J.P. Syvertsen University of Florida, IFAS, Citrus Research and Education Center. 700 Experiment Station Road, Lake Alfred.
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1 ,.. \ ::>'\ \)'O?! <:> q.,...j j AMR. Soc HORT SC 19(6):818! Light Acclimtion in Citrus Leves.. CO Assimiltion nd Light, Wter, nd itrogen Use fficiency J.P. Syvertsen University of Florid, FAS, Citrus Reserch nd duction Center. 7 xperiment Sttion Rod, Lke Alfred. FL 3385 Additionl index words. grpefruit, ornge Abstrct. etcq ssimiltion (A) rtes of 'Duncn' grpefruit (Citrus prdisi Mcr.) nd 'Pinepple' ornge (c. sinensis L.) seedlings grown under 3 different photosynthetic photon nux densities (PPFD), were mesured in n open gs exchnge system under controlled environmentl conditions. Apprent quntum yield (f), mesophyll conductnce to CO (G m ), lef conductnce to H vpor (G,), trnspirtion () nd wter use efficiency (WU) lso were exmined. Leves of both species grown under high PPFD (full sunlight) hd the gretest mximum rtes of A, but the low PPFD (9% shde) leves hd the highest e. The WU of low PPFD grpefruit leves ws less thn tht of the high PPFD leves but incresed within weeks fter being moved into full sunlight. Trnsferring seedlings from low to high PPFD decresed e of grpefruit but not of ornge leves. Chnges in A were more strongly correlted to G m thn to G,. Crbon dioxide ssimiltion rte ws positively correlted to totl lef nitrogen content. Citrus lef photosynthetic chrcteristics nd resources use efficiency not only cclimte to the light regimes under which they expnd nd mture. but leves re cpble of cclimting to new light regimes, even fter full mturtion. Bjorkmn () recently hs reviewed how leves cclimte to from interior positions (15), there is no report of citrus nitrogen chnges in the rdition environment to mximize photosyn use efficiency. Such informtion cn provide insight regrding thetic efficiency under prticulr set of conditions. Leves resource prtitioning (3. 9, 3) during cclimtion in tree cngrowing in full sunlight re not only thicker with more densely opy microclimtes. pcked mesophyll (4, 19) thn leves growing in shde. but lso Shde leves typiclly hve incresed quntum yield (j), n hve higher lightsturted CO ssimiltion rtes (A) (, 7, ll, estimte of quntum use efficiency during CO fxtion, s shown, ). Furthermore, sun leves hve higher nitrogen use ef by greter initil slopes in the quntum yield region of the A ficiency thn shde leves. s estimted by expressing A on vs. photosynthetic photon flux density (PPFD) response curve totl lef nitrogen () bsis. (5, 6). Although citrus leves (, 4). High j is, of course, n importnt dvntge in shded from exterior cnopy positions hve higher contents thn leves environments (7). Since the mjority of leves in tree cnopy re growing under reduced light, higher of shde leves llows them to cpitlize on existing light microclimtes (18). Although the plsticity of in sun nd shde leves hs been Received for publiction : Apr Florid Agriculturl xperiment Stlions Journl Series o The ssistnce of M.L. Smilh. Jr.. is grtefully c described for mny crops (, 4) ntive shrubs nd trees (1, knowledged. The cost of publishing lhis pper ws defryed in prt by the 8, ), there is no vilble informtion on how j vries with pyment of pge chrges. Under postl regultions. this pper therefore must the PPFD environment of citrus trees. This reltionship cn be hereby mrked dvertisement solely to indicte this fct 81 J. Amer. Soc. Hort. Sci. 19(6): '.
2 . for horticulturl purposes. Furthermore, cultivted species of citrus hve long lived leves (up to 3 yers) which re not only exposed to grdully chnging light environments during norml cnopy development. but lso cn be subjected to immedite increses in light exposure fter hedging. Khiri nd Hll (14) described how chnges in nonstomtl spects of A enbled citrus leves to dpt to chnging light conditions. The dptive mechnisms tht del with ntomicl molj)hologicl, nd physiologicl chnges (4. 13) tht cn led to efficient light, wter, nd nitrogen resource utiliztion by =' citrus leves during chnging microclimtes re not fully under stood. The pulj)ose of this study ws to determine the photoc synthetic chrcteristics of sun nd shdecclimted citrus leves,. s:j nd to relte these chrcteristics to the time course of chnges in resource use efficiency during light cclimtion. o " Mterils nd Methods Thirty seedlings ech of species. Citrus prdisi Mcf..Duncn grpefruit' nd C. sinensis L..Pinepple ornge', were grown either outdoors (high PPFD. mximum PPFD = 3 jj.mol s t m ), under 5% shde (intermedite PPFD) or 9% J shde (low PPFD). When seedlings were 9monthsold, mture g leves within the sme ge group were tgged for study (6). Hlf the seedlings of both species in the low nd intermedite C PPFD were trnsferred to high PPFD to simulte the contrsting O light environment tht occurs fter hedging. n ddition, nf J:> the high PPFD seedlings were trnsferred into 5% shde (inq) termedite PPFD) to simulte chnges in the light environment f tht occur during the course of norml cnopy development. s:: Thus. there were totl of 6 PPFD tretments: the 3 originl :3 growth conditions (high. intermedite, nd low PPFD) nd 3 trnsfer tretments, herefter referred to s low to high, intermedite to high, nd high to intermedite. Photosynthtic CO ;ssltriltion nd trnspirtion rtes () were clculted from CO nd H vpor fluxes (1), using the tgged leves in n open gs exchnge system. The lef conductnce to H vpor (G ) ws clculted from ; G 1 /1.56 ws used to clculte the lef conductnce to CO nd the CO, compenstion point vlue of 45 jj.l (16) w's used s th minimum internl CO concentrtion m clcultmg mesophyll conductnce to CO (G m ) (1). The gs exchnge system contined n Anrd dul gs nlyzer tht simultneously mesured CO nd wter vpor in the mesurement ir strem. Leves were enclosed in wellstirred temperturecontrolled lef chmber (5) where boundry lyer conductnces exceeded 1 cm s. The chmber ws illuminted with 5 W qurtz iodine lmp. All A. except PPFD response curves, were evl uted under constnt environmentl conditions of sturting PPFD (68 jj.mol s 1 m ), mbient ir contining 35 ± jj.1 CO, lef temperture of 6 ± 1 C nd bsolute humidity difference from lef to ir of 6 ± jj.g cm 3. Preliminry mesurements indicted tht these stndrd conditions were nonlimiting nd there were no differences in temperture optim for A of leves growing in the different PPFD conditions. Four seedlings, from ech of the high nd low PPFD growth conditions, were used to chrcterize PPFD sturtion responses nd pprent quntum yield (. 4), while ll other mesurement conditions were held constnt. The drk respirtion of one lef on ech seedling ws determined nd the liner increse in A ws evluted for t lest 4 levels of PPFD, ttenuted using cheese cloth filters, between nd 1 jj.mol s t m. Apprent tion of th regression of A vs. incident PP FD. PPFD sturin responses then were chrcterized by incresing PPFD in nonconsecutive steps (using filters) to levels where there were no more increses in A. Chnges in net gs exchnge chrcteristics tht occur during light cclimtion were evluted in nd group of 1 seedlings. + from ech originl PPFD. by mesuring A nd of lef / ech under the stndrd nonlimiting conditions nd, 4. or 6 wec:ks fter trnsfelting seedlings into new PPFD. Wter use efficiency (WU, mmol CO influx/mol H:O efflux) ws clculted for ll PPFD tretments. CO ssimiltion rtes,. nd WU of low PPFD leves were evluted in 3rd group of 3 seedlings.3,1. 17, nd 4 dys fter trnsferring to high PPFD in n effort to elucidte more fully the time course of light cclimtion in low to high PPFD leves. Dt from these groups of seedlings were used to chrcterize the reltive mportnce of G nd G m in determining mximum A during growth under widely different PPFD conditions nd during cclimtion to chnging PPFD. n ddition. A ws tested for correltion with lef nd chlorophyll content described previously (6), nd the mount of CO fixed per unit lef totl (A) lso ws tested for correltion with using liner regression nlysis. Results,c:ves grown in high PPFD hd higher mximum A thn low PPFD leves (Fig. ). The PPFD response curves of both species seemed similr in shpe. but grpefruit leves tended to hve somewht higher mximum rtes of A. CO ssimiltion rtes of leves. even cclimted to full sunlight, pper to ightsturte t reltively low levels of PPFD s previously noted by Kriedemnn (17). Leves grown under the low PPFD hd higher o thn high PPFD leves (Fig. ), but vrition mong ornge dt obscured ny significnt differences <Tble ). n grpefruit leves. decresed in the low to high PPFD tretment. vlution of A of grpefruit leves under the optiml conditions nd sturting levels of PPFD (Figs., 3) confirm the differences in A reltive to growth conditions. Mximum CO: ssimiltion rtes, nd WU of leves grown in high nd medium PPFD were similr. Mximum PPFD of the intermedite tretment (11 jj.mol s 1m ) were pprently not low enough to result in ny significnt differences from the high PPFD tretment. Furthermore, CO ssimiltion rtes, nd WU of leves trnsferred from high to medium PPFD or visevers did not differ significntly from their originl vlues. Within weeks fter trnsferring seedlings from low to high PPFD conditions, however, there were signiticnt decreses in A nd in both grpefruit nd ornge leves. These reductions were trnsient, s rtes recovered to originl vlues by week 6. n grpefruit, the reduction in ws greter thn the concomitnt reduction in A, which resulted in significnt increse in WU (Fig. ). Chnges in of the other PPFD tretments were similr to chnges in A; there were no significnt differences in WU through time. Similr reductions in A in response to trnsferring the 3rd group of plnts from low to high PPFD. occurred within 4 dys (Fig. 4). n this group of plnts, men A nd, consequently, WU of ornge leves were significntly higher thn grpefruit leves. Trnspirtion rtes did not chnge significntly. Reovery of A occurred t bout the sme rte s in the previous group nd WU incresed significntly fter 5 dys of being under high PPFD. J. Amer. Soc. Hort. Sci. 19(6):
3 ':t Grpefruit / 8f 7 f e,et f:!,. / :. 4 f.4p 3 9 (f) f:!,. f:!,. e 1 :L {..., c. 9 Ornge 'iii Cl 8 <,./ 7 (,), f:!,..l.. 6ff:!,. n f:!,. 6f Sf..D Sfe' 4 l e,' 9 3, r,; J " f, o PPFD ( Jmol s m ) Fig.. Light responses of CO ssimiltion rte (Al nd pprent quntum yield (J.mol CO ssimilted per incident J.mol PPFD. dshed lines) of grpefruit nd ornge leves grown for 5 months under low (el oro) PPFD nd fter being moved from low into high (l:.) PPFD fo 14 dys. Curved lines ere fit by eye. Combining the individul A dt from Figs., 3, nd 4, A ws more strongly correlted with Gm thn with G 1 (Tble ). Using the men A dt from Fig. nd 3 long with men vlues of lef chlorophyll nd nitrogen content (6), the correltion between A nd lef chlorophyll content ws wek, wheres lef nitrogen ws positively correlted with A. The lirpetruit C'l 8 8 (/) rl 4 :t b 4 : r1 C'l ' 3 r':' G46 o G (/) :f: 1 r rr 1 o "_Vfl<' UJ '. G46 o G 4 o G , w ::::> ' " o G48 o G 4 b r Time (weeks) 41 [/.co Fig.. Men mximum CO ssimiltion (Al, trnspirtion () nd wter use efficiency (WU) of grpefruit leves grown (G) for 5 months under low (solid brs), medium (shded brs), or high (open brs) PPFD nd lso, 4. nd 6 weeks fter being trnsferred to high or medium PPFD. Different letters refer to significnt (P <.5) differences s determined using DMRT; brs without letters do not differ significntly. reltionship between A nd pprently ws due to chnges in G m rther thn G s G m is more strongly correlted to vritions in lef nitrogen content (Tble ). xpressing the A on lef nitrogen bsis (), s n estimte of nitrogen use efficiency, results in reltively low rnge of (1.95.) nd no significnt correltions between nd lef nitrogen content. 814 J. Amer. Soc. Hort. Sci. 19(6):
4 ... ' Ornge 1 1 r '(/) 6 6 b : 4 4 "'" 4:... o,! G46 3 r l :[ 3 r '(/) 'll b 1 1 "'" w U' G46 o G 4 o G4 6 6 r v: ' o w ;::) 1 1 3: t 11 rl o G46 G4 G 4 ' r/ o LL1L Time (weeks) Fig.3 Men mximum CO: ssimiltion (Aj, trnspirtion () nd wter use efficiency (WL J of ornge leves grown (G) for 5 months under low (solid brs). medium (shded brs). or high (open brs) PPFD nd lso. 4. nd 6 weeks fter being trnsferred to high or medium PPFD. Different letters refer to significnt (P <.5) differences s determined using DMRT; brs without letters do not differ significntly. Discussion Most plnt species. including some tree fruit species (1), cclimte photosyntheticlly when grown t different PPFD. Citrus leves re typicl in this respect, s mximum rtes of CO ssimiltion of low PPFD leves were only hlf tht of high PPFD leves. n ddition, the light use efficency or,)f leves grown in low PPFD ws greter thn tht of high PPFD leves. The of citrus leves cclimted to chnges in PPFD nd ws ccompnied by chnges in mximum rtes of CO J Amer. Soc. Hort. SCi. 19(6):8l ' 1(1) 1 T :t 6 "'" c( 5 (\... 3 'en 1 w.., e 4 eu.i :::> Time (dys) Fig 4. Men mximum CO ssimiltion tal. trnspirtion t) nd wter use efficiency (WU) :t SD of ornge (squres J nd grpefruit (circles) leves tht were grown for 5 months under low (solid symbols) PPFD nd then trnsferred to high (open symbols) PPFD. ssimiltion High rtes of A corresponded to increses in lef tssue density nd correlted with highest lef nitrogen content (6) Differences between p of low nd high PPFD grpefruit leves were greter thn tht of ornge leves. Such species differences were supported by responses in physicl chrcteristics of grpefruit to chnges in PPFD. Mture grpefruit trees re typiclly lrger thn ornge trees, nd this size difference my result in grpefruit leves cclimting to incresed shde. Vritions in mximum A nd expressed on n incident PPFD bsis hve been found to be due lrgely to differences in lef bsorbnce () This finding ws supported by the high of low PPFD leves which hd higher chlorophyll content, perhps bsorbed more of the incident PPFD t the low mesurement levels, nd were probbly less retlective thn the more glossyppering high PPFD leves. xpressing (; on n bsorbed PPFD bsis would be helpful in interpreting these responses. Furthermore. gs exchnge responses my hve been somewht different if leves hd been evluted in sunlight rther thn under n rtificil light source, s the spectrl distribution of qurtziodine differs from tht of sunlight (1). The correltion between A nd G reveled tht A nd vried together nd resulted in little chnge in WU under the constnt mesurement conditions. There ws n indiction tht A incresed more thn in grpefruit leves tht cclimted from low to high PPFD (Fig. 4). resulting in increses in WU (J:) R... :tj...:.c.; ',l.
5 tions of the CO, ssimltion vs. rnge of 1 mol s l m incident PPFD mesured over the Apprent quntum Constnt yield. Correltion PPFD (f.lmol (f.lmol CO!f.lmol coefficient conditions CO) PPFm (r) Grpefruit Low t.98 High b.93 Low to High 36 4 b.96 Ornge Low High Low to High 'Apprent quntum yields (slope within ech species tht re followed by unlike letters differ significntly (P <.5) s judged by t tests compring the slopes. Low nd high quntum yields re plotted in Fig. 1. Low PPFD leves incresed in lef density nd nitrogen content (6) when trnsferred into high PPFD conditions. The reltively low rtes of A long with lef contents comprble to other wellfertilized crops (3. 3). results in reltively low Ai. Mximum Ai of 67 mmol CO g 1 hs been reported for peches (6). ccounts for much higher percentge of the vrition in A of other crops ( ) thn of citrus. onetheless. lef nitrogen ws positively correlted with G m, though ccounted for only 6% of the vrition in G m. The nonsignificnt reltionship between Ai nd lef pprently ws function of the wek correltion between A nd. Differences in lef metbolism of deciduous fruit nd citrus hve been described (1'+ l. With such smll smple size nd wek correltions. it is difficult to drw strong conclusions. but it does seem tht my not be s closely relted to A in CitruS s in other plt species. or perhps the reltively low G 1 my override ny relti'onship between A nd. Photoinhibition of the low to high PPFD tretments (4) lso my hve depressed levels of A independent of content. Leves trnsferred from low to high PPFD consistently hd significnt increses in G m fter 46 weeks. These results re consistent with those of Khiri nd Hll (14) who found dy to dy chnges in G m responsible for cclimtion to high light conditions during mesurements of A. Mesophyll conductnce to CO reltes to ll nonstomtl spects of A nd cn include physicl component of CO diffusing through lef tissues s Tble. Summry of liner regressions relting m;:imum CO s similtion rtes (Al to totl lef conductnce to HO vpor (G ) mesophyll conductnce to CO (Gm). lef chlorophyh (Chi) nd nitrogen () content. nd lso relting conductnces nd nitrogen use efficiency (Ai) to lef nitrogen content. Dependent ndependent Correltion coefficient vrible vrible Vintercept Slope n (r) AY G **z A Gm \ 1.98** A Ch S A * Gm 3 o ! * G S Al r: 18.4 S ;:*.**.;;5. P <.5 (*). P == <.1 (**). not Significnt (S). YUnits == A!fl.mol s 'rr 1)'G <l!ldgm(cms),chl(f.lgcm1. (mg cm 1. A/ (mmol g S ). 816 out estimtes ot pnotoresplrtlon. S Ulllll,;Ull LV CPdld'C 1C:'C components. The photochemicl component of G m ws ltered when plnts were grown in vrying PPFD (4. 4) or moved into new PPFD (14). n this study, lef chlorophyll nd nitrogen content (6) incresed with the observed increse in G m supporting the ide of incresed photochemicl processes. Lef tissue density lso incresed significntly in the low to high PPFD plnts, which could hve influenced CO diffusion processes. As in previous studies (14), the increse in G m in these species ws not ccompnied by n increse in G,. explining why there ws no concomitnt increse in trnspirtion nd why WU tended to increse. t is possible tht different initil plnt growth rtes nd chnging growth rtes in response to chnging PPFD levels plyed role in the observed vritions in G m nd A. This role could hve been medited through incresed demnds by the ctively growing plnt for photosynthtes from the mture le:lves used in this study. The low to high PPFD lef itself probbly incresed its photosynthte sink cpcity s shown by increses in tissue density, nitrogen content (6) nd likely increse in Frction protein (3). The exct reltionship between CO ssimiltion nd photosynthte sink demnd during light cclimtion remins to be ssessed. t is cler from the net gs exchnge chrcteristics of citrus leves grown in contrsting PPFD. tht citrus is shde dpted nd cn respond to chnging light regimes. Chnges in physicl chrcteristics. chlorophyll, nd nitrogen content of leves during light cclimtion (6) support the observed physiologicl responses. Under the optimum moisture nd fertility conditions of this study. leves cclimted to deep shde pproched physiologicl responses of sun cclimted leves fter 6 weeks in fuji sunlight. This response nd tht of resource use efficiency should hve prcticl pplictions when considering light. wter, nd requirements during cnopy development nd its modifiction by hedging. Literture Cited l. Bzzz. F.\. nd R.W. Crlson Photosynthetic cclimtion to vribility in the light n\'ironment of erly nd lte successionl plnts. Oecologi Bjorkmn. O cologicl dpttion of the photosynthetic pprtus. pp n: G. Akoyunglou (ed.). Photosynthesis V. Photosynthesis nd productivity. photosynthesis nd envi ronment. Blbn nt. Phildelphi. P. 3. Brown. R.H A difference in use efficiency in C 3 nd C 4 plnts nd its implictions in dpttion nd evolution. Crop 3ci. 18: Bunce. J.A.. D.T. Ptterson. M.M. Peel. nd R.S. Alberte Light ccltmtion during nd fter lef expnsion in soyben. Plnt Physiol. 6:5558. :! Dejong. T ',, eo:: ssimiltion chrcteristics of five Pru /lls tree fruit species. J. Amer. Soc. Hort. Sci. 18(): Dejong, T.J Lef nitrogen content nd CO e ssimiltion cpcity in pech. J. Amer. Soc. Hort. Sci. 18(6): Dennis, W.P. nd J. Woledge \983 The effect of shde during lef expnsion on photosynthesis by white clover leves. Ann. Bot :3 hlennger. J. nd O. Bjorkmn Quntum yields for e uptke in C, nd e.. plnts. Plnt Physio!. 59: Field, C nd H A Mooney Lef ge nd sesonl effects on light. wter nd nitrogen use efficiencv in Cliforni shrub Oecologl Hofmn. G led.) scotbles. A hndbook of dt for bologicl nd physicl SCentists seo. Lincoln, b. 5 p. HolMgren. P 1968 Lef fctors ffecting lightsturted pho J. Amer. Soc. Hort. Sci. 19(6): \..." v r/
6 1. Jrvs. P.li rhe estimtion 1 resistnces to crbon dioxide trnsfer. pp n: Z. Sestk. J. Clsky, nd P.G. Jrvis (eds. l. Plnt photosynthetic production: mnul of methods. Junk. The Huge. etherlnds. 13. Kppel. F. nd J.A. Flore ffect of shde on photosynthesis. specific lef weight. lef chlorophyll nd morphology of young pech trees. J. Amer. Soc. Hert. Sci. 18(4): Khiri. M.M.A. nd A.. Hl! Temperture nd humidity effects on net photosynthesis nd trnspirtion of citrus. Physio!. Plnt. 36: Keo. R.C.J. nd J.W. Sites Minerl composition of citrus leves nd fruit s ssocited with position on the tree. Prof.. Amer. Soc. Hort. Sci. 68: Kto. T Mjor nitrogen compounds trnsported in xylem vessels from roots to top in citrus trees. Physio!. Plnt. 5: Kriedemnn. P.. \968. Some photosynthetic chrcteristics of citrus leves. Austr!. J. Bio!. Sci. 1: Mbh. B....L. McWillims. nd K.J. McCree CrbGil blnce of Peperomi obrusijoli plnts during cclimtion to low PPFD. J. Amer. Soc. Hort. Sci. 18(6): obel, P.S Photosynthetic rtes of sun versus shde leves of Hyptis emoryi Torr. Plnt Physio!. 58:183. nd nviron. O:U')44. \. Osmond. C nterctions between irrdince. nitrogen nutrition. nd wter stress in the sunshde responses of Solm;um dulcmr. Oecologi 57: Ptterson, OJ.. 5.: Duke. nd R.. Hoglnd ffects of irrdince during growth on dptive photosynthetic chrcteristics of velvetled nd colton. Plnt Physio!. 61: Pvlik. 8.M utrient nd productivity reltions of the dune grsses Ammophil renri nd i.vmus mollis.. Blde photosynthesis nd nitrogen use efficiency in the lbortory nd field. Oecologi 57: Powles. S.B. nd C. Critchley ffect of light intensity during growth on photoinhibition of intct ttched ben letlets. Plnt Physio!. 61: Syverr.sen. J.P. nd M.L. Smith. Jr An inexpensive lef chmber for mesuring nel gs exchnge. HortScience 18(5): Syvertsen. J.P. nd M.L. Smith. Jr Light cclimtion in citrus leves.. Chnges in physicl chrcteristics. chlorophyll nd nitrogen content. J. Amer. Soc. Hort. Sci. 19(6):878\1. 7. Zelich.. \971. Photosynthesis. photorespirtion nd plnt productivity. Acdemic Press. Y. 347 p.
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