Evolution of a cormophytic plant body in lower'vascular plants

B. K. Nayar

Nayar BK 1992 Evolution of a connophytic plant body in lower vascular plants. Palaeobotanist 41 75-86.

Possession of a cormophytic plant body and stelar system distinguishes vascular plants from thallophyticancestors. Based on morphology and development of sporophyte and gametophyte of pteridophytes it is arguedthat current interpretations of morphology and evolution of these features in terms of Axial theory and Stelar theoryare untenable in these primitive vascular plants. The leaf, and not the axis/stem, is the primary organ and the first toevolve. The leaf along with its associated roOt constitutes a Phyllorhize which is the basic unit of construction of theplant body; a succession of phyllorhizes interconnected by the leaf base regions result in the cormophytic plantbody. Shoot apical meristem functions only in initiating leaves and branches and what appears as stem is a productof conjoined leaf bases, the shoot meristem contributing little to its construction. Vasculature is developed only intissues derived from leaf· and root·meristems; no vasculature is developed in tissue derived from the shootmeristem. Stelar cylinder consists of secondarily interconnected basal regions of leaf vasculatures and sometimesalso vasculature of leaf· associated roots. The pattern of growth (different in taxa having erect rhizome andplagiotropic rhizome) determines the nature of the stelar cylinder. Evolution apparently followed the same coursein gametophytic and sporophytic generations, and evolution of pteridophyte gametophyte indicates that theprimitive form was an amorphous cushion' shaped thallus devoid of meristem and vasculature. It is shown how aphyllorhize unit evolved from such a plant body. Morphological, anatomical and ontogenetic evidences arepresented in support of the contention that the pteridophyte plant body is formed' of conjoined leaf bases and itsstele is the product of leaf base· vasculatures interconnected in a regular pattern. Also, it is shown that stelarevolution did not follow the sequence suggested by Stelar theory.

Key-words-Evolution, Vascular plants, Anatomy, Phyllorhize concept.

B K. Naym', Department of Life Sciences, University of Calicut, Kerala, India.

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ACCEPTAj'.JCE of evolution as causativediversity of life forms initiated theunderstanding the process of biological

ro the vastquest forevolution,

Essays in Evolutionary Plant Biology

Edtrors , B. S. venkatachala, David L. Dllcher & Hati K. MaheshwariPublisher' Birbal Sahni Institute of Palaeobotany, Lucknow

76 THE PAlAEOBOTANIST

and during the past 100 years a vast wealth ofinformation was collected which makes it possibletoday to circumscribe and characterise the six majorgroups of plants and aIso understand the process by\vhich the diversiry within each of these groupscame aboLit. Currently it is possible to reconstructwith reasonable accuracy the process of evolutionwithin each such group like the bryophytes,pteridophytes, gymnosperms and angiosperms, andalso to understand the position each occupies inrelation to the other groups in terms of evolution.Howc\'er, ""'hen it comes to possible inter­relationships between these major groups, thesiwation is different; nothing more than intelligentguesw_'ork propagated as hypotheses is available tobridge the gap between the major groups. And thewidest gap of all is the one betvveen vascular plantson the one hand and nonvascular plants orthallophytes on the other, though it is accepted thatall vascular plants evolved from Chlorophyceanancestors Morphological differences betweenthalloph)tes and vascular plants are so vast that ithas not so far been possible to explain how thesediffcrences came about. The major distinguishingfeaturc of \'ascular plants is their cormophytic planthock, ie .. a plant body constructed of stem, leaf androot. each haVing a characteristic morphology whichis bask:"II\' thc same in all and the like of whichdocs nllt exist in any thallophyte. Another majordiffcl'cnce is the vasc..:ular system or stele \vhich isuni\'ersal in \'ascular plants but tOtally absent intha Iloph \'tes.

Currently all interpretations of vascular plantmorphology are based basically on the Axial theoryand StelaI' theory, both of which are hypotheses""'hich seek to explain the fundamental nature of thevascular plant body. The former contends that thestem or axis is the most fundamental organ and firsttll c\'l)he, lea\'es and roots are but appendagesbllr!1e on the pre-existent axis. On this basis theC\'l)!utillnary gap between vascular plants andthallllpll\.tcs is sought to be bridged by explaininghll\\' the axis evolved from a thallose plant body, andse\'eral hypotheses have been proposed. But thecxtensive studies of fossil as well as extant plantshave so far failed to provide any tangible evidence insupport of the A;"ia 1 theory. Stela r theory maintainsthat all \'asculature of the plant body tOgetherconstitutes an organ haVing a definite morphology'\\ihich .exhibits distinct evolutionary trends fromsimple to more complex forms, It is based on theA;"ial theor~' and attempts to explain vasculature ofleaf and root as originating from the axis to supplythese organs, the \'asCldature of the axis being morefundamental. A"'is \'asculature is presumed to be a

solid central cylinder whi<;:h during evol'utionunder\-yem modifications through parenchymati,sation of certain of its regions so that a pith, leafgaps, etc. were formed and the haplostelic protostelebecame siphonostelic, dietyostelic, polystelic oreustelic. I3mver's (1930) Size and Form hypothesisseeks to proVide a rational basis for stelaI' evolution,maintaining that presumed physiological constraintsinduced by increase in size resulted in progressivechanges in form.

LEAF AS THE PRIMARY ORGAN

Tn order to gain an insight into the processthrough which the cormophytic plant body with itsstele evolved, a detailed study of morphology of thegametophyte and sporophyte of pteridophytes wasundertaken, and the present account is based onthese studies. Pteridophytes are selected becausethey are among the earliest to possess a cormophyticconstruction and stelar system. The studies suggestthat the pteridophyte plant body is not constructedas explained by Axial theory nor can its vascularsystem be accepted as an organ, In addition, stelarevolution in pteridophytes does not follow theprinCiples of Stelar theory and Size and Formh)11othesis. All evidences indicate that. the leaf.instead of the stem, is the primary organ, and that itis the leaf which gave rise to the cormophytic plantbody as well as to the stele. The stele is a compositebody consisting of interconnected basal regions ofvascula tu res of successive lea Yes.

The leaf is essentially a subcylindrical axis witha continual growing apical end (apical meristem)and a roOt at its basal end in continuation of the leafaxis and with an apical meristem of its own. The leafaxis bears at regular intetvals a series of discretelateral merisrems similar to its apical meristem;these form a longitudinal row on either side. Inaddition, it bears throughout its length a laminarmeristem on either side, consisting of a longitudinalrow of meristematic cells interconnecting the lateralmeristems, Laminar meristem as well as lateralmeristems behave differently at different regions ofthe leaf axis. Tn the anterior half the lateralmeristems grow out as branches similar to the leafaxis and the laminar meristem continues up thesebranches, In some cases the laminar meristem in theanterior half is uniformly active and this results in asimple leaf lamina with the lateral branches of theaxis constituting the main lateral veins (Text-figure1). Tn others the activity of the meristem is inhibitedexcept on the lateral branches, resulting in a pinnatelamina (Text-figure 2); the inhibited regions oflaminar meristem develop into aerating bands

NAYAR-CORMOPHYTIC PlANT BODY IN LOWER VASCULAR PlANTS 77

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characrerisric of all fern leaves. When rhe process ofinhibirion of acriviry of laminar merisrem is repearedon rhe lareral branches of rhe axis as well, moredissecred leaf forms result. Commonly rhe laminarmerisrem is inhibired in rhe posrerior half of rhe leafaxis, developing only an aeraring band on eirherside. Ar rhe basal region rhe lareral merisrems alsoremain dormanr or nearly so. This resulrs in a leafhaving a naked periole. However, one or a fewlareral merisrems close ro rhe basal end of the leafaxis develop inro lareral roars. All lareral merisrems,as also rhe merisrem from which rhe basal roor

develops, are iniriared similarly from soliraryperipheral cells of rhe leaf axis. The inirial celldivides by rhree successive anriclinal walls, eachwall being oblique and rhe rhree inrersecring so rharan obpyramidal cenrral daughrer cell resulrs,surrounded by sisrer cells on rhe lareral andposrerior sides and having rhe peripheral (exposed)wall of rhe inirial cell as irs fourth side (Text·figure4A-D); rhe cenrral daughrer cell consritures rheapical merisremaric cell. Excepr in rhe case of rhefew ar rhe basal region of rhe leaf axis, whichdevelop inro roars, rhe apical merisremaric cell curs

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off daughter cells against the three lateral obliquesides in regular succession; no daughter cell is cutoff against the exposed peripheral wall, with theresult that the meristematic cell continuesthroughout as a superficial cell (Text-figure 3E, F).However, in the case of the roOt, daughter cells arecut off against all four sides (including theperiferal Side) of the apical cell (Text-figure 4A-F).The first daughter cell cut off against the peripheralside bc:;haves like other peripheral cells of the leafbase, dividing anticlinally and periclinally so that theroot apical cell becomes deep seated in the cortex ofthe leaf base. A root cap develops from similardaughter cells cut off later. The leaf with itsassociated roots constitutes a phyllorhize unit. A

succession of such phyllCJrhize units builds thecormophytic plant body, the stem being theconjoined basal ends of successive leaves, i.e., d

collection of leaf bases.

ORIGIN AND EVOLUTION OF THECORMOPHYTIC PLANT BODY

It should logically be presumed that both thegametophytic and the sporophyric generationsfollowed basically the same course in evolution,since both have the same genetic constitution andgrow under the same environment. Based on acomparative study of over 3,000 taxa ofpteridophytes, I have recently given an account

NAYAR-CORMOPHYTIC PLANT BODY IN LOWER VASCULAR PLANTS 79

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Text-figure II, 12-11. Juvenile plants of Drynaria quercijolia at different stages of development up to the 5-1eaved stage, showingvasculature and formation of a haplostelic protostele; in figure K the leaves and roots are shown cut off at base leaving theconjoined leaf bases which constitute the axis possessing a protostele; 12. Hypothetical drawings to explain the formation ofprotostele followed by dicryostele, by vascular bridges interconnecting bases of vasculature of successive leaves following thecommon pattern found among Filicopsida; figure A shows vasculature of the first three leaves, of which I and ii have cylindricalvasculature and ill has a channel-shaped vasculature, all the three interconnected by solitary vascular bridges; figures B-F showconfiguration of vasculature as further leaves are borne one by one 0, U, Iii, basal regions of vasculature·of successive juvenileleaves alongwith basal region of vasculature of associated roots and vascular commissures interconnecting leaf base vasculatures).

(Nayar, 1981, 1992) of the extent of morphologicalvariation and the evolutionary trends followed bythe gametophyric generation, concluding that themost primitive type is a dorsiventrally compressed,amorphous, cushion-shaped thallus as inEquisetales, devoid of any distinct meristem. Duringevolution twO separate growing meristems wereacquired by the cushion-shaped gametophyre, onering·like and lateral along the margin of the cushionand the other median at the centre of the expanded

dorsal side, the former leading to horizontal growthand the latter ro vertical growth. The earlier, moredominant and widespread among extantpteridophyres, is the lateral ring-like meristem. Thegrowing meristem of the common cordate-thalloidgametophyre (the most common form among extantpteridophyres) evolved from this lateral ring-likemeristem. During evolution, the ring-like meristembecame discontinuous, ultimately leaving only up tothree active regions as in Hymenophyllum and only

80

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Text-figure 13, 14-Dorsal (A) and ventral (B) views of vasculature at shoot apex of Microsorum pteropus (13) and M. linguaeforme(14), showing basal region of vasculatures of the youngest two leaves and their associated roots, vasculature of the dormant leafon the dormant branch of shoot apex dichotomy and vascular bridges between root vasculatures (b, basal region of vasculature ofbranch; r, vasculature of root; rb, vasculature associated with branch; r1, vasculature of root associated with first leaf; riJ,vasculature of roOt associated with second leaf; I, II, basal regions of vasculature of the first and second leaf from apex).

one in most other taxa. A creeping subcylindricalthallus results when the meristem is active at onepoint only. Margin to margin fusion of plate-likephotosynthetic lobes (of the type found in/:-qllisetu11l) borne on the dorsal side of such athallus to form one large expanded lobe (Wing) oneither side of the subcylindrical thallus gave rise tothe common cordate-thalloid type of gametOphyte.The second meristem acquired by the gametOphyteduring evolution (i.e., the dorsal median one or theapical meristem which leads to vertical growth) isfound only in a few, like some Lycopodiales, amongextant pteridophytes. In the Phlegmaria group ofLycopodium this meristem is prominent andpersistent so that the adult gametophyte iscylindr,ical and erect-growing with its lateralmeristem displaced to form a spiral (instead of aring) around the thallus. Also, the lateral meristembecomes discontinuous and gives rise to slender,cylindrical, horizontal branches which, on accountof the continuous upward growth of the thallus, are

borne at different levels up the erect thallus.It seems reasonable to presume that the

primitive sporophyte would also have been anamorphous cushion-like body similar to theprimitive gametophyte. Like the gametophyte itevolved into a cordate-thalloid form (Text-figure 2A,B) but possessed an active apical meristem locatedat the posterior end of the midrib on the dorsal side.If the midrib of such a thallus were to bear alternatelateral branches with the wings borne laterally onthe midrib as well as the branches, and if theposterior end of the midrib were to grow OLit in theopposite direction as a root (Text-figure 2C), aphyllorhize unit would result except that such a unitwould be devoid of any organised mechanical orconductive tissue. Obviously a thallose plant bodydevoid of mechanical and conductive tissue isconsiderably handicapped for a terrestrial existence.In the thalloid sporophyte this need is met by thedevelopment of vascular tissue and this would havebeen in the form of a cylindrical central strand in the

NAYAR-CORMOPHYfIC PlANT BODY IN LOWER VASCUlAR PlANTS 81

midrib. Similar vascular development takes place inthe root and the twO get interconnected so that thevascular strand is continuous in the leaf and itsassociated root. Thus the earliest vascular systemevolved, permitting the sporophyte to beconsiderably larger, functionally more effective andbetter adapted for a terrestrial environment. As inthe gametophyte of Phlegmaria group ofLycopodium, the apical meristem of the sporophyteis persistent on such a phyllorhize unit and producesa succession of discontinuous lateral meristems inspiral order. Each of these develops into aphyllorhize unit similar to the first one. Though aphyllorhize unit can have an independent existence,it is more advantageous if vascular systems ofsuccessive units are interconnected, especiallybecause the root, being a subterranean organ, has amore protected environment as compared to theaerial leaf and therefore could function muchlonger. If the vasculature of the younger leaves isconnected to the vasculature of roots associated witholder leaves, the younger leaf can take advantage ofthe longer life span of the older root even after theleaf associated with it has become disfunctional.Such interconnection would also provide additionalmechanical strength. Because of this, vasculatures ofsuccessive phyllorhizes would have becomesecondarily interconnected by a vascular bridge, theinterconnected vasculatures of successivephyllorhizes form the stelaI' cylinder. Persistent leafbases with interconnected vasculature constitute thestem.

EVIDENCE FROM EXTANTPTERIDOPHYTES

Growth and development in extantpteridophytes provide ample evidence that thecormophytic plant body of Filicopsida evolved alongthe above lines. The early juvenile plants of all ofthem consist merely of a single reaf associated with abasal root, with a central cylindrical vascular strandformed independently in the leaf and root and laterbecoming interconnected. It is of interest to notethat in a majority of taxa there initially exists noshoot meristem in juvenile plants. A shoot meristemappears after the first leaf has established itself.Similarly, during apogamous development of thesporophyte, initially .only a solitary leaf is producedwhich later gives rise to a basal root. A shoot apex isestablished at a much later stage only, commonlyafter the first two leaves are produced (Nayar &Bajpai, 1964). In all the fern taxa investigated indetail, vascular development takes placeindependently in the developing leaf and associated

root and this vasculature is unconnected to any othervasculature in the plant body (Nayar, 1985; Nayar &Molly, 1989; Nayar et at., 1980). Undifferentiatedcells next to the basal ends of the leaf-and rootvasculature later get differentiated into vasculartissue, the process progressively extending until thetwo are interconnected. Afterwards similar secondaryvascular differentiation is initiated next to the basalregion of the leaf vasculature and progressivelyextends posteriorly till a vascular bridge isestablished with vasculatures of the earlier twoleaves and thus getting connected with the anteriorend of the stelaI' cylinder (Nayar & Gopalakrishnan,1990; Nayar & Molly, 1989).

Irrespective of the adult condition, leaves areborne in spiral order, and the stem is erect·growingand short in the initial stages (i.e., in early juvenileplants) in all the taxa investigated. The shoot apicalmeristem consists of a conventional obpyramidalapical cell (Bierhorst, 1977) having four triangularsides of which the anterior one is peripheral at thestem apex and the other three lateral but obliquelyconverged to a p.oint opposite the peripheral side.All divisions in this cell are unequal, one daughtercell being much smaller than the other, plate-likeand next to one of the three lateral oblige walls(cutting face of the apical cell) so that the largerdaughter cell continues to have the form andfunction of the apical meristematic cell (Text figure5 A-D). The smaller plate-like daughter cell byrepeated equal divisions forms a plate of small cellswhich ultimately develop into stem tissue, exceptone of the peripheral daughter cells which givesorigin to a leaf apical cell. This condition persists inmany taxa, the activity of the shoot apical meristemcontinuing unchanged throughout. But in somePolypodiaceae (Nayar, 1985; Nayar & Molly, 1989),Davalliaceae, Lomariopsidaceae, etc. the stem laterbecomes elongated and creeping (plagiotropic),with leaves borne in twO dorsal rows and each leafassociated with an abaxially lateral branch bud at thebase. This change is initiated by the shoot apexacquiring the habit of undergoing an equaldichotomous division soon after producing eachleaf; commonly this occurs when the juvenile planthas produced 5-10 leaves but in some likeStenochlaena and Microsorum linguaeJorme itoccurs only after 15-20 leaves are borne. The shootapex dichotomises either by the apical meristematiccell dividing to form a pair of daughter meristematiccells (as in most Polypodiaceae) or by themeristematic cell ceasing to function, followed bythe formation of a pair of meristematic cells fromperipheral cells closeby at the anterior region of theshoot apex (as in Stenochlaena). In the former case

82 THE PALAEOBOTANIST

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NAYAR-CORMOPHYTIC PlANT BODY IN LOWER VASCUlAR PlANTS 83

the meristematic cell divides equally by a verticalwall extending from the posterior pointed end of thecell to the middle of its anterior peripheral wall sothat a pair of similar tetrahedral daughter cells areformed (Text-figure 4). Each of these functionsindependently so that the stem dichotomises intotwo branches. Each daughter apical cell dividesunequally so that plate-like daughter cells are cut offin succession against the lateral cutting faces. Thefirst plate-like daughter cell is cut off against theseparating wall becween the cwo daughter apicalcells. A leaf apical cell is differentiated from one ofthe daughter cells derived from the first plate-likedaughter cell of each of these apical cells and thusthe first leaf on the two branches of the dichotomy is­on the side facing each other. Where shoot apexdichotomy is initiated by the apical meristematic cellceasing to function, a periclinal division divides themeristematic cell into an outer and inner daughtercells. A series 0f anticlinal divisions in the outer(peripheral) daughter cell results in a group of cellswhich are similar to other peripheral cells at theshoot apex. A peripheral cell next to this group oneither side then functions as an initial cell whichgives rise to a new tetrahedral meristematic cell bydividing thrice by oblique anticlinal walls. The leafmeristem which is formed first on each of theresultant da ughter shoot apices is on the side facingthe other. Soon after the shoot apex dichotomises,one branch of the dichotomy, which is away fromthe subtending developed leaf, becomes sluggishand dormant. The other branch (i.e., the one nearestthe subtending leaf) continues growth. The dormantbranch ultimately gets pushed aside as the leaf baseof the first leaf on the dominant branch grows, and isoften carried forward by the developing leaf base,appearing as a branch bud characteristicallyassociated on the abaxial base of each developedleaf (Text-figure 7).

In some like Stenochlaena (Text-figure 9) theshoot apex dichotomises only after producing a pairof alternate leaves, but the second leaf becomessluggish and dormant so that it appears associatedwith the dormant branch anterior to it. However, itdevelops an elongated leaf base, with the result thatthe dormant branch is carried up the internodedeveloped by the first leaf of the dominant branch ofthe dichotomy. Also, this results in characteristicpeculiarities in the architecture of the stelarcylinder. In Nistarika (Text-figure 10), though theshoot apical cell dichotomises after each leaf andone of the branches of shoot apex dichotomyremains dormant, the leaf meristem produced by thedormant branch continues to be active, producing afully developed leaf. This results in the stem bearing

four, instead of two, dorsal rows of leaves, the cwolateral rows alone being associated with a branchbud. In Microsorum linguaeforme (Text-figure 8)the shoot apex dichotomises as in otherPolypodiaceae, after each leaf is developed. Butbefore any leaf meristem is differentiated on thebranches of the dichotomy, each branch apexdichotomises again so that fbur daughter shootapices result. Of these four, the pair away from theleaf becomes dormant as also the daughter apexnearest the leaf, the medianly placed one of the pairnearest the leaf alone continuing growth. Thisresults in the stem having leaves in one row onlyand each internode bearing a pair of oppositebranch buds of which the one away from thesubtending leaf is larger and bears two apices (Text­figure 8).

In all the fern taxa investigated, the shoot apicalmeristem is sluggish and contributes little to theconstruction of the plant body except that one of theperipheral cells formed by the repeated division ofeach plate-like primary daughter cell of the shootapical cell functions as the leaf initial cell. The leafmeristem is far more active than the shoot meristemand dominates the shoot apex, tissue derived from itconstituting the internode subtending thedeveloping leaf. As the internode develops andelongates, it carries the shoot apical meristemforward with it, till the next leaf is initiated from theproducts of the next plate-like daughter cell of theshoot apical cell and the process is repeated. Thus,the stem which appears to bear the leaves is in factmade up of leaf bases of successive leaves and thevasculature in this stem is the vasculature developedin the leaf base (Nayar & Molly, 1989; Nayar &Gopalakrishnan, 1990). Detailed ontogenetic studiesalone reveal thiS in the case of a majority of taxa, butin some which possess a long creeping stem (i.e.,much elongated internodes) such as manyThelypteridaceae.. Hyp 0 lep is, Stenochlaena, etc.external morphology also proVides clues. The mostcharacteristic feature of all leaves is the possessionof a lateral laminar meristem which extendsthroughout the length of the leafaxis; it develops anexpanded lamina in the anterior half of the leaf buton the petiole region it forms only the aeratingbands. In all the above taxa aerating bands areprominent and extend down the entire length of thesubtending internode also. In the case ofStenochlaena, which has pinnate leaves with pinnaealternating on either side in regular succession,highly reduced pinnae in continuation of the cworows of developed pinnae occur down the entirelength of the aerating band both on the petiole aswell as the subtending internode. Both these clearly

84 THE PALAEOBOTANIST

indicate that the internode is part of the leaf base.As mentioned above, each leaf is associated with

a basal roOt in all ferns and all lea ves, including thefirst juvenile leaf, bear a basal root. No root otherthan associated with leaves occur in any taxa. Inaddition to the basal root, other roots are borne bythe leaf base in the majority of ferns. These originateon the adaxial side of the leaf base and are in twoalternating rows, occupying the same position as thelateral pinnae (Text-figures 1, 2), i.e., in successionof the pinnae and interrupting the aerating bands.They originate in a similar manner from peripheralcells of the leaf axis. These additional roots are thusmodified pinnae. Nephro/epis, a taxon having anerect stem and spirally arranged leaves, possesses aunique organ, the stolon, which is root like in beingpositively geotropic, slender and much elongated,but having a stem like morphology in bearingpaleae, lacking a root cap and having an apicalmeristematic cell which is superficial throughout,i.e., one which does not produce any daughter cellagainst the anterior peripheral side as occur in thecase of root apical cell. Stolons vary in number andare associated with the leaf base. Each leaf bears asuccession of adaxial roots in alternate successionalong the aerating band as in other taxa and thestolons are in continuation of the two rows butfurther up the leaf base and in alternate succession.Roots, stolons and pinnae thus constitute anuninterrupted row on either lateral side of the leafaxis, and all of them originate in a similar mannerfrom superficial initial cells aloflg the aeratingbands, i.e., interrupting the laminar meristem. Thus,these unique organs are equivalent to the pinnaeand roots.

ORIGIN AND ARCHITECTURE OF STELE

Initiation and development of vasculatureprovide further evidence to the phyllorhize concept(Nayar, 1985) presented here. In all taxainvestigated, vascular differentiation takes placeassociated with the growing apices of leaf and rootonly, tissue derived from the leaf. and root meristemalone developing into vascular tissue. No vasculartissue is developed from tissue derived directly fromthe shoot meristem. A cylindrical vascular stranddevelops next to the growing apical region of theroot early during development. Simultaneously anintact s::hannel-shaped vascular strand isdifferentiated behind the leaf apical dome. Both areunconnected with any other vascular tissue. As theleaf and its associated root grow, progressivedifferentiation of tissue derived from the apicalmeristem of these organs extends the vasculatures.

keeping pace with the growth of the organs. Sincethe leaf and its associated root grow in oppositedirections the basal ends of the two vascular strandsface each other though separated by undifferentiatedparenchyma tissue of the leaf base. However,secondary differentiation of the interveningparenchyma into vascular tissue takes place, theprocess starting with cells abutting on the basal endof the two vascular strands and progressivelyextending. Ultimately the root vasculature getsconnected medianly to the basal abaxial (convex)side of the leaf vasculature. Secondary vasculardifferentiation at the basal end of the leafvasculature continues, the channel-shaped strandextending down the leaf base and soon splittingmedianly into two strap-shaped strands. One ofthese ultimately gets connected to the nearestmargin of the vasculature of the next older leaf whilethe other gets connected to the nearest margin ofthe vasculature of the leaf next older. No vasculardifferentiation takes place other than associated withleaves and roots, i.e., in tissue derived from leafmeristem, and there is no vascular or provasculartissue in the region anterior to the youngest leaf.

Vasculatures of early juvenile leaves andassociated roots are slender cylindrical and rod-like.They get interconnected by the interveningparenchyma cells between their basal ends gettingdifferentiated secondarily into vascular tissue. Later,secondary differentiation of vascular tissue next tothe basal end of vasculature of the leaf establishes aslender cylindrical vascular bridge with the basalregion of vasculature of the next older leaf. Thebasal regions of vasculature of successive leavesalong with the vascular bridges which interconnectthem constitutes a haplostelic protostele in the stem(Text-figure 10). Such protostelic condition persistsin some taxa such as Hymenophyllaceae whichcharacteristically possess small leaves. In the others,successive juvenile leaves and their vasculature areprogressively larger. Increase in size of the leafvasculature is accompanied by a change in its shape;from cylindrical it becomes progressively strap­shaped and later channel-shaped. Simultaneouslythe form and pattern of vascular interconnectionbetween successive leaves also change. The vascularbridge which interconnects successive leavesbecomes dorsiventral and channel·shaped and latermedianly split into a pair of strap-shaped bands; oneof the bands gets connected to the nearest margin ofvasculature of the next older leaf while the othergets connected to the nearest margin of the olderleaf next in succession, the two older leaves beingon opposite sides of the youngest leaf (Text-figure12B). Because successive leaves are initiated from a

NAYAR-CORMOPHYTIC PlANT BODY IN LOWER VASCUlAR PlANTS 85

daughter cell each of the plate-like primary cells cutoff in succession against the three cutting faces ofthe shoot apical cell, each set of three leavesconstitutes a helix of the spiral phyllotaxy (Nayar &Gopalakrishnan, 1990). Thus the vasculature of leafbases along with the interconnections belVJeen themconstitute a dissected hollow cylinder (Text-figure12C, D). The vascular bridge of the youngest leafwhich interconnects it with the second older leafcrosses the plane of the fifth older leaf (i.e., 6th leaffrom shoot apex) and this results in a leaf gapadaxial to the latter (Text-figure 12E, F). Thus leafgaps occur associated with the fifth and older leavesonly (Nayar, 1985). The resultant dictyostelicvascular cylinder, pierced by leaf gaps, is thus theprod uct of characteristic interconnections developedsecondarily belVJeen channel-shaped vasculatures ofsuccessive leaves and not formed byparenchymatisation of central region of a solidvascular cylinder as maintained by the Stelar theory.The progression from protostele to dictyostele doesnot occur due to presumed physiological constraintsas maintained by the Size and Form hypothesis.

In taxa having a plagiotropic stem (Davalli­aceae, Lomariopsidaceae, Polypodiaceae) the shootapical meristem dichotomises after each leaf andonly one of the branches of the dichotomy continuesgrowth (Nayar & Molly, 1989). Consequently theleaves are borne in lVJO rows only (Text-figure 7).Each leaf is associated with one or more adaxialroots. The shoot meristem is very sluggish while thedeveloping leaf apex is markedly active. As a resultthe latter dominates the apical region, pushing asidethe shoot apex away from the median position andoften carrying it forward as a lateral appendage onthe elongating leaf base. The prominent, elongatedleaf base becomes the youngest internode of thestem. Thus, the stem is formed entirely from theactivity of successive leaf meristems. Origin anddevelopment of vasculature are as in taxa having anerect stem, but the adaxial roots of each leaf,particularly those on the ventral margin, growforward through the internode formed by the sameleaf, often extending into one or lVJO anteriorinternodes as well, before emerging from theanterior end ventral to the shoot meristem.Vasculature of these roots run in the internodesparallel to the channel-shaped vasculature of the leafbase, with their basal ends connected to the marginof the channel-shaped leaf vasculature (Text-figure13). The pair of vascular bridges developed asposterior extensions of each leaf vasculatureinterconnect the leaf vasculature with the nearestmargins of the vasculatures of the next lVJO olderleaves. But since leaves are restricted to two dorsal

rows, such interconnection does not result in acylindrical dictyostele but only to a channel-shapedone with its free margins facing ventrally.Vasculatures of forward running roots of ~o to foursuccessive leaves, however, run belVJeen andparallel to the margins. Vascular bridges developsecondarily belVJeen nearby root vasculatures so thata loose reticul urn is formed by the root vasculaturesbridging the free margins of the channel-shapedstele and making it a reticulate cylinder (Text-figure13B). Thus, the dorsal half of the resultantdicryostele is made up of interconnected leafvasculatures while the ventral half is made up ofinterconnected root vasculatures (Nayar, 1985; Nayar& Molly, 1989). In Davalliaceae andLomariopsidaceae secondary differentiation ofintervening parenchyma belVJeen the basal regionsof root vasculatures ultimately results in an intactbroad ventral vascular strand which inLomariopsidaceae is channel-shaped and large.

Variations from this basic pattern, induced bychar;:Jcteristic differences in the cyclic activity ofshoot apical meristem in some taxa, provideadditional evidence for the explanation given herefor the construction of the stele and cormophyricplant body. Thus, in Microsorum linguaeJonne,which bears only a single dorsal row of leaves,vasculatures of successive leaves are interconnectedby strap-shaped basal extensions, each of the lVJOextensions associated with every leaf becomingconnected to the nearest margin of vasculature ofthe next older leaf. The interconnected vasculaturethus is channel·shaped and open on the ventral side(Text-figure 14). Each leaf bears up to 14 adaxialroots, the roots growing fOlward through the leafbase of the anterior two leaves. Vasculatures of theseroots run parallel to the free margins of the channel­shaped vasculature, and get secondarilyinterconnected to form a reticulum bridging themargins. Though vasculatures of roots borne on thesame side of the leaf base establish interconnectionsearly, no such interconnection is formed belVJeenroots of opposite sides so that the stele remainschannel·shaped up to the level of the 5th or 6th(from shoot apex) internode where vascular bridgesbelVJeen them develop. However, such bridges areless frequent so that the median row of lacunae inthe resultant dictyostelic vascular cylinder isconspicuously longer and broader (Nayar & Molly,1989).

Stenocblaena has a polycyclic dictyostele, acentral cylinder of about six stout meristeles and anouter cylinder of many slender meristeles (Text­figure 15). The lVJO cylinders are connected by thebasal regions of the vasculatures of leaves and roots.

86 THE PAlAEOBOTANIST

The shoot apex dichotomises after producing twoleaves (Text-figure 9). As the channel-shapedvasculature developed by the leaves extendsposteriorly it splits into three (instead of two as inother taxa) strap-shaped bands. The median one ofthese gets connected medianly to the concaveadaxial surface of the vasculature of the next olderleaf while the two lateral ones unite with the nearestmargin of the vasculature of the same leaf (Text­figure 17). This results in a cylindrical tube-like stelein the subtending internode, but since the youngerone of the twO leaves becomes dormant and remainsassociated with the dormant branch of the shootapex dichotomy (Text-figure 9), it gets pushed awayto one side and its vasculature (which by then getsinterconnected with vasculature of the first leaf onthe dormant branch) appears as vasculature of thebranch (Text figure 17D). The tube-like vasculatureof the branch is attached to the main vasculature ofthe internode without any associated gap. Also, thereare no leaf gaps on the main cylinder because of thecharacteristic median vascular bridge betweensuccessive leaves (Text-figures 16,17). In contrast toother ferns having a plagiotropic stem, roOtvasculatures do not contribute to the construction ofthe main vascular cylinder of the stem (Text-figure17). Root vasculatures pass obliquely through thecortex of the leaf base. Secondary differentiation ofvascular tissue occurs in the developing leaf after themain vasculature has developed and establishedinterconnections. Undifferentiated tissue at isolatedregions next to the abaxial convex surface of thechannel-shaped leaf vasculature gets differentiatedinto vascular tissue resulting in a {Ow of slendercylindrical vascular strands which extend parallel tothe main vasculature of the leaf base. These getconnected with the margin of vasculature of the nextposterior leaf on the same side (Text-figure 16B).Similar secondary differentiation of vascular tissueoccurs associated with root vasculatures also,interconnecting the basal regions of successive rootson the same side (Text-figure 16D). Occasionalvascular bridges interconnect nearby vascularstrands associated both with the leaves and roots,and thus a loose cylindrical reticulum is formed; thisconstitutes the outer cylinder of the polycyclic stelarcylinder (Text-figure 16B, D). In juvenile plants suchsecondary development of vasculature does notoccur and the juvenile stem has a simple dicryosteleand is ewet with spirally arranged leaves as in otherferns. A plagiotropic stem and characteristic stelararchitecture follows when the shoot apex acquires

the habit of regular dichotomy, and this happenswhen the juvenile plant has produced more than 20leaves.

Leaf vasculature is undissected at origin in allthe taxa studied, and gets differentiated next to theleaf apical dome before the leaf axis increases ingirth (Text-figures 13, 14, 16). Increase in girth isabrupt and occurs by repeated division of allundifferentiated cells. This stretches the channel­shaped intact vascular strand and in responseparenchymatous lacunae are developed, dissectingthe strand into a reticulum. The extent of dissectiondepends on the level at which vasculardifferentiation takes place behind the leaf apex andthe extent of increase in the girth of the leaf axis. Insome like Microlepia (Nayar et al., 1980) theparenchyma constituting the lacunae later getssecondarily differentiated into vascular tissue, withthe result that the leaf as well as stem vasculaturebecomes undissected at maturity.

Thus, the three classical hypotheses, Axialtheory, Stelar theory and Size and Form hypothesis,which are the cornerstones for all considerations oftaxonomy, phylogeny, etc. of lower vascular plantsmay have to be rejected and replaced by thePhyllorhize Theory outlined here.

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Nayar BK 1985. In support of Phyllorhize. Cun-. Sci. 54 : 1025­1035.

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Nayar BK & Gopalakrishnan V 1990. Apical organisation and vas·cular differentiation in relation to organogenesis and stelarmorphology in Blechnum orientale. indian FernI 7 : 24·34.

Nayar BK & Kaur S 197 J Prothalli of homosporous ferns. Bol.Rev. 37 : 295·396.

Nayar BK & Molly MJ 1989 An ontogenetic interpretation ofstelar cylinder in Polypodiaceae. indian Fern j. 6:

217·237Nayar BK, Molly MJ & Jacob M 1980. Apical organisation and

vascular differentiation in Microlepia. Proc. Indian Acad.Sci (PI Sci) 89 : 381·393