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THE
VOL. 59
BOTANICAL
REVIEW
No. 1
JANUARY-MARCH, 1993
I. Abstract.1....
Zusammenfassung-..
..2
II. Introduction..
III. TerminologyPertainingto LaticiferStructure
....3
IV. Conceptson Formation
of
Laticifers-------------------------------------...
A. IntercellularSpace
Concept- .
..--B. CellularConcept..5
V. Classificationand Distributionof Laticifers
..--7
VI. Originand Development of the NonarticulatedLaticifer
.10
A. Euphorbia-typeLaticifer.11l
B. Variationsof the Euphorbia-typeLaticifer
VII. Mode of Growthof the NonarticulatedLaticifer.-.
VIII. Wall Structureof the NonarticulatedLaticifer
..
..
IX. Cytologyof the NonarticulatedLaticifer
.
X. Summary- .------------------------.--..
XI. Acknowledgments...20
XII. LiteratureCited..
.20
2
4
4
--
..
.
14
15
17
18
19
I. Abstract
This reviewdescribesthe developmentof the laticiferconcept,with emphasisupon
the nonarticulatedtype, from early observationsof plant exudates and "juices"to
the presentationof laticifersby Esau(1953). Classicalwritersand herbalistsdescribed
practicalapplicationsof these substances.With the advent of the microscopeearly
investigatorsbelieved that these substancesoccurredin structurespresent in most,
if not all, plants and, wrongly,equatedthese structuresto the circulatorysystem in
animals. Introductionof the term, latex, into botany derived from its early use as a
term for a blood component by physicians,and not for analogy to milk. However,
the originof the terms, laticiferand laticiferous,remainsuncertain.Initial studies of
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The Botanical ReviewS59: 1-23, Jan.-Mar., 19931
? 1993 The New York Botanical Garden
Zusammenfassung
Die vorliegendeUbersichtbeschreibtdie Entwicklungdes Milchrohrenkonzeptes,
beginnendmit den friihen Beobachtungenan Pflanzenausscheidungenund "Pflanzensaften"bis hin zu ihrer Darstellungbei Esau (1953). Dabei stehen ungegliederte
Milchr6hrenim Vordergrund.Die klassischenSchriftstellersowie die Verfasserder
Krauterbiicherhaben die Nutzanwendungendieser Stoffegeschildert.Mit der Erfindungdes MikroskopswurdenfriiheForscherzu der Annahmeverleitet,daBderartige
Stoffein Strukturenvorkamen,die den meisten,wennnichtallenPflanzengemeinsam
seien. Diese Strukturenwurdendann, falschlicherweise,mit dem Kreislaufder Tiere
homoligisiert.Die Einfuhrungdes Begriffs"Latex"in die botanischeTerminologie
beruhtauf der friiheniirztlichenVerwendungdieses Begriffsfureinen Blutbestandteil,
und nicht auf einer Analogie zu Milch. Die genaue Herkunft der Bezeichnungen
"Milchr6hre"und "Milchsaftfuhrend"bleibt jedoch im Dunkeln. Erste Untersuchungen an Milchr6hrenwaren von der Kontroversegepriigt,ob es sich um sehr
starkgestreckteZellen oder um HohlraumezwischenZellen handelt.Mit der Bestatigungder zellularenNatur der Milchrohrenfand ihre Einteilungin gegliederteund
ungegliederteMilchrohrenstatt. Es konnte gezeigt werden, daB ungegliederteMilchrohrenschon in den friihen EmbryonalstadienmilchsaftfuhrenderPflanzen angelegtwerden.Die ontogenetischeHerkunftgegliederteMilchr6hrenkonntevon den
friihenBearbeiternnicht geklartwerden;sie stelltenjedoch fest, daBneue MilchrohrenzellendurchkambialeAktivitatabgegliedertwerden.Es wurdeauch beschrieben,
daB ungegliederteMilchrohrenwaihrenddes Wachstumsin bereits vorhandeneGewebe eindringen,wobei ihre Zellspitzensich zwischen die ZellwiindezweierbenachbarterZellen drangen.Die coenocytischeNatur ungegliederterMilchr6hrenkommt
durchKemteilungenan der Spitze der Milchrohreund damit des Sprosseszustande,
wobei sich die Tochterkernenach ihrer Abgliederungentlang der gesamten Zelle
verteilen.
II. Introduction
The conspicuousmilky content in certainplants has attractedcuriosityfor many
centuries. Early scholars recognizedthat the colored, milky substances,as well as
those of a mucilaginousor resinouscharacter,were restrictedto particularplants. In
the classicalliteraturetherewereoccasionalreferencesto the collectionof theseplants
for their peculiar contents. Presumablysuch substances were utilized for various
practicalpurposes.Theophrastus(1916) referredto the milky juices of the spurges
which were collected for medicinal purposes.He also referredto the juices of other
LATICIFERS
THE BOTANICALREVIEW
its due proportion of latex" (Spry, 1767). Like blood, the latex in the plant was
thoughtto be containedin a vessel system. Latexalso coagulatedupon removalfrom
the plant, as did blood. Schultz communicatedhis observationsto Lindley (1848),
who publishedthem in some detail. In this work, Lindley also referredto the milky
substanceas latex. The termlatex remainedwell entrenchedin the botanicalliterature
thereafter.Duringthe first half of the 18th century,many of the anatomicalstudies
upon plants were performedby investigatorswith some medicaltraining.Thus, it is
understandablehow any term with medical implications would be injected into
botany.
The term laticiferalso has appearedin the literature(Esau, 1953; Jackson, 1928),
and was more convenient than such terms as laticiferousvessel or laticiferousstructure. Since the composition of latex was quite variable,it was difficultto define as a
substance (Bonner & Galston, 1947). Historically, latex was characterizedby its
capacityto coagulatewhen removed from the plant;its compositionwas completely
unknown. Superficially,latex may appearnearly clear (Nerium),or white and very
turbid (Euphorbia).It also may be colored, either yellow-brownas in Cannabis,
yellow-orangeas in Papaver,or red as in Sanguinaria.However, these observations
providedno data on the chemical composition of latex. In early studies of laticifers
the most preciselyidentifiedsubstancefoundin latexwas starch(Hartig,1843;Potter,
1884; Trecul, 1865a).
LATICIFERS
matrix representedthe cell wall. Elongatedvasa propriawere producedby the longitudinalextension of particulardrops of the nutrientsap.
Plant growthwas the result of continuedformationof new utriclesor cells among
those alreadyformed. The cell wall matrix was representedas a homogeneoussubstance, precludingthe existence of any intercellularspaces. This conclusion was
somewhatin contrastto that of Grewwho recognizedintercellularspaces.However,
Grew was not certainof their relationshipto his "lactiferousvessel."
The cellular nature of Malpighi's vasa propriawas expounded by several early
investigatorsand was contemporarywith the intercellularspace concept (Moldenhauer, 1812; Trecul, 1865b; Unger, 1847; Wolff, 1869). However, the concepts expressedby these investigatorswere quite dissimilar.
A more accurateinterpretationof cellulararrangementwithin the plant body was
presentedby Moldenhauer(1812) who employed a macerationtechniqueto isolate
individualplant cells. He theorizedthat if cells could be isolated, then each cell must
possess its own wall. Similarly,any two adjacentcell cavities must be separatedby
two walls. Utilizing this theory he investigatedand redescribedthe vasa propriaof
Malpighiwith some degreeof accuracy,referringto them as cells. He describedthe
vessel-likenatureof the laticifersin Musa, Asclepiasand Chelidonium.However,he
did not considerthe resin canals of Pinus to be similarto the laticifer.Moldenhauer
emphasizedthat the presenceof a discretelayer of cells surroundingthe resin canal
and the presenceof a special membranelining the inner side of the canal suggested
that the canals were not related to laticifers.
The significanceof Moldenhauer'stheorywas not recognizedimmediately,but the
theory did aid in defining the cellular nature of plant tissues in general. Several
investigatorssuggestedthat laticiferousstructureswere very elongatedcells (Dippel,
1865;Faivre, 1868;Hanstein, 1864;Hartig,1862;Schacht,1851, 1856;Unger, 1840,
1847; Vogl, 1863). The formationof the laticiferousvessel was vividly describedby
Ungerfrom observationsthat he made on Ficus benghalensisL. Vessels were formed
from superimposedrows of cells. The greatlengthof these vessels was attainedupon
resorptionof transversewalls that separatedthe cellularcomponents.He noted that
the walls of these vessels were initially quite delicate. During their subsequentdevelopment,the cells laid down additional,but ratherirregular,thickeningsupon their
walls.
Laticiferswere dispersedthroughoutthe plant body and, accordingto Unger, the
vessels were joined into a complex system by means of lateralbranches.Although
correct in many essentials his description of the formation of the laticifer in this
plant was proven later to be incorrect.Nevertheless, since his interpretationwas
published during the period in which the intercellularspace concept was widely
recognized,it did stimulate furtherinvestigationson this topic.
Schacht(1851) investigatedthe laticiferousstructuresin various generaincluded
in the Apocynaceae( Vinca),Asclepiadaceae(Hoya,Gomphocarpus),
Caricaceae(Carica), Cichoriaceae(Lactuca, Sonchus), Euphorbiaceae(Euphorbia),Papaveraceae
(Papaver,Chelidonium).In all instances he found that laticifers were of a cellular
origin. He describedthem as resultingfrom the fusion of many or a few cells into a
vessel. Since he was unable to find the laticiferousvessels formed into an anastomosing system in all of the plants that he investigated,he dismissed the possibility
that they served any circulatoryfunction similar to that presentin animals.
Schacht(1851) clearlydescribedthe formationof the laticiferin Caricaas arising
from rows of superimposedcells, the transversewalls of which were resorbed.The
LATICIFERS
Table I
Classification of Laticifers (Chauveaud, 189 1)
{
original
subsequent
Arisingduringpost-embryoni
separate
fused
anastomosing
series
Dalechampia,Bertya.
isolated
Glaucium.
continuous
tubes
Laticiferous
tissues
articulated
cells
10
Table II
Classificationof Laticifers(Esau, 1953)
Nonarticulatedlaticifers:
Unbranched:
Apocynaceae,Eucommiaceae,Moraceae,and Urticaceae(in part).
Branched:
Apocynaceae,Asclepiadaceae,Euphorbiaceae(in part),and Moraceae.
Articulatedlaticifers:
Nonanastomosing:
Convolvulaceae,Liliaceae,Papaveraceae,Sapotaceae,and Urticaceae (in part).
Anastomosing:
Campanulaceae,Caricaceae,Compositae(Cichoriaceae),Euphorbiaceae (in part),and Papaveraceae.
1884; Fraser, 1931; Parkin, 1900; Scott, 1884). Thus, intrusive growth may not be
restrictedto the nonarticulatedtype of laticifer.
It should be noted also that both the articulatedlaticifer, as in Hevea, and the
nonarticulatedtype, as in Euphorbia,occurredin the Euphorbiaceae(Schaffstein,
1932). It had been reportedby Schaffstein(1932) that both laticifertypes could occur
in the same plant as was the case in Stapelia and Trichocaulon(Asclepiadaceae).
LATICIFERS
11
lamina. These new laticifer initials, by means of coalescence with adjacent cells,
progressivelydeveloped into a ramifiednetworkof tubes that extended throughout
the entire leaf.
Upon reinvestigatingsimilar generautilized by Dippel, David (1872) was not in
complete agreementwith Dippel's conclusions.Accordingto David the laticifersin
the Apocynaceae, Asclepiadaceae,Euphorbiaceaeand Moraceaewere single cells
(nonarticulated),which "elongatedto a significantlength by means of active and
passive stretchingand also by means of branchinginto the intercellularspaces."The
laticiferouscells couldbe presentin both the cortexand the pith (Euphorbiasplendens,
Ficus elastica L., Nerium oleander,Hoya carnosa R. Br.) or were confined to the
cortex (E. cyparissiasL., F. carica).
David (1872) maintainedthatnew laticiferswereformedprogressivelyfromcertain
cells of the groundtissue below the terminalmeristemduringthe growthof the plant.
Each new laticiferfrequentlybranchedas it elongated,but no anastomosescould be
observed between adjacentbranches.He was not certain of their relationshipwith
the vascularbundles. In the stem the laticiferswere randomlydistributed,while in
the petiole and the blade of the leaf they were associatedwith the vascularstrands.
David, in contrastto Dippel, observed that the brancheswhich extended into the
petiole fromthe stem continuedinto the blade of the leaf to forma continuoussystem
(Euphorbia).However, in Ficus, Nerium, and Hoya it did appear to him that the
"leaf specific"laticifer,as describedby Dippel, did occur.Mayus (1905), in contrast
to Dippel, recognizedthat the entirelaticiferoussystem of the leaf was a continuation
of branchesfrom the stem. Tips of laticifer cells were observed in these plants to
penetrateamong mesophyll cells to and between radial walls of epidermalcells to
the cuticle of the leaf (Chauveaud,1891; Gaucher, 1902; Groom, 1889).
Both Dippel (1865) and David (1872) observed that the laticifercould be distinguished from adjacentcells in the embryo and meristems well before the cellular
elements of either the xylem or phloem became identifiable.David found no indication in his material that new laticifers were produced by cambial activity, as
suggestedby Dippel.
A. EUPHORBIA-TYPE LATICIFER
12
LATICIFERS
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LATICIFERS
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LATICIFERS
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LATICIFERS
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in length of other cells is absent in this laticifer.Thus, unlike other cell types, this
laticifercan grow intrusivelyas a single cell throughoutdifferenttissues of the plant
body. This featuresets the nonarticulatedlaticiferapartfrom other cells.
The detectionby classicalworkersof a coenocyticprotoplastin the nonarticulated
laticiferemphasizedthe occurrenceof an alterationin the mitotic apparatusresulting
in the loss of the mechanismcontrollingcell plate and wall development.All nuclei
in a nonarticulatedlaticifer, including those in the growing tips of the laticifer in
plant meristems, representprogenyfrom the originalnucleus of the laticiferinitial.
This laticifer,therefore,is cytologicallyisolatedfrom the meristemswhereasfor other
tissues the meristemscontributenew cells with their nuclei to the developingtissue.
XI. Acknowledgments
The authorwishes to thank Dr. SigridLiede for preparingthe Germantranslation
of the abstractfor this review.
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