Plant Physiol. (1968) 43, 1617-1624

Seasonal Course of Photosynthesis, Respiration, and Distribution of'4C in Young Pinus resinosa Trees as Related to Wood Formation

John C. Gordon and Philip R. LarsonNorth Central Forest Experiment Station, Forest Service,

United States Department of Agriculture, Rhinelander, Wisconsin

Received April 22, 1968.

A bstract. Rates of net photosynthesis and dark respiration, and distribution of 14C weredetermined for new (current season's) and old (previous season's) needles at 10 times duringthe seasonal development of young Pinus resinosa Ait. trees. The seasonal changes in thesefactors associated with the development of the new shoot were related to known seasonalpatterns of wood formation.

Net photosynthesis per gram of needle dry weight (photosynthetic efficiency) was maximumin the old needles at the time of first new needle elongation; at the same time translocationof 1l+C from old to new needles was greatest. Photosynthetic efficiency of new needles wasmaximturm at the end of the period of rapid new needle elongation, when the new needles alsobegan exporting much greater quantities of 14C to other plant parts. In iparticular, the amounttranslocated from the new needles to the stem was greatly increased. At this time thiok-walledxylem cells were first observed in the stem.

These results, together with those of previous studies, indicate that the production ofthick-walled xylem tracheids normally associated with latewood is physiologically correlatedwith maturation of the current season's needles. Because there is a lesser demand for photo-synthate in the new shoot and a high rate of photosynthesis in the whole plant at the time ofnew needle maturity, a sharply increased amount of photosynthate becomes available for wallsynthesis by cambial derivatives.

The seasonal course of photosynthesis and res-piration of different-aged needles in the crown, alndthe relative contribution of these needles to sttemgrowth must be known to understand wood forma-tion in pine trees. Earlier workers have investigatedthe effect of needle age on CO., exchange (5), theseasonal course of CO., exchange (17, 23), and theeffects of partial defoliation and foliar bagging onstemii anid needle growth (10, 11, 13). Recently,radioactive carbon has beeln used to study seasonalphotosynthate produictioln and distribution in pineseedlings ( 1, 19, 20) and otlher woody' l)lallts (7).No l)revious sttudies, however, have examinied inteln-sively the patterlls of photosylnthesis anL(l resl)irationin, and translocation of photosynthate froll, dlifferent-aged liee(lles dluring an entire seasonl of develol)ment.The l)url)ose of this stu(ly was to (leteri lline thesel)atterns an(l to evaluate theil- possille significanceto woodl forination, p)articularlyv the earlyvwoo(l-late-wool tralnsitioln. A physiological correlation be-tweeni the formiation of thick-walled latewoodtracheids anid the increased availability of currentphotosynthate to the cambial region has been in-ferred from previous studies (13,14). It was sug-gested that the increase in secondary wall thickeningassociated with latewood coincided with the time thecurrent-year needles became self-sufficient and beganexporting photosynthate. This study presents directevidence indicating that this correlation exists.

Materials and Methods

Younig red pine trees i(Pimts resinosa Ait.).grown 4 years in a nursery, were potted in Septem-her anid placed in a cold-frame to overcome dor-mancv. Before potting, all branches, lateral buds,and needles older than 1 year were removed so thatonly a vertical stem bearing the previous season'sneedles and terminal bud remained. Young red pinessimilarly prruIned have been used in numerouts studiesof cambial activity (12, 13, 14) witlh excellent re-stilts. Growth of the pruned trees is ulliforml, ailnlthe compl)lements of current season's (new) an(lprevious season's (old) needles are easilv isolated.

TlI late December 1966, the trees were mlloved toa greenlhouse where they were expose(d to 18-hortip)hotoleriods and day-niighlt temperattui-es of approxi-mately 220 and 160, respectively. At each of 10times dtlring (levelopmenit and maturatioln of the lnewshoot, 4 trees were brought to tlle laboratory andlrates of photosynthesis and res,piration were meas-ured for old and, when present, new needles. Sub-sequently, on the same day, 2 of the trees were fed14CO2 (23 j,c each) photosynthetically through theold needles and 2 were fed a similar amount throughthe new needles. The feeding was done in a speci-ally constructed chamber (15) for 2 hours, anduptake exceeded 90 % except as noted in the text.After feeding, all 4 trees were returned to the

1617

PLANT PHYSIOLOGY

greenhouse. Needle samples consisting of 2 old and3 new fascicles were collected at 2, 24, 48, and 72hr after feeding and radioactivity in the alcohol-soluible and insoluble fractions determined.

At the end of 72 hr, the trees were harvested anddivided into new and old needles, buds, stem, androots; the stem was subdivided into the 1963-65,1966, and 1967 internodes.1 Each plant part wasdried anid weighed; and the radioactivity in thealcohol-soluble and insoluble fractions was deter-mined.

Stem length (shoot extension) and needle elon-gation were measured at weekly intervals throughoutthe course of the experiment and at time of harvest.The 10 treatment times were carefully selected tocoincide with particular stages of shoot developmentbased on prior knowledge of red pine grown undersimilar condition's. The first treatment, designatedas week 0. was made at the time of bud break.

Rates of net photosynthesis and dark respirationwere measured by determin'ing rates of CO, uptakeand evolution with an infra-red COO analyzer. Eachtree was enclosed in a plexiglass chamber connectedto the sample cell of the analyzer by a closed gascircuit containing a drying tower, a flow meter, anda flask of distilled water that rehumidified airre-entering the chamber. Air flow through the cir-cuit was maintained at 1 liter per minute by adiaphragm pump. Circuit volume, including thechamber, was approximately 34 'liters. Photosyn-thesis was measured under a total radiant flux den-sity at mid-chamber of 1.2 X 106 ergs per cm2 persee sulpplied by 4 General Electric PAR 150-wattflood lamps immersed in a water bath above thechamber. Chamber temperature was miaiintained bya copper cooling coil and 2 small, high-speed blowers.Mean chamber air temperatures for all measurementswere 24 ± 10 in light and 19 + 10 in the dark.

Rates for both complements of needles on a singletree were obtained by first placing the tree in thechamber and exposing it to the light source for a15-min conditioning period. The CO, concentrationof the chamber was then adiusted to 0.032 % (v/v)and the CO. concentration of the system recordedfor 10 min. The chamber was then darkened andCO2 concentration recorded for another 10 min.Finally, the old needles and lower stem were enclosedin a polyethvlene bag and the measuremlelnt procedurerepeated. Preliminary tests indicated that baggingeffectively isolated active needles for the peried ofmieasurement. During all measurements. pots wer-eisolated from the system by polyethylene bags sealed.around the base of the stem. All mea-urementswere made in the morning to avoid variation (lue to

1 "Internode" refers to the extension growth of thetree as measured betveen branches or branch whorls on'the main axis and not in the strict botanical sense, tothe stem segment between needle fascicles.

diurnal changes in rates of gas exchange. Rates ofphotosynthesis and respiration in mg CO. per hrand per gram of needle dry weight were computedfrom the taingenit of the recorder trace at the pointwhere the trace crossed the chart graduation indi-cating a CO, concenitration of 0.030 % (v/v) (4).

To (letermine rcadioactivity, th,e plant materialwas oven dried at 7,00. ground to pass a 40-meshscreen in a micro-Wilev mill, and extracted withboiling 80 % methanol for 15 min. The alcohol-soluble and insoluble fractions were taken to drynessaIIdl wx-et-combusted ('22) ; tlhen the evolved '4CO.was collected in a solution of ethanolamine andethylene glycol monomethyl ether (1:2 v/v). Thescintillation medium was prepared according to themethod of Jeffav and Alvarez (8) and radioactivitydetermined in a liquid scintillation spectrometer.Each sample was counted for six 10-min periods andthe mean of the 6 quench-corrected values expressedas cpm/uniit of p)lant material.

Results

Ne;w. Shoot De'velopmnent. Shoot extension andneedle elongation exhibited the normal patterns foryoung red pine trees as found in previous studies(fig 1A). Measurable bud elongation began about2 weeeks after exposure to greenhouse conditions,and shoot extension was complete 7 weeks later.Needle elongation in red pine is partially arrestedduring the grand period of shoot extension. How-ever, since re(l pine needles have an indeterminatebasal meristeim. the normal /7- to 10-week period ofelongationi caln be either prematurelv terminated orp)rolonged by prevailing conditions of weather orlocal environment. In trees of the present study,vigorous needle elongation began about 3 weeksafter miieasurable bud growth was recorded, at whichtime shoot extension was almost 90 % complete.Continiued needle elongationl beyond week 13 can beattributed to the 18-hr photoperiod (12, 14).

Stem tissue constitutes a relatively small propor-tion of the total dry weight of a new red pine shoot.Dry weight of the new stem increased slowly whereastotal dry weight of the new needles increased rapidlyduring the 19-week growth period (fig 1A).

Photosynthesis and Respiration. Rates of photo-synthesis per gram of needle dry weight (photosyn-thetic efficiency) and respiration per gram of needle(Iry weight on a whole-tree basis are known to varythroughout a growing season (17, 23). However,wheni the whole-tree values are partitioned and therates for old and new needles determined separately,2 quite different patterns emerge (fig 1B). Inevaluating these data, it must be recognized that themeasurements were made at discrete intervals andthe peaks of activity may have actually occurredbetween measurements.

The first rate measurements on old needles coin-cided with the first measurements of bud elongation(week 0). Net photosynthesis rate at this time was

1618

1619GORDON AND LARSON- PHOTOSYNTHESIS AND 14C DISTRIBUTION IN PINE,

IrJ)

(9D

(9

F-

(9

L]f-Ili

z

LL0-

D0

LLCL0C

C\i

(9)0

TIME - WEEKS FROM FIRST MEASUREMENTFIG. 1. Growth of the nmxv shoot (A); and rates of net photosvinthesis and dark respiration per graml of liee(le

dry Nveight for new and old needles (B); and whole seedlings (C) at 10 times during seasonal deve&opment. \VJeek0 represents bud break. In B and C the positive ordinate represents CO. uptake, the negative ordinate CO., release,anld ,he dasshed line no net CO., exchange. Vertical bars represent meanis of 4 trees.

already appreciable. It increased rapidly and( reaclhe(da miaximum wvhen- the new needles began vigorouselongation. Thereafter, it decreased and reached a

minimumti during week 13. In the final measuire-

ment at week 19, rate of photosynthesis for the oldneedles was greater than at either of the 2 precedingmeasuremients. Dark respiration of the old needleswas someewhat nmore unifornm than photosynthesis.

An apparent decline during the final weeks of shootextension (week 5) was immediately followed, by a

sharp increase whein shoot extension ceased ( week7). Respiration then declined slowly until termin.a-tionl of the experiment.

The first rate measuremiienits of the new needleswere made at week 3 shortly after they had emergedfromii their fascicle sheaths and were beginning to

z0

a

(f)LYcrcC)

crc

0

U)

CO

LJI

z

Uf)0

0

a-a-

LU.z

I

-I.-

-l

PLANT PHYSIOLOGY

elonigate. lPhotosynthesis rate increased rapidly froma net CO loss to a miiaximum1l at week 9; this imlaxi-mutmn was slightly higher than that for the old needles

at week 3. Therefore, under the conditions of thisstudy-, photosynthetic efficiency of the niewA, needl,esculminiated near the end of their muost rapid growthphase. Newineedle respiration rate attained a mnaxi-mutmill shortly after needle elongationi began and de-clined rapidly after shoot extension ceas,ed. There-after, it renmained nearly constalnt for 6) weeks beforedropp)ing to a rate ahout eqeual to that of the oldneedles at the end of the experimiienit. Since stemrespirationi is also higlh during shoot extension(18, 20), the first 2 measuremiielnts of new needlerespirationi could perhaps be miiore appropriatelycall,ed shoot respiration. The data, nevertheless,indicate rapid conversion of carbohydrates to meta-bolic energy in the elongatinig stein anid needles, asreported by other investigators ('18. 20).

Photosynthesis rates on a whole-tree basis showed2 weak maxima (fig IC). The first peak coincidedwvitlh the nmaximunm rate for old needles at week 3.The second broad peak coincidedl with the transitionbetween the decreasing photosynthletic rate of theold aind the increasing rate of the new- needles atweek 7, and the maximiiumi rate of the new needlesat week 9. Over the major portion of the growingseason, the combined contril)ution of both sets ofneedles maintained a relativelv uniformii rate ofphotosynthesis. It shotuld be eniplhasized that theplhotosynthesis rates presented are rates per gramof ineedle dry weight. A decline in this quantitydoes not necessarilv in(licate a decline in the totalquantity of CO., fixed 1v the whole tr-ee pertunit oftimiie (photosyntlhetic capacity Coinparisoiis ofplhotosynthetic capacity amonIig treatmiienits are qties-tioni.able in ani experimiieint of tli.s n1atture because of1)osil)le differences ini initiall tree -i ze. However,calculation- i of photosyniithetic cal)acity dlid show a

stea(lv increase until wveek 9, at which tillme it was

aplproxinmatelv double its in itial valtue. Similarly.rate., of photosynthesis and respiratioln computed onla freshl weight basis coincided closelv wsitlh those offigutre 1. It has beeni fotund that freslh and dry

wl eights of pine needles are highly corr-elated (6).Trauslocation. Respiration (ltrinig the 72 lhr

following treatimienit accounted for the loss of only a

smiiall fraction of the total '4C apl)lied, except for thefirst treatment of the niew shoot ( week 3) in whiclrespiration was higlh. Therefore. loss of "4C froImltreated needles was assumed to be priiliarily bytranslocation to otlher parts of the tree. Likewise,incorporation into an alcohol-insoltuble forml wasasstliuied to indicate coniversioni to large mlolectulesill the tisstue sampled.

Old needles always lost most of the 4C appliedto tlenm within 72 hr, and mucthl of it withini the

fir.,t 24 hr (fig 2A). Translocation of activityfrolmi the old needles -was appareintly v-ery rapiddurinig the grand period of shoot extenision and theearly stages of new needle development, a period

S r S MEASUREME NT'IG. 2. 4C in the alcolhol-soluble (unshaded) and

insoluble (shadedl) fractions of new and old needlescollected at 2, 24. 48, an(l 72 hr after feeding of 14CO2for eacli of the 10 treatmenit times, expressed as couIntsper niiin per mg needle dry weight. A) Activity in theold needles after o0l( ieedles were fed. B) Activityin the news needles after o0l( needles were fe(l. C) Ac-tivity in the ne\x- needfles after new needles were fed.

Vertical bars represent means of 2 trees.

which also coincile(d with the higlhest photosyntheticrate of the ol(1 needles. Also during th,is l)eriod.very- little activitv was trianisformed into the alcohol-insoluble fraction of thle ol0( needles, and the amiiounltincorporatedl di(d not change greatly between 2 and72 h r. Howvever, following the cessatioln of shootextension ( week 7 ). the quantity of 14C convertedto alcohol-insoluible material in the old needles in-creased, partictularly in tlle 2-lhr samples. It iso.ossible that these materials represent accumulation

of reserve foods for- the next season's bud growth,since it hlas been de(iloinstrated that third-year needlescontribute to the growth of thle newv shoot (10, 13).

Translocation of activity into the new needleswllen the ol0( needles were treated (fig 2B) wasgreatest duriing wveek 3 when the new needlles beganelongating. (gain, nliost of the transfer occuirredlwithin the first 24 hr. From week 3 to 7, over halfof the 14C translocatedl wras quickly converte(d toailcohol-inisoltuble material in the new needles, indi-cating rapid incorlporation into protoplasm and cellwvall constituents. \fter week 7, very little activ itywas exported fronl old to new needles.When tlle newx ineedles were fed '4CO9 (fig 2C),

thex retained swame I1 even duirinig week 3 whe

1620

GORDON AND LARSON-PHOTOSYNTHESIS AND '+C DISTRIBUTION IN PINE

the new shoot showed a net release of CO., in light.Much of this activity was converted to alcohol-insoluble material during the first 24 hr. Duringweeks 4 through 7, the amount of 'AC fixed by thenew needles increased and remained at a high level.However, the activity per unit of dry weight de-creased dturing the period of vigorous needle elonga-tion becatuse of increasing dilution by unlabeled drymatter. AVeek 9 represents the transition stagewhen export from the new needles was accelerated.In subsequent wveeks, this increase in export of 14Cis evident by the marked reduction of activity be-tween the 2- and 24-hr sampling periods. Theamount of alcohol-insoluble material retained by thenew needles also declined after week 9. At no timeduring development did treatment of the new shootwith 1QCO., restult in high activity in the old needles,although a small, but fairly consistent, amount wasalways present. This activity, which was noticeablyhigher during weeks 3 through 5, was probably du1eto reabsorptioni of respired 14CO2 (7), and was de-tectable because of the high sensitivity of the wetcomiibustioni recovery process.

A more complete picture of the contribution ofeaclh age complement of needles can be obtained fromthe distribution of 14C throughout the entire tree atthe end of 72 hr (table I). Although the percentagevaluies of 1"C distribution from the different comlple-ments of needles may be compared, attempts totranslate these percentages to absolute amounts mustbe made with care. The total activities presentedin table I represent only approximations of netphotosyntlhesis during the 2-hr feeding period for thefollowing reasons. The 72-hr total is a function ofthe amllounilt of "1CO. respired during 72 hr and of

the amount originally absorbedi during feeding.However, when 14CO., uptake was complete within2 hr, it was not necessarily proportional to photo-synthetic capacity, since additional 14CO0 might havebeen taken up in the same time if it had been offered.In the first 2 treatments of the new needles (weeks3 and 4), when they were short and respirationrates high, they absorbed only 52 % and 78 % of thetotal '4CO2 offered; in all other treatments uptakewas 90+ % and can be regarded as complete.

Distribution of activity in the needles and newshoot as a percentage of total activity confirms thepatterns previously described for the periodic needlesampling. Export of 14C from the old to the newneedles was maintained at a relatively high levelthrough week 7 while the new needles were vigor-ously elongating, but dropped sharply to only 2.5 %of the total in veek 9. For the new shoot as awhole, this value decreased fromii 39.7 % in week 7to 2.9 % in week 9. \When the new needles werefed, up to 97 % of the activity was retained by thenew shoot from week 4 through week 7, and it againdropped to 80 % in week 9. Over half of theactivity in the new needles was transformed toalcohol-insoluble material at the end of 72 hr re-gardless of the source (table II) indicating rapidconversion of the 14C into structural components.

The relatively high proportion of 14C in the 1967stem internode of trees in which the new needleswere fed during week 3 was perhaps due in part tostem photosvnthesis which occurs at this early stageof development (20). On the other hand, the 1'Cin the roots of these same trees presumablv camefrom old needles that had reabsorbed 14CO. respiredfrom the new needles.

Table I. Distribution of 14C in Y'oung Red Pine Trees 72 Hfours After FCeeding Wl'ith 14CO,,The data are given in percent of total activity.

Weeks after first measuremenit at bud breako0 21 32 42 5 7 9 11 13 19

BudNew nieedlesOQd needles1967 interniode1966 internode1963-65 interniodeRootsTotal activity-

7.8

39.8

8.216.827.4

19935

BudNew nieedlesOld needles1967 internode1966 internode1963-65 internodeRootsTotal activity°

47.3

20.1

5.29.517.9

17435

. .

48.517.913.92.94.012.8

20362

. . .

20.625.44.37.7

13.428.6

20704

... 60.7 91.9

... 15.4 4.7...... 8.9 1.2

... ... 1.6 0.4

... ... 2.4 0.5.. ... 11.0 1.3.... 3223 11936

Old needles fed 1"CO.,0.1 0.6 0.0

19.7 31.0 2.531.1 20.6 35.35.9 8.1 0.45.4 6.2 3.34.6 13.0 11.2

33.2 20.5 47.319329 23590 22967

New needes fe(d 14CO.,0.2 0.1 0.7

92.8 95.1 72.43.2 1.0 7.40.8 1.9 6.80.6 0.2 2.20.7 0.3 2.01.7 1.4 8.5

19104 24230 304041 New nee-dies were not present at weeks 0 and 2 during early shoot elongation.2 A new bud had not vet formed in weeks 3 and 4.3 CPM in tlhousands.

Tree palrt

0.14.0

30.00.65.16.2

54.022284

2.068.11.86.61.82.7

17.026959

0.36.6

34.10.73.06.5

48.816994

2.153.62.44.82.03.3

31.824209

0.63.7

57.40.51.63.2

33.012445

6.648.10.85.31.83.8

33.621945

162",1

2PLANT PHYSIOLOGY

Table II. Percent(tje of i tal 14C Actlvitv in thef Alcohiol Insoluble Fraction f1)Differeil7/1,1tIAfler Fceding WI 14C0

Port.' , II2Hurs

Weeks after first iileasuireinlellt at bud b,reakTree part 0 2 3 4 5 7 9 11 13 19

01(l... 67 61

31 31 47 3258 68 ...

... ... ~63 4228 36 44 4224 32 39 3155 42 47 3939 51 58 41

eNew... .. ~~77 84

... ... 58 56

... ... 64 5854 50

... ... 44 3964 46

... ... 70 82

ieedles6231504946484946nleed]es7051476242384468

fe(6643f)07360444454f eli6743716049334866

14CO,5628333543

5947

1 4COi.679726028325359

; Q)27

4040405'426513165

44366262

1;3060465849rx)448

C-436

5439296356

4633554840304939

4432585350384345

Distribution of 14C to differeilt internodes of thestem throughout the seasoil from eaclh complementof needles also exliibited iinteresting pattei-lls (tableI). The contr,ibution of the old needles to growtllof the 1967 stem initerinode relaille(i higlh throulghweek 7 when it dropped suddenly fromii 8.1 % of tiletotal activity to 0.4 %, in week 9. At tile saime time.the contributioll of the newv Ileedles to the 1967internode, to wiliclh tllev wNere attached, increaseclfrom 0.8 % in week 5, to 1.9 % in week 7, and then6.8 % in week 9. The relative contributioni of eaclicomplement of ineedles to the 1967 illterniode in week-

9 was nlaintained in sulbsequellt wveeks.

Similar patternls wN-ere exhibited by the distribui-tion of activity to the older stem internodes. Theold needles contributed all appreciable and fairlyconsistent amount of activity to the 1966 stem inter-node, to whicii they w-ere attaciled, fromii eek 4through wveek 7 and activitv declined thereafter.In the 1963-65 internodes, a pronounced declineoccurred during week 11. Because of slight differ-ences in initial lellgtll of tIle older steili interinodes,the total activity value. wereeoillewhat imlore variablethan in otlier plIant parts. Tile coiltribution of thenew needles to growthl of tile ol(ier iilterilodes was

in direct contrast to thlat of the old needles. Exportfroml the new nee(les iilcrease(i nilall-fold from a

negligible qualntity in week 7 to a fairly sizeableamount in terimls of steili growtth during Week 9 andlthereafter. Microscopic observatiolls also sliowecithat secondary Nvall tliickening of tracheids in theolder iilternodes increased considerablv in 2 treesduring week 7 anld in all trees during week 9.Tracheids of tile curreilt-vear interilode graduallyincreased in w7all thickiless dulring subsequelnt weeks.

Three steill iilte-ilo(les. all devoid of ineedles, were

combine(l in tile 1963-65 iiterilode segiment. Al-

thotuglh the loweri-llost 1963-6-1 stemil intern d(les. pro-duced during the seedling stage, w ere extremlelysihort, the combined cailbial suirface if the 33-yearsegmenit was nionetheless larger tlbaln that if the 1966ilnterniode anld w\as undoubtedly l)arti;dlly respoiisiblefor the consistently greater activity in tbe basalinternlodal saIllIples. An ad(litionial faictc ir mav liavebeell the amount of activity in tran,sit at tble tilie ofsampling. However, the percenltage of activity re-

covered in the alcohol-insoltlble fraction of the olderstem internodes remained bigbh altholugh variable,througiloutt the enltire season ( table II). Theseresuilts suiggest that a considerable quantity of the'wC was incorporated into stemll tissue. and that theseasonal cbanges in activity of the older iiteriiodesdid ilot simplv represent translocatalble coimpoundsin tranisit to the roots.

Tranislocation of activity to the l "otS coincidedxv-itlb the cilanges inl export all(d import i-,f activityin the o0l( aid new ileedles. Following treatileintof the o0l( needles, translocation to tile r-oots was

Iligli at wveek 0 when the btud was jtist beginning toelongate, buit it decrease(d rapidly as the new silootexpailded and the needles began vigo0)ll0)0l elongationlActivity in tile roots again increase(l i)eginillg inl

week 4, when translocationi to tile new -iloot (leclined,aildi then increased markedly in w eek J whben trans-

location to the roots fronl the old neediles inlore tl.andoubled. Translocation to the root.s fromii tbe ilew

nee(iles also increatse(d rapidly beginnling ill w-eek 9.The developing bud for the follow iilg seasoln

becalme visibly evi(leilt ill week ilear tile end(l oftIle stenl elongation stage. Activity trallSlocalte(l tothe buid froml tile new ilee(lles lbegall increasillg at

w-eek 9, and bv week 19 the total activity exportedto tile bud had reaclbed 6.6 %. The anlotllut ofactivity contribute(d to the developing l)u(l froull theold llee(lles wass llegligii)le thlrotlgllout thy sealon.

New needlesOld needlesBud1967 stem1966 stem1963-65 stemnRootsWhole tree

New needlesOld needlesBud1967 steni1966 stemn1963-65 stemRootsWhole tree

1622

1623GORDON AND LARSON-PHOTOSYNTHESIS AND 14C DISTRIBUTION IN PINE

Discussion

The relative metabolic activity of differentmeristeniatic areas is important in determining thedistributioni of organic and inorganic constituentsin plants (16, 21). In this study of red pine, thedistributioni of 14C photosynthates may be interpretedby considering the source-sink relationships asso-ciated with the constantly changing patterns oforgan developmiient throughout the season. \Vhenconsidered seasonally, plant development presentsa continuumii and. as such, it is difficult either toseparate it intlo discrete stages or to assign degreesof importanice to 1 stage or another. Nevertheless.for our objecti-e of understanding the earlywood-latewood trainsition of wood formation, 1 develop-mental stage asstumed particular importance. Thisstage occturred near the end of rapid new needleelongationi when translocation of 14C photosynthateabruptly shifted from ian upward to a predominantlvdownward direction. This growth phase might bemore appropriately termed "new needle maturity,"for it signifies a metabolic state rather than a simplecessation of needle elongation. The metabolicchanges in the neiw needles evidently trigger verypronounced chlaniges throughout the tree. The peakof photosynthetic efficiency of the new needles anda large increase inl the export of photosynth'ate fromthe new needles occturred simultaneously. As indi-catc(l by this shift, the new needles not only wrereself-stufficieint. hut were now exporters of photo-synthate.

Coincidenit witlh these chaniges in the new needleswas an almost comiiplete reversal of translocationfrom the old needles. Very little photosynthate was

exported upward to the new shoot, and translocationwas now alimiost exclusively downward withl a new

surge goitng to the roots from needles of both ages.

Althouglh these changes were by no means as abruptas the discrete measurements imply, it 'is reasonableto assumiie thcat week 9 was representative of thetransitioil. These patterns of translocation of bothcomiiplemlenits of needles also created a temporarystate of imbalance within the tree. The increased'"C activity in the old needles when the new needleswere fed, for example, probably resulted from bi-directioinal translocation and diffusion as discussedrecently by Canny and Aglkham (3). It is note-

wor-tllhy, in this regard, that only 9 % of the 14Cisolated fromii these old needles was in an alcohol-insoluble form (table II).

These shifts in translocation have important con-

sequenices for wood formation. The transition fromearlywvood to latewvood formation in red pine beginsfirst at the stem base and progresses upward as theseason a(dvances (14). Latewood tracheids may bedistinguislhed from those of earlywood by a decreasein radial diameter and an increase in secondary wallthickening. Although these dimensional changesgenerally occtur simultaneously in nature, they can

be altered in1dependently by appropriate growth con-

trol (13, 14). Therefore, the gradient in the Ap-pearance of latewood tracheids upward in the stemwith time may or may not involve changes 'in bothtracheid dimensions, depending upon' the physio-logical state of the crown organs and the proximityof the crown to the xylem examined.' Evidence hasbeen presented supporting the hypothesis that tracheidradial diameter is regulated by auxin translocatedfrom the elongating shoot and needle meristems (14).Applying this hypothesis to our study, the prolonga-tion of needle growth and auxin synthesis by thelong photoperiod would promote continued formationof large-diameter tracheids. The increase in second-ary wall thickness, on the other hand, would occurwhen the metabolic sink created by the new shoothad been satisfied and its photosynthetic productionbecame available to the developing xylem;(13). Thecambium, being a diffuse meristem, is not a con-centrated sink for photosynthates and cannot completeeffectively with the mass meristems of the developingshoot early in the growing season. However, whenthe new needles reached a certain state of mattura-tion, they became .active exporters of photosynthate.The elimination-of' the new needles as a metabolicsink for photosynthate from the old needles, togetherwith the sudden availability of photosynthate fromthe new needles themselves, provided an increasedsupply for the developing xylem tracheids. Thesechanges, occurring in week 9, alo coincided withan increase in secondary wall thickening in the olderstem internodes. The earlywood-latewood transitionis always gradual in the juvenile wood of youngtrees and the crown-formed wvood of older trees.An abrupt latewood transition, or sometimes aprecocious change in only one tracheid dimension,can be induced by appropriate environmental condi-tions., The simultaneous appearance of latewoodtracheids with both narrow radial diameters andthick secondary walls results from the fortuitousoccurrence of both a decline of auxin synthesis andan increased availability of photosynthates associatedwith new needle maturity. Thus, both xylemtracheid diameter and wall thickening appear to bephysiologically correlated with needle development.

The final set of measurements in week 19 de-serves special consideration, since growth was thensomewhat atypical of the normal seasonal pattern.As mentioned previously, the trees were growingunder an artificially extended photoperiod that pro-moted slow needle elongation beyond the normaltermination date. Long days also promoted preco-cious bud development and, instead of proceedinginto dormancy, the buds broke into a second flushof growth. The renewal of metabolic activitv un-doubtedly accounted for the pronounced increase in'4C exported to the bud from the new n,eedles, andfor the increase in photosynthetic efficiency of bothcomplements of needles. There appeared to be astrong interaction between vigorous growth of theterminal meristem and increased photosynthetic effi-ciency of the older needles both at the beginning of

PLANT PHYSIOLOGY

the season ln (lduring the second flush. This in-crease in CO, assimilation may be related either tothe release of growth hormone byr the elongatingshoot as suggested by Bidwell and Turner (2), tothe provision of a new sink for photosvnthate (9),or to both mechanisnms.

The results of this study contribtute to the un,der-standing of latewood formiiation in trees and addsupport to prior hypotheses. Although the picttire isstill by no means complete, it appears that metabolicevents controlling shoot development, and morespecifically needle elongation, regulate the seasonalcourse of events in the cambium. Research is con-tinuing on the role of needle growth, maturation, and(senescence on tracheid(levelopment in the xylemi ofred pine.

Acknowledgments

The technical assistanice of G. . Buchschaclher anidG. L. Garton is gratefullI- ackinowledge(l. The ouIngred pines were supplied h- the nursery of the Rhine-lander Division, St. Regis Paper Comrpany.

Literature Cited

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2. BIDWELL, R. G. S. XN D W. B. TUTRNER. 1966. Ef-fect of groi\-th regulators on CO, assimilationin leaves, anid its correlationi with bud break re-sponse in photosynthesis. Plant Physiol. 41: 267-70.

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