Living Cells in Wood 3. Overview; Functional Anatomy of the Parenchyma Network Sherwin Carlquist The Botanical Review ISSN 0006-8101 Bot. Rev. DOI 10.1007/s12229-018-9198-5 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 article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Bot. Rev. https://doi.org/10.1007/s12229-018-9198-5 Living Cells in Wood 3. Overview; Functional Anatomy of the Parenchyma Network 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] # The New York Botanical Garden 2018 Abstract The very different evolutionary pathways of conifers and angiosperms are very informative precisely because their wood anatomy is so different. New informa- tion from anatomy, comparative wood physiology, and comparative ultrastructure can be combined to provide evidence for the role of axial and ray parenchyma in the two groups. Gnetales, which are essentially conifers with vessels, have evolved parallel to angiosperms and show us the value of multiseriate rays and axial parenchyma in a vessel-bearing wood. Gnetales also force us to re-examine optimum anatomical solu- tions to conduction in vesselless gymnosperms. Axial parenchyma in vessel-bearing woods has diversified to take prominent roles in storage of water and carbohydrates as well as maintenance of conduction in vessels. Axial parenchyma, along with other modifications, has superseded scalariform perforation plates as a safety mechanism and permitted angiosperms to succeed in more seasonal habitats. This diversification has required connection to rays, which have concomitantly become larger and more diverse, acting as pathways for photosynthate passage and storage. Modes of growth such as rapid flushing, vernal leafing-out, drought deciduousness and support of large leaf surfaces become possible, advantaging angiosperms over conifers in various ways. Prominent tracheid-ray pitting (conifers) and axial parenchyma/ray pitting to vessels (angiosperms) are evidence of release of photosynthates into conductive cells; in angiosperms, this system has permitted vessels to survive hydrologic stresses and function in more seasonal habitats. Flow in ray and axial parenchyma cells, suggested by greater length/width ratios of component cells, is confirmed by pitting on end walls of elongate cells: pits are greater in area, more densely placed, and are often bordered. Bordered pit areas and densities on living cells, like those on tracheids and vessels, represent maximal contact areas between cells while minimizing loss of wall strength. Storage cells in rays can be distinguished from flow cells by size and shape, by fewer and smaller pits and by contents. By lacking secondary walls, the entire surfaces of phloem ray and axial phloem parenchyma become conducting areas across which sugars can be translocated. The intercontinuous network of axial parenchyma and ray parenchyma in woods is confirmed; there are no “isolated” living cells in wood when three-dimensional studies are made. Water storage in living cells is reported anatomi- cally and also in the form of percentile quantitative data which reveal degrees and kinds of succulence in angiosperm woods, and norms for “typically woody” species. The diversity in angiosperm axial and ray parenchyma is presented as a series of probable Author's personal copy S. Carlquist optimal solutions to diverse types of ecology, growth form, and physiology. The numerous homoplasies in these anatomical modes are seen as the informative results of natural experiments and should be considered as evidence along with experimental evidence. Elliptical shape of rays seems governed by mechanical considerations; unusually long (vertically) rays represent a tradeoff in favor of flexibility versus strength. Protracted juvenilism (paedomorphosis) features redirection of flow from horizontal to vertical by means of rays composed predominantly or wholly of upright cells, and the reasons for this anatomical strategy are sought. Protracted juvenilism, still little appreciated, occurs in a sizeable proportion of the world’s plants and is a major source of angiosperm diversification. Keywords Flow in rays . Gnetales . Growth flushes . Juvenilism . Succulence . Xeromorphy Introduction As the physiology of water conduction in vessels and tracheids has become better understood, attention has turned to the roles that ray and axial parenchyma in func- tioning of secondary xylem of conifers and angiosperms. This wave of interest, most recently represented by the thoroughly-referenced papers by Morris et al. (2015, 2017) and Morris and Jansen (2016), seeks to clarify what living cells, including living fibers, do with regard to wood function. The approaches to study of parenchyma function must of necessity be different from those applied to sap-conducting cells of the wood. Axial parenchyma, and, indirectly, ray parenchyma are concerned in suppression and reversal of embolisms (Braun, 1984; Holbrook and Zwieniecki 1999;Holbrooketal. 2002; Johnson et al., 2012; Lens et al., 2013; Nardini et al., 2011;Salleoetal.,2004, Salleo et al., 2009; Secchi et al., 2016; Trifilo et al., 2014). These authors do not examine the role of ray parenchyma, but there is no other source for the sugars and ions than via the rays. In examining the function of axial and ray parenchyma, assembling of quantitative data has, to a large extent, been the method of choice (Morris et al. 2015, Morris et al., 2017 and literature cited therein). The present paper attempts to use new data in comparative anatomy obtained with light microscopy, ultrastructure as seen with scanning electron microscopy (SEM), and observations on growth form and habit primarily. References to experimental work in physiology are considered a vital parallel source of information, and are cited here, as they were in Carlquist (2012a). The value of comparative anatomical data is consider- able in interpreting the functioning of wood, because wood anatomical diversity ultimately must be explained in terms of selection for structural features. The many parallel acquisitions of wood character states in clade after clade represent the results of natural experiments performed on immense numbers of individuals in thousands of species over many million years. There has been some appreciation of the value of anatomical data (e.g., Morris & Jansen, 2016). Such works, rich in illustration, as Moll and Janssonius (1909-1936) and Metcalfe and Chalk (1950) are cited by Morris and Jansen (2016). To those we must add such works as Greguss (1955, 1959), Meylan and Butterfield (1978), and many other important sources. Many of these are expensive and found in a relatively small number of libraries, and are not available on the internet, Author's personal copy Living Cells in Wood 3. Overview; Functional Anatomy of the... which increasingly has become the source of references and the basis for documenta- tion in research. Simultaneously, there has been a disappearance from many colleges and universities of courses in plant anatomy, so that those able to do interpretive work in wood anatomy are fewer. Those with encyclopedic knowledge of comparative wood anatomy of large numbers of species, such as I. W. Bailey, C. R. Metcalfe, and S. J. Record, are almost non-existent today, although some a few specialists conversant with comparative wood anatomy of some families and clades do, fortunately, exist. Exper- imental studies of wood function are, by contrast, relatively recent and easy to access. The complexity and diversity of wood anatomy and the difficulty of access to the field have worked to the disadvantage of visual understanding of the function-structure continuum. The present paper is an attempt to work with microscopy and some allied data by way of supplying the visual component. This is done by presenting illustrations for a number of modes of structure in wood anatomy and attempting to show how they may be related to functional aspects. Cross-comparisons of wood of unrelated or distantly-related groups can be highly informative. Metcalfe (1983, p. 4) says, “The development of the vessel has had a profound effect on the xylem of angiosperms….it has made specialization possible in other directions: specialization of fibers [i.e, change from tracheids to libriform fibers]….and this in turn has been linked with changes in the distribution of parenchy- ma cells.” Now that we know that Gnetales are conifer derivatives (Bowe et al., 2000; Burleigh & Mathews, 2004), and that Gnetales have attained, parallel to angiosperms, essentially all of the important anatomical features of angiosperm wood (Carlquist, 2012b), we have a source for demonstrating quite dramatically pathways of wood evolution in vessel-bearing angiosperms and their significance. The wood of Gnetales,