Monocot Xylem Revisited: New Information, New Paradigms Sherwin Carlquist
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Monocot Xylem Revisited: New Information, New Paradigms Sherwin Carlquist The Botanical Review ISSN 0006-8101 Volume 78 Number 2 Bot. Rev. (2012) 78:87-153 DOI 10.1007/s12229-012-9096-1 1 23 Your article is protected by copyright and all rights are held exclusively by The New York Botanical Garden. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your work, please use the accepted author’s version for posting to your own website or your institution’s repository. You may further deposit the accepted author’s version on a funder’s repository at a funder’s request, provided it is not made publicly available until 12 months after publication. 1 23 Author's personal copy Bot. Rev. (2012) 78:87–153 DOI 10.1007/s12229-012-9096-1 Monocot Xylem Revisited: New Information, New Paradigms Sherwin Carlquist1,2 1 Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, CA 93105, USA 2 Author for Correspondence; e-mail: [email protected] Published online: 5 April 2012 # The New York Botanical Garden 2012 Abstract Five sources of data force extensive revision of ideas about the nature and evolution of monocot xylem: scanning electron microscopy (SEM) studies of thick sections; availability of molecular phylogenies covering a relatively large number of families and genera; information on ecology and habitat; data concerning habit; and observations from xylem physiology. These five new sources of data, absent from the studies of Cheadle, plus added information from light microscopy, lead to a fresh understanding of how xylem has evolved in monocots. Tracheary elements hitherto recorded as vessel elements with scalariform end walls prove in a number of instances, to retain pit membranes (often porous or reticulate) in the end walls. There is not an inexorable progression from "primitive" to "specialized" xylem in monocots; apparent accelerations or reversions are also possible. The latter include such changes as the result of production of narrower vessel elements; or production of less metaxylem, which is probably heterochronic in nature (an extreme form of juvenil- ism). Tracheary elements intermediate between vessel elements and tracheids must be recognized for what they are, and not forced into mutually exclusive categories. Original data on tracheids and various types of vessel elements is related here to ecology and habit of groups such as Asteliaceae, Boryaceae, Cyclanthaceae, Orchid- aceae, Pandanaceae, Taccaceae, Typhaceae, dracaenoid Asparagaceae, and Zingiber- ales. Data from palm xylem shows a nearly unique syndrome of features that can be explained with the aid of information from physiology and ecology. Vessellessness of stems and leaves characterizes a large number of monocot species; the physiological and ecological significance of these is highlighted. An understanding of how non- palm arborescent monocots combine an all-tracheid stem xylem with addition of bundles and vegetative modifications is attempted. The effect of the disjunction between xylems of adventitious roots and stems, providing a physiologically dem- onstrated valve ("rectifier") effect is discussed. "Ecological iteration" has occurred in some monocot lineages, so that early-departing branches in some cases may have more "specialized" xylem because of entry into xeric habitats, whereas nearby crown groups, which may have retained "primitive" xylem, probably represent long occu- pation of mesic habitats. Cheadle's use of xylem for "negations" of phyletic pathways can no longer be accepted. Symplesiomorphic mesomorphic xylem patterns do characterize many of the earlier-departing branches in the monocots as a whole, however. Cheadle's idea that monocots and non-monocot angiosperms attained Author's personal copy 88 S. Carlquist vessels independently is improbable in the light of molecular trees for angiosperms. Vessels in roots seem an adaptation to major swings in moisture availability to adventitious roots as compared to taproots. The commonness of all-tracheid plans in stems and leaves in earlier-departing monocot clades is a feature that requires further clarification but is primarily related to the xylem disjunction that adventitious roots have. Secondary vessellessness or something very close to it can be hypothe- sized for Campynemataceae, Philesiaceae, Taccaceae, and some Orchidaceae. Eleven salient shifts in our conceptual views of monocot xylem are proposed and conclude the paper. Monocot xylem is not a collection of historical information, but a rigor- ously parsimonious system related to contemporary habits and habitats. Keywords Ecological plant anatomy. Heterochrony. Microstructure . Monocot cambium . Neotracheids . Vessellessness . Xylem evolution Introduction Evolutionary concepts in plant anatomy are limited by the fields of knowledge available and taken into account. Certainly we have good descriptive accounts of monocot anatomy in general, based mostly on light microscopy, from the Anatomy of Monocotyledons series begun by C. R. Metcalfe (1960), and now extended by the work of others (e.g., Tomlinson, 1961, 1969, 1983). Cheadle's work on monocots, begun as data summaries (Cheadle, 1942, 1943a, b), was extended, with the collab- oration of Hatsume Kosakai (e.g., Cheadle & Kosakai, 1971) to provide family by family examinations of xylem. The end walls and lateral wall pitting of vessels are the focuses of the Cheadle and Kosakai work. Work on monocot xylem has been organized on the basis of systematic groupings, which is ideal for data retrieval (e.g., Wagner, 1977). There is an implication, begun in the nineteenth century by the work of Solereder, that anatomy will yield data useful for the construction of a natural system. Cheadle (1942) also offers some gradate phylogenetic progressions, based mostly on the end walls of vessel elements: long scalariform perforation plates are consid- ered indicative of "primitive" conditions, simple perforation plates are considered at the opposite extreme, indicators of specialization. The organographic distribution of vessels and their specialization levels were traced by Cheadle and associates. Chea- dle's central phylogenetic thesis is that vessels originated in the roots of monocoty- ledons and advanced upward during evolution into stems, inflorescence axes, and finally leaves (Cheadle, 1942). He also found (1943a, 1943b), not surprisingly, a similar organographic sequence in vessel specialization (many bars to few to none on perforation plates). He envisioned a sort of inexorable trend which could be tracked by means of specialization index numbers. Cheadle's concepts, however, prove to be rather more problematic than has been realized, for reasons that will be presented below. There are five main sources of new information that now change our ideas on how monocot xylem evolved. The first of these is the construction of molecular trees. Although certainly topologies of these trees are not certain, they have reached sufficient stability and have sufficient levels of likelihood that they must be used as Author's personal copy Monocot Xylem Revisited 89 the framework on which we judge ideas of xylem evolution. Prior to Chase et al. (1993), a natural system for the angiosperms was a goal that could only be dimly reached, because anatomy and other indicators do not, as we see in retrospect, form coherent and clearly directional patterns. The ideas of symplesiomorphy, apomorphy, and homoplasy were not features of earlier attempts at a natural system: lists of resemblances were the tool employed, and relationship was judged on the basis on numbers of similarities rather than what character states they represented. The taxonomic groups chosen for comparison sometimes did not even include the groups that now prove, in the light of molecular phylogeny, to be most closely related. In any case, molecular trees now drive the interpretation of xylem evolution, and xylem configuration is no longer a tool in the construction of natural systems, although distinctions of systematic value can still be yielded by xylem. The second factor that has changed is the widespread use of scanning electron microscopy (SEM). Until recently, use of SEM in studies of monocot xylem was occasional, rather than frequent. SEM proves essential in revealing the occurrence of pit membranes in end walls of tracheary elements, thereby showing that such elements probably should be called tracheids, rather than vessel elements. The production of porose or reticulate pit membranes in these end wall pits, however, has implications not so much for terminology as for the conductive physiology of the xylem. SEM studies, by showing that what hitherto had been regarded as vessel elements are physiologically definable as tracheids invite comparisons with systematics, organography, and ecology, and give us a new understanding of monocot xylem evolution. SEM studies have been changing in methodology (Carlquist & Schneider, 2006), and thickness of pit membranes is now a concern (Jansen et al., 2009). Earlier students of monocot xylem developed ideas on monocot xylem evolution with little reference to ecology. Xylem is quite often a design for dealing with ecological regimens (Carlquist, 1975). There are multiple plant designs within a given habitat, but each design can be closely cued to xylem function. Ecological information may seem imprecise or highly complex and not capable of analysis by someone interested primarily in xylem, but knowledge of a plant's