Lichens: the Interface Between Mycology and Plant Morphology Author(S): WILLIAM B
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Lichens: The Interface between Mycology and Plant Morphology Author(s): WILLIAM B. SANDERS Source: BioScience, Vol. 51, No. 12 (December 2001), pp. 1025-1036 Published by: University of California Press on behalf of the American Institute of Biological Sciences Stable URL: http://www.jstor.org/stable/10.1641/0006- 3568%282001%29051%5B1025%3ALTIBMA%5D2.0.CO%3B2 . Accessed: 22/05/2013 17:34 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. University of California Press and American Institute of Biological Sciences are collaborating with JSTOR to digitize, preserve and extend access to BioScience. http://www.jstor.org This content downloaded from 143.107.247.159 on Wed, 22 May 2013 17:34:00 PM All use subject to JSTOR Terms and Conditions Articles Lichens: The Interface between Mycology and Plant Morphology WILLIAM B. SANDERS here do the lichens belong in the biological Wsciences? They are composed of fungus and alga, but WHEREAS MOST OTHER FUNGI LIVE AS AN neither mycologists nor phycologists have been eager to claim them. In most lichens, it is the fungus that builds the struc- ABSORPTIVE MYCELIUM INSIDE THEIR tural tissues of the thallus (body), as well as the characteris- FOOD SUBSTRATE, THE LICHEN FUNGI tic fungal fruiting structures. Its predominance is such that we often speak loosely of a “species of lichen,” when we mean CONSTRUCT A PLANT-LIKE BODY WITHIN more precisely a species of lichen fungus; the lichen algae, of course, have their own separate scientific names. WHICH PHOTOSYNTHETIC ALGAL SYM- The lichen-forming fungi represent nearly one-fifth of all known species of fungi (Hawksworth et al. 1995), yet they are BIONTS ARE CULTIVATED rarely 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 in Lichens must first be appreciated in the context of other botany secure. Although lichens, as photosynthetic living fungi. As absorber heterotrophs, the primeval fungi evolved things, fit within the broad biological concept of “plant,”this a simple and enormously successful growth form: the term has been increasingly co-opted for use in a narrower, phy- mycelium. This loosely organized network of branching, fil- logenetic context that excludes all but green algae and their amentous cells (hyphae) is ideally suited to an organism that embryophyte (“land plant”) descendants. The lichens do re- lives inside its food source. The hypha’s exclusively linear ceive brief consideration as a classic example of symbiosis. But growth generates a vast absorptive surface area with very in treating them solely as a community-level ecological phe- modest increases in cell volume. nomenon, we overlook their organismal-level features and Only at the reproductive phase, when spores must be pro- their significance in mycology and botany. duced in quantity and borne away to fresh substrate, do cer- For the fungi, symbiosis with microalgae represents an tain fungi organize tissues and build complex structures that important nutritional innovation, one that evolved inde- emerge from the substrate, such as mushrooms. Such fruit- pendently in a number of different lineages (Wainio 1890, ing structures have diversified tremendously, as reproduction Gargas et al. 1995). These fungi have distinguished themselves and means of dispersal became specialized for exploitation of by a notable accomplishment: their transformation into very different food sources under diverse ecological conditions. “plants.” This metamorphosis is particularly visible in the But it is almost entirely within these reproductive phases more conspicuous macrolichens, in which fungus and alga are generally well-integrated in an often strikingly plant-like, su- perorganismal thallus (Figure 1). Although the structural William B. Sanders ([email protected]) is a research as- tissues are usually fungal, thallus form and function are emer- sociate at the University Herbarium, University of California, Berke- gent properties that have no real parallels among nonlichen ley, CA 94720-2465. He has combined his training in mycology and fungi. These properties the lichen thallus shares instead with in developmental plant morphology to focus on studies of lichen struc- plants. Thus, the lichens are not only of great significance in ture and development. He has lived and carried out research in Cal- the evolution of fungi; they can also offer important insights ifornia, Spain, and Brazil. © 2001 American Institute of Biological into fundamental principles of plant morphology. Sciences. December 2001 / Vol. 51 No. 12 • BioScience 1025 This content downloaded from 143.107.247.159 on Wed, 22 May 2013 17:34:00 PM All use subject to JSTOR Terms and Conditions Articles Figure 2. Lobe of a foliose lichen in longitudinal section. The algal symbiont (Scytonema sp.) is confined to a discrete layer surrounded by tissues of the lichen fungus Figure 1. Leafy (foliose) and shrubby (fruticose) lichens Coccocarpia palmicola (Spreng.) L.Arvidss. and D.Gall. of the genera Parmotrema, Ramalina, Teloschistes, and Scale bar = 20 µm. Heterodermia colonizing a tree branch behind dunes on Santa Catarina Island, Brazil. autonomous lichen colonizes inorganic or indigestible sub- that morphological evolution of nonlichen fungi has oc- strates and often occurs in extreme microhabitats with little curred (Poelt 1986). The vegetative mycelium, by contrast, has to offer the hunter–gatherer of ephemeral food resources. been very highly conserved throughout hundreds of mil- Agriculture has profound effects on the crop as well as on lions of years of evolution. It characterizes most of the sapro- the cultivator. Many of our most important crop plants trophic, parasitic, and mycorrhizal Eumycota (true fungi). The have been genetically selected for so long that they no longer mycelium also evolved independently in phylogenetically resemble any “natural” species, nor could they survive as distinct organisms traditionally treated as fungi, such as the such. Maize (corn), for example, is a crop whose exact ori- oomycetes. These are impressive indications of the mycelium’s gin is controversial, and one that cannot effectively perpet- ideal suitability to the “endotrophic” absorber lifestyle. uate itself outside human cultivation (Mangelsdorf 1974). But when a fungus establishes a symbiosis with a mi- Some lichen algae may be in a comparable situation. Species croalga, the usual spatial relationship of fungus to food source of the unicellular green alga Trebouxia (Figure 3) are the most is turned inside out. Surrounding the diminutive photosyn- common algal symbionts in lichens of temperate and boreal thetic cells, the fungus now finds itself on the outside (Figure climates. Yet Trebouxia’s immediate affinities among non- 2). To maintain and display the incorporated algae effec- lichen algae are unclear, and the genus has been only spo- tively, the fungus must build a protective, functional green- radically reported to occur outside lichen thalli (Tscher- house, usually emergent from the substratum. The hyphal mak-Woess 1978, Bubrick et al. 1984). It has been asserted building block is metamorphosed to produce a variety of that reportedly free-living Trebouxia cells represent transient tissue types, and a complex thallus replaces the mycelium. populations liberated from damaged or degenerated thalli or thallus fragments (Ahmadjian 1988). Such liberated al- Farmers of the fungal kingdom gal cells might then be likened to volunteer plants that es- Symbiosis with microalgae engenders a whole new fungal cape from cultivation. Whatever their origin or degree of sta- lifestyle: It represents nothing less than the advent of agri- bility, free-living Trebouxia populations can play an culture (see also Goward et al. 1994, p. 10). While their non- important role in lichen establishment. They can offer po- symbiotic brethren continue as hunter–gatherers of tran- tential symbionts available to compatible lichen fungi ger- sient carbon sources, the lichen fungi have become indoor minating from spores in the vicinity (Beck et al. 1998). gardeners, cultivating and perpetuating their internalized But not all lichen algae have been so thoroughly domesti- source of food. This agrarian control over food resources cated by the lichen fungus. Examples include algae of the confers both stability and the potential to occupy entirely new closely related genera Trentepohlia, Phycopeltis, and Cephaleu- ecological niches. In human development, agriculture per- ros, which are very important lichen symbionts in tropical and mitted the rise of populous, sedentary, highly complex civi- warm-temperate regions. These algae commonly occur free- lizations by providing a resource base far larger and more re- living as well as lichenized, not infrequently within the same liable than that available from the unmanipulated habitat. On a single leaf (an important substratum for trop- environment (Schwanitz 1966, Heiser 1990). For the fungi,“al- ical lichens), one can sometimes find Cephaleuros