author(s): william b. sanders on behalf of the american ... · author(s): william b. sanders...

Lichens The Interface between Mycology and Plant MorphologyAuthor(s) WILLIAM B SANDERSSource BioScience Vol 51 No 12 (December 2001) pp 1025-1036Published by University of California Press on behalf of the American Institute of Biological SciencesStable URL httpwwwjstororgstable1016410006-3568282001290515B10253ALTIBMA5D20CO3B2

Accessed 22052013 1734

Your use of the JSTOR archive indicates your acceptance of the Terms amp Conditions of Use available at httpwwwjstororgpageinfoaboutpoliciestermsjsp

JSTOR is a not-for-profit service that helps scholars researchers and students discover use and build upon a wide range ofcontent in a trusted digital archive We use information technology and tools to increase productivity and facilitate new formsof scholarship For more information about JSTOR please contact supportjstororg

University of California Press and American Institute of Biological Sciences are collaborating with JSTOR todigitize preserve and extend access to BioScience

httpwwwjstororg

This content downloaded from 143107247159 on Wed 22 May 2013 173400 PMAll use subject to JSTOR Terms and Conditions

December 2001 Vol 51 No 12 bull BioScience 1025

Articles

Where do the lichens belong in the biological sciences They are composed of fungus and alga but

neither mycologists nor phycologists have been eager to claimthem In most lichens it is the fungus that builds the struc-tural tissues of the thallus (body) as well as the characteris-tic fungal fruiting structures Its predominance is such that weoften speak loosely of a ldquospecies of lichenrdquo when we meanmore precisely a species of lichen fungus the lichen algae ofcourse have their own separate scientific names

The lichen-forming fungi represent nearly one-fifth of allknown species of fungi (Hawksworth et al 1995) yet they arerarely given adequate attention in mycology It seems their be-havior is too different from that of other fungi for many my-cologists to feel comfortable with them Nor is their place inbotany secure Although lichens as photosynthetic livingthings fit within the broad biological concept of ldquoplantrdquo thisterm has been increasingly co-opted for use in a narrower phy-logenetic context that excludes all but green algae and theirembryophyte (ldquoland plantrdquo) descendants The lichens do re-ceive brief consideration as a classic example of symbiosis Butin treating them solely as a community-level ecological phe-nomenon we overlook their organismal-level features andtheir significance in mycology and botany

For the fungi symbiosis with microalgae represents animportant nutritional innovation one that evolved inde-pendently in a number of different lineages (Wainio 1890Gargas et al 1995) These fungi have distinguished themselvesby a notable accomplishment their transformation intoldquoplantsrdquo This metamorphosis is particularly visible in themore conspicuous macrolichens in which fungus and alga aregenerally well-integrated in an often strikingly plant-like su-perorganismal thallus (Figure 1) Although the structuraltissues are usually fungal thallus form and function are emer-gent properties that have no real parallels among nonlichenfungi These properties the lichen thallus shares instead withplants Thus the lichens are not only of great significance inthe evolution of fungi they can also offer important insightsinto fundamental principles of plant morphology

Lichens must first be appreciated in the context of otherfungi As absorber heterotrophs the primeval fungi evolveda simple and enormously successful growth form themycelium This loosely organized network of branching fil-amentous cells (hyphae) is ideally suited to an organism thatlives inside its food source The hypharsquos exclusively lineargrowth generates a vast absorptive surface area with verymodest increases in cell volume

Only at the reproductive phase when spores must be pro-duced in quantity and borne away to fresh substrate do cer-tain fungi organize tissues and build complex structures thatemerge from the substrate such as mushrooms Such fruit-ing structures have diversified tremendously as reproductionand means of dispersal became specialized for exploitation ofvery different food sources under diverse ecological conditionsBut it is almost entirely within these reproductive phases

William B Sanders (wsandersssclberkeleyedu) is a research as-

sociate at the University Herbarium University of California Berke-

ley CA 94720-2465 He has combined his training in mycology and

in developmental plant morphology to focus on studies of lichen struc-

ture and development He has lived and carried out research in Cal-

ifornia Spain and Brazil copy 2001 American Institute of Biological

Sciences

Lichens The Interfacebetween Mycology and Plant Morphology

WILLIAM B SANDERS

WHEREAS MOST OTHER FUNGI LIVE AS AN

ABSORPTIVE MYCELIUM INSIDE THEIR

FOOD SUBSTRATE THE LICHEN FUNGI

CONSTRUCT A PLANT-LIKE BODY WITHIN

WHICH PHOTOSYNTHETIC ALGAL SYM-

BIONTS ARE CULTIVATED


1026 BioScience bull December 2001 Vol 51 No 12

Articles

that morphological evolution of nonlichen fungi has oc-curred (Poelt 1986) The vegetative mycelium by contrast hasbeen very highly conserved throughout hundreds of mil-lions of years of evolution It characterizes most of the sapro-trophic parasitic and mycorrhizal Eumycota (true fungi) Themycelium also evolved independently in phylogeneticallydistinct organisms traditionally treated as fungi such as theoomycetes These are impressive indications of the myceliumrsquosideal suitability to the ldquoendotrophicrdquo absorber lifestyle

But when a fungus establishes a symbiosis with a mi-croalga the usual spatial relationship of fungus to food sourceis turned inside out Surrounding the diminutive photosyn-thetic cells the fungus now finds itself on the outside (Figure2) To maintain and display the incorporated algae effec-tively the fungus must build a protective functional green-house usually emergent from the substratum The hyphalbuilding block is metamorphosed to produce a variety oftissue types and a complex thallus replaces the mycelium

Farmers of the fungal kingdomSymbiosis with microalgae engenders a whole new fungallifestyle It represents nothing less than the advent of agri-culture (see also Goward et al 1994 p 10) While their non-symbiotic brethren continue as hunterndashgatherers of tran-sient carbon sources the lichen fungi have become indoorgardeners cultivating and perpetuating their internalizedsource of food This agrarian control over food resourcesconfers both stability and the potential to occupy entirely newecological niches In human development agriculture per-mitted the rise of populous sedentary highly complex civi-lizations by providing a resource base far larger and more re-liable than that available from the unmanipulatedenvironment (Schwanitz 1966 Heiser 1990) For the fungildquoal-gaculturerdquo has led to the development of structurally elabo-rate self-sufficient long-lived thalli The nutritionally

autonomous lichen colonizes inorganic or indigestible sub-strates and often occurs in extreme microhabitats with littleto offer the hunterndashgatherer of ephemeral food resources

Agriculture has profound effects on the crop as well as onthe cultivator Many of our most important crop plantshave been genetically selected for so long that they no longerresemble any ldquonaturalrdquo species nor could they survive assuch Maize (corn) for example is a crop whose exact ori-gin is controversial and one that cannot effectively perpet-uate itself outside human cultivation (Mangelsdorf 1974)Some lichen algae may be in a comparable situation Speciesof the unicellular green alga Trebouxia (Figure 3) are the mostcommon algal symbionts in lichens of temperate and borealclimates Yet Trebouxiarsquos immediate affinities among non-lichen algae are unclear and the genus has been only spo-radically reported to occur outside lichen thalli (Tscher-mak-Woess 1978 Bubrick et al 1984) It has been assertedthat reportedly free-living Trebouxia cells represent transientpopulations liberated from damaged or degenerated thallior thallus fragments (Ahmadjian 1988) Such liberated al-gal cells might then be likened to volunteer plants that es-cape from cultivation Whatever their origin or degree of sta-bility free-living Trebouxia populations can play animportant role in lichen establishment They can offer po-tential symbionts available to compatible lichen fungi ger-minating from spores in the vicinity (Beck et al 1998)

But not all lichen algae have been so thoroughly domesti-cated by the lichen fungus Examples include algae of theclosely related genera Trentepohlia Phycopeltis and Cephaleu-ros which are very important lichen symbionts in tropical andwarm-temperate regions These algae commonly occur free-living as well as lichenized not infrequently within the samehabitat On a single leaf (an important substratum for trop-ical lichens) one can sometimes find Cephaleuros both free-living and in various stages of incorporation into a thallus ofthe lichen genus Strigula (Figure 4)

Figure 1 Leafy (foliose) and shrubby (fruticose) lichensof the genera Parmotrema Ramalina Teloschistes andHeterodermia colonizing a tree branch behind dunes onSanta Catarina Island Brazil

Figure 2 Lobe of a foliose lichen in longitudinal sectionThe algal symbiont (Scytonema sp) is confined to adiscrete layer surrounded by tissues of the lichen fungusCoccocarpia palmicola (Spreng) LArvidss and DGallScale bar = 20 microm


When lichenized Cephaleuros grows much more slowly andmay not form reproductive structures Indeed lichenizationcan reduce or eliminate the pathogenic effects of this algarsquos vig-orous growth on cultivated plants (Joubert and Rijkenberg1971) Thus lichenization can have different ecological im-plications for different algal symbionts For some algae likeTrebouxia the symbiosis can be essentially obligatory forsurvival in many habitats For others such as Cephaleuros lich-enization might be a nuisance at least under conditions in

which the alga could otherwise survive and reproduce with-out supporting a fungus

These ecological considerations beyond the nutritional in-teraction of the symbionts can determine whether onechooses to view the lichen symbiosis as mutualistic (Honeg-ger 2001) or parasitic (Ahmadjian 1993) For a highly coevolved and dependent lichen alga such as Trebouxia rec-ognizing advantage or disadvantage in the symbiosis mightbe as difficult as attempting to judge whether maize has


Articles

Figure 3 Thallus tissue of Neuropogon sp showing dividing cells of the green algal symbiont Trebouxia Scale bar = 20 microm

Figure 4 Surface of leaf with epiphyllic alga Cephaleuros both free-living (C) with erect trichomes and sporangiophoresand incorporated into smooth white and yellow thalli of the lichen fungus Strigula smaragdula Fr (S) at the margins (seealso Ward 1884) Scale bar = 1 mm

Figure 5 (a) Crustose lichen Cryptothecia rubrocincta (Ehrenberg) Thor on tree branch and (b) crustose red alga onintertidal reef

Figure 6 (a) Foliose thallus of the lichen Flavoparmelia caperata (L) Hale growing on a cactus stem at the University ofCalifornia Berkeley Botanical Garden and (b) thallose bryophyte Anthoceros (hornwort) on soil bank at Puerto BlestArgentina

Figure 7 (a) Pendulous fruticose thallus of the lichen Usnea repens Motyka (an epiphytic form) at Ibitipoca Minas GeraisBrazil (b) Unidentified moss on branches at Puerto Blest


ldquobenefitedrdquo from its agricultural association with humansHowever there is little justification for viewing lichenizationas disadvantageous to Trebouxia (cf Ahmadjian 1993 pp3ndash4) if one maintains that this alga cannot really exist free-living (Ahmadjian 1988)

Lichens as ldquoplantsrdquoThe fungus must provide its algal symbiont with an envi-ronment that makes effective use of physiologically favorableconditions It must display the photosynthetic cells advanta-geously to the light while filtering excessive or harmful radi-ation It must facilitate adequate hydration while permittingcarbon dioxide to diffuse into the thallus during photosyn-thetically active periods In short the lichen faces the same ba-sic functional challenges as do terrestrial plants

The structural solutions in turn are remarkably similar(Jahns and Ott 1997) Many lichens produce a simple crus-tose thallus intimately attached to the substratum as do cer-tain species of red and brown marine algae (Figure 5) Oth-ers have foliose dorsiventral forms with a discrete lowersurface attached to the substratum at specific points remi-

niscent of a plant leaf or a thallosebryophyte (Figure 6) Still othersform fruticose thalli with erect orpendent branching axes usuallywith radial or bilateral symmetry(Figure 7) Some of these fruticoselichens can even show differentia-tion into stem-like supportive axesof structural tissue bearing leaf-likeassimilative squamules that containthe algal cells (Figure 8) Erect fru-ticose lichens with highly branchedaxes can resemble miniature shrubs(Figure 9)A few species are actuallymarketed commercially to repre-sent trees in model railroads andarchitectural scale models (Figure10) The numerous convergencessuggest that these growth forms areuniversally practical designs for dis-playing photosynthetic surfaces us-ing cell wallsmdashof any originmdashasstructural building material

An examination of the thallusanatomy of macrolichens often re-veals further plant-like features Atransverse section through the thal-lus of a typical foliose lichen showsa tissue organization analogous inmany respects to that of a leaf (Fig-ure 11) The algal cells are usuallyarranged in a discrete layer just be-low the upper cortex of fungal tissuelike a densely packed chloroplast-rich palisade parenchyma tissue Ef-

ficient gas exchange in this photosynthetically active stra-tum is facilitated by the air spaces in the loosely organizedmedullary region below as occurs in the spongy mesophyllof the plant leaf A thin coating of hydrophobic protein andinsoluble secondary substances over the medullary hyphae andassociated algal cells can serve to maintain these spaces freeof water as well as to seal a conduit between fungus and alga(Honegger 1997)

Like an epidermis the upper cortex of the lichen protectsthe photosynthetic cells below slowing evaporation and fil-tering harmful or excessive radiation with the assistance of pig-ments and secondary substances (Rikkinen 1995) Unlikethe cutinized plant epidermis however the lichen cortex pre-sents no impermeable barrier to water diffusion On the con-trary the corticated thallus surfaces must serve in absorptionof water as well as light as do the leaves of mosses and at-mospheric vascular epiphytes (Figure 12)

In certain lichens occurring in habitats that receive high lev-els of light the lichen cortex can form a thick optical filterthrough which light diffuses downward and laterally to ver-tically arranged tiers of photosynthetic cells (Figure 13) as in


Articles

Figure 8 Fruticose thallus of Cladonia sphacelata Vain with stem- and leaf-likecomponents The brownish vertical axes consist entirely of fungal tissue the algal cellsare localized within the greenish lobed squamules borne along the axes Scaleapproximately twice actual size

Figure 9 Shrub-like thallus of fruticose lichen Cladonia subreticulata Ahti shownabout actual size

Figure 10 Dyed lichens (Cladina sp) representing trees in a scale model Thecommercially packaged lichen was purchased in the hobby section of a hardware storein Berkeley California Scale is about one-quarter actual size (Model designed andconstructed by architecture students Elano Collaccedilo Patriacutecia Izabel and WallaceAmorim Jr at Universidade Federal de Pernambuco Recife Brazil)


the so-called window leaves of South African succulent plantssuch as Lithops (Vogel 1955 Malcolm 1995) This systempermits the display of considerable photosynthetic tissue tothe light while greatly reducing the external surfaces exposedto evaporative water loss When the lichen cortex is satu-rated with water diffusion of carbon dioxide through the thal-lus to the algal layer is impeded (Lange and Tenhunen 1981)Thus most of the larger lichens have some type of cortical per-foration such as cyphellae pseudocyphellae (Figure 11) orepicortical micropores (Hale 1981)

These pores most likely facilitate gas exchange (Green et al1981) as do plant stomata but unlike the stomata they can-not be actively regulated by closure to conserve water Norwould their closure effectively conserve water because evap-oration occurs over the entire thallus surface The lichenthallus is poikilohydric It survives drought by physiologicaltolerance of desiccation rather than by maintaining thallus hy-dration For many lichens that colonize exposed sites rapidwater loss under full sunlight limits daily photosynthetic ac-tivity to brief periods (such as early mornings) in the dessi-cated state the lichen can survive extreme conditions over longperiods of time (Lange et al 1975)

The typical foliose lichen thallus is attached to the substrateby rhizines which are short hyphal bundles of determinate(limited) growth that emerge from the lower surface How-ever some lichens produce more elaborate branching fungalstructures of indeterminate growth that penetrate the substrateextensively These structures known as rhizomorphs can re-semble the roots of conventional plants (Figure 14) They donot contain algae Lichen rhizomorphs can penetrate both cal-careous and siliceous rock substrates (Figure 15) as well as soilapparently by both mechanical and chemical means (Sanderset al 1994) Their development is often much more extensivethan would be expected of a structure that merely fixes thethallus to the substrate

Rhizomorphic excavation may increase the substratersquos ca-pacity to store capillary water available to the thallus How-ever the rhizomorphs themselves do not show distinctivespecializations for transport (Sanders and Ascaso 1997) suchas the vessel hyphae observed in rhizomorphs of certain non-lichen fungi (Duddridge et al 1980) Where rhizomorphsoccur superficially thallus squamules can arise secondarily

from them (Figure 14) This situ-ation occurs when rhizomorphichyphae capture compatible algaeencountered in the substratuminitiating development of the lich-enized thallus component (Figure16) Thus the lichen rhizomorphscan have a colonizing functioncomparable to that of rhizomesand shoot-bearing roots of manyconventional plants (Sanders1994) By producing a rhizomor-phic system the lichen can main-tain its presence within the sub-stratum even as erosion continuesto expose new surfaces for pioneer

colonization by competitors

Role of apices andmarginsThe structural convergences withplants show further parallels whenthe patterns of lichen growth anddevelopment are considered Lichen


Articles

Figure 11 Transverse section through foliose thallus ofthe lichen Pseudocyphellaria aurata (Ach) Vainio Uupper cortex A algal layer M medulla L lower cortexP pore (pseudocyphella) in lower cortex facilitating gasexchange The medulla shows extensive deposits ofbrownish secondary substances Scale bar = 250 microm

Figure 12 Tree branch colonized by a fruticose lichen (Ramalina sp) at left and

atmospheric bromeliad (Tillandsia sp) at right near Caruaru in Pernambuco Brazil

In both epiphytes the photosynthetic surfaces are also used for absorption of water

Figure 13 Transverse section through thallus of lichen Psorinia conglomerata (Ach)

G Schneider with an undulating layer of green algal cells arranged below a deep

translucent optical filter of fungal cortical tissue (C) Scale bar = 50 microm


thallus growth is polar occurring at localized usually pe-ripheral zones of growth As in conventional plants growthis potentially indeterminate and development open Open de-velopment allows the continued production of new lobesbranches or other units of construction in a modular fash-ion (Figure 17) Generation of form (morphogenesis) and ini-tiation of certain thallus structures (organogenesis) are oftenlocalized at apices or margins that function analogously to theapical meristems of plants Examples include the initiation ofapical branching (Figure 18) the formation of appendagessuch as apical cilia (Figure 19) and the generation of theperforated tissue that gives rise to the reticulate thallus of Ra-malina menziesii the lace lichen (Figure 20)

At the anatomical level cell differentiation and organiza-tion into thallus layers frequently occur in a gradation rem-iniscent of histogenesis at plant apices At the thallus apex ormargin fungal and algal cells are interspersed in an undif-ferentiated mixture (Figure 21a) With distance from the tipthe two symbionts become stratified into distinct thallus lay-ers the rate of algal cell division declines (Greenhalgh and An-glesea 1979) and the fungal cells of the cortex acquire theirfinal shape and typically thickened walls Differentiation of the

cortex can proceed more rapidly on one surface rela-tive to the other producing an inrolling of the apexcomparable to that of the fern leaf crozier (Figure 21)

Diffuse growth processesEven when morphogenetic and histogenetic eventsare clearly localized at apices and margins overall thal-lus growth may not necessarily be limited to thesezones Diffuse or nonapical growth of the thallus canalso occur and might be common in fruticose lichensin which attachment to the substratum is limited to thebase leaving the rest of the thallus free Diffuse growthis sometimes referred to as intercalary growth al-though the latter term is more correctly applied togrowth zones that occur intercalated between regionswhere growth has ceased (Fritsch 1935 Esau 1965) Thereticulate thallus of the lace lichen provides the mostdramatic example of diffuse growthAlthough new per-forate tissue and apical branches are formed exclu-sively at the apical margin of the thallus nets (Figure20) considerable tissue expansion occurs diffuselythroughout the reticulum (Sanders 1989 1992) Someumbilicate lichens (ie foliose lichens attached to rockby a single central ldquoumbilicusrdquo) also appear to show dif-fuse growth (Hestmark 1997) Diffuse growth proba-bly occurs in other species as well (Honegger 1993) butat present lichen growth patterns remain largely un-studied

The presence of diffuse growth in at least somelichens raises fundamental questions about the mech-anisms of thallus growth at the cellular level Can thesegrowth processes be compared with those exhibited bynonlichen fungi or even those of conventional plantsBecause thallus structural tissue is fungal in most

lichens it might be expected that the component fungal cellsare behaving essentially as hyphae However growth of the veg-etative fungal hypha occurs exclusively at the tip In this zonethe wall exhibits plasticity and new cell wall components areadded to the existing structure during growth (Wessels 1986)

Exclusively apical growth of component fungal cells can-not account for diffuse growth of the lichen thallus The me-chanical tissue of R menziesii for example is constructedof elongate fungal cells forming an anastomosing networkembedded in thick deposits of cell wall material (Figure22) With extensive diffuse growth of the thallus these fun-gal cells must somehow maintain plasticity along theirlength Such diffuse plasticity is indeed known in certain spe-cialized cells of nonlichen fungi such as those of the mush-room stipe (Craig and Gull 1977 Mol and Wessels 1990) orzygomycete sporangiophore (Burnett 1979) The specializedhyphae of these nonlichen fungi have been shown experi-mentally to incorporate structural components into a cellwall extending along its entire length allowing the wall tomaintain its integrity while elongating diffusely Unfortu-nately similar experiments cannot be readily performedwith lichen thalli


Articles

Figure 14 Toninia sp a soil-inhabiting lichen with a thallus

composed of inflated squamules (S) interlinked by root-like

rhizomorphs within the substrate Young squamules (arrows) are

forming on the rhizomorphs Scale bar asymp 1 mm

Figure 15 Rhizomorphic hyphae of Acarospora scotica Hue (arrow)

within siliceous rock substrate a fragment of the substrate (F) is

being incorporated into the rhizomorph The embedded polished

and stained surface of the cleaved substrate is imaged with SEM in

backscattered electron mode (Sanders et al 1994) Scale bar = 8 microm

Figure 16 Young squamule forming on rhizomorphs of Aspicilia

crespiana Rico from capture of compatible algal cells contacted

within the substrate Scale bar = 50 microm


Nonetheless ultrastructural examination of thallus tissuein R menziesii suggests that the cells behave very differentlyfrom the diffusely growing hyphae studied in mushroomstipes or sporangiophores Unlike those hyphae a fungalcell in the structural tissue of R menziesii does not possessa precisely delimited cell wall that maintains its integritythroughout thallus expansion Instead new wall layers are

continually produced to the cell interior as older layers aredisrupted by the continued diffuse growth of the thallus(Figure 23) Remnants of the older wall layers accumulate inmassive quantities between neighboring cells forming adense intercellular matrix New branch cells grow through thiswall material and produce their own series of wall layerswithin it (Figure 23) profoundly altering the usual adja-


Articles

Figure 17 Open development by repetition of a determinate module (a) The lichen Cladonia penicillata (Vain) Ahti andMarcelli The verticillate thallus is formed of lobed chalice-shaped modules that proliferate mainly from the center (forcontrasting developmental interpretations cf Goebel 1928 pp 71ndash73 and Hammer 1996) (b) The cactus Opuntiapalmadora the plant body is formed of flattened succulent determinate stem segments that proliferate along their upperedge

Figure 18 Initiation of dichotomous branching (a) Apex of lichen Pseudephebe sp (whole-mounted in water) Scale bar =40 microm (b) Apex of Lycopodium sp a vascular plant (stained and sectioned) Scale bar = 250 microm

Figure 19 Apex of lichen Teloschiste flavicans (Swartz) Norman showing cilium (C) produced at point of dichotomy ofapical branches The inrolled branches (arrows) continue to grow and rebranch with successive production of cilia (Sanders1993) Scale bar = 50 microm

Figure 20 Development of the lichen Ramalina menziesii Tayl in the field four stages of development of the same thallusnet shown at the same scale Letter ldquoardquo identifies the same perforation in all four stages Note development of new perforatedtissue and lobations at the apical margin


cent wall boundary relationship between neighboring cells(Sanders and Ascaso 1995) Cell behavior in this type of tis-sue is neither like that of nonlichen fungi nor like that of con-ventional plants It is an example of the significant structuraland functional transformations that a fungus can undergoin forming a lichen thallus

From mycelium to integrated tissueOntogeny of the lichen thallusThe plant-like features of lichens become all the more re-markable when one considers that the ontogeny of the lichenis profoundly different from that of conventional plants Aspore produced by the lichen fungus germinates to producehyphae that will have to contact and capture a compatible alga


Articles

Figure 22 Detail of a longitudinal section through tissueof the reticulate thallus of Ramalina menziesii Within thedense cortical tissue lumina of fungal cells embedded inan intercellular matrix run lengthwise interweave andanastomose (fuse) Scale bar = 40 microm

Figure 23 Ramalina menziesii Transmission electronmicrograph of fungal tissue in transverse section Noteconcentric electron-dense and electron-transparent cellwall layers and their remnants which accumulate as anextensive matrix between cell lumina New branch cells(arrows) penetrate through the matrix of old wall layersproducing new wall layers of their own Scale bar = 5 microm

Figure 21 (a) Longitudinal section through the apex ofRamalina menziesii The dividing spheroidal algal cellsand interpenetrating fungal cells are present as anundifferentiated mixture at the apical margin the algalcells become stratified into a distinct central layer withdistance from the margin The accelerated differentia-tion and expansion of the cortex (arrows) on one surfacerelative to the other produces the inrolling of the margin(b) Leaf tip of Sadleria cyatheoides Kaulf a leptospor-angiate fern Precocious expansion of cells on the abaxialsurface of the leaf apex produces the characteristicinrolling of the tip that may serve to protect its delicategrowing tissues


(Figure 24)Alternatively the fungus and alga can be dispersedtogether in thallus fragments or in various types of special-ized vegetative propagules (Figure 25) In either case thefungus grows out hyphally and the alga unicellular or fila-mentous grows and divides initially without much apparentcoordination with the fungal hyphae The algal cells are en-circled and are gradually enveloped by the fungus which ra-diating out over the substrate can also encompass othercompatible algae as well as fuse with other protothalli form-ing from similar propagules (Figure 26 Schuster et al 1985)

The initially independent cellular growth eventually be-comes integrated giving rise to a thallus with emergent prop-erties of form and development that bear little resemblanceto those exhibited by its components previouslyA key processin this transition appears to be the secretion of abundantcell wall substances that bind the fungal cells together in a com-mon cortical matrix (Ahmadjian and Jacobs 1983 Jahns1988) Usually this material is of fungal origin (Figures 22 and23) but in the so-called gelatinous lichens whose thalli arecomposed mainly of blue-green algal cells the thick inter-cellular matrix consists of copious algal sheath material (Fig-ure 27) The formation of secondary cytoplasmic connections(anastomoses) between laterally adjacent fungal cells is alsoof fundamental importance in integrating the fungal cells intotissues (Poelt 1986) These integrative processes facilitate atransfer of growth properties from formerly independentcellular elements to the newly constructed surfaces and vol-umes of the thallus

Relationship of cells to the plant bodyThe lichen thallus is constructed of cellular elements of ini-tially independent growth that are secondarily integratedinto a coherent unified body This kind of ontogeny exem-plifies the principles that the cell theory promoted by Schlei-den (1838) and Schwann (1839) attributed to multicellularplants and animals According to this theory cells are primaryelemental organisms that build up the multicellular organismby surrendering their individuality and autonomy to form anintegrated federation (Schleiden 1838) The basis of nutritionand growth is attributed to the individual cellular elementsrather than to the organism as a whole (Schwann 1839)

Although the cell theory has been extremely influentialmost plants are actually much better described by the op-posing organismal theory (Kaplan and Hagemann 1991) Theorganismal view emphasizes that plant cellularity is a sec-ondary phenomenon arising from a compartmentalizationprocess that subdivides an organism that is integral from in-ception Growth and morphogenesis are manifestations of theorganism not its cellular compartments Autonomous cellproperties and cell specializations are features that are ac-quired only at a later stage of tissue development in plants(Kaplan 1992) By contrast the lichen fits the tenets of thecell theory quite well The thallus is unquestionably composedof distinct elemental organisms Individual fungal hyphae andalgal cells exhibit autonomy at the earliest stages of lichen ontogeny


Articles

Figure 24 Germination of a fungal spore (S) Numerous

germination hyphae are growing out radially and

associating with algae encountered on the substrate

(arrows) Scale bar = 50 microm

Figure 25 Germination of soredia lichenized propagules

containing both fungal and algal symbionts The fungal

hyphae grow out over the substrate surface and the algal

cells divide Scale bar = 20 microm

Figure 26 Contact and merging of neighboring lichen

protothalli during early ontogeny Scale bar = 50 microm


Thus lichens and conventional plants differ profoundlyin their ontogenetic relationship of cell to body (Figure 28)Yet their morphological convergences are so striking thatone cannot help but conclude that the form of the plantbody really has no necessary relationship to the manner inwhich it is composed ofmdashor subdivided intomdashcells Ratherit appears that cell shape and patterns of cell division aredetermined by mechanical and biophysical constraintsthat have little relationship to the overall form of the veg-etative structure (Cooke and Lu 1992) The lichen thallusprovides convincing evidence that plant form is a propertythat resides not in cells but rather in body surfaces and vol-umes regardless of whether these surfaces and volumes arepresent from inception or secondarily assembled in thecourse of development The lichen thallus extends theprovince of plant morphology from the organismal to thesuperorganismal level

Just as the phylogeny of lichen fungi cannot be under-stood without mycology their form and function cannot beappreciated without botany They have the genes of a fun-gus but they have adopted the lifestyle of a plant Of coursewith phylogenetic reconstruction being the overwhelm-ing concern of so many organismal biologists nowadayssome may find it unacceptable to refer to lichens as ldquoplantsrdquo(Honegger 1993) in the broad nonphylogenetic sense ofthis ancient word But it is not merely out of respect for

tradition that contemporary botany texts still treat a hopelesslypolyphyletic array of ldquoplantsrdquo including the seaweeds andthe lichens There is good biological justificationmdashstructural functional and ecologicalmdashfor considering allthese organisms together Highlighting these convergencesneed not and should not mean neglect of phylogenetically rel-evant characteristics and their central significance in biosys-tematics The two perspectives are fully complementary andare equally necessary for a complete understanding of thecourses that evolutions follow in generating biodiversity

AcknowledgmentsI thank the Federal University of Pernambuco Recife forthe opportunity to serve as visiting professor at that institu-tion from October 1998 to October 2000 during which timethis article was written and presented in various forms I amindebted to Dr Isabelle I Tavares for her counsel and gen-erosity The manuscript benefited from critical reading by Isabelle I Tavares Donald R Kaplan Richard L MoeWilliamStein and two anonymous reviewers Facilities at the Scien-tific Visualization Center (University of California Berkeley)were utilized in composition of the figures T Ahti I Tavaresand E Timdall provided determinations of some of the lichenmaterial illustrated


Articles

Figure 27 Section through a lobe of a foliose gelatinouslichen The bulk of the thallus consists of filamentouschains of the blue-green alga Nostoc (vertical arrow)whose thick sheaths compose the structural matrix of thethallus Scattered hyphae (horizontal arrow) of thelichen fungus (Collema sp) penetrate through thismaterial Note the lack of organization into layers(compare with Figures 2 and 11) The gelatinous lichensare exceptional in that the algal symbiont is thepredominant structural component of the thallusDespite these fundamental differences in anatomicalconstruction the gelatinous lichens do not markedlydiffer morphologically from many lichens with astratified fungus-dominated construction Scale bar =60 microm

Figure 28 Relationship of cell to body in conventional plantsversus lichens (a) Shoot apex of the flowering plant Coleuslongitudinal section Cells arise by the continued partitioning orsubdividing of the organism during growth (see Kaplan andHagemann 1991) Scale bar = 100 microm (b) Branching isidium(thallus surface appendage) of the lichen Sticta fuliginosa(Hoffm) Ach Component cells of two different organisms fungus(vertical arrows) and alga (horizontal arrows) originate fromseparate filaments that coalesce and organize secondarily toproduce a thallus that functions as an integrated plant Scale bar = 25 microm


References citedAhmadjian V 1988 The lichen alga Trebouxia Does it occur free-living Plant

Systematics and Evolution 158 243ndash247mdashmdashmdash 1993 The Lichen Symbiosis New York John Wiley and SonsAhmadjian V Jacobs JB 1983 Algal-fungal relationships in lichens Recog-

nition synthesis and development Pages 147ndash172 in Goff LJ ed AlgalSymbiosis Cambridge (UK) Cambridge University Press

Beck A Friedl T Rambold G 1998 Selectivity of photobiont choice in a de-fined lichen community Inferences from cultural and molecular stud-ies New Phytologist 139 709ndash720

Bubrick P Galun M Frensdorff A 1984 Observations on free-living TrebouxiaDe Pumaly and Pseudotrebouxia Archibald and evidence that both sym-bionts from Xanthoria parietina can be found free-living in nature NewPhytologist 97 455ndash462

Burnett JH 1979 Aspects of the structure and growth of hyphal walls Pages1ndash25 in Burnett JH Trinci APJ eds Fungal Walls and Hyphal GrowthCambridge (UK) Cambridge University Press

Cooke TJ Lu B 1992 The independence of cell shape and overall form inmulticellular algae and land plants Cells do not act as building blocksfor constructing plant organs International Journal of Plant Science153 S7ndashS27

Craig GD Gull K 1977 Stipe elongation in Agaricus bisporus Journal of Gen-eral Microbiology 102 337ndash347

Duddridge JA Malibari A Read DJ 1980 Structure and function of myc-orrhizal rhizomorphs with special reference to their role in water trans-port Nature (London) 287 834ndash836

Esau K 1965 Plant Anatomy 2nd ed New York John Wiley and SonsFritsch FE 1935 Structure and Reproduction of the AlgaeVol 1 Cambridge

(UK) Cambridge University PressGargas A De Priest PT Grube M Tehler A 1995 Multiple origins of lichen

symbioses in fungi suggested by SSU rDNA phylogeny Science 2681492ndash1495

von Goebel K 1928 Organographie der Pflanzen I Allgemeine Organogra-phie 3rd ed Jena (Germany) Gustav Fischer

Goward T McCune B Meidinger D 1994 The Lichens of British ColumbiamdashIllustrated Keys Part 1 Foliose and Squamulose Species Victoria(Canada) Ministry of Forest Research Program

Green TGA Snelgar WP Brown DH 1981 Carbon dioxide exchange inlichens Carbon dioxide exchange throught the cyphellate lower cortexof Sticta latifrons Rich New Phytologist 88 421ndash426

Greenhalgh GN Anglesea D 1979 The distribution of algal cells in lichenthalli Lichenologist 11 283ndash292

Hale ME 1981 Pseudocyphellae and pored epicortex in the ParmeliaceaeTheir delimitation and evolutionary significance Lichenologist 13 1ndash10

Hammer S 1996 Modular growth in verticillate podetia of Cladonia My-cologia 88 533ndash538

Hawksworth DL Kirk PM Sutton BC Pegler DN 1995 Ainsworth amp BisbyrsquosDictionary of the Fungi 8th ed Oxon (UK) CAB International

Heiser CB Jr 1990 Seed to Civilization Cambridge (MA) Harvard UniversityPress

Hestmark G 1997 Growth from the centre in an umbilicate lichen Liche-nologist 29 379ndash383

Honegger R 1993 Developmental biology of lichens New Phytologist 125659ndash677

mdashmdashmdash 1997 Metabolic interactions at the mycobiont-photobiont interfacein lichens Pages 209ndash221 in Carroll GC Tudzynsky P eds The MycotaV Plant Relationships Berlin SpringerndashVerlag

mdashmdashmdash 2001 The symbiotic phenotype of lichen-forming ascomycetesPages 165ndash188 in Hock B ed The Mycota IX Fungal AssociationsBerlin SpringerndashVerlag

Jahns HM 1988 The lichen thallus Pages 95ndash143 in Galun M ed CRC Hand-book of Lichenology Vol 1 Boca Raton (FL) CRC Press

Jahns HM Ott S 1997 Life strategies in lichensmdashSome general considera-tions Bibiliotheca Lichenologica 67 49ndash67

Joubert JJ Rijkenberg FHJ 1971 Parasitic green algaeAnnual Review of Phy-topathology 9 45ndash64

Kaplan DR 1992 The relationship of cells to organisms in plants Problemand implications of an organismal perspective International Journal ofPlant Sciences 153 S28ndashS37

Kaplan DR Hagemann W 1991 The relationship of cell and organism in vas-cular plants Are cells the building blocks of plant form BioScience 41693ndash703

Lange OL Tenhunen JD 1981 Moisture content and CO2 exchange oflichens II Depression of net photosynthesis in Ramalina maciformis athigh water content is caused by increased thallus carbon dioxide diffu-sion resistance Oecologia 51 426ndash429

Lange OL Schulze E-D Kappen L Buschbom U Evenari M 1975 Adapta-tions of desert lichens to drought and extreme temperatures Pages20ndash37 in Hadley NF ed Environmental Physiology of Desert OrganismsStroudsburg (PA) Dowden Hutchinson and Ross

Malcolm WM 1995 Light transmission inside the thallus of Labyrinthaimplexa (Porpidiaceae Lichenized Ascomycetes) Bibliotheca Licheno-logica 58 275ndash280

Mangelsdorf PC 1974 Corn Its Origin Evolution and Improvement Cam-bridge (MA) Harvard University Press

Mol PC Wessels JGH 1990 Differences in wall structure between substratehyphae and hyphae of fruit-body stipes in Agaricus bisporus Mycolog-ical Research 94 472ndash479

Poelt J 1986 Morphologie der Flechten Fortschritte und Probleme Berichteder deutschen botanischen Gesellschaft 99 3ndash29

Rikkinen J 1995 Whatrsquos behind the pretty colors A study on the photobi-ology of lichens Bryobrothera 4 1ndash239

Sanders W 1989 Growth and development of the reticulate thallus in thelichen Ramalina menziesii American Journal of Botany 76 666ndash678

mdashmdashmdash 1992 Comparative in situ studies of thallus net development in mor-phologically distinct populations of the lichen Ramalina menziesii Bry-ologist 95 192ndash204

mdashmdashmdash 1993 Apical formation of cilia and associated branching of theaxis in the lichen Teloschistes flavicans International Journal of Plant Sci-ence 154 75ndash79

mdashmdashmdash 1994 Role of lichen rhizomorphs in thallus propagation and sub-strate colonization Cryptogamic Botany 4 283ndash289

Sanders WB Ascaso C 1995 Reiterative production and deformation of cellwalls in expanding thallus nets of the lichen Ramalina menziesii Amer-ican Journal of Botany 82 1358ndash1366

mdashmdashmdash 1997 Fine structural features of rhizomorphs (sensu lato) pro-duced by four species of lichen fungi Mycological Research 101 319ndash328

Sanders WB Ascaso C Wierzchos J 1994 Physical interactions of two rhi-zomorph-forming lichens with their rock substrate Botanica Acta 107432ndash439

Schleiden MJ 1838 Beitraumlge zur Phytogenesis [Muumlllers] Archiv fuumlr AnatomiePhysiologie und Wissenschaftliche Medicin (1838) 137ndash177

Schuster G Ott S Jahns HM 1985 Artificial cultures of lichens in the nat-ural environment Lichenologist 17 247ndash253

Schwanitz F 1966 The Origin of Cultivated Plants Cambridge (MA) Har-vard University Press

Schwann T 1839 Mikroskopische Untersuchungen uumlber die Uebereinstim-mung in der Struktur und dem Wachsthum der Thiere und PflanzenBerlin Verlag der Sanderrsquoschen Buchbehandlung (G E Reimer)

Tschermak-Woess E 1978 Myrmecia reticulata as a phycobiont and free-livingmdashFree-living TrebouxiamdashThe problem of Stenocybe septata Lichen-ologist 10 69ndash79

Vogel S 1955 Niedere ldquoFensterpflanzenrdquo in der suumldafrikanischer WuumlsteBeitraumlge zur Biologie der Pflanzen 31 45ndash135

Wainio EA 1890 Eacutetude sur la classification naturelle et la morphologie deslichens du BreacutesilActa Societatis pro Fauna et Flora Fennica Helsinki (Fin-land) Heacuteritiers J Simelius

Ward HM 1884 On the structure development and life history of a trop-ical epiphyllous lichen (Strigula complanata Feacutee) Transactions of the Lin-nean Society of London Botany 2 87ndash119

Wessels JGH 1986 Cell wall synthesis in apical hyphal growth InternationalReview of Cytology 104 37ndash79


Articles



Articles

Where do the lichens belong in the biological sciences They are composed of fungus and alga but

neither mycologists nor phycologists have been eager to claimthem In most lichens it is the fungus that builds the struc-tural tissues of the thallus (body) as well as the characteris-tic fungal fruiting structures Its predominance is such that weoften speak loosely of a ldquospecies of lichenrdquo when we meanmore precisely a species of lichen fungus the lichen algae ofcourse have their own separate scientific names

The lichen-forming fungi represent nearly one-fifth of allknown species of fungi (Hawksworth et al 1995) yet they arerarely given adequate attention in mycology It seems their be-havior is too different from that of other fungi for many my-cologists to feel comfortable with them Nor is their place inbotany secure Although lichens as photosynthetic livingthings fit within the broad biological concept of ldquoplantrdquo thisterm has been increasingly co-opted for use in a narrower phy-logenetic context that excludes all but green algae and theirembryophyte (ldquoland plantrdquo) descendants The lichens do re-ceive brief consideration as a classic example of symbiosis Butin treating them solely as a community-level ecological phe-nomenon we overlook their organismal-level features andtheir significance in mycology and botany

For the fungi symbiosis with microalgae represents animportant nutritional innovation one that evolved inde-pendently in a number of different lineages (Wainio 1890Gargas et al 1995) These fungi have distinguished themselvesby a notable accomplishment their transformation intoldquoplantsrdquo This metamorphosis is particularly visible in themore conspicuous macrolichens in which fungus and alga aregenerally well-integrated in an often strikingly plant-like su-perorganismal thallus (Figure 1) Although the structuraltissues are usually fungal thallus form and function are emer-gent properties that have no real parallels among nonlichenfungi These properties the lichen thallus shares instead withplants Thus the lichens are not only of great significance inthe evolution of fungi they can also offer important insightsinto fundamental principles of plant morphology

Lichens must first be appreciated in the context of otherfungi As absorber heterotrophs the primeval fungi evolveda simple and enormously successful growth form themycelium This loosely organized network of branching fil-amentous cells (hyphae) is ideally suited to an organism thatlives inside its food source The hypharsquos exclusively lineargrowth generates a vast absorptive surface area with verymodest increases in cell volume

Only at the reproductive phase when spores must be pro-duced in quantity and borne away to fresh substrate do cer-tain fungi organize tissues and build complex structures thatemerge from the substrate such as mushrooms Such fruit-ing structures have diversified tremendously as reproductionand means of dispersal became specialized for exploitation ofvery different food sources under diverse ecological conditionsBut it is almost entirely within these reproductive phases

William B Sanders (wsandersssclberkeleyedu) is a research as-

sociate at the University Herbarium University of California Berke-

ley CA 94720-2465 He has combined his training in mycology and

in developmental plant morphology to focus on studies of lichen struc-

ture and development He has lived and carried out research in Cal-

ifornia Spain and Brazil copy 2001 American Institute of Biological

Sciences

Lichens The Interfacebetween Mycology and Plant Morphology

WILLIAM B SANDERS

WHEREAS MOST OTHER FUNGI LIVE AS AN

ABSORPTIVE MYCELIUM INSIDE THEIR

FOOD SUBSTRATE THE LICHEN FUNGI

CONSTRUCT A PLANT-LIKE BODY WITHIN

WHICH PHOTOSYNTHETIC ALGAL SYM-

BIONTS ARE CULTIVATED



Articles














Articles
















Articles













Articles

















Articles

















Articles









Articles










Articles

















Articles

























































Articles



Articles














Articles
















Articles













Articles

















Articles

















Articles









Articles










Articles

















Articles

























































Articles






Articles
















Articles













Articles

















Articles

















Articles









Articles










Articles

















Articles

























































Articles











Articles













Articles

















Articles

















Articles









Articles










Articles

















Articles

























































Articles










Articles

















Articles

















Articles









Articles










Articles

















Articles

























































Articles










Articles

















Articles









Articles










Articles

















Articles

























































Articles





Articles









Articles










Articles

















Articles

























































Articles





Articles










Articles

















Articles

























































Articles







Articles

















Articles

























































Articles







Articles

























































Articles























































Articles


author(s): william b. sanders on behalf of the american ... · author(s): william b. sanders...

Documents