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MYCOTAXON Volume 97, Pp MYCOTAXON Volume 97, pp. 91–109 July–September 2006 Thallus development and the systematics of Chytridiomycota: an additional developmental pattern represented by Podochytrium Will H. Blackwell, Peter M. Letcher & Martha J. Powell* *[email protected] Department of Biological Sciences, The University of Alabama Tuscaloosa, AL 35487 USA Abstract—Use of thallus developmental patterns in the systematics of chytridiomycetous fungi has been controversial, especially regarding the taxonomic rank or level at which use is appropriate. This review analyzes and interprets developmental thallus morphology among a spectrum of Chytridiomycota. Investigation of this topic revealed an additional mode of development, represented by the genus Podochytrium, distinct from developmental patterns previously recognized. Some genera that may seem morphologically comparable based on the mature thallus may in fact attain this morphology by different patterns of development. Although thallus development is of questionable macrosystematic and phylogenetic utility among chytrids because of convergence, patterns of thallus development can nonetheless be helpful in distinguishing one chytrid genus from another. Key words—apophysis, bipolar growth, prosporangium, sporangium, zoospore cyst Introduction and historical overview Traditionally, two main, somewhat opposing viewpoints have expressed the optimal means of delimiting major systematic groupings (orders, families, subfamilies) of Chytridiomycetes (especially among eucarpic, monocentric taxa)—that of F. K. Sparrow and of A. J. Whiffen. Sparrow (1933a, p. 63) commented that “the operculum [of the sporangium] impresses one as a morphological structure of some significance.” Sparrow (1942, 1943) subsequently emphasized use of sporangial operculation versus inoperculation in delimiting major groupings of chytrids; a similar, if preliminary, view was presented in outline form by Gäumann & Dodge (1928). Secondarily, Sparrow (1943) emphasized habit in classification, i.e., whether the sporangium occurred extramatrically (epibiotic or interbiotic sporangia) or intramatrically (endobiotic sporangia). By comparison, Whiffen (1944) emphasized differences in thallus development for broad systematic purposes in chytrids. Of primary 92 importance in Whiffen’s system is whether the sporangium develops directly from the zoospore cyst or from a portion of the germ tube of the zoospore cyst, a distinction Petersen (1910) briefly noted. Whiffen (1944) did not consider the presence or absence of operculation significant in chytrid macrosytematics; Haskins & Weston (1950) likewise questioned the taxonomic value of operculation. Both Sparrow and Whiffen gave credence, though not identical importance in the general classification of chytrids, to whether the thallus was monocentric or polycentric. In any case, the classifications by Sparrow and Whiffen are not substantially congruent. Sparrow (1943, 1960) recognized three families of eucarpic, monocentric chytrids in Chytridiales and two families (three if including the variable Physodermataceae) of polycentric members of this order. Whiffen (1944) recognized just two families of eucarpic, monocentric chytrids in Chytridiales and only one polycentric family. Karling’s (1932) early emphasis on holocarpic versus eucarpic thalli found some consistency of application at the family level, e.g., the Olpidiaceae (Sparrow 1960). Roane & Paterson (1974) supported Whiffen’s (1944) viewpoint on the importance of thallus development, expanding on Whiffen’s system. Barr (1978) likewise felt that thallus development was more significant than operculation in the systematic delimitation of major groupings of chytrids. However, Barr (1978) placed primary emphasis on whether the nucleus of the zoospore cyst remains within the cyst or migrates into the zoospore germ tube during thallus development. Longcore (2002) pointed out, as demonstrated by Powell & Koch (1977), that migration of the cyst nucleus into the germ tube allows a chytrid to establish zoosporangia endobiotically or intramatrically (i.e., within the substrate); such a migration is thus a feature of biological significance. Barr (1978) in fact viewed such endobiotic chytrids, generally, as derived compared with epibiotic chytrids. Both Barr (1990) and Longcore (2002) used the terms “endogenous” (meaning, zoospore nucleus remaining in the cyst) and “exogenous” (meaning, zoospore nucleus migrating out of the cyst, into the germ tube) in this new context. A problem with this terminology is the possible confusion with older usage of the same terms for general thallus development (Karling 1936, 1977; Sparrow 1943, 1960; Hanson 1946). In traditional usage “exogenous” is equivalent to “extramatrical” (epibiotic or interbiotic) sporangial position, and “endogenous” is equivalent to “intramatrical” (endobiotic) sporangial position. In the common genus Rhizophydium, for example, one encounters the apparent contradiction that thallus development is “exogenous,” when speaking of sporangial position, but “endogenous” when speaking of the zoospore cyst nucleus (i.e., that the nucleus is retained within the cyst). Determining whether the zoospore cyst nucleus migrates or not (Powell & Koch 1977, Barr 1978, 1990; Longcore 2002) is crucial to understanding 93 differences in thallus development. To solve the semantic problem, concerning movement of the cyst nucleus, it is simpler to speak of “non-migratory” in place of “endogenous” (i.e., nucleus retained in the cyst), and “migratory” in place of “exogenous” (i.e., nucleus moves out of the cyst). In the latter case, nuclear migration is usually from the zoospore cyst into the germ tube, as would be understood from Barr and Longcore. However, a different migration of the cyst nucleus may occur. If the zoospore cyst functions as, or develops into, a prosporangium, migration of the nucleus may be into the sporangium from the prosporangium, as in Polyphagus. “Prosporangial migration” is important in Podochytrium development, as will be seen under our discussion of that developmental type. Thus, replacement terminology (“migratory” and “non- migratory”), regarding the destination of the zoospore cyst nucleus, allows retention of “exogenous” and “endogenous” in original context—i.e., location of sporangial thallus, apophysis, resting spore, etc., relative to the substrate— important, particularly, in describing the unusual progression of development in Chytridium lagenaria. One may extrapolate from Barr (1980) that both traditional points of view (Sparrow 1943, emphasizing operculation; and Whiffen 1944, emphasizing thallus development) have had relevance, and some consistency of application, in delimiting major groupings of chytrids. As Barr suggested, however, these traditional approaches have not provided entirely satisfactory or even mutually compatible, systematic answers. Accordingly, Barr (1980, 1990, 2001) increasingly emphasized zoospore type and fine structure for improved systematic understanding of Chytridiomycota (Longcore 2002, Letcher & Powell 2005). Barr’s (1980) delineation of chytrid groupings, based fundamentally on zoospore ultrastructure, derived a classification in which a new order of Chytridiomycota—the Spizellomycetales—was recognized. Blackwell et al. (2004) discussed differing points of view on chytrid systematics, concluding that, whereas ultrastructural features of the zoospore are essential as a primary suite of characters in chytrid systematics, arguments can still be made for taxonomic use of both operculation and thallus development. However as Blackwell et al. (2004) indicated, both classical and modern features employed in chytrid systematics are best used in consort, not competitively. A collaborative approach, though, implies detailed assessment of the taxonomic level or levels at which different kinds of taxonomic characters, or suites of characters, are most meaningfully brought to bear. The applicability of traditional features of thallus morphology and thallus development among chytrids now appears to be significant mainly at lower levels of classification (genus, species), and not primarily in deciphering higher ranks or categories (orders, families); this viewpoint is also supported in recent molecular systematic studies (Letcher et al. 2005) and is explained in our Discussion. 94 Although variation and taxonomic significance of operculation should be thoroughly reinvestigated, the focus of our present paper is thallus development. We pursue this focus because the additional developmental type we recognize is represented in Podochytrium, a genus containing only inoperculate species. Thus, herein we consider primarily how insights from examination of thallus development (sensu Whiffen 1944, Roane & Paterson 1974, Barr 1978) may refine the concept of Podochytrium and similar genera of Chytridiomycota. This evaluation is best accomplished in the context of a review of known chytrid thallus types to strengthen understanding of thallus development. It will be important to see how improved knowledge of thallus development will interface with the emerging resolution that molecular analyses bring to chytrid phylogeny (James et al. 2000, Letcher & Powell 2005, Letcher et al. 2004, 2005), particularly as these analyses become refined at the generic and specific levels. Thallus developmental types in Chytridiomycota In ascribing systematic significance in Chytridiomycetes to thallus development, Whiffen (1944) outlined five basic types of development among monocentric, eucarpic members of the
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