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Copyright© 1979by AnnualReviewsInc. All rights reserved
THE CONTROL OF VASCULAR
1DEVELOPMENT
~7674
Terry L. Shininger
Department
of Biology, Universityof Utah, Salt LakeCity, Utah84112
CONTENTS
INTRODUCTION
..........................................................................................................
PROCAMBIUM:
DEVELOPMENT
IN THESHOOT
..............................................
THE CONTROL OF PRIMARY VASCULAR DIFFERENTIATION
IN THE
SHOOT
..........................................................................................................
PROCAMBIUM:
DEVELOPMENT
IN THEROOT
................................................
CYTOLOGICAL AND BIOCHEMICAL ASPECTS OF VASCULAR
DIFFERENTIATION
..................................................................................
Cytological
Aspects.
.....................................................................................................
Biochemical
Aspects
....................................................................................................
THE CONTROLOF NON-PRIMARYVASCULARDIFFERENTIATION ..........
Differentiation
fromtheCambium
............................................................................
Experimentally
Induced
VascularDevelopment
........................................................
Wound-induced
vascularization
..................................................................................
Vascularization
incultured
tissue..............................................................................
CONCLUSIONS
..............................................................................................................
313
314
316
317
319
319
322
323
323
324
324
325
331
INTRODUCTION
Vasculardevelopmentis a central themein aspects of biology as diverse as
evolution and cell biology. Ourcurrent conceptionof the control of developmentof this tissue is extremelyrudimentaryin comparisonto the strides
whichhave been madein other aspects of biology in recent years. Perhaps
this is not surprising considering the complexity and subtleness of the
~Abbreviations used: AT, adenine thymidine; BAP, benzylamino purine; BUdR,bromuridine deoxyriboside; EM,electron microscope; ER, endoplasmie retieulum; FUdR,fluorouridine deoxyriboside; CA, gibberellin; NAA,naphthalene acetic acid; PAL, phenylalanine
ammonia-lyase; QC, quiescent center; TdR, thymidine deoxyriboside.
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314
SHININGER
problem.Thestudy of the control of vascular development,however,offers
an openfield of investigationfor the imaginativeinvestigatorinterested in
either basic aspects of eukaryotic developmentalbiology in general or in
vascular plant physiologyand development
specifically. There havebeena
numberof reviewsof the subject froma variety of points of view: primary
vascular development(29, 30); shoot apical meristembiology (140);
apical meristembiology (131); phloemregene.ration(60); eukaryoticdevelopment(135); and xylemdevelopmentin general (101, 102). Thepresent
review is an attempt to integrate morerecent workon the developmental
biology of vascularization with the earlier physiological and anatomical
literature. Thegoal is to identify what wepresently knowabout vascular
developmentand to point out directions future workmighttake in order
to expandour conceptualization of vascular development.
Vasculardevelopment
involves first the formationof cells (procambium)
which are committedat somepoint to becomexylem and phloemas opposedto pith, cortex, mesophyll,and epidermis. Secondly,it involves the
overt cytodifferentiation of these procambialcells into xylem,phloem,and
cambium.Whatis the nature of these pote:atial vascular cells whichare
currently called procambiumduring primary development or cambium
during secondary development?Havethey, at the time at which they
becomecytologicallyidentifiable, actually progressedtowarddifferentiation
into xylemor phloem,or are they simply ordinary meristematic cells?
Answersto these questions can only be obtained whenthe followingquestions are also answered:(a) Whatare the early biochemicalmarkers
vascular development?
(b) Whatregulates the spatial distribution of vascular cell formation within the stem, leaf, or root? (c) Whatmechanisms
operate to prevent the formationof vascular elementsin maturetissues or
to stimulate their formationin maturetissues?
PROCAMBIUM:
DEVELOPMENT
IN
THE SHOOT
The anatomical approach to vascular developmentin shoot apical meristems has generated somecontroversy concerningwhat should properly be
called procambium.
Until overt cytodifferentiation occurs, however,it is
only possibleto define these cells as beinglarger or smaller, denseror less
dense, etc relative to surroundingcells. Onecannotdefine these cells in
terms of either their developmentalcommitment
or their real developmental state. Thus,it seemspresumptiveat this point to state morethan that
onecan observesomeof the cytological changesin the progressionof calls
towardmaturationas part of the vascular system.As yet, experimentshave
not beendonewhichwouldallow one to define the stage at whichthe cells
are committedto xylemor phloemdifferentiation unless they haveovertly
differentiated.
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CONTROLOF VASCULARDEVELOPMENT 315
Esau(30) has taken the simplest view that in angiospermsthe residual
meristem,a residiumof the shoot apical meristem,extends fromthe region
of the apical initials into the differentiating region of the meristemwhere
differential parenchymatization
of the pith andcortex reveal its existence.
Portionsof the residual meristemare consideredto differentiate into procambium,a meristem for the vascular system. Wardlaw(140) takes
different point of view based on his workwith ferns. Heobserveda zone
of cells whichextends into the apical domeabove the insertion of the
youngestleaf pdmordium
and whichhe considers to be procambium.
In his
view, vascular developmentis initiated prior to the developmentof leaf
primordia.Thedevelopment
of the leaf primordia,in fact, causesdisruption
of this initially continuousprocambium,
resulting in the formationof parenchymatous
leaf gapsin the stem. Surgical removalof the primordiaresulted
in eliminationof gapformation(I 39). ThusWardlaw
believes that the cells
abovethe leaf primordiarepresent procambialcells committedto vascular
developmentunless specifically altered by influences from developing
leaves. Theinterpretationof the histologicalpreparationsis clearly a subjective matter since one does not knowfrom these kinds of experimental
approacheswhether the cells are committedto vascular development,to
another fate, or not committedat all. Wardlaw’s
viewcan only be accepted
whenrigid criteria of procambium
are developedand whenthose criteria
are successfullyappliedto the cells he observedin the apical domeor when
those cells are successfully isolated andinducedto developinto vascular
cells in vitro with relatively simpleinput.
Experimentalapproachesto the nature of procambium
and the role of
leaves in vascular developmentwere taken by Helm(50) and Young(146).
Bothobservedthat in angiospermsthe removalof the youngleaf primordia
caused the already recognizable procambium
to develop into parenchyraa
and not to developinto vascular tissue nor even remain identifiable as
procambium.Furthermore,Young(146) found that supplying auxin in the
place of an excised leaf primordium
preventedthe changein the appearance
of the procambium
but did not stimulate its developmentinto vascular
tissue. Morerecently, McArthur
&Steeves (75) attemptedto clarify questions about the nature of procambium
and the effects of leaves in Geurn
chloense. In this angiospermthe removalof the leaf primordia did not
eliminate leaf gap parenchyma
formation within the presumptivevascular
cylinder as observedby Wardlaw
(139) in ferns, althoughthe cells did not
differentiate into parenchyma
as observedby Helm(50) and Young(146).
McArthur
& Steeves (75) concludedthat the early phaseof vascular developmentis not underspecific control of the leaf since "provascular"tissue
increasedin longitudinalextent in the absenceof the leaves. In Geurnthey
found that vascular developmentprogressed normally whenauxin plus
sucrose was applied in the absence of the leaf pdmordinm
but not with
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316
SHININGER
auxin alone. In the absenceof knowledgeof the effect of the auxin plus
sucrose in Young’s(146) workwith Lupinus,it is not possible to makeany
generalizations concerningthe nature of the stability of provascular or
procambialtissues in the absenceof developingleaves. However,from the
fact that presumptivevascular tissue did not undergoparenchymatization
in Geumwhile it did in Lupinusin the absenceof leaves, it maybe that
there are distinct differencesin the regulation of the formationandin the
stability of these cells.
Procambium
is considered to "differentiate" continuously acropeta[ly
(e.g. it appears to developfrom differentiated regions towardundifferentiated regionsin the meristem)in the shoot(29, 76, 77, 136). Ball (3)
procambium
formationto be initiated near a leaf base andto then differentiate both basipetally andacropetally. Esan(30) questionedthis interpretation on the groundsthat it is extremelydi$cult to discriminateprocambium
without intimate knowledgeof the pattern of vascular developmentin the
given shoot. Again,identification of these cells is a relatively subjective
matter. In axillary shoots procambium
maydevelop acropetally from the
mainshoot to the axillary bud (29, 42), or basipetally fromthe bud to the
shoot (44). Thedirection is reported to be basipetal in adventitious buds
(140). To state that the procambium
is propagatedcontinuouslyacropetally
within the meristemwouldbe conceptuallyclearer, because"differentiate"
has a specific meaningwhichhas not yet been demonstratedfor procambium.
If one accepts that procambium
is a meristemproducing the vascular
tissues, then it is clear that the continuedfunctioningof this meristemin
the shootdependsuponleaf formation.Theeffect of the leaf is in somecases
replaceableby auxin or auxin plus sucrose. It :remainsquestionablewhether
or not early changesin cellular appearancerepresentobligate changesin the
course of vascular development.Withoutspecific characteristics attributable to procambium,
e.g. a specific enzymeactivity, protein complement,
ete, it is virtually impossibleto adequatelystudy the development
of procambium
per se, but rather, onemustdeal witth the later stages of vascular
element maturation.
THE CONTROL OF PRIMARY VASCULAR
DIFFERENTIATION
IN THE SHOOT
Primaryvascular tissue developmenthas been pursued both descriptively
andexperimentallyin Coleusby Jacobsand collaborators. Theyreport that
in Coleusthe differentiation of the phloemprecedesthe differentiation of
the xylemwith the first formedphloemelementsappearing at the base of
a leaf, andthendifferentiation proceedsacropetallyinto the leaf andbasipe-
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CONTROLOF VASCULAR
DEVELOPMENT 317
tally to connectwith the maturevascular cells (reviewedin 60). Aday
so later the xylemelementsappear in the procambium
at the samelevel at
whichthe first phloemelementshadearlier differentiated andthe xylemtoo
subsequentlydifferentiates bidirectionally. Jacobs& Morrow
(61) pursued
the questionof the role of the leaf in the inductionof vasculardevelopment
andfoundthat the relative rates of auxin productionby the leaf correlated
well withthe rates of xylemdifferentiationin the leaf trace. Theyconcluded
that auxin limits primaryxylemdifferentiation in the leaf trace of Coleus.
Wangermann
(138) subsequently demonstratedthat exogenousauxin could
replacethe leaf effect in the differentiationof the primaryxylemof Coleus.
It is of interest that the primaryxylemin Coleusconsists only of vessels,
andthus this workagrees well with the results in Phaseolusof Jost (65),
whofound that xylem developmentstopped whenleaves were excised.
However,
Jost (65) foundthat the application of auxin only restored vessel
element differentiation. Leaf removalcaused cessation of xylemfiber
differentiation from the cambiumin Xanthium,but vessels developedin
normalnumbers(106). NAA
restored normalvascular developmentin that
case (107).
Kinetinwasfirst implicatedin vascular development
in intact plants as
a result of the studies of Sorokin, Mathur& Thimann(122). Sorokin
Thimann
(123) concludedthat kinetin wasresponsible for the differentiation response,althoughthe effects of the kinetin stimulationof growthwere
not experimentallyseparated from the xylogenesisresponse.
Whileit is generallybelieved that the leaf plays a dominantregulatory
role in the overt cytodifferentiationof the procambium
into vasculartissues,
the variouscontributionsofa leafvs the rest of the shoothavenot beenfully
revealed. Auxinis one of the principal regulatory agents supplied by the
leaf. Althoughsucrosehas beenshownto improvethe auxineffect, it is not
likely that this is ordinarily derivedfromthe leaf, becausenet exportation
of sucrose from developingleaves is unlikely until after leaves are well
beyondthe stages under consideration in early vascular development.It
seemsthat elucidation of the other regulatory components
in primaryvas¯ cular differentiation could be revealedin a rather straightforwardwayvia
meristemculture.
PROCAMBIUM: DEVELOPMENTIN THE ROOT
Vasculartissue development
in the root wasreviewedextensivelyby Torrey
(131) andby Esau(30). Asthey haveindicated, the root meristemis a
complexexperimental tissue because there are no complications due to
terminal appendages.Herethe stages of vascular development
occurred in
a true linear sequence. The major questions concerning developmentin
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318
SHININGER
roots have revolved around: (a) the nature of the pattern-forminginfluences, e.g. is it fromwithin the meristemor imposedby maturetissues;
(b) the nuclear cytology of procambium
developmentinto xylem; and (c)
the ultrastructural changesin the cytoplasmassociated with phloemdevelopment.This section deals primarily with the pattern-formingirdtuenees.
Asin the shoot, procambium
is distinguishedearly fromother tissues in the
root by enlargementof cells whichwill constitute the epidermisandcortex.
This results in a central procambialcylinder rather than a ring (131). This
central cylinder, whoseoutermostboundaryis the pedcycle, eventually
differentiates with a variety of flexible arrangements(within and between
organisms)into vascular and, in somecases, pith tissue. At a youngstage
the cells withinthe central cyclinderdo not haveuniquecytologicalfeatures
at the electron microscopelevel whichmightsuggest their early commitmentto different fates (89).
In Torrey’sview(131)the ability of the central cylinderto differentiate
into vasculartissue with a variety of patterns s~uggeststhat the termprocambiumis appropriate. This interpretation of procambium
cannot carry any
connotation of a commitment
to vascular developrnent and suggests that
procambium
in the root, as in the shoot, oughtto be considereda meristem
within which vascular developmentmaybe induced, as was suggested
earlier in this review.
Theformationof procambium
fromthe apical initials follows a continuous acropetal sequence (reviewed in 131). Procambium
developmentinto
vascular tissue is markedby the radial enlargementof the future metaxylem
vessel elementsvery close to the apical initiMs (10, 11). This produces(in
cross-sectional view)a linear array of xylem.(or a triareh or hexarch,etc
array of xylem)with phloemdevelopinglaterally to the xylemor between
the points of the triarch, hexarch,etc arrays of xylem.Development
at any
point in time is further advancedin the basipetally located cells producing
an axial developmental
sequence.Details of overt differentiation in root and
shoot systemsat the cytological, cytoehemical,and biochemicallevels are
treated together in the next section.
Thesequenceof vascular development
al]iows for the possibility of pattern induction either by the maturetissues or patterning inherent in the
design of the apical meristem. Thoday(126) suggested that the medstem
could be autonomous
in pattern formation. Biirming(11) performedexperimentswhichwereperhaps overinterpreted to support that concept. Clowes
(13) took a moredirect experimentalapproachof surgical manipulation
either the apexor the maturetissues and foundan effect on the pattern of
vasenlar development
(triarela/hexareh, etc) only whenthe apexper se was
treated but not whenthe mature tissues were manipulated. Torrey (129,
130) and Reinhard(98) unequivocallydernonstrated that the apex deter-
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CONTROLOF VASCULARDEVELOPMENT 319
minesthe pattern of vascular development.Theycultured 0.5 mmroot tips
(129, 130) or 0.7 mmroot tips (98) aseptically on definedmedium
andfound
that these very smallroot tips (thoughnot necessarilyother smallpieces of
the root) producedroots with vascular calls with normalorganization.
Torrey(130) observedthat the numberof xylemstrands (tdarch, hexareh,
ere) differentiating in the procambium
corrdated well with the diameterof
the procambialcylinder. Auxintreatment of these cultured root tips both
increased the size of the procambialcylinder and converted the normal
triarch xylempattern to hexarch(130). Odhnoff(87)found that GAcaused
xylemto differentiate closer to the root tip and concludedthat GAhas a
direct effect on xylogenesis.
Morerecently Feldman& Torrey (37) found that in Zea mays (cv.
Kelvedon)the complexityof the vascular pattern and the size of the QC
could be manipulated coordinately. Whenthe QCis small the vascular
pattern is simple, and whenit is large the pattern is morecomplex.As a
result of changingthe size of the QC,there is a shift in the position of the
proximalmeristemfrom whichall of the cells of the axis except the root
cap are derived. Feldman(35) found that in corn the vascular pattern
evident within 63 to 110 btmof the root cap junction. Heproposedthat
changesin the size of the QCshift the point of pattern initiation to areas
of the procambium
whichdiffer in diameter, and thus moreor less area is
actually availablefor the patterninginfluenceto operate.
CYTOLOGICAL AND BIOCHEMICAL ASPECTS
OF VASCULARDIFFERENTIATION
CytologicalAspects
Basiccytologicalaspects of overt vascular cell differentiation weresummarized by Esau(30). Thestatus of phloemcytologyspecifically at the light
and EMlevels was summarizedby Esan (31) and Cronshaw(17). Torrey,
Fosket & Hepler (135), O’Bden(86), and Roberts 002) reviewed aspects
of xylemcell differentiation. Thefollowingdiscussionbeginswith an accountof the cytologyof overt vascularcell differentiation andthen proceeds
to a moredetailed presentationof aspects whichhavereceivedconsiderable
attention regardingmechanisms
or possible markersof differentiation.
Within the phloemthe sieve elements undergoconsiderable elongation
duringdifferentiation fromprocambium
(33). Theydevelopa thickenedcell
wall whichdoesnot lignify. Sieveareas format rather specific positionsin
the wall. Neuberger& Evert(84) considerthe initiation of wall thickening
to be an early diagnostic feature. Significant changesin the nucleus or
nucleolus havenot been reported except that nuclear degenerationmaybe
nearly completedwhenwall thickening and modification are completed.
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320
SHININGER
Thedevelopment
of callose (,8-1,3-glucan)is anotherdiagnostic feature
sieve cells. Callosedevelopsas a padcoveringthe developingsieve area. At
maturitythe poresof the sieve area are lined with callose, but they are not
pluggedin ftmetioningcells. Thereare also early structural changesin the
plastids of sieve elements,the mainchangebeingthe formationof a protein
crystalloid within the plastid (83). In manyspecies P-proteinformation
diagnosticof sieve elementdevelopment
(28, 31). P-proteincan be observed
in extremdyyoungedls and maybe the first indication of the fate of the
cell (32). P-proteinhas beenidentified in phloemsince Hartig’s(49) description of phloem"slime," but it is not present in all speciesand mayexist in
phloemcells other than the sieve elements(31, 34). Northcote& Wooding
(85) observedP-protein to be boundin membrane
whichthey interpre/ted
as ERin origin, Sieve elementsare characterized by extensive development
of the ER. The cell biology and biochemistry of P-protein development
couldbe a fertile area of research. Theinterested reader shouldconsultthe
following accounts of phloemdevdopment:(a) root protophloem(33);
gymnosperm
phloem(82-84); (c) the general reviewby Cronshaw
(17).
basic features are similar in eachplant systemas well as in callus (144)and
hormone-inducedphloemdevelopmentin excised tobacco pith (17).
protein structure per se has beenexploredalso (88).
Cytological aspects of xylemcell differentiation were reviewed by
O’Brien(86) and by Torrey, Fosket&Hepler(135). Regardlessof the origin
of the cell (procambium
or matureparenchyma),there are several overlapping stages of development.Theproblemis to ascertain whichof these are
critical and then to determinehowthey are regulated. Cell expansionis
normal in devdopmentfrom procambiumor cambiumbut not pronounced
(if it occursat all) in development
frommatureparenchyma.
Thus,nuclear
or nueleolar changes relevant to expansion growth in proeambiummay
confusestudies of xylogenesis.This problemshould not occur in xylogenesis in cultured parenchyma.This problemthen becomesone of identifying the time and place of xylemdevelopmentin order to study nuclear
changes.
Secondarywall deposition and lignification are diagnostic features of
xylogenesis.Thecontrol of specific patterns of wall depositionhas received
considerableattention (reviewedin 102, 135). Pickett-Heaps(94) observed
changesin the distribution of mierotubulesduring xylemdevelopment.He
foundthat initially they wereevenlyspacedalong the cell wall, but later
they groupedinto bandsand the cell wall thickeningsweredepositedadjacent to these bundles of mierotubules.Pickett-Heaps(94) showedthat the
antimicrotubular drug colchicine disrupted the microtubulesand the wall
pattern. Cellulosemicrofibril orientation wasalso altered by colchicinein
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CONTROLOF VASCULARDEVELOPMENT 321
developingxylemcells (51). Howmicrotubulesaffect call wall deposition
remains an unsolved problem.
Lignindepositionis consideredto be an early aspect of xylogenesisand
it accompaniessecondarywall deposition (145). However,as O’Brien(86)
pointedout, wereally do not havea stain for lignin at the EMlevel. Thus
it is not possible to study very reliably with EMtechniqueshowlignin
deposition and wall formation are coordinated. ¯
Whensecondarywall deposition and lignification near completion,portions of the primary wall maybecomehydrolyzed. This is followed or
accompanied
by protoplast autolysis. Little if anythingis knownabout the
control of these processes.At maturitythe water-conducting
cells (vessels,
traeheids) consist of daboratelyconstructedcells without protoplasts but
with variously modifiedwall regions whichallow rather free liquid movement.
Asnoted previously, in the root the metaxylem
is first detected by the
radial expansionof these cells very near the apical initials (131), Large
increases in nuclear DNA
in these cells werereported (125). Theseobservations generatedthe conceptthat increasedploidy wasbasic to xylemdevelopment
(73). Aswill be seen, this correlationis not universalwithina tissue
or betweenorganisms.
Corsi & Avanzi(15) reported an eightfold increase in the DNA
of metaxylemcells of.4lliumceparelative to pericyclecells whichremainedat the
2Clevel. Theyalso reported changesin the DNA/histone
ratios, but it is
not clear that these wereconsistent or significant. Innocenti&Avanzi(56)
interpret their observationsof this systemas follows:Thedevelopingmetaxylemcells first undergochromosome
endo-reduplicationvery close to the
apical initials. This is followedby amplificationof the nueleolarorganizer
region of the DNA
(rDNAcoding for rRNA)whichin turn is followed
extrusion of the nucleoli. Metaxylem
ceils showeda sixfold increase in
rDNA
(2). This cycle is repeatedin the 2 to 5ramregion fromthe tip (cap
included in measurements)and the cells then stop DNA
synthesis. During
this time the metaxylem
cells undergoexpansionfrom 20 ktmin length to
750/zm.Innoeenti (55) reported a decrease in the histone/DNA
ratio
developingmetaxylem.The workcannot be evaluated adequately since the
data werenot presentedexceptas ratios. Similar results werereportedfrom
workin trachearyelementdifferentiation in the corn leaf (70, 124). Asthese
investigators indicate, these observationsneedcloser examinationin systems moresuitable for biochemicalwork. However,these studies suggest
someexperimentalapproachesthat are not readily apparentfrom biochemical methods.Theprimaryconfusingaspect of these studies is the inability
to separate events relevant to expansionfromthese relevant to overt xylo-
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SHININGER
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genesis. Aswill be seen, biochemicalapproacheshavefailed (unnecessarily)
to separate replication-relevanteventsfromt~rachearyelementdifferentiation.
Biochemical Aspects
Thereare a fewstudies of vascular developn~tentat the biochemicallevel.
Thornber& Northcote (128) studied changes in carbohydrate and lignin
contents of cells developingfromthe cambium.Theresults wereconfusing
becauseof the inadequatemethodsfor such studies at that time. Jeffs &
Northcote(63) found an increase in the xylose/arabinose ratio in bean
callus after 1 to 2 monthsof hormone-stimulated
xylogenesis. Newmethods
are nowavailable, and such analyses have been elegantly performedon
primarycell walls (67) but not related to secondarywall development
vascularization.
Lignification of secondarycell walls begins very soon after secondary
thickening is initiated (52, 145). TheenzymePALcatalyzes the conversion
of phenylalanineto cinnamicacid and is a key reaction in the diversion of
carbonfromprotein synthesis to lignin synthesis. PALactivity in various
tissues is correlatedpositively with vascular development
in the plant (105)
and in hormone-treatedcallus (104). Most recently Haddon& Northcote
(46) followed the time course of PALactivity during vascular, nodule
formation in bean callus. In this case the increased PALactivity correlated fairly well with the initiation of xyloglmesis
in the early stages. PAL
activity declined later whenit wouldseemthat it oughtto remainat least
constant.
Haddon& Northcote (46, 47) also examinedB-1,3-glucan synthetase
activity as a marker of callose formation during phloemdevelopment.
B-1,3-glucansynthetase activity followed a time course similar to PAL
activity andto sieve cell differentiation.It is ditficult to analyzethis work
since hormone-treated
replicating (but nondifferentiating)controls werenot
examined.
Dalessandro& Northcote(21-23) initiated studies of the activities
various enzymesinvolved in nucleosidediphosphatesugar reactions which
are expected to be involved in carbohydrate metabolismassociated with
vascular development.Enzymeactivities were measured:(a) in the cambium,differentiating xylemor differentiated xylemof twoangiospermsand
two gymnosperms,
or (b) in cultured Jerusalemartichoke tuber tissue
whichhormone-inducedvascular developmentoccurred. Enzymeactivity
(cpmin product/mgprotein) did not reveal consistent or large differences
in the various tissues examinedin ~ TheJerusalemartichoke experiments
suffered fromthe lack of adequatecontrols.
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CONTROLOF VASCULARDEVELOPMENT 323
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THE CONTROL OF NONPRIMARY
DIFFERENTIATION
VASCULAR
Differentiation
from the Cambium
As the primaryvascular tissues differentiate from procambium
and the
tissue ceaseselongation,someof the procambialcells initiate replication in
whichthe cell plate is formedin the longitudinalplane. Thesecells are now
consideredto be cambium
and they will formall of the secondaryvascular
cells, e.g. the wood(xylem,cells differentiated interior to the cambium)
and
phloem(cells differentiated exterior to the cambium).
In the stemthe cells
betweenthe vascular (fascicular) bundlesmayinitiate replication to form
the interfascicular cambium.Whenthis happensthe cambiumbecornes a
sheath of meristematiccells. Theinitiation of replication in the fascicular
and interfascicular cambium
and seasonal reactivation of the cambiaare
attributed to factors derivedfromthe shoot (48, 118). Coster(16) suggested
that a hormonewas responsible and Snow(118) demonstrated the hormonalnature of the cambialstimulus. Snow(119)effectively replacedshoot
stimulation with exogenousauxin. However,auxin is not alwayssufficient
(96).
Siebers (112-114)studied the activation of the interfascicular cambium
ofRicinus communis.Hefound that the activation of this cambium
and the
differentiation of xylemoccurredin inteffascicular tissue isolated andcultured on simple mediawithout exogenousauxin. However,youngertissue
required kinetin (I 13). Heconcludedthat the development
of this meristem
was determinedat a very youngstage during proeambium
developmentand
was not dependentupon homogenetieinduction from the fascicular cambium.
Generally, studies of vascular developmentfrom the cambium
have centered on explorations of the effects of combinations of hormonesor
photoperiodon both cambialdivision and differentiation in qualitative
terms. Auxinstimulation of cambial division in decapitated plants may
result in division and vascular differentiation (119) or cambialdivision
without normaldifferentiation (65, 95, 118-121). In somecases normal
vascular development
maybe elicited by GA(68) or mayrequire auxin plus
GA(25, 141). GAtends to be sufficient in rootedtissue but not in isolated
stems.
Removalof youngleaves and buds from Xanthiumallows cambialactivity to ~ontinue,onceinitiated, but the majorityof the cells (fibers) do not
differentiate. However,vessel elements, though smaller than normalin
diameter,developin normalnumbers
(106). In this case fiber differentiation
is restored briefly by allowingone leaf to developacropetal to this region
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324
SHININGER
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of the stemor by addingan auxin (NAA)
instead (107). Thederivatives
the cambium
in Xanthiumare not programmed
as a result of their cambial
origin; rather, there mustbe hormonalinput to the newcells either during
cell formationor subsequentto cell formationor both. If the auxin application is delayed,the cells derivedin the meantime
fail to respondin terms
of fiber differentiation and remainas thin-walled unlignified parenchyma
(107). Similar results wereobservedin other systems(6, 53).
Experimentally
lnduced Vascular Development
tissue
development
mayoccur in portions of the plant other than fromprocambium
in root and
shoot meristems.Thebulk of the vascular tis~mesare secondaryand produeed by the vascular cambium.However,the literature on secondary
vasculartissue formation,althoughextensive,,.reflects a great interest in the
alteration of subtle characteristicsof the ditferentiatedcells, e.g. wallthickness, cell length,etc. Verylittle of this literature deals specificallywith the
problemof the control of vascularcell differentiation. Theliterature on the
carfibiumwas reviewedby Brown(8) and by Phillipson, Ward& Buttertield
(93)! While someexperimental work on vascular developmentfrom the
cambium
will be consideredin this section, the emphasisof this section will
be on experimentally induced vascular developmentin explanted parenchymatoustissue, callus, or woundedstems.
WOUND-INDUCEDVASCULARIZATION Vascular
Vascular regeneration Vascular regeneration in parenehymaof wounded
stemswasfirst reportedby Criiger (18). It wasobservedto progressbasipetally around a wound(115), and Janse (62) suggested that a hormonal
stimulus wasresponsible, yon KaanAlbest (66) demonstratedthat leaves
acropetal to the woundproducedfactors necessaryfor vascular regeneration. She also showedthat the vascular systemper se must be woundedto
obtain regeneration. Xylemregeneration mayinvolve the transformationof
somecells directly into xylemwithoutcell division (I 17), althoughonedoes
not knowwhat unobservedbiosynthetic evenlls maybe prerequisite. Parenehymais not converteddirectly to sieve elementswithoutcell division (66).
The major break in understanding vascular regeneration came from
Jaeobs’ work(57-59), whichshowedthat the role of the leaf in xylem
regeneration wasreplaceable by auxin. Subsequently, La Motte & Jacobs
(71, 72) showedthat phloemregenerationwassimilarly controlled. Surprisingly, in viewof studies in other systems,sucrosedid not limit in the Coleus
system(59, 72). In Coleusthe leaves needto be present for 48 hours after
woundingto obtain a xylogenic response (100). Aninductive effect was
evident since the vascular strands did not completedifferentiation until 72
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CONTROLOF VASCULARDEVELOPMENT 325
hours after wounding(I). The dependenceof phloemregeneration on roots
is variable. Houck&La Motte(54) report that roots are essential but can
be replaced by a cytokinin (zeatin). However,previous workhad shown
role for the roots in the sameclone of Coleus(59).
Thestudies on hormoneinvolvementare, with the exceptionof the auxin
studies, in conflict. In additionto the differencesreported concerningthe
role of roots and cytokinin noted above, there is a clear indication that
kinetin inhibits woundvessel regenerationin a different clone of Coleus
(40). In that cloneGAenhancedthe auxin effect on regeneration(103).
Thompson
(127) found GAto haveno effect on regeneration in the Princeton clone of Coleus. The mannerof hormonepresentation maybe critical
because Thompson
(127) found that concentrations of auxin which are
effective whenapplied apically are not effective in regenerationwhenapplied basally.
Ultimately, regeneration is a wound-induced
redevelopmentof somemature parenchyma,but it is importantto establish howthese newlyformed
cells are "plumbed"
into the vascular system.Is the newvascular tissue in
the woundregion "plumbed"directly into the old vascular system, e.g. old
cells -~ newcells -~ old cells, or is there a moreextensive replacement
resulting in the insertion of the regeneratedcells into a newvascularstrand,
e.g. newcells -* new(regenerated)cells -~ newcells? Thesequestionswere
posed by Benayounet al (5). Theyinterpret their workto support the
replacementview, e.g. newcells ~ new(regenerated)cells ~ newcells.
their workthe act of woundingactually causes a reduction in the rate of
formationof vascular cells. It is probablethat a variety of patterns of
regeneration maybe produced(D. E. Fosket, personal communication).
Jacobs(60) has reviewedthe earlier workon regeneration.
VASCULARIZATIONIN CULTUREDTISSUE Significant
progress toward understandingthe control of vascular developmentcamewhenCamus
(12) showedthat strands of xylemelementscouldbe inducedto differentiate
in the parenchymatous
ceils of endivecallus as the result of the insertion
of a growingbud. Ball (4) observeda similar effect whenbudswereregenerated in Sequoiasernpervironscallus. Oneof the roles of the inserted bud
is to supplyauxin (12). Wetmore
&Sorokin(143) performedsimilar experimentswith lilac callus andbudsandfoundthat auxinimitatedthe budeffect
in formingxylemstrands only whensupplied froma point source. Theneed
for sucrose was demonstratedby Wetmore
& Rier (142), and it wasshown
in Parthenocissustricuspidata callus that tracheary elementproduction
varied quantitatively with changesin sucroseconcentrationwhenauxin was
hdd constant (99). Furthermore,the ratio of xylemto phloemvaried with
sucrose concentrationif auxin levels were constant: low sucrose (ca 1%)
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326
SHININGER
elicited relatively morexylemwhilehigh sucrose(ca 4%)elicited relatively
more phloem.
Thosereports of carbohydrateeffects led to the investigationof effects of
alternative carbohydratesupplieswhichare still not satisfactorily resolved.
In Phaseolusneither glucose plus fructose nor glucose alone replaced sucrose in producingorganized nodules of xylemand phloem(64). However,
glucosealone causedthe productionof scattered xylemelements.Fructose,
mannose,xylose, rhamnose,arabinose, galactose, mannitol, or ~t-methyl
glucosideat 2%did not elicit anydifferentiatiton, whilecellobiose,lactose,
and raflinose (2%)all elicited somexylemdit~:rentiation but not organized
nodules of xylemand phloem.Thesucrose elect on noduledifferentiation
waspartially replaced quantitatively by 2%maltoseor ,t~-trehalose (64).
Sequentialtreatments of sucrose then IAA,or’ IAAthen sucrose, indicated
that nodule formation occurred only whenIAApreceded or was accompanied by sucrose (64).
Helianthustuberosa tissue forms traeheids i.n responseto NAA
and BAP
in the presenceof sucrose or glucose or trehalose, or to a lesser extent
maltose,whileother carbohydrates
are very muchless effective (78). Soluble
starch (4%)stimulatedxylogenesisin H. tuberosaquantitatively abovethat
produced by optimal (4-8%) sucrose (78). Phillips & Dodds(90)
unable to confirmeither that observation or the trehalose stimulation.
Minocha& Halpedn(78) observedan inhibition of differentiation without
concomitanteffects on cell division whenincreasing amountsof glucose
werepresentedwith optimal levels of sucrose. Increasedamountsof glucose
or sucrose alone did not have the same effect, but data on the glucose
response was not included, Theypostulate: a competitive uptake effect
whichcould be tested. Replottingtheir data (percentageof differentiation
vs total cell number)indicates that the glucoseeffect maybe a simpleshift
of the percentageof differentiated cells eurw~up on the cell numberscale.
Whetherthis meansa simpledelayin the initiation of xylemdifferentiation
or a decreasein rate of formationof xylemcannotbe deduced.Weare not
at a point wherethe specific effects of carbohydratesourceson differentiation can be explainedsatisfactorily. Thesituation is madeevenworseby the
inability of investigators to see the sameqmditafiveresponsesin the same
tissue. However,it appears that only those carbohydrateswhichsupport
significant cell division also supporttraehem~elementformation.Thedisproportionateeffect of carbohydrates
on ditSerentiationrelative to cell division should be investigated in a time course experimentto determinehow
carbohydratesaffect the initiation andrate of xylogenesis.
Therequirementfor auxinobservedin va~;culardifferentiation relative to
primary, secondary,or regeneratedvascular cells is also observedconsistently in all formsof tissue culture, e.g. callus (12), pith (14), pea
parenchyma
(134), Jerusalemartichoke tuber parenchyma
(20, 78), or
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CONTROLOF VASCULARDEVELOPMENT 327
tuce pith (19, 24). Thespecific roles of auxin havenot beendecipheredbut
maybe related to aspectsof cell division or geneexpressionor carbohydrate
metabolismor all these. Foskct(39) foundthat IAAdid not alter the time
lag preceding woundvessel memberformation in Coleus whereexogenous
auxinincreases the numbers
of vascularcalls formedbut is not essential for
their formation. Auxinhas only a small affect on DNA
synthesis in Coleus
(39) and no affect by itself in pea (116), and so it cannot be assumed
increase the numbersof differentiated cells via increasing the numbers
availablefor differentiation. It is not clear howauxinaffects RNA
or protein
synthesis in those systemswhereauxinsuffices to inducevascular differentiation since "state-of-the-art" biochemicalapproacheshavenot beenutilized.
Cytokininswerefirst shownto stimulatexylogenesisin culturedtissue in
conjunction with exogenousauxin by Bergmann
(7). That observation was
confirmedin a qualitative mannerin several systemsby Torrey(132). The
first quantitative analysis wasachievedby Fosket &Torrey(41), whoused
a soybeancallus whichrequired these hormonesfor replication as well.
Increasingconcentrationsof kinetin stimulatedxylogenesisrelatively more
than replication. Thesoybeansystemusedno longerexists. It is an unfortunate fact that callus cultures are notoriouslycapriciousanddevelopaltered
hormoneresponsesas they age. It is essential to developand employadequatemeansof tissue preservationif these studies are to achievetheir true
potential in developmental
studies.
Torrey& Fosket(134) observedsimilar responsesto auxin and cytokinin
in pea root parenchyma.This system is knownto contain a heterogeneous
cell population. However,xylogenesis occurs in the hormone-stimulated
replicating cortical parenchyma
(134). Phillips & Torrey(91) refined
analysis by punchingout the central vascular cylinder. Theyestablished
that xylogenesisandreplication of these cells absolutdyrequiredauxinplus
cytokinin andthat replication precededxylogenesisby several days. Shininger &Torrey(111)then establishedthat, like the soybeansystem,increasing concentrationsof eytokininstimulatedthe rate of xylemcell formation
relatively morethan cell replication. Furthermore,these cells showeda
continuousrequirementfor the hormonesfor xylogenesiswhile cell divisions wereinducedby shorter periods of cytokinin treatment and continued
after cytokinin "removal."This maynot be true in the Jerusalemartichoke
tissue since preliminary worksuggestedthat xylogenesiscould continue
after cytokininwithdrawal(78). Cytokininis required in lettuce pith (19),
carrot tissue (80), and Zinniamesophyll(69) as well as pea (91, 111, 134)
andartichoke(78). Thespecific role of cytokininremainsto be determined
in all systems.
Cell replication is observedto precede and accompany
xylogenesis in
nearly all culture systems.In those cases wherereplication is not observed
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328
SHININGER
it has not beenshownthat DNA
synthesis did not occur. Withinthe plant,
cell division normallyaccompaniesprimarymadsecondaryvascular developmentas well as wound-inducedor hormone-inducedvascular devdopment. Onrare occasionstracheary elementformationcan also be observed
in single calls in suspension
cultures, but in general,replicationis coincident
(133). Dothese observedcell divisions haveany bearing on the problem
the regulation of vascular differentiation? I think they do.
In animal systems a considerable body of evidence has developed to
supportthe conceptthat someformsof differentiation require cell replication (reviewedin 97). Rigorousevidencein plant systemsis minimaland,
like animalsystems,dependsuponthe use ofitthibitors (reviewedin 102and
109).
In plants the first direct approachto the questionwasfocusedon the need
for cell division in toto. Fosket (38) found that both FUdR
and mitomycin
C blockedreplication and xylogenesisin Coleusexplants. TheFUdReffect
was prevented by simultaneousTdRtreatment. This indicates a need for
someaspect of the division process. Althoughcolchicinehad similar effects
in this system,it is less clear wherethe effect wasmanifest(D. E. Fosket,
personal communication).Turgeon(137) concludedthat DNA
synthesis
not necessary for vascular differentiation, :~inee FUdRdid not prevent
xylogenesisin lettuce pith. This interpretation maybe prematurebecause
it was not shownrigorously that DNA
synthesis wasprevented. It is not
adequateto demonstratea lack of increase i~n cell numbersor to measure
DNAmicrospectrophotometrieally in 0.5%of the cells (when 6%will
differentiate) andconcludethat DNA
synthesis wastotally blocked.In fact,
FUdR
had a pronounced
effect on vascular ,differentiation since it reduced
vascular differentiation to 3%of the control level.
Theevidencefromgamma
plantlets (45) is frequently used to support the
viewthat vascular development
does not require recent cell divisions. However, recent cell divisions haveonly beenconsideredessential as a result of
studies whereit is knownthat they are occurringcoincidentlyin time with
the agents whichactually induce differentiation. It is not knownwhen
induction takes place relative to overt cytodifferentiation in the gamma
plantlets. Wedo not yet knowwhyreplication is essential althoughthe pea
systemis yielding somenewinsight.
Endopolyploidyis frequently observedto be correlated with in vivo
xylogenesis(73). Phillips & Torrey(92) andDodds&Phillips (26) carefully
eliminatedthis possibility as beinga causal relationshipin pea andJerusalemartichoke respectivdy. However,the needfor normalreplication in the
pea system remains.
Shininger(108) demonstrateda reversible FUdRinhibition of xylogenesis in the pea system, and with the use of BUdR(a thymidine analog)
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CONTROL OF VASCULAR DEVELOPMENT
329
demonstrateda specific role of DNAsynthesis per se in the differentiation
process. BUdRdid not block cell replication. Both FUdRand BUdReffects
are prevented and reversed by simultaneous or subsequent TdRtreatment.
Both replication and xylogenesis were blocked within 48 hours of FUdR
treatment and both recovered within 72 hours of TdRaddition (108). How
BUdRelicits its effect is unknown. BUdRincorporation into DNAis
considered essential (74). BUdRis incorporated into the DNAof pea cells
(108). In Tetrahymena BUdRblocks RNAsynthesis in synchronized ceils
but only if it is available to cells during DNA
synthesis and most specifically
during replication of the ribosomal genes (74). Lykkesfeldt &Andersen(74)
postulated that this BUdR
effect results from its incorporation into AT-rich
regions. Thus, the transcription of all AT-rich regions maybe selectively
inhibited, and this could conceivably block RNAsynthesis related to xylogenesis but not that whichis necessary for cell replication.
Factors other than hormoneshave not been extensively investigated relative to their use in studies of vascular development. Increased pressure
stimulates xylemdifferentiation in stems (9). The mechanismhas not been
investigated, but Roberts (102) suggested it occurred through induced ethylene production. Doley & Leyton (27) found lowered water potential
stimulate xylogenesis and suggested that this might be the basis of the
observed sucrose stimulation. Other investigators have not found osmotic
agents in general to stimulate vascular developmentas efficiently as sucrose.
In Jerusalem artichoke tuber tissue it was observed that (a) reducing the
nitrogen concentration of the medium, and (b) reducing the volume
mediumare both stimulatory to xylogenesis (90). The volumeeffect does
not seem due to a "conditioning" of the medium(90).
Light generally inhibits xylogenesis. In the Jerusalem artichoke, a brief
exposureto dim white light inhibited cell replication and xylogenesis relative to a dim green light control (90). Continuouswhite light (relative
a brief exposureto white ligh0 had little effect on replication but inhibited
xylogenesis (90). Similar results have been observed in the pea system (T.
L. Shininger, unpublished observations). In carrot culture, light can be
requirementfor xylogenesis (79-81), but if so, it is replaceable by cytokinin
(79). Studies of the light effect in other systems need to be conductedmore
conscientiously.
Temperature as a probe of vascular development has not been utilized
generally. Gautheret (43) reported that in the Jerusalem artichoke callus
temperatures less than 17°C were inhibitory. This was confirmed in freshly
excised tubers as well (90). Naik (82) reported that a high temperature
(35°C) stimulates xylogenesis in this system, but this was not confirmed
subsequent work (90). In any case, these effects have not been distinguished
from effects on replication.
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330
SHININGER
In a recent series of experimentswith the pea system, I havefoundsome
specific effects of temperatureon xylogenesis(110). Briefly, low (10°C)
high (30°C)temperaturesinhibit xylogenesisrelatively morethan replication. Lowtemperature wasstudied extensivdy, and it wasfound to delay
the initiation of xylemcell appearanceby several days. However,once
initiated, these cells appearedat essentially normalrates. Cell replication
wasnot affected in this ease. This is not causedby an affect on overt
cytodifferentiation becausetransfer of cells to low temperatureafter the
initiation of xylogenesisdid not cause a drop in the rate of xylemcell
appearancefor at least 7 days. When
cultures wereinitiated at lowtempera.
ture and then shifted up, there was no transient increase in the rate of
vascular cell appearanceto suggest they had accumulatedat a specific
temperature-sensitivepoint in development.]Brief low temperaturetreatments(24, 48 hours, etc) indicated that xylogenesiswastemperaturesensitive before replication of the cortical parenchyma
wasinitiated. Theresults
suggest that since xylogenesis can be uncoupledfrom the early roundsof
replication, these early replications haveno uniquerole in development.
Sinceit is unlikelythat cells committed
to xylogenesisexist in the cortical
parenchyma,it follows that xylogenesisin this system can be inducedby
definedexogenous
stimuli whenever
the cells ~Lrereplicating at an appropriate temperature.
°Thepea systemoffers someinteresting points for further analysis. At 25
both xylogenesis and nonxylemcell formatiion shownearly exponential
kinetics. Howthis relates to the fate of individualreplicatingcells is not yet
known.The possibilities are that one cell provides two daughters which
differentiate or that onecell providesonecell for continuedreplication and
one for vascular developmentor somecomplication of this scheme.Observations of sections havenot yet revealed isolated single tracheary elements, but it is prematureto state that they are not to be found in this
system.
It is also interesting to note that in this systemonecan observelinearity
betweenthe log of the vascular cell numberand log of the nonvascular
cell number.This relationship is not disturbed by temperaturechanges.Nor
is it altered by changesin cytokininconcentrationwhichare known
to affect
the rates of xylemand nonxylemcell formation differentially. This may
meanthat the rates of these processesare coupled.If so the result of this
is that chan~esin replication rates generatetissues with different percentages of vascular elementsrather than a proportionateincrease in the number of xylemand nonxylemcells. The log/log relationship is disturbed by
BUdR.Myreanalysis of other systemsindicates that whereadequatedata
exist the samerelationship occurs(41, 90). Exactlyhowthese responsesare
coupledremainsto be investigated. It seemsclear that this relationship
indicates a basic developmentalcontrol mechanism.
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CONTROLOF VASCULARDEVELOPMENT 331
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CONCLUSIONS:
Control of Vascularization
in the Shoot and Root
Theprocessof vascularizationinvolvesfirst the productionof a population
of cells in whichvasculardifferentiation can be induced.Theprocessought
to be viewedas a continuumof developmentalevents involving as a first
identifiable step the distinguishingof the potential vascularcells fromthe
nonvascularby differential parenchymatization.Thenonparenchyma
cells
maynowbe considered to be in the pathwayto vascular developmentbut
are not obligatedto that fate becauseremovalof exogenousstimuli (auxin,
sucrose) allows themto divert to the parenchyma
state. Procambium
is
term that shouldbe employed
to describe potential vascular cells whichare
at this state of development.
It shouldbe possible to further breakdownthe
stages of differentiation within this concept of procambium.Whenthese
cells irreversibly changecytologically toward either the xylemor the
phloem,they can be consideredovertly differentiated and no longer procambial. In shoots, stimuli are derived in part fromthe developingleaves
and in part fromthe matureshoot. In the root these factors maybe derived
in part from the terminal portions of the meristem(root cap, QC,and
proximalmeristem)and in part from moremature sections of the root.
In the shootit is clear that the leaves play an impo~antregulatory role
in the formationand development
of procambium
as it is currently identified. However,we do not have a meaningfulconcept of procambium
at a
biochemicalor ultrastruetural level, and the development
of concepts at
these levels is important.Bothauxin andsucroseare critical to procambium
formationandto the formationof vascular cells in cultured tissue. Wedo
not knowthe roles of either of these agents in the differentiation process.
Overtdifferentiation probablycan be monitoredat the biochemicallevel
andcertainly can be monitoredat the ultrastructural level. It is conceivable
that phloemdifferentiation could be followed immunologieallyin those
organismswhichform P-protein or biochemieallywith careful analyses of
fl-1,3-glucansynthetaseactivity in conjunctionwith cytologicalstudies. It
is not clear if significant nuclearor nucleolarchangesoccurin sieve element
differentiation. Thechangesin the nuclei of differentiating trachearyelements mayhave been misleading, however.
Biochemicalanalyses of tracheary elementdifferentiation maybe more
ditiieult until secondarycell wall compositionis characterizedin greater
detail. Lignifieation probably can be used as a valid marker of xylem
differentiation, especially since onereally wantsa markercharacteristic of
terminalaspectsofcytodifferentiation.Thereexists the possibility that there
is considerablymoremicrotubularprotein in differentiating xylemcells if
microtubulesare really associated with secondarywall deposition. Sucha
quantitative changemightbe detectable.
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332
SHININGER
DNA
synthesis seemscritical to xylemdifferentiation. Withbiochemical
markersof xylogenesis,it maybe possible to determinethe reason for the
need for DNA
synthesis.
Thevarious roles of auxins, cytokinins, and occasionally gibberellins
need meaningfulexploration. Wedo not have an adequate understanding
of these hormoneseven in simpler response systems. These hormonescan
only be understoodwhenplant scientists generally becomewilling to explore hormoneresponses with truly rigorous and contemporarybiochemical or genetic approaches.The exploitation of temperatureand light may
be useful and, becauseof the "neatness" of such experiments,the results
might be extremely important.
Thedevelopment
of suspensioncultures that will differentiate reasonably
synchronouslywouldbe extremelyuseful. Therecent workof Torrey (132)
makesone optimistic commentabout that approach.
The recent manipulationsof the QCeffect on developmentand attempts
at physiological replacement of the QCwidth hormonesboundto resin
coated beads (36) provide impetusto explore these systemsmoreimaginatively. Finally, the autonomous nature of t!he root tip makes it ideal for
exploration of manyof the sorts of questions whichpreviously have been
consideredonly in tissue culture. Thechief advantageof the root tip culture
is the productionof vascular cells in predictable time and space. Thusit
ought to be possible to define procambium
in the root in terms of its
responses to specific metabolic analogs or physical treatments in ways
analogousto the early workof Torrey(132,).
Literature Cited
1. Aloni,R., Jacobs, W.P. 1977.Thetime
courseof sieve tube andvessel regeneration and their relation to phloemanastomosesin matureinternodesof Coleus.
Am. J. Bot. 64:615-21
2. Avanzi,S., Maggini,F., Irmocenti, A.
M. 1973. Amplilieation of ribosomal
eistrons during the maturation of
metaxylem
in the root of Alliumcepa.
Protoplasma76:197-210
3. Ball, E. 1949. Theshoot apexand norreal plant of Lupinusalbus L. bases for
experimentalmorphology.Am. J. Bot.
36:4~)-54
4. Ball, E. 1950.Differentiationin a callus
culture of Sequoiasempervirens.Growth
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5. Benayoun,
Regeneration around woundsand the
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6. Benayoun,J., Sachs, T. 1976. Unusual
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Differenzierung
in Gewebekulturen
yon
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8. Brown,C. L. 1975. Secondarygrowth.
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9. Brown,C. L., Sax, K. 1962. Theirdlueneeof pressureonthe differentiationof
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zierungs-vorg’fingein der Crueifemwnrzel. Planta 39:126-53
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cultures of Acerpseudoplatanu~
J. Exp.
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de
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