepprd nd Evenden, 1992; Weng et l., 2008). Recent studies demonstrted tht lefy vegetles such s spinch (Zhu et l., 2003; Di et l., 2006) or lettuce (Blsco et l., 2008; Voogt et l., 2010) cn store iodine in their edile tissues, mking them good cndidtes for iodine iofortifiction progrms. The im of the present work is to evlute the ility of tomto plnts to sor nd store iodine in vegettive tissues nd fruits. Due to its widespred distriution nd * Correspondence: Dr. P. Pert; e-mil: pierdomenico.pert@sssup.it

2 J. Plnt Nutr. Soil Sci. 2011, 174, Tomto iodine iofortifiction 481 its esy growth on commercil scle, tomto would represent preferred crop in iofortifiction progrms. Moreover, the possiility of fresh consumption of its fruits prevents the risk of iodine loss with certin cooking methods. To chieve our gols, rdioctive iodine ( 125 I s NI) ws used for visulizing iodine distriution nd storge inside plnt tissues, while potssium iodide (KI) ws supplied to study iodine toxicity nd the overll mount stored in tomto fruits. Different kinds of tretments s well s different growth sustrtes were compred to set up the est experimentl conditions for enhncing iodine concentrtion in fruits of this species. 2 Mterils nd methods 2.1 Plnt mteril All the experiments were crried out using tomto (Solnum lycopersicum L. cv. MicroTom). Tomto seeds were sown on wet filter pper under continuous light until germintion. When the cotyledons were well expnded, the plnts were trnsplnted into soil or trnsferred into hydroponic system. This ltter ws sed on thick grvel (3 5 mm in dimeter) nd nutrient solution whose composition ws s follows (in mm): NO 3 -N 12; NH 4 -N 0.5; P 1.30; K 8; C 4; Mg 1.19; N 9; SO 4 -S 1.59; Cl 9.87; (in lm): Fe 19.5; B 28.6; Cu 3.6; Zn 4.5; Mn 10.9; Mo 0.2. Electricl conductivity (EC) ws 2.84 ds m 1, nd ph 5.8. Fresh solution ws dded weekly. Plnts grown in soil (Hwit Flor, Vecht, Germny) were wtered twice week. All plnts were grown in plstic pots (dimeter 5 cm) in growth chmer, with 80 lmol m 2 s 1 PAR (Gro- Lux, Sylvni, OH, USA), 12 h light photoperiod, 24 C temperture, 55% reltive humidity. 2.2 Regents nd chemicls Potssium iodide ws purchsed from Sigm-Aldrich (St Louis, MO, USA), while the rdioctive iodine ( 125 I s NI) from Perkin Elmer (Wlthm, MA, USA). 2.3 Iodine-uptke experiments Tomto plnts, grown in hydroponics or soil, were treted with rdioctive iodine strting t the ge of: (1) 2 weeks, (2) 1 month, or (3) 2 months fter germintion. Iodine ws supplied s root or lef tretment, nd in oth the experiments, totl of three iodine-feeding tretments were performed, t 2-dy intervls. In the root-tretment experiments, the iodine stock solution (N 125 I, 10 lci ml 1 ) ws diluted to the finl ctivity of 0.25 lci ml 1, nd 1 ml ws supplied directly to the grvel of the hydroponic system or to the soil of ech treted plnt. At the end of the experiment, fter the three feeding tretments, totl mount of 0.75 lci iodine ws supplied per plnt. In the lef-tretment experiments, 25 ll of rdioctive iodine (N 125 I, 10 lci ml 1 ) were spotted on lef lde. The first true lef or well expnded lef t the second rnch ws treted in 2-week-old or 1-/2-month-old plnts, respectively. Also in this cse, three iodine-feeding tretments were performed, for totl mount of iodine supplied per plnt equl to 0.75 lci. Ech experiment ws replicted three times. 2.4 Nitrte experiment Two groups of 2-week- nd 2-month-old tomto plnts grown in hydroponics were treted with rdioctive iodine (N 125 I, 0.25 lci ml 1 ). Strting from the eginning of the iodine tretment, one set of oth 2-week- nd 2-month-old plnts ws mintined in the usul complete hydroponic solution, while nother identicl set ws grown in modified nutrient solution in which the nitrte concentrtion ws diluted 1:10 (reching finl concentrtion of 1.2 mm nitrte). Three root iodine feeding tretments (1 ml for ech tretment) were crried out, t 2-dy intervls, for totl mount of iodine supplied per plnt equl to 0.75 lci. Ech experiment ws replicted three times. 2.5 Visuliztion of rdioctive-iodine uptke At the end of ech experiment, oth lef- nd root-treted plnts were cut t the hypocotyl level, gently wshed, lotted onto filter pper, nd then exposed for 2 d to multipurpose phosphor storge screen (Cyclone Storge Phosphor System, Pckrd, CT, USA) in order to otin digitl imge of the rdioctivity distriution. For the lef tretment, ech N 125 I-treted lef ws removed from the originl plnt nd exposed on seprte screen. When possile, sepls nd fruits from ech tretment were collected t the end of the experiment. s were cut into severl longitudinl sections in order to disply where iodine ws stored. All the digitl imges were otined nd nlyzed using phosphoimger (Cyclone Storge Phosphor System, Pckrd). Dt re presented s DLUs (digitl light units), nd the scnned imges re shown using flse colors, where red nd lue indicte high or low level of rdioctivity, respectively. 2.6 Iodine toxicity To investigte the effects of iodine on tomto plnt physiology nd fruit production, dose-response experiment ws crried out. Plnts t the flowering stge (out 45 d old) nd grown in hydroponics were treted. Different concentrtions of KI (0, 5, 10, 20 mm), dded to the hydroponic solution, were tested, nd three tretments (once week) were crried out. During this period, the plnts were oserved nd photogrphed. Twenty-four dys fter the eginning of the tretment, ll the plnts were collected to nlyze the iodine content. s were smpled t the mture green stge for ll the iodine tretments nd lso t the red ripe stge for the 5 mm KI tretment, nd nlyzed seprtely. Three replictes were nlyzed for ech tretment. 2.7 Iodine mesurements The iodine content inside plnt vegettive tissues nd fruits ws mesured using the inductively coupled plsm mss spectrometry (ICP-MS) technique (Yoshid et l., 2007). Iodine ws determined using n isotope dilution with 127 I. The iodine concentrtion in the smples ws evluted using clirtion curve otined with the stndrd dditions method. Three replictes were nlyzed for ech tretment. Anlyses were crried out y Neotron Sp (Moden, Itly).

3 482 Lndini, Gonzli, Pert J. Plnt Nutr. Soil Sci. 2011, 174, Results 3.1 Iodine uptke in tomto plnts: storge nd distriution Root tretment Plntge 2weeks 1 month 2 months Plnts t different developmentl stges were root- or leftreted with rdioctive iodine. After the tretment, iodine ws clerly detectle in ll the treted plnts (Fig. 1). Regrdless of the plnt ge, the mount of iodine ccumulted fter the root tretment ws higher thn tht stored in lef-treted plnts (Fig. 1). Two-week-old plnts ccumulted more iodine thn the older ones, oth fter root nd lef tretment (Fig. 1). In the youngest plnts, especilly in the roottreted ones, iodine ws widely distriuted in the eril prts, eing strongly ccumulted oth in the stem nd in the leves (Fig. 1). In dult plnts, iodine ws prevlently stored in the stem nd in the min veins of the leves (Fig. 1). In 2- month-old plnts, iodine ws ccumulted not only in vegettive orgns ut lso, lthough t lower levels, in fruits (Fig. 1). When plnts were grown in soil, the mount of rdioctive iodine ccumulted fter root tretment ws drmticlly lower, oth in young nd dult plnts (Fig. 2, ). 3.2 Iodine uptke nd nitrte Lef tretment Low High Sep. Sep. Nitrte my interfere with iodine uptke (Roord vn Eysing nd Spn, 1985). For this reson, n experiment ws performed to compre iodine uptke nd ccumultion in plnts in the presence of different nitrte concentrtions. Young nd dult tomto plnts, previously grown in full-strength hydroponic solution, were treted with iodine in the presence of high (12 mm) or low (1.2 mm) nitrte concentrtion. The ltter ws modified only t the eginning of the iodine tretment to void tht plnt root rchitecture nd growth were influenced y different nitrte levels. The results show tht when plnts were mintined in the presence of low nitrte, iodine uptke nd ccumultion were negtively ffected (Fig. 3 c). This ws prticulrly evident in 2-week-old plnts (Fig. 3, c), ut lso in plnts t the reproductive stge the finl iodine levels detected in the presence of low nitrte were lower (Fig. 3, c). The reduction in iodine ccumultion of plnts treted with low nitrte concentrtion ws more evident in the vegettive rther thn reproductive orgns (Fig. 3, ). 3.3 Phytotoxic effects of iodine Figure 1: () Iodine root nd lef tretment on 2-week-, 1-month-, nd 2-month-old MicroTom hydroponiclly grown tomto plnts. Iodine ws supplied s N 125 I, nd three tretments were performed t 2-dy intervls. A representtive plnt for ech condition is shown. In the lef tretment, ech single treted lef is shown esides the corresponding plnt. Arrows indicte the position of the treted lef tht ws removed from the plnt fter the tretment. In 2-month-old plnts, sepls (referred s Sep.) nd fruits were exposed seprtely. Blue/red colors indicte low/high iodine content, respectively. () Histogrms showing the iodine mount tken up y tomto plnts t the different developmentl stges fter eing root- or lef-treted. Vlues re expressed s DLU (Digitl Light Unit) mm 2. Dt re mens of three replictes ± SD. In order to detect possile phytotoxic effects nd consequences for fruit production, n iodine dose response experiment ws crried out supplying KI t incresing concentrtions (0, 5, 10, 20 mm) to plnts t the flowering stge. After 3 weeks of iodine tretments, ll the plnts survived nd produced fruits (dt not shown), ut those treted with iodine showed symptoms of phytotoxicity (Fig. 4). The min physiologicl effects oserved were lef chlorosis nd urns, minly locted t the tips of the leves nd ecoming more evident when the iodine concentrtion incresed (Fig. 4). Toxicity symptoms initilly ppered on the lower leves nd moved grdully towrds the upper prts of the plnt. Generlly, the lowest rnches were those mostly injured nd discolored quickly, ecoming rownish nd, finlly, turning necrotic. At the highest iodine concentrtions (10 20 mm), tomto rnches showed strong epinsty in comprison to the control plnts nd the lef edges were down-curved (Fig. 4). Another effect ws the presence of smll white spots on the dxil lef surfce (Fig. 4c). This ws lso oserved for the lowest iodide concentrtion pplied (5 mm) nd generlly incresed with the iodide concentrtion, grdully moving

4 J. Plnt Nutr. Soil Sci. 2011, 174, Tomto iodine iofortifiction 483 Plnt ge 2weeks 1 month 12mM NO 3 1.2mM NO 3 2-week-old 2-month-old 2-week-old 2-month-old Root tretment -Hydroponics Root tretment -Soil Low High Sep. Low Sep. High c Figure 2: () Iodine root tretment of 2-week- nd 1-month-old tomto plnts grown in solution culture or in soil. Iodine ws supplied s N 125 I, nd three tretments were performed t 2 d intervls. A representtive plnt for ech condition is shown. Blue/red colors indicte low/high iodine content, respectively. () Histogrms showing the iodine mount tken up y tomto plnts t the two different developmentl stges nd grown on the two different sustrtes. Vlues re expressed s DLU (Digitl Light Unit) mm 2. Dt re mens of three replictes ± SD. towrds the upper leves. A difference in color ws oserved etween the iodide-treted plnts nd the control ones, the former leves eing drker green (Fig. 4d). This effect ws evident prticulrly for the lowest concentrtions used (5 10 mm). A slight nthocynin ccumultion ws oserved in the stem nd long the min veins of the iodine-treted leves (dt not shown). However, no phytotoxic effects were oserved in fruits nd flowers (Fig. 4e, f), prt from some white spots on few fruits treted with 10 mm KI, similr to those oserved on leves (Fig. 4e). Regrdless to the iodine concentrtion supplied, flowers nd fruits grew nd developed normlly (Fig. 4e, f). 3.4 Iodide concentrtion in tomto vegettive tissues nd fruits Plnts treted with KI in the dose-response experiment were collected t the end of the tretment nd nlyzed for their Figure 3: Iodine root tretment of 2-week- or 2-month-old plnts concomitntly fed with high (12 mm, ) or low (1.2 mm, ) nitrte. Iodine ws supplied s N 125 I directly in the growth medium, nd three tretments were performed t 2 d intervls. A representtive plnt for ech condition is shown. In 2-month-old plnts, sepls (referred s Sep.) nd fruits were exposed seprtely. Blue/red colors refer to low/high iodine content, respectively. (c) Histogrms showing the mount of iodine tken up y 2-week- or 2-month-old plnts fter iodide tretment in the presence of the two different nitrte concentrtions. Vlues re expressed s DLU (Digitl Light Unit) mm 2. Dt re mens of three replictes ± SD. iodine concentrtion in vegettive tissues nd fruits. High concentrtions of iodine were found in leves nd stems (Fig. 5). The iodine concentrtion incresed in proportion to its concentrtion in the hydroponic medium (Fig. 5). The highest vlue (pproximtely 9000 mg [kg FW] 1 ) ws oserved in plnts treted with 20 mm iodide (Fig. 5). However, lso t concentrtions of 5 nd 10 mm, the iodine concentrtion ws very high, pproximtely 3000 nd 5000 mg (kg FW) 1, respectively (Fig. 5). Green fruits contined lower levels of iodine, reching the mximum concentrtion (30 mg [kg FW] 1 ) in plnts treted with 20 mm KI (Fig. 5). At the lowest concentrtion supplied (5 mm), the iodine content in fruits ws still high enough (10 mg [kg FW] 1 ) to fulfill the gol of iofortifiction progrm (Fig. 5). Tomto fruits treted with 5 mm KI were lso collected t the red ripe stge nd nlyzed. Red fruits showed the sme iodine concentrtion s green fruits (Fig. 5). 4 Discussion Most of the ttempts to develop iodine iofortifiction of crops hve filed, prticulrly those imed t incresing iodine con-

5 484 Lndini, Gonzli, Pert J. Plnt Nutr. Soil Sci. 2011, 174, c d e f mg kg 1 (FW) mg kg 1 (FW) KI control 5mM 10mM 20mM Figure 4: Effects of iodine on tomto plnts fter tretment with different KI concentrtions. For ech concentrtion, three different tretments (once week) were pplied. Pictures in the first column show the sence of phytotoxicity symptoms in untreted plnts, in comprison with the min effects oserved on the leves in KItreted plnts, which re, respectively: () chlorosis nd urns; () epinsty; (c) presence of white spots; (d) drk-green color. s (e) nd flowers (f) smpled from iodine-treted plnts re not different from their reltive controls. Figure 5: Iodine concentrtions in vegettive tissues () nd fruits () of plnts treted with vrious iodine (KI) concentrtions. For ech concentrtion, three different tretments (once week) were pplied. Plnt tissues nd fruits were collected 24 d fter the eginning of the iodine tretment. Control refers to vegettive tissues or fruits smpled from KI-untreted plnts. Iodine ws mesured using the ICP-MS technique. Vlues re expressed s mg kg 1 on the sis of fresh weight (FW). Dt re mens of three replictes ± SD. centrtion in fruits (Mckowik nd Grossl, 1999). Our results otined for tomto showed tht when iodine ws supplied in the growth medium, root uptke nd xylem trnsport were highly efficient, s the element ws found widely distriuted in the shoot. Iodine ws ccumulted in the stem nd in the min veins of the leves, ut in mny cses, prticulrly in young plnts, it lso spred to cover the entire lef lde (Fig. 1). Previous results otined in cge indicted tht lso in this species iodine distriution in the shoot ws not uniform nd iodine ws stored predominntly in the min lef veins (Weng et l., 2008). Hydroponics ws more effective thn soil in promoting iodine sorption (Fig. 2, ), proly ecuse in soil iodine cn e retined y orgnic mtter, eing therefore less ville for plnt uptke. The overll mount of iodine tken up y tomto plnts ws generlly higher when iodine ws supplied to the roots rther thn onto the lef lde (Fig. 1, ). These results imply tht root tretment is most effective in terms of iodine uptke nd storge. Hydroponic culture, with iodine dded to the nutrient solution, thus, gives excellent possiility for tomto iofortifiction. A possile inhiitory effect of nitrte on hlide, prticulrly romide, uptke, s consequence of competition during plnt uptke, hs een descried (Roord vn Eysing nd Spn, 1985), lthough results re controversil (Shepprd nd Evenden, 1992). Our results show tht nitrte did not inhiit iodine uptke (Fig. 3). On the contrry, plnts concomitntly fed with iodine nd 12 mm nitrte showed higher iodine ccumultion thn plnts fed with iodine nd 1.2 mm nitrte (Fig. 3). The iodine content in fruits ws less negtively ffected y low nitrte (1.2 mm) thn in vegettive orgns (Fig. 3, ). This my suggest tht low nitrte could negtively ffect the xylem trnsport of iodine with limited effect on iodide content of fruits, which lrgely depends on the phloem trnsport (Ho et l., 1987). The possile role of phloem in iodine trnsport ws ruled out y Herrett et l. (1962) nd Mckowik nd Grossl (1999). In contrst, we found tht phloem route for iodine trnsport is present in tomto plnts. Spotting rdioctive iodide on single lef resulted in widespred distriution of iodine in ll the surrounding tissues of the shoot (Fig. 1, ). Tomto fruits re reltively isolted from the xylem strem, nd therefore, they ccumulte little mount of minerl elements tht re minly trnslocted long the trnspirtion strem (Ho et l., 1987; Mingo et l., 2003). Therefore, n dequte ccumultion of iodine inside fruits depends on phloem trnsport. The fct tht in tomto moderte phloem flux of iodine ws o-

6 J. Plnt Nutr. Soil Sci. 2011, 174, Tomto iodine iofortifiction 485 served is prticulrly noteworthy ecuse, in order to otin n effective iofortifiction strtegy in this species, it is crucil to ensure n dequte concentrtion of iodine inside fruits. Iodine tretments to plnts t the reproductive stge demonstrted tht iodine could e trnsported into fruits (Fig. 1). Plnts treted with iodine often show toxicity symptoms, with crop-specific effects. Our dt indicte tht tomto plnts, despite the presence of some phytotoxicity symptoms, tolerte reltively high concentrtions of KI (20 mm) without severe injuries (Fig. 4). Plnts treted with the lowest iodide concentrtions were drker green (Fig. 4d), suggesting slight production of ntioxidnt compounds, such s nthocynins, in response to iodine. In lettuce, iodine cn increse the mount of ntioxidnt compounds, proly interfering with the oxidtive stte of the plnt (Blsco et l., 2008). It is noteworthy, in the frmework of iodine-iofortifiction progrms, tht iodine ppliction up to 20 mm, strting from the eginning of the reproductive stge, did not importntly ffect tomto vegettive nd reproductive growth nd development. During tomto ripening, the trnsloction of nutrients from roots to fruits is higher t the green stge nd flls down in lter phses (Srivstv nd Hnd, 2005). It is resonle to ssume tht iodine could e more esily trnslocted during the erly fst growth of the fruits. The quntittive dt otined y ICP-MS showed tht huge mount of iodine ws stored in oth vegettive tissues nd in green fruits, reching the mximum concentrtion of out 9000 mg kg 1 nd 30 mg (kg FW) 1, respectively (Fig. 5, ). Even t the lowest concentrtion of KI supplied (5 mm), the iodine concentrtion in tomto fruits ws high (out 10 mg [kg FW] 1 ). The iodine concentrtion did not chnge when fruits reched the mture red stge (Fig. 5), suggesting tht, once inside the fruit, iodine concentrtion ws stle. 5 Conclusion Our results indicte tht iodine uptke nd trnsloction in tomto plnts re efficient nd led to considerle iodine ccumultion in fruits. The fruit concentrtion of iodine detected in 5 mm iodide treted plnts ws more thn enough to cover dily humn intke of 150 lg. Nitrte, t lest in the rnge which is commonly used in hydroponics, hd no negtive effect on iodine uptke, nd thus modifictions of the usul nutrient solution used to grow tomto commercil vrieties re not required. Acknowledgments We thnk Prof. A. Prdossi of the Deprtment of Crop Plnt Biology of the University of Pis, for criticl reding of the mnuscript nd useful suggestions, nd the stff of the Deprtment of Endocrinology nd Metolism t the University of Pis, who kindly supplied the rdioctive iodine. 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