University of Dayton
eCommons
Biology Faculty Publications
Department of Biology
1979
Control of Partitioning and Export of Carbon in
Leaves of Higher-Plants
Donald R. Geiger
Follow this and additional works at: http://ecommons.udayton.edu/bio_fac_pub
Part of the Plant Sciences Commons
eCommons Citation
Geiger, Donald R., "Control of Partitioning and Export of Carbon in Leaves of Higher-Plants" (1979). Biology Faculty Publications.
Paper 31.
http://ecommons.udayton.edu/bio_fac_pub/31
This Article is brought to you for free and open access by the Department of Biology at eCommons. It has been accepted for inclusion in Biology
Faculty Publications by an authorized administrator of eCommons. For more information, please contact [email protected],
[email protected].
Control of Partitioning and Export of Carbon in Leaves of Higher Plants
Author(s): Donald R. Geiger
Source: Botanical Gazette, Vol. 140, No. 3 (Sep., 1979), pp. 241-248
Published by: The University of Chicago Press
Stable URL: http://www.jstor.org/stable/2474571 .
Accessed: 14/11/2013 10:23
Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .
http://www.jstor.org/page/info/about/policies/terms.jsp
.
JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of
content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms
of scholarship. For more information about JSTOR, please contact [email protected].
.
The University of Chicago Press is collaborating with JSTOR to digitize, preserve and extend access to
Botanical Gazette.
http://www.jstor.org
This content downloaded from 131.238.108.32 on Thu, 14 Nov 2013 10:23:55 AM
All use subject to JSTOR Terms and Conditions
BOT. GAZ.140(3):241-248. 1979.
? 1979 by The Universityof Chicago. 0006-8071/79/4003-0017$00.81
CONTROL
OF PARTITIONING
AND EXPORT
OF HIGHER
OF CARBON
IN LEAVES
PLANTS'
DONALD R. GEIGER
Biology Department,Universityof Dayton, Dayton, Ohio 45469
Withinsource leaves, partitionof assimilatedcarbon and exportare regulatedin responseto both leaf
and plant ontogenyand to environmentalconditions.Systemgoals, adaptive responses,controlmechanisms,and informationfloware developed fromthe viewpointthat a well-adaptedplant is an integrated
system.Regulation of partitioningand export involves both feedforward
controland feedbackhomeostasis. Export is controlledby regulationof metabolismwhich supplies assimilatedmaterialto be translocated, by controlof effluxinto the free space of materialdestined for export,and by regulationof
phloemloading. Controlof exportby the lattertwo processesdependson responsivemetabolicprocesses
that can supply sucroseand othertransportmoleculesupon demand. An integratedmodel incorporating
these featuresposits that controlof exportby mechanismslocated in the source leaves is an important
means of regulatingtranslocation.
Introduction
conTranslocationundervarious environmental
stagesofplantdevelopment
ditionsand at different
ofpartition
showsa remarkable
degreeofregulation
and exportof materialderivedby photosynthesis.
Controlof initiationof exportand regulationof
partitionof metabolitesare evidentduringplant
development
(FELLOWSand GEIGER 1974;TURGEON
and WEBB 1975). Environmentalconditionsand
experimentalmanipulationswhich alter carbon
economywithinthe plant producemarkedchanges
in rates of exportand in patternsof distribution
betweenregionsof theplant (THORNE and KOLLER
1974; GEIGER 1976; BODSON et al. 1977; BORCHERS
and SWANSON 1977).
WELL-ADAPTED SYSTEMS
A successfully
adapted plant is a finelyadjusted
systemwith the capacity to respondto stages of
by welldevelopmentand changesin environment
developedadaptivemechanisms.Exportof assimilates is an aspectof plantfunctionwhichis subject
to close regulation.Regulationof exportprovidesa
means of maintainingor restoringcarbonbalance
withinexporting
leavesand betweenpartsofa plant.
In addition,it allowsa plant to respondto changes
stages of development
in requirements
at different
conditions.Until
and underdiverseenvironmental
we understandregulationof export,we have onlya
ofplantfunction.
veryincompleteunderstanding
as adaptive
Analysisof exportand partitioning
mechanisms
whichare partofintegratedsystemsof
1 Adapted frommaterialpresentedforthe AmericanAssociation for the Advancementof Science Symposium"Plant
Growth Regulators: Their Potential for Increasing Agricultural Productivity"held at Houston, January8, 1979, and
for the MSU-DOE Plant Sciences Laboratory Workshop
"Partitioningof Assimilates"held at Michigan State University,May 7-9, 1979.
ManuscriptreceivedApril 1979.
controlsin higherplantsmay providenew insights
into plant function.Analysisand research,based
on the conceptsof "source strength"and "sink
hav, providedinsightsand workinghystrength,"
pothesesforvigorousresearchin the area of translocation (WARREN WILSON 1972; WAREING and
PATRICK 1975). It is anticipatedthat an approach
will
natureofplantfunction
based on theintegrated
of researchon exportand
add to the productivity
partitionin thewholeplant.
ELEMENTS OF THE PLANT SYSTEM
A well-adaptedplant appearsto have integrated
systemswithseveralkeyelements:
1. SYSTEM GOALS.-Inherited patterns of adapta-
tioncontribute
to the adaptivesuccessof the plant
conditionsand
withina range of environmental
developmentalstages. Balanced allocationof fixed
carbonamongparts of the plant withretentionof
adequate carbonreservein sourceleaves is an example of such a systemgoal whichlikelyleads to
survivalsuccess.
2. ADAPTIVE RESPONSES AND SET POINTS.-These
means,on a morelimitedscale,promotethe attainmentof systemgoals. Adjustmentof partitionof
carbon into starchsynthesis,therebyprovidinga
certainminimumlevel of starchthat allowsexport
thenight,is a possibleadaptiveresponse.
throughout
The sucroselevel may functionas a set point for
helpingachievecarbonbalance undera givensituation.
3. CONTROL MECHANISMS.-Physiological and
metabolicfunctionsprovide the basic means by
oftheplantcarryout adaptiverewhichsubsystems
sponsesor attainand maintaina certainset point.
ofan enzymemayserveas a
inhibition
End-product
thathelpsattaina certainlevelof
controlmechanism
metaboliteand thus helps carryout an adaptive
responseto changingconditions.
4. INFORMATION FLOW.-This involves communi-
241
This content downloaded from 131.238.108.32 on Thu, 14 Nov 2013 10:23:55 AM
All use subject to JSTOR Terms and Conditions
BOTANICAL GAZETTE
242
cationof information
concerningan environmental
conditionor of a statewithintheplantto a control
of a hormonebetweenthe
The transfer
mechanism.
and a targetorganor transmittal
siteofitssynthesis
ofpressurewithina fileofsieve elementsare examtransfer.
ples ofinformation
Analysisof thesecontrolsystemsnot onlyprombut also may
isesto giveinsightsintoplantfunction
help improvecrop yield. The hope for increasing
yield is based on the beliefthat adaptive mechanismsoftheplant,whichareorientedto reproductive
successand continuanceof membersof the species,
are not always optimallyadapted to humankind's
goal ofincreasedcropproduction.
VARIOUS
CONTROL PATTERNS
[SEPTEMBER
controloperatesoffreguFeedforward
environment.
processesor in
laritiesin thepatternofdevelopment
successfulpatternsof responseto a givenenvironmentalstimulus.
Examinationof adaptive responsesand control
dealingwithregulationof export,both
mechanisms
as well as feedbackconin the lightof feedforward
Whilethe suggested
insights.
new
to
lead
trol,will
analysismay raise morequestionsinitiallythan it
yieldsanswers,I anticipatethat new workinghypotheseswillemergeand thatthesewillhelp orient
productivefutureresearchin theareas ofregulation
ofpartitionand export.
MEANS
TO CONTROL EXPORT
Studieson thecontrolof exportprovideevidence
that there are a numberof regulatoryprocesses
affectingtranslocation(fig. 1). There are three
groupsof processeswhichregulateexportfroma
sourceleaf.
The firstgroupofprocesses(fig.1, 1-7) resultsin
metabolic controlof availabilityof sucrose and
moleculesforexport.Products
otherphloem-mobile
of carbon fixationmay be directedinto starch
synthesis(1) or may exitfromthe chloroplastby a
(2). Undercertainconditions
mechanism
transporter
starchmay be mobilized(3) and the solubleintermediatesexit throughthe chloroplastenvelope(2).
and growth
synthesis,
photorespiration,
Respiration,
A portion
from
export.
compounds
carbon
(4) divert
of the fixedcarbon is directedinto synthesisof
sucrose and other phloem-mobilemolecules (5).
These compoundsmaybe stored(6) to be mobilized
at somelatertime(7). As a group,thesemetabolic
processescontroltheavailabilityofsucroseandother
moleculesforexport.
The secondprocess(fig.1, 8) controlsthe exitof
sucrose or other exportablemoleculesfrom the
mesophyllinto the freespace. Molecules destined
orstoragevia
forexportmovefromsitesofsynthesis
thesymplastto theregionneartheminorveinsieve
tubes and companioncells where they enter the
freespace,possiblyfromphloemparenchymacells.
This controlprocessregulatesexportby compartmentalisolationfromthe site ofphloemloading.
The thirdtypeofcontrolprocess(fig.1,9) directly
affectsphloemloadingby regulatingthe activeuptake of sucroseor othermoleculessuch as amino
acids intosievetubes.Aspectsofthismodelrelating
to exitof sucrosefromthe mesophyllinto the free
space and to phloemloadingwerediscussedby GEIonly controlof partitioning
GER (1975). Therefore,
and exportwillbe discussedhere.
Observationsof patternsof regulationof export
lead to the realizationthat some responseshelp
systemwhile
maintaina givenstatein thecontrolled
othersexhibitanticipatorycontrol.ROSEN (1975)
comparedthesetwopatternsundertheheadingsof
feedback and feedforward
adaptive mechanisms,
is an adaptationof his
The following
respectively.
analysis to the contol of partitioningand export
withinsourceleaves.
Feedback homeostatsmaintainsome functionof
a controlledsystemat a constantlevel,helpingto
maintain constantsystemquality in the face of
environmental
changes.A given feedbackcontrol
willregulatea particularquantityin the
mechanism
to error;that is, to
specifically
system,responding
thedeviationfroma set conditionin theplant.The
controlmechanismsenses the state of the system
onlyindirectly.
directlyand theenvironment
controlssensea presentstate which
Feedforward
is relatedto some futurestate of the system.For
state,suchas a favorable
instance,an environmental
photoperiod,bringsabout flowerinitiation,which
The enwilloftenbe followedby fruitdevelopment.
vironmental
cue probablybringsabout the changes
and
inplantfunction
neededto providefornutrition
ofthefruit.The patternofresponseto
development
the state sensed is determinedwithinthe genetic
makeupof the plant. Similarly,a givendaylength,
lightquality,and lightintensityhelp determinea
certaingrowth
patternofa leafwhichis suitedto the
seasonal conditionsahead. Controlis not based on
an errorsignalbut on perceptionof a state which
a sequence.The signaleventis one that is
triggers
generallyfollowedby certaineventsor conditions.
In a sense,thereis a modelof the patternof the
anticipatedeventsbuilt into the plant. Sometimes
this sequence takes the formof a developmental
processsuch as sourceleafmaturation;othertimes
Metaboliccontrolof availabilityof compounds
patternofadaptationin responseto
it is a successful
forexport
the onset of an environmental
state, as with seaSYSTEM GOAL
sonal responsessuch as flowerdevelopmentor the
regulaMetabolic controlof availabilityof compounds
initiationof cold hardiness.In feedforward
able to be exportedappears to be particularlyimtion,thereis needforsomemechanismto sensethe
This content downloaded from 131.238.108.32 on Thu, 14 Nov 2013 10:23:55 AM
All use subject to JSTOR Terms and Conditions
GEIGER-CONTROL
1979]
OF PARTITIONING
AND EXPORT
SOURCE
MESOPHYLL
CHLOROPLAST
243
SINKS
PATH
FREE
SPACE
*
MINOR
VEIN
PHLOEM
*
SIEVEELEMENTS *
OF DEVELOPING
CELLS
TISSUES
ANDSTORAGE
REGIONS
CYTOPLASM
plasmalemma
plasmalemma
of
of
phloem arenchyma sieveelements
and companion
ce[ls
chloroplast
envelope
cel[s
starch
89
andother
-intermediates-,_O
p, ntrmeiaes
-mobile
homintermediates
4
4
competing
uses offixed
carbon
uptake
zzii]and
sucrose
C02
IL..metabolism
sink
compounds
competing
uses offixed
carbon- growth
6
tissues
7
synthesis
respiration
photorespiration
//
s
t
e
stored
~~~~~~~sucrose
~~~~~~~~~~outside
export
X
FIG. 1.-Possible controlpoints forregulatingthe partitioningof assimilatedcarbon and the exportof phloem-mobilecompounds. Steps 1-9 are discussedin the text; step 10 is the controlexertedby the structuralfeaturesof the path of translocation;
step 11 is the controlexertedby transportout of the sieve tubes and conversionof transportmoleculesin sinkregions.
portantfor achievingthe generalsystemgoal of
maintaining
carbonbalance undervariouslevelsof
nutritionalstatus. Plants are able to adapt to a
wide rangeof daylengthsand variationsin photon
fluxdensities.Underthesevariousconditions,
steps
1 through7 (fig.1) providebalanced allocationof
carbonwithinsourceleaves and betweenthemand
the sink regions.Leaves differin the patternof
carbonmetabolismduringdevelopmentand in the
allocationof carbonforvariouspools and processes
under differentenvironmentalconditions.It is
necessaryto maintaincarbonbalance in the midst
of leaf-metabolism
changeswhichoccurin response
to environmentalconditionsand developmental
stages. In nature,success in meetingthis goal of
balancedcarbonnutrition
is gaugedby competitive
and adaptive abilityleading to survivaland dispersal. In agricultural
practice,success in relation
to thissystemgoal is measuredin termsof a favorable harvest index and yield under a range of
conditions.
ADAPTIVE
RESPONSES
AND SET POINTS
Recentdata enableus to identify
severaladaptive
responsesrelatedto thissystemgoal. For a source
leaf with a given nutrientstatus and at a given
developmental
stage,exportofrecently
fixedcarbon
is linearlyrelatedto therateofnetcarbonexchange
exceptat photonfluxdensitiesnear the lightcompensationpoint (SERVAITES and GEIGER 1974; Ho
1976, 1978). Leaves with a highercarbon status
exportat a higherrate fora givennet carbonexchangerate and also at a higherrate in the dark
(Ho 1977). Plants accommodateto shorterphotosyntheticperiods by storing,duringthe day, a
largerproportionof the fixedcarbonforexportat
night(BODSONet al. 1977; CHATTERTON and SILVIUS
1979). Under some conditionspart of the stored
assimilatedcarbon is exportedduringthe subsequent light period (PEARSON 1974; Ho 1976;
1977). Changes in
GORDON, RYLE, and POWELL,
statusor daylengthcause changesin the
nutritional
proportionof fixedcarbonwhichis exported,with
over5-10 days.
adjustmentsoccurring
While regulationof transportfroma leaf is an
carbon
or restoring
meansofmaintaining
important
balance fora matureleaf,the natureof set points
and adaptiveresponsesis farfromclear.It appears
that thelevelof starchat the end of a nightperiod
under a given set of conditionsis relativelyfixed
1976; CHATTERTON and SILVIUS 1979).
(CHALLA
It is not knownwhetherthe levelof starchis regulatedby a feedbackmechanismor is theresultofan
mechanismactivatedby some
adaptivefeedforward
cue and relatedto energydemand
environmental
duringthedarkperiod.
CONTROL
MECHANISMS
INFORMATION
AND
TRANSFER
A number of workinghypothesesconcerning
whichcontrolexportin responseto the
mechanisms
statusofsourceleaveshave been
carbonnutritional
advanced.A key hypothesis-thatsucroseconcentrationin the sourceleafmesophyllcontrolsexport
(Ho 1976)-is anotherwayofstatingthatmetabolic
controloftheavailabilityofcompoundsforexportis
exportand in achievingthe
in controlling
important
goal of carbonbalance, both withinsource leaves
and fortheplant.Duringthelightperiod,netcarbon
exchangerate and reservecarbonstatus are major
This content downloaded from 131.238.108.32 on Thu, 14 Nov 2013 10:23:55 AM
All use subject to JSTOR Terms and Conditions
244
BOTANICAL GAZETTE
and export
of sucroseconcentration
determinants
rate (Ho 1978). At night,the level of starch,and
perhapsotherreserves,is the chieffactorgoverning sucroselevel and export(Ho 1978). Shortening
period resultsin increased
of the photosynthetic
partitionof fixedcarbon into starch duringthe
day (CHATTERTONand SILVIUS1979).
following
Little is known concerningthe ways in which
carbonstatus of a leaf controlsallocationof fixed
carbon amongstarchstorage,growth,respiration,
and sucrosestorageoutsidethe exportpool. Nor is
muchknownabout mobilizationof starchor stored
sucrosein responseto leaf carbonstatus. Regulationoftheprocesseswhichcontroltheavailabilityof
sucroseand otherexportcompoundsto leaf carbon
statusneedsto be studied.
Leaf carbonmetabolismduringleafdevelopment
is also the subject of close control(TURGEON and
WEBB 1975). Dramaticchangesin carbonmetabolism occurduringleafdevelopmentand affectsynthesisofsucroseand othercompounds(GIAQUINTA
1978). It remainsto be elucidatedto what extent
synthesisand metabolismof exportablecompounds
controlexportduringleafdevelopment.
of compoundsavailable
Controlof efflux
forphloemloading
SYSTEMGOALS
ofcompoundsutilizedin phloem
Controlofefflux
loadingappearsto help providethe additionalcarbon requiredby sink regionsunderfavorableinorganic nutrientstatus. Availabilityof adequate to
abundantlevelsof potassium,nitrogen,and phosgivesrise to various
phorusin variousproportions
patternsof growthwhichare recognizedin agronomicliterature.Above-adequatelevels of potassiofassimilatedcarbonexum increasetheproportion
ported to sinks,includingfruitsand tubers (HAEDER,
MENGEL, and FORSTER 1973; MENGEL and VIRO
cited
1974;MENGEL and HAEDER 1977andliterature
therein).
Integral functioningof a plant necessitatesa
balancebetweenthe availabilityof inorganicnutrientsto growingregionsof a plantand thesupplyof
requiredforgrowthto thesesinks.
organicnutrients
Mechanismsexistwhichare orientedto providing
adequate exportof assimilateto meet the organic
nutrientrequirementsset by a given level and
balanceofinorganicnutrients.
ADAPTIVE
RESPONSES
AND SET POINTS
potassiumpromote
Increasedlevelsof free-space
exportfromsugar-beetsourceleaves (DOMAN and
GEIGER 1979). Increasedlevelsofpotassiumdo not
increasenet carbonfixationbut increaseallocation
offixedcarbonforexport.At least forpotassium,it
appears that adequate to abundantlevelspromote
of assimilatedcarbon
exportof a greaterproportion
to sinkregions.
[SEPTEMBER
FLOW
AND INFORMATION
CONTROLMECHANISMS
GEIGER
and
The resultsofrecentstudies(DOMAN
1979) suggesta workinghypothesisforregulation
of exportby potassium.Applicationof potassium
ions to the freespace of sugarbeet source leaves
promotes effluxof '4C-labeled compoundsfrom
to approximately
in 1'4CO2
leaves photosynthesizing
out
the same extentthat it promotestranslocation
of the leaves. The same levelsof potassiumdo not
increasethe loadingand exportof '4C-sucrosesupplied to sourceleaves. Potassiumincreasesphloem
sucroseconcentraloadingand exportby increasing
tion in the freespace. Similareffectsfornutrient
phosphorusand nitrogenare suglevelsofinorganic
gested by the observationthat deficienciesof
phosphorusand nitrogencaused a decreasein the
intosolutionsof assimilatedcarbonfromthe
efflux
mesophyllofbeet leaves (KAMANINAand ANISIMOV
1977).
in the source leaf
The potassiumconcentration
about the
free space likelyprovidesinformation
potassium status of the plant. In so doing, the
potassium level may help set the rate of export by
regulatingthe effluxof sucrose destined forphloem
loadingand export.It remainsto be establishedif
this mechanismis the basis forincreasedphloem
broughtabout by an inloadingand translocation
creasein potassiumnutritionof plants underfield
conditions.The mechanismmay be part of a feedsystemofprocesseswhichreadiestheplant
forward
forincreasedgrowthin responseto favorableinorganicnutrientstatus.
Directcontrolofthe phloemloadingprocess
SYSTEMGOALS
Boththerapidchangesin sinkdemand,associated
conditions,and the
withchangesin environmental
gradual changes involved in progressive stages of
developmenthelp restoreor maintaincarbon balance. Direct controlof phloemloadingseemsto be
in theresponseofexportto changesin
instrumental
sinkdemand.Initiationof exportfroma maturing
sourceleaf appears to occurwhenphloemloading
in
highsoluteconcentration
developsa sufficiently
the minorvein phloemof the leaf (FELLOWSand
GEIGER 1974). The increase in phloem loading
appears to be part of a feedforwardmechanism consisting of a series of events which anticipate the
mature state of the leaf as a source of fixedcarbon
forthesinkregions.Phloemloadingalso appearsto
adjustrapidlyto changesin sinkdemandoccasioned
by shadingor by loss of sourceleaves. In both the
genetically programmed response and in a precipitous change, the plant appears adapted to restore
carbonbalance,in part,by
and maintainsufficient
changingthe rate of phloemloadingand exportin
thefaceofmarkedchangesin sinkdemand.
This content downloaded from 131.238.108.32 on Thu, 14 Nov 2013 10:23:55 AM
All use subject to JSTOR Terms and Conditions
GEIGER-CONTROL
1979]
ADAPTIVE
RESPONSES
OF PARTITIONING
AND SET POINTS
whererelaStudiesofexportundercircumstances
tivelyrapidchangesin sinkdemandoccurhave led
A rapid changein sink
to severalgeneralizations.
demandinitiatedby removalor shadingof leaves
changein export
bringsabouta rapidcompensatory
withoutchangingthe net carbonfixationrate over
the shortterm,probably1-2 days (GEIGER 1976;
BORCHERS and SWANSON 1977). Exportappears to
changein a mannerwhichrestoresand maintains
balance in growth.For example,if the sourceleaf
that serves as a major supplierof one-halfof a
developingsinkleafis darkenedor excised,another
sourceleafthatis theprimarysupplierfortheother
half of the developingsink leaf rapidlyincreases
export(BORCHERS and SWANSON 1977). The rate
sourceleafmaintains
oftransport
fromtheremaining
exportto its originalprimarysinkwhileincreasing
exportto compensatecompletelyfor the loss of
materialfromtheothersourceleaf.This adjustment
maintainsbalanced growthin both halves of the
of theproducts
leafwhilechangingthepartitioning
in thesourceleaf.
ofphotosynthesis
Followinga rapidchangein sinkdemand,suchas
that producedby shadingor source leaf excision,
there is a gradual increasein net photosynthetic
sourceleaves over
carbonfixationin the remaining
5-10 days (THORNE and KOLLER 1974; literature
citedin GEIGER 1976). Increasesin ribulosebisphosorphosphoenolpyruvate
carboxylphatecarboxylase
thatan
ase perunitleafarea supportthesuggestion
apparatusis induced
increasein thephotosynthetic
(WAREING, KHALIFA, and TREHARNE 1968; THORNE
and KOLLER 1974).
With the systematicchangeswhichare part of
ofa plant,bothexport
theontogenetic
development
and net photosynthetic
carbon fixationincrease
concomitantlywith the increased sink demand
(FLINN
1974; literaturecited in GEIGER 1976) or
withsourceleafmaturation(FELLOWS and GEIGER
it seems that
1974). Under these circumstances,
adjustmentsare anticipated,as would be expected
fora feedforward
response(ROSEN1975).
MECHANISMS
AND INFORMATION
FLOW
In ontogenetic
of a leaf,the advent
development
of phloemloading is part of the series of events
leading to attainmentof source leaf status. The
mechanismby whichthe phloemloadingcapacity
of source leaves is acquired by the
characteristic
membranesof theminorveinphloemis notknown.
Possiblitiesincludeinsertioninto the membraneor
activationof the sucrosetransportsystemor possibly a modificationof symplastictransportby
closure of plasmodesmatalconnectionsbetween
minorvein phloemand the surrounding
mesophyll.
The mechanismfortheinitiationofphloemloading
AND EXPORT
245
and regulationof its onsetneedsto be investigated
further.
The increasein phloemloadingand exportassosinkdemandis morerapid,
ciated withheightened
occurringsoon afterthe onsetof conditionswhich
promotesink demand.A feedbackcontrolsystem
to a setpointis suggestedby thistypeof
responding
response. Increased export from the remaining
source leaves, followingsource
photosynthesizing
leaf removal or shading,is likely to reduce the
of the contentsof the sieve
sucroseconcentration
tubes and companioncells of the minorveins in
pressurein
theseleaves. A decreasein hydrostatic
thesieveelementsof theminorveinswouldaccompany thedecreasein theirsucrosecontentfromthe
steady-statelevel associatedwith the formerrate
of export.It seems a tenablehypothesisthat the
sieve tubes respondto the decreasein solute conincreasein
centrationor turgorby a compensatory
phloemloading.MILBURN (1974) proposedthat a
pressurein
sinkinducespressureflowby regulating
the sieve tubes and that solutesare mobilizedand
loaded rapidlyin responseto exudationfromstem
of increasedeffluxof solutes
incisions.Information
froma sourceleaf intosinkswouldbe transmitted
to its minorveins by the decreasedturgorin the
sievetubes.
Severalpiecesof evidencesupportthe occurrence
of thisproposedresponseof increasedloading.The
of solutein variouscells of sugarbeet
distribution
sourceleaves (GEIGER et al. 1973), carriedout by
plasmolysisof tissue followedby electronmicroscopy gave values forwaterpotentialof the minor
veinsievetubecontentsin excessofthoseassociated
Other methods
with a 1-M solute concentration.
lessthanhalfthisvalue
revealsoluteconcentrations
for sieve tubes of herbaceous plants (GEIGER,
SAUNDERS, and CATALDO 1969; FISHER 1978). Various possiblesourcesof errorcan be dismissedfor
the mostpart, leavingus with the likelihoodthat
the minor veins had loaded sucrose from the
responseto the turgor
in a compensatory
mesophyll
reductioncaused by immersionof the leaf in the
mannitolosmoticum.
Somewhatmoredirectevidenceof compensatory
phloemloadingcomesfroma seriesof experiments
by GEIGER et al. (1974). Applicationof 0.8 M mancarbonderivedfrom20 mM
nitolto a leafexporting
14C-sucrosewhichwas suppliedto the abradedsurdecreasein
faceof a sourceleafcaused a temporary
export.By the end of 30-60 min,exportincreased
rate.The abilityof the leaf to
to the pretreatment
maintaina highrateofexportofsucrosefroma leaf,
the freespace of whichwas in contactwith0.8 M
by
mannitol,supportstheexistenceof a mechanism
whichthesourceleafis able to adjustphloemloading
The decreasedosmoticpotentialof
compensatorily.
the free-spacesolutionappears to have withdrawn
This content downloaded from 131.238.108.32 on Thu, 14 Nov 2013 10:23:55 AM
All use subject to JSTOR Terms and Conditions
246
BOTANICAL GAZETTE
[SEPTEMBER
water and reduced the pressureinside the sieve
cell complex,therebyinitiatingintube-companion
creasedloadingoftheminorveinphloemand restoringexport.
or turgorperResponsesto soluteconcentration
mit phloemloading to respondto increasedsink
aboutthelevelofdemand
demand,withinformation
sievetubeturgororsoluteconcenmediatedthrough
trationchanges.Accordingto this model,the set
pointvalue forsieve tube turgorpressureor solute
the actual source
largelydetermines
concentration
withthe maximumpotentialforphloem
strength,
potentialsourcecapacity.
loadingrate determining
Presumablyit is the turgoror soluteconcentration
set point or the capacityfor active transport,or
both, which increasesduringthe maturationof
of theirsourcestatus.Exleaves and development
perimentsare needed to verifythese postulated
and meansofinformation
transfer.
mechanisms
of photosynthesis
in the sourceleaf and relatein a
special way to the systemgoal of maintenanceof
carbonbalance in the matureleaves of the plant.
Processesin this categoryrespondto leaf carbon
statusand specifically
to factorssuchas starchlevel,
photoperiod,
and net carbonfixationrate.
On the otherhand, mechanismswhich control
phloemloadingmoredirectly(fig.2, 8 and 9) are
dependentfortheireffectiveness
upon theabilityof
sourceleafmetabolism
to respondto thedemandfor
substancesto be exported.The resultsof experimentsdescribedin theprecedingsectionshowthat
sourceleafmetabolismis able to adjust rapidlyto
meet the demand for increasedsucrosesynthesis.
Furthermore,
theseadjustmentsare made without
increasednetcarbonfixation,
at least overtheshort
term.
A phosphate/triose-phosphate
exchangeshuttlein
thechloroplast
envelope(HELDTet al. 1977) appears
to be the key to increasedsucrose synthesisin
Controlof exportand responsesof source
responseto thedemandcreatedby increasedphloem
leaf metabolism
loading. Stoichiometric
relationshipsamong synMechanismswhichregulateexportby controlling thetic reactionsinvolvingC02, triose phosphate,
the availabilityof sucroseforphloemloading(fig. sucrose,and starch (WALKERand HEROLD1977)
intothewholeof
of
appear to providethe basis for responsiveness
2, 1-7) presumablyare integrated
sourceleafmetabolismto a demandforsucrosefor
These controlprocessesdeal
sourceleafmetabolism.
and allocationof theproducts export.Particularlyimportantis the balancedstoiwiththepartitioning
MESOPHYLL-
4
CHLOROPLAST
INTERMED
IATES
71
r
TRIOSE-P
.-1
t
\SUCROSE-P
Pi
t
74
TRIOSE-P
~~~~~CO2
'
--
CO2 SUCROSE--
TRANSPORTji
SUCROSE XU
T~~-- O2SURIOSE-P4
~~~~~SUCROSE
~~~~~~~
wIOSE-P
>
*t
DTRIOSEp
CO2TOSUCROSE ~~~~~~~~~~~~~~~~~~~~~~~SCRS
________
INFOR
MAT
ION
FREEE i
RSPAC
SU
i<A4[FRESA
~~TRIOSE-P
3 POINT
POSSIBLECONTROL
PHLOEMPARENCHYMA
SE-CCCOMPLEX
GROWTH
SYNTHESIS
RESPIRATION
PHOSPHATR
EXPORTED
SUCROSE
TU OO
N~~~~~~~~~~~~~~~~~HC
POOE
STARCH
D
SPACE_ 4-MINOR VEIN--_
14-FREE
PLASMLEMMA
PLASMPALEMMA
p.
P1
STARCH
\
CYTOPLASM
CHLOROPLAST
ENVELOPE
|D
EFFLUXE
w
OFAC
| SUCROS
|
SUCROSE
SIEVOEEEET
\
SPA
RESPIATIO
_______________________________________________________CR_E
FIG. 2.-Detail of a model forcontrolof partitioning
of assimilatedcarbon and exportshowingproposedmechanismsforthe
regulationof phloemloading (steps 8, 9) as well as those involvedin supplyingsucrosein responseto increasedphloemloading
(steps 5-7).
This content downloaded from 131.238.108.32 on Thu, 14 Nov 2013 10:23:55 AM
All use subject to JSTOR Terms and Conditions
1979]
GEIGER-CONTROL
OF PARTITIONING AND EXPORT
chiometrybetweenthe supply of inorganicphosphate requiredforthe exit of triosephosphateand
thereleaseof inorganicphosphateduringsynthesis
of sucrosefromtriosephosphate.Joinedwith the
ofsucrosephosphatesvnthetase
feedbackinhibition
by sucrose,thisbalancedstoichiometry
permitsleaf
metabolismto providesucroseat a rate called for
by processeswhichregulatephloemloading.
247
respondto the set point of sieve tube turgoror
soluteconcentration,
withefflux
beingpromotedby
the steepenedsucrosegradient.The levelof the set
point and the rate at whichphloemloading can
occur constitutethe controlsfor source capacity.
Increase in sink demand,whichlowersthe solute
contentof the sieve tubesfromone or moresource
leaves,lowerssoluteconcentration
and turgorin the
sieve tube-companioncell complexof the minor
veinsand bringsabout a compensatory
increasein
loadingin the affectedsourceleaf. Both increased
effluxof sucroseand increasedloading cause increasedturnoverof cytoplasmicsucrose.As a consequence,the rate at whichinorganicphosphateis
generatedduringsucrosesynthesisincreases,promotingexitoftriosephosphatefromthechloroplast
and, in some cases, the mobilizationof starch to
triosephosphate.
Clearly these suggestionsare based on both a
considerableamountof speculationalongwithconsiderabledata and analysis.More experiments
are
needed to test the hypothesesadvanced. It seems
likelythattheanalysesbased on theconceptof the
plantas a well-integrated,
responsivesystemwillbe
productive.
Summary
Two major groupsof processesregulateexport.
One groupcontrolsthe availabilityof sucrosefor
exportin keepingwiththe ontogenetic
stage of the
leaf and in responseto factorssuch as leaf carbon
statusand netphotosynthesis
rate.The systemgoals
ofcarbonbalancewithinthesourceleafand between
thesourceleafand therestoftheplantare servedby
theseregulatory
processes.
A secondsetofprocessesregulatesphloemloading
ofsucrose
moredirectly,
controlling
eithertheefflux
destinedforloadingor the active transportstep of
phloemloading.These controlmechanisms
are more
responsiveto conditionsoutside the source leaf,
such as the inorganicnutrientstatus and sink
demand,and servesystemgoals relatedto overall
plantcarbonbalanceand allometric
growth.A mark
of thissetofcontrols
is itsdependenceonresponsiveAcknowledgments
ness of sourceleaf metabolismto supplywhat is
The support of National Science Foundation
neededforsynthesisof sucroseforphloemloading.
Certainsubstancesin the freespace may promote grantPCM77-15875is gratefully
acknowledged.I
of sucroseforsubsequentloadingand export. also wishto thankmycolleaguesforhelpfuldiscusefflux
sionsofideas containedin thispresentation.
ofsucroseduringphloemloadingmay
The transport
LITERATURE CITED
BODSON,M., R. W. KING, L. T. EVANS,and G. BERNIER.
1977. The role of photosynthesisin floweringof the longday plant, Sinapis alba. Australian J. Plant Physiol. 4:
467-478.
BORCHERS,C., and C. A. SWANSON.1977. The kinetics of
compensatedtranslocationin Phaseolus vulgarisL. Plant
Physiol. 59 (suppl.): 125
CHALLA, H. 1976. An analysisof the diurnalcourseofgrowth,
carbon dioxide exchangeand carbohydratereservecontent
ofcucumbers.Agr.Res. Rep. 861. CentreforAgrobiological
Research,Wageningen,The Netherlands.
CHATTERTON,N. J.,and J.E. SILVIUS. 1979. Partitioninginto
starchin soybeanleaves. I. Effectsofphotosynthetic
period
duration.Plant Physiol. (in-press).
DOMAN, D. C., and D. R. GEIGER. 1979. Effectof exogenously
suppliedfoliarpotassiumon phloemloadingin Beta vulgaris
L. Plant Physiol.,vol. 64.
and
FELLOWS,R. J., and D. R. GEIGER. 1974. Structural
physiologicalchanges in sugar beet leaves duringsink to
sourceconversion.Plant Physiol. 54:877-885.
FISHER, D. B. 1978. The estimationof sugar concentration
in
individualsieve-tubeelementsby negativestaining.Planta
139: 19-24.
FLINN, A. M. 1974. Regulation of leafletphotosynthesis
by
developingfruitin the pea. Physiol.Plantarum31:275-278.
GEIGER, D. R. 1975. Phloemloading.Pages 395-431 in M. H.
Z1MMERMANN and J. A. MILBURN, eds. Transportin plants.
I. Phloem transport.Springer-Verlag,
New York.
. 1976. Effectsof translocationand assimilatedemand
on photosynthesis.Can. J. Bot. 54:2337-2345.
GEIGER, D. R., R. T. GIAQUINTA, S. A. SOVONICK, and R. J.
FELLOWS. 1973. Solute distributionin sugar beet leaves in
relationto phloemloadingand translocation.Plant Physiol.
52:585-589.
GEIGER, D. R., M. A. SAUNDERS, and D. A. CATALDO. 1969.
Translocationand accumulationof translocatein the sugar
beet petiole. Plant Physiol. 44:1657-1665.
GEIGER, D. R., S. A. SOVONICK, T. L. SHOCK,and R. J.
FELLOWS. 1974. Role of freespace in translocationin sugar
beet. Plant Physiol. 54:892-898.
GIAQUINTA, R. T. 1978. Source and sink leaf metabolismin
relation to phloem translocation.Carbon partitioningand
enzymology.Plant Physiol. 61:380-385.
GORDON, A. J.,G. J. A. RYLE, and C. E. POWELL. 1977. The
strategyof carbon utilization in uniculm barley. I. The
assimilated"4C.J. Exp.
chemicalfate of photosynthetically
Bot. 28:1258-1269.
HAEDER, H. E., K. MENGEL, and H. FORSTER. 1973.The effect
of potassiumon translocationof photosynthatesand yield
patternof potato plants. J. Sci. Food Agr. 24:1479-1487.
HELDT, H. W., C. J. CHON, D. MARONDE, A. HEROLD, Z.
STANKOVIC, D. WALKER, A. KRAMINER, M. R. KIRK, and
U. HEBER. 1977. Role of orthophosphateand otherfactors
in the regulationof starchformationin leaves and isolated
chloroplasts.Plant Physiol. 59:1146-1155.
Ho, L. C. 1976. The relationshipbetweenthe rates of carbon
transportand photosynthesisin tomato leaves. J. Exp.
Bot. 27:87-97.
on the ratesofphoto. 1977. Effectsof CO2 enrichment
This content downloaded from 131.238.108.32 on Thu, 14 Nov 2013 10:23:55 AM
All use subject to JSTOR Terms and Conditions
248
BOTANICAL GAZETTE
synthesisand translocationof tomato leaves. Ann. Appl.
Biol. 87:191-200.
. 1978. The regulationof carbon transportand the
carbon balance of mature tomato leaves. Ann. Bot. 42:
155-164.
KAMANINA, M. S., and A. A. ANISIMOV. 1977. Escape of
assimilatesfromthe mesophyllinto the void space ofleaves
under differentconditions of mineral nutrition. Soviet
Plant Physiol.24:628-632.
MENGEL, K., and H. E. HAEDER. 1977. Effectof potassium
on the rate ofphloemsap exudationand the compositionof
phloemsap ofRicinuscommunis.Plant Physiol.59:282-284.
MENGEL, K., and M. VIRO. 1974. Effectof potassiumsupply
on the transportofphotosynthatesto thefruitsof tomatoes
(Lycopersiconesculentum).Physiol.Plantarum30:295-300.
MILBURN, J. A. 1974. Phloem transportin Ricinuts:concentration gradientsbetween source and sink. Planta 117:
303-319.
PEARSON, C. J. 1974. Daily changes in carbon-dioxideexchange and photosynthatetranslocationof leaves of Vicia
faba. Planta 119:59-70.
ROSEN, R. 1975. Biological systemsas paradigmsforadaptation. Pages 39-72 in R. H. DAY and T. GROVES,eds.
Adaptive economicmodels. Academic Press, New York.
J. C., and D. R. GEIGER. 1974. Effectsof light
intensityand oxygenon photosynthesisand translocation
in sugar beet. Plant Physiol. 54:575-578.
THORNE, J. H., and H. R. KOLLER. 1974. Influenceof assimidiffusiveresistances,translate demand on photosynthesis,
location, and carbohydratelevel of soybean leaves. Plant
Physiol. 54:201-207.
TURGEON, R., and J. A. WEBB. 1975. Leaf developmentand
phloem transport in Cucurbita pepo: carbon economy.
Planta 123:53-62.
1977. Can the chloroplast
WALKER, D. A., and A. HEROLD.
support photosynthesisunaided? Plant and Cell Physiol.
(special issue on PhotosyntheticOrganelles),pp. 295-310.
WAREING, P. F., M. M. KHALIFA, and K. J. TREHARNE. 1968.
Rate limitingprocess in photosynthesisat saturatinglight
intensities.Nature 220:453-457.
WAREING, P. F., and J. PATRICK. 1975. Source-sinkrelations
and the partitionof assimilatesin the plant. Pages 481-499
in J. P. COOPER,ed. Photosynthesisand productivityin
differentenvironments.Vol. 3. International Biological
Programme.CambridgeUniversityPress,London.
WARREN WILSON, J. 1972. Control of crop processes. Pages
7-30 in A. R. REES, K. E. COCKSHULL, D. W. HAND, and
R. G. HURD, eds. Crop processes in controlledenvironments.AcademicPress,New York.
SERVAITES,
This content downloaded from 131.238.108.32 on Thu, 14 Nov 2013 10:23:55 AM
All use subject to JSTOR Terms and Conditions