Fe Requeriments of C3 and C4 Plants

8/13/2019 Fe Requeriments of C3 and C4 Plants

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Nm Phytol.(1984) 97, 000-000

IRON REQUIREMENTS O F Cg AND Q PLANTSBY G.S.S M I T H , I. S. CORNFORTH AND H.V. HENDERSON

Ruakura Soil and PlantResearch Station, Ministry of gricultureandFisheries,Private Bag, H amilton, New Zedland{Accepted 10 April 1984

S U M M A R YPlants having the C,iphotosynthet ic pathway required h igher concentrat ions of iron in thenutrient solution formaxim um growth w hen grown in sand cu ltur e th an th ose wdth the C^pathwa y. T he re were only small differences am ong species in the concentration of iron requ iredin the leavestoachieve near ma ximu m dry m atter yield. Th is suggests that C3 and C4 plantsdiffer inthe ir ability toabsorb iron from the root zone. Higher c oncen trationsofiron wererequ ired in the nu trien t solution for ma xim um g rowth of both theC3and C, plants whe n nitra te,rather than am mo nium nitrate , was the sole source of nitrogen. It seems likely that when nitratewas used, there wasadecreaseinavailabilityofirontothe plant asaresultofthe increasedalkalinity in the root zone. By contrast, the root zone was acidified w hen am mo nium nitrate wasapplied. Iro n con centrations g reater than 2 to 5 / tg Fe ml~' in the nutr ient solution red uced thedry matter yieWsofa numb erofplants grown with am mo nium nitrate as the nitrogen source ,probably because of a decrease inthe absorptionofphosphoru s by the roots .Key w ords : C3 plants , Cj p lants , i ron requirem ents , n i t rate , amm onium ni t rate , phosph orusuptake, root zone pH.

I N T R O D U C T I O NIn a recent investigation of the uptake by pasture plants grown in sand culture oftretnorgenic mycotoxins produced byPenicilliumspp. (W hitee t al.,1980). It wasobserved that C4 species readily became chlorotic. The chlorosis could not beattribu ted to the mycotoxins and was only alleviated when the plan ts were sprayedwith1 % ferrous sulphate. This responsewasunexpected because the c oncen trationof iron (3ptg Fe m l"-' as ferric citrate) in the nu trien t solution applied to the plan tswas greater than that commonly used in other sand culture experiments (Hewitt,1966).While there are many reports of plants developing iron chlorosis when grownin sand or water culture ((Hageman et aL, 1961; Hewitt, 1966; Brooking, 1976;Asher, 1977), and of differences among p lant species and cultivars in susceptib ilityto iron deficiency (Weiss, 1943; Vose, 1963; Brown tal., 1972; Marschner,Romheld Azaraba di, 1978), there app ears to have been no systematic com parisonof Cg and C^ plants. This paper examines difTerences in the iron requirements ofa num ber ofC3and C^ plan ts.

M A T E R I A L S AN D M E T H O D S


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544 G. S. SMITH et al.Table 1. Plantspecies usedin theexperiment

C3 speciesGrassesBrowntop grostis capillaris L.{A .tenuis Sibth.)Cocksfoot Dactylis glomerataL. cv. Grasslands .\panuiPerennial ryegrass Lolium perenne L. cv. Grasslands Nu[LegumesLucerne Medicago sativaL. cv. WairauRed clover TrifoUum pratenseL. cv. Grasslands TuroaWhite clover Trifohum repens L. cv. Grassland Pitau

C speciesKikuyu Pennisetum clmidestinumHochst. ex ChiouMaize Zea maysL. cv. PioneerPaspalum Paspalum dilatatumPoir. cv. Grasslands 15Sorghum Sorghum bicolor(L.) Moench

then washed with deionized water (Hewitt, 1966). Two seeds of maize andsorghum were sown per pot, while ISO seeds of all other species were sown perpot. The experiment was carried out in a glasshouse with a mean daily airtem peratu re of 22 C (IS C m in to 27 C max). M ercury -vapour lamps (PhilipsH L R G ) giving a photosy nthetically active radiation of 400 /tmolm^^ s~S wereused tO' extend the length of the day to 16 h.Treatments and nutrientsolutions

Iron was applied as ferric citrate at concentrations of 0-312, 0-6S2, 1-25, 2-5,S-0 and 10-0/


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Iron requirements of C3 and C^ plants 545Table 2. Concentration ofmacro andmicroeleinents {fig ml^^) in theammoniumnitrate{A) andnitrate-only B) nutrientsolution before application toplants

NH.,-I\N O , - NPSaM gCaN a

Macroe lementsA

133133253521819 826566

B

26526357219 82633 66

C uF e.MnM oZn

JVIacroelementsA

0-50-043-00-50-010-25

B0-50-043-00-50-010-25

me asurem ents were made on 20 ml of solution displaced from around the roots.Preliminary ex perimen ts had shown that up toSOm l of solution could be displacedhy applying deionized water to the surface of the sand before it was diluted.Statistical analysisAnalyses of variance were carried out on the variables within each speciespresented in the tables. Between species, or photosynthetic pathway group,analyses were performed on summary results calculated for each species. Therelationship between dry matter yield Yd)and iron concentration in the nutrientsolution{x),and between iron concen tration in the leaf YL)and iron con centrationin the nutrient solution (x) was approximated by an inverse polynonnial.

Ydor YL =xl{l bx cx )with parameters a, b,and c.Use of this function has advantages over ordinary quadratic polynom ials in thatit is non-negative, boun ded, has no built-in syoimetry about the optim um and hasan asymptote when c = 0. The relationship between iron concentrations in theroots and iron concentrations in the nutrient solution was described by astraight-line relationship on log transformed data.

R E S U L T SEffect of nitrogen source and plant species on pH in the root zonePlants grown on tbe ammonium nitrate-based nutrient solution reduced thepH from 6-0 to between 4-1 and 5-2, while those grown on the nitrate only basedsolution increased the pH from 6-0 to between 7-0 and 7-5 (Table 3). By contrastthere were only small differences among tbe plant species. For example, when the


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546 G. S. SMITH et alT a b l e 3 . Effect of nitrogen source and plant species on the pH in the root zone

Plant species

Cg speciesBrowntopCocksfootPerenniai n^^grassL u c e r n eRed cloverWhite c loverC4 speciesKikuyuMaizePaspalumS o r g h u m

Mean Cg grassesMean Cj l egumesMean C^ speciesLSD (5%)

NitrogenA m m o n i u m n i t r a t e

4-g4-74.44-65-24-94 -]4.44-34-14-64.94-20-3

sourceNitra te only

7.47-57-57-07-17-27 47'37'17'57-57-17-30-2

Effect on dry matter yieldsThe iron requirements of the C^ species were greater than those of the Cgplants irrespective of the nitrogen source (Figs 1, 2). For example, maximumgrowth of the C3 plants grown on the nitrate-base d solution occurred when theiron concentration in the solution ranged from 2 to /tg Fe ml~^, but for the Cjspecies, dry matter yields were still increasing with iron concentrations of up to10 /igFennl~ in the solution . Sitnilarly, when nitrogenwassuppliedasammoniumnitrate the iron requirements of the Cg and Cj plants v?ere between 1 to2-5figFe ml^^ and2 5to 3-0figFe ml '',,respectively. In general, dry matter yieldsof all plants were greater when nitrogen was provided as nitrate (Figs 1, 2).M oreover, a higher concen tration of iron in the nu trien t solution was required by-plants for maximu m growth when grown on the nitrate-based solution then on theammonium nitrate-based solution.Growth of a number of plants was also adversely afFected by iron. Dry matteryields of brownto p, cocksfoot, and to a lesser extent of kikuyu, m aize, ryegrass andsorghum were reduced by iron concentrations greater than 2 to /ig Fe ml ^ insolution, particularly when the plants were grown on the amm onium nitrate-basedsolution.Chemical compositionChlorophyll All species were chlorotic when grown on the lowest ironconcentration, the severity of the disorder being reflected in the chlorophyllconcentration of the shoots (Table 4). Chlorosis was generally greater when all thenitrogen was provided as nitrate and in those species which were particularlysensitive to low concentrations of iron in the nutrien t solution (e.g. brow ntop andsorghum). The iron treatments had no significant effect on the chlorophyll a to


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Iron r quir m ntsof and plants 7

"024 8 16 32 " 0.24 8 16 32Iron concentrotion in nutrient solution {\ =O- 5\2 u.q Femr')

Fig.] . Effect of ironin the nutrient solutionontotaldrymatter yields shoots plus roots)ofCgplants when nitrogen was provided either as ammonium nitrate O )oras nitrate x},Vertical barsindicatethe residual standard deviation aboutthelines fittedto theobservations.

0 124 8 ts 32 0 Z4 8 16 32Iron concentrotion in nutrient solution [l iiO'3l2//g Femr')

Fig.2. Effect ofironin thenutrient solutionontotaldrymatter yields shoots plus roots)ofCplants when nitrogen was provided eitherasatnmonium nitrate O) oras nitrate x).Vertical barsindicatetheresidual standard deviations aboutthelines fittedto theobservations.


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5 8 G S SMITHetal

fl

s

li

C 2t{ T

S

T r


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Iron r quir m ntsofCga nd plants 549Browntop (6014^

IZ8(129 68 0

- Lucerne

0 24 8 16 32 ' " 0 2 4 8 16 32Iron concentrotion in nutrient solution (( O -3 (2 ^g Fe m f")Fig.3 . Effect of iron in the nu trient solution on iron concentrations in the leaves ofCj,plants whennitrogen was provided either as ammonium nitrate (O) or as nitrate (x ). Arrows indicate ironconcentrations associated with 90% maximum total dry matter yield. Vertical bars indicate theresidual standard deviation about the lines fitted to the observations.

53200 59 0756 04 5

8 ^ i

[ 1 1 1

So'rghum

^ 0'2 4 8 16 32 0 2 4 8 16 32Iron concentration in nutrient solution (l O-3l2/ig Fem r ' )

Fig. 4 Effect of iron in the nutr i ent solution on iron conc entrations ou the leaves of C^ plan ts whennitrogen was provided either as arsimonium n itrate (O ) oi 3 s. nitrate ( x ) . Arro ws ind icate ironconcentrations associated with 90% maxiinum total dry matter yield. Vertical bars indicate theresidual standard deviation about the l ines f i t ted to the observations.


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55O G. S. SM I TH et aL1600

2 4 8 i6 32 I E 4 8 16 32Iron concentrotion in outrient solution ( =O-3l2^g Femf')logscale)Fig 5. Effect ofironin the nutrient solution on ironconcentrationsin the roots ofCgplants whennitrogenwas provided either as ammonium nitrate (O) or as nitrate (x). Vertical bars indicatetheresidual standard deviation about the lines fitted to the observations. The results were logtransformed.

dry matter yield was 90 of the maximum, was estimated for each species usingthe data in Figs 1 to 4. The results (Table 5) indicate little difference in theconcentration of iron in the leaves among the species, but the C^ plants requiredmore iron in the nutrient solution than the C^ plants to achieve these leafconcentrations.Phosphorus concentrations Increasing concentrations of iron in the nutrientsolution reduced the concentration of phosphorus in leaves, but not in the roots,of browntop, cocksfoot, ryegrass, kikuyu, maize and sorghum when grown on theammonium nitrate-based solution (Table 6). Dry matter yields of all of thesespecies were reduced by the higher concentrations of iron in the nutrient solution(Figs 1,2).Increasing the supply of iron greatly reduced the phosphorus: iron ratio in theleaves from relatively high values in the iron-deficient plants to values of less than

25 in plants whose dry matter yields were affected by excess iron (Table 6).


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ron requirements of and plants 5 5 18 0 0

6 0 0300'1 5 0

7 5 '^n

1

\

r

1

3200 -

(600 -

8 0 0

4 0 06 0 0 -3 0 0 -f 5 0 -

f 2 4 S [6 32 I .2 4 8 16 32Iron concentration m nutnent solution [i = O' 3 2^g Feml"- ')(log scale)

Fig . 6. Effect of iron in the nutr ien t solution on iron conc entratio ns in the roots of C^ plants w hennitrog en was provided either as am mo niu m n itrate (O ) or as nitrate ( x).. Vertical bars indicatethe residuaJ standard deviation about the lines fit ted to the observations. The results were Jogtransformeid..

(Table 7). Except for nitrogen, the concentrations of the elements were broadlysimilar for both the Cj and C, plants. For nitrogen, the concentrations weregenerally lower in the leaves of the C^ plants than in the leaves of the Cg plants.Manganese concentrations were slightly greater, while calcium concentrationswere less, in the leaves of plants grown on the ammonium nitrate solution. Thehigher concentrations of calcium in the leaves of plants grown on the nitrate-onlybased solution reflect the greater quantities of calcium used in this nu trient solution(Table 2).D I S C U S S I O N

T he concentrations of iron required in the nu trient solution for oiaximum growthof C^ plants were very much greater than those for Cg plants. Romheld &Marschner (1979) previously found that maize{Zea maysL. cv. Velox), a plant,required concentrations of iron (as Fe EDDHA in the nutrient solution) up to 50times greater than those required by sunflower Helianthus annuusL. cv. Sobrid),a Cg plant, for maximum growth. However, no systematic study had previouslybeen made of gand C^ plants. In the present investigation there were only smalldifferences among the species in the concentration of iron required io the leavesfor near maxinaum dry nriatter yield (Table 5). This suggests that the C3 and C^plants differed in their capacity to absorb iron from the root zone, especially when


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552 G . S . S M I T H et al.Table 5 . Concen tration of iron required in the leaves and in the nutrient solution toachieve 90 maximum dry matter yield of C j and C ^ plants grow n either withamm onium nitrate or with n itrate only as the nitrogen source

Plant speciesC3 species

BrowntopCocksfootPerennia l ryegrassLuce rneRed cloverWhite c loverC^ speciesKikuyuMaizePaspa iumS o r g h u m

Mean C3Mean C^L S D { 5 % )

Leaf iron(/ig Fe g ^ dry ma tter}A m m o n i u m N i t r a t eni t ra te

10 4606 57 64 879626 48 95 07 26 627

only

10065858758936 78 08362817321

Nutr ient solut ion i ron(/ig Fe ml ').Ammoniumnitra te

0-480-240-280-520-480-480-520-640-881-040-410 7 70 2 6

Nitra teonly

1-441-001-361-840>S61602-325-967-044-081-304-852-0

types have been based on their capacity to reduce Fe * to Fe '' (Brow n, 1976). Inresponse to a deficiency of iron, ' iron-eflBcient' plan ts have a greater capacity toreduce iron fro^m. Fe * to Fe^^ by lowering the pH at the root surface. T his isprobab ly caused by the release of H ions, organic acids such as citric acid, andreducing compounds such as riboflavin (Brown, Weber &Caldwell, 1967; Brown& Am bler, 1974; Rom held, M arschner & K ramer, 1982). Other factors, such asthe form of nitrogen absorbed by plants, also influence the pH ofthe root zone.Numerous studies, including the present investigation, have shown that whenammonium is absorbed by plants there is an increase in acidity in the root zoneas H ions exchange from the roots into the surroun ding m edium to compensatefor excess cation uptake, whereas, with nitra te, large quantities of HCO g or OHions are excreted by the roots to compensate for excess anion uptake (Trelease &Trelease,1935;D ijkshoorn, 1962; Kirk by, 1969; Raven&Sm ith, 1976; M iddleton& Smith, 1979). It seems likely that the higher iron requirements of both the C^and Cj plants when n itrate was the source of nitrogen were due to less Fe^^ beingformed as a result of the increased alkalinity of the root zone. Similar results havebeen noted with other plant species when they were grown on a nitrate-richme dium (Sideris & Youn g, 1946; Van Den Driessche, 1978; Foy, Flem ing &Schwartz, 1981). However, in terms of 'efficiency' of the individual species,, therewas no indication in the present experim ent that the Cg plants w ere able to acidifythe root zone toagreater ex tent than theC plants (Table3 ).T he possibility cannotbe completely excluded, however, because it was not possible to sample thesolution imm ediately adjacent to the root. Th ere is also considerable evidence


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Iron r quir m ntso Cjand C^ plants 55

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C) O O O O O O

C CDO O O O O

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f ^ OM pO O O O O C O

^ TN o tNa> D cp0 0 0 0 0

p rj 00 -

, 0 o r Tr rp.fp rp p6 o Coc

pocbooo

'7tp-7^pp'7 P C Z > O O oooc-6 C d cscboci

f-~ IT) * -fSIp ^O O O T^ --^ T^ O

*-^ O^ ' *~H 00 ^ 'CN y^ O' O* *Oc J r o r N ' ^ ' T j - r o O ( N ' C N c o c s tc D c b c b o o o o c b o O ' O t

in, ir-*O r~i

^ o ri CN csoro fNrp (Nl rp 'COr^ CO pO O 6 O C>6 CiO O O ^ CCO CN ro tNOO o O O C


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55 4 G . S . S M I T H et althat these elements were present in high enough concentrations to have seriouslyaffected the iron requirements of the Cj and C^ plants. Except for lowerphosphorus concentrations in particular cases, the concentrations of all essentialelemen ts in the leaves were within the ranges considered to be optimal for grow thof these types of plant (Benton-Jones, 1967; McNaught, 1970).T h e observed depressions in dry matter yield du e to excess iron when amm oniumnitrate was the nitrogen source were probably caused in part by a decrease inphos phoru s uptake. T he phosp horus concentrations in the leaves of plants severelyaffected by iron were below the optimal ranges for growth (Benton-Jones, 1967;M cN augh t, 1970). Similar effects of iron on phosp horu s concentrations have beenshown hy Dahiya & Singh (1976) and Brown & Jones (1977) for sorghum , andby W atanahe , Lindsay & Olsen (1965) for maize. Iron readily forms precipitateswith phosphates and these may occur in the nutrient medium and on the surfaceofthe roots (Sideris Young, 1956), as well as internally (Rediske & Biddulph,1953) thereby m aking both elem ents less available for plant growth. In the p resentstudy, iron appears to have affected the absorption of phosphorus by the roots toa far greater extent than trans po rt from roots to shoots. If there had been a greatereffect on transp ort to the leaves, a differential accum ulation of pho sphorus wouldhave been expected to occur in the roots. In fact, increasing concentrations or ironin the nutrient solution had no significant effect on the concentrations ofphosphorus in the root. There were also no distinctive leaf symptoms associatedwith the reductions in dry matter yields, although the development of brownlesions have been observed on the older leaves of rice (Tanaka, Loe & Navasero,1966) and m aize (Odurukw e & M ayn ard, 1969) affected by excess iron.Bienfait Van Der Mark (1983) concluded that the regulation ofFe in plantsmay also be of considerable importance in relation to the detrimental effects of ironon growth. Ferrous iron is readily oxidized by oxygen at pH values commonlyfound in plant ceils (pH 5-0 and ahove).

The superoxide (O^ ) that is formed in this reaction is highly reactive and cancause considerable damage to membranes and proteins, especially when there isinsufficient superoxide dismutase present to keep the concen tration of Ov, in thecells at low levels (Halliwell, 1974; T rels tad , Lawley Ho lmes, 1981). Th e controlmechanisms for maintaining low concentrations of Fe* ''in the tissues m ay be lesswell developed in those plants whose growth was reduced by the relatively highconcentrations of iron in the nutrient solution.Before a satisfactory explanation can be offered for the difference in capacity ofthe Cg and C^ plants to absorb iron, more detailed measurements are needed onthe uptake of iron by roots of these two groups of plants. Furthermore, the studyneeds to be extended to include a much greater number ofC3and C^ plants .


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ro requirements ofCgandC^ plants 55REFERENCES

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Fe Requeriments of C3 and C4 Plants