Origins and Nature of Vessels in Monocotyledons. 12. Pit Membrane Microstructure Diversity in Tracheary Elements of Astelia

Xylem of stems and roots of three species of Astelia, a monocot with relatively unspecialized xylem, was examined with scanning electron microscopy (SEM) to better understand structural conditions intermediate between tracheids and vessel elements. Both macerations and hand-sectioned material were studied. Tracheary elements of roots of Asteliaceae can be characterized as tracheids, with some degrees of transition to vessel elements. Pit membrane remnants, which take the form of pores, reticula, or threads, are present commonly in end walls of tracheary elements of roots of Astelia. Stems of Astelia have tracheids with less-conspicuous porosities in the pit membranes of end walls than those of roots. Sectioned materials show that the porose (reticulate) cellulosic layers of the primary wall, which is embedded in a matrix of amorphous material, can be exposed to various degrees by the sectioning process; the cellulosic network faces the lumen, and the amorphous material is the compound middle lamella. Astelia shows stages of transition between vessel elements and tracheids. These character expressions relate to occupancy of moist habitats (Astelia) with steady availability of moisture during the year. There appears to be little difference between a terrestrial species (A. chathamica) and the scandent/epiphytic species A. argyrocoma and A. menziesiana in terms of tracheary element microstructure, suggesting that habitat is more important than habit as a determinant of tracheary element microstructure and the degree to which lysis of pit membranes occurs. Freehand sectioning of ethanol-fixed materials, as in earlier studies in this series, provides a reliable way of observing pit membrane/ perforation structure when viewed with SEM. Astelia is one of several monocots that demonstrate the difficulty of discriminating between tracheids and vessel elements. Astelia is now considered an early departing branch of the clade Asparagales (APG III 2009). It is of special interest with respect to microstructure of tracheary elements because, like Orchidaceae (also of Asparagales, but not a sister group to Asteliaceae), Astelia has tracheary elements intermediate between tracheids and vessel elements. Orchidaceae were reported to have vessels in roots only, with scalariform perforation plates in vessels in roots (Cheadle 1942). Our studies of xylem of Orchidaceae (Carlquist and Schneider 2006) confirmed Cheadle’s findings, but we were able to take advantage of scanning electron microscopy (SEM). We showed that pit membrane remnants (microfibrillar webs) occur in the perforations of vessels in roots of the majority of the orchids that we studied. The presence of such webs, not visible with light microscopy, suggests that the transition from tracheids to vessels (in which absence of pit membranes in perforations has usually been assumed when using light microscopy) is incomplete. The tracheary elements of stems and inflorescence axes of Orchidaceae are best called tracheids, but they have variPacific Science (2010), vol. 64, no. 4:607–618 doi: 10.2984/64.4.607 : 2010 by University of Hawai‘i Press All rights reserved 1Manuscript accepted 8 December 2009. 2 Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, California 93105. 3 Corresponding author (e-mail: s.carlquist@verizon .net). 4 E-mail: [email protected]. ous degrees of porousness in pit membranes of end walls, suggesting a ‘‘pre-vessel’’ configuration. Cheadle and Kosakai (1971) reported vessels with long scalariform perforation plates in roots of Astelia and Milligania but tracheids in stems of the two genera. Cheadle and Kosakai (1971) did not have the advantage of SEM and therefore could not observe degrees of transition (as represented by pit membrane presence in perforation plates) between vessel elements and tracheids. Astelia proved to be ideal material for showing the microstructure of tracheary element walls in monocots and degrees of intermediacy between tracheids and vessel elements. Understanding of tracheary elements is complicated, rather than simplified, by examples from monocots such as Asteliaceae and Orchidaceae. The definitions in current use are based in light microscopy, in which end walls of vessels clearly have perforations devoid of pit membranes, whereas end walls of tracheids have pits with pit membranes. In addition, colloidal India ink particles have been used to demonstrate the size of openings in perforations, through which such particles pass, as compared with the supposed nonporousness of pit membranes of tracheids (Cheadle 1942). However, a number of monocots have pit membranes with pores on end walls of tracheary elements of various sizes when seen with SEM (Carlquist and Schneider 2006). Partial pit membranes (‘‘pit membrane remnants’’) are characteristically present in perforation plates of vessels in a number of dicots (Carlquist 1992). India ink particles may be a test for pore size, but are the size of such particles relevant to physiological differences between tracheids and vessel elements? What is the physiological value of presence of porose pit membranes in end walls of ‘‘vessel-like’’ tracheary elements? In what ecological habitats and regimens are tracheary elements intermediate between vessel elements and tracheids found? If imaging of tracheary elements with SEM is the only accurate way to establish present of pit membranes in end walls, can the definitions established by means of light microscopy be maintained? If they are maintained, what caveats must be employed? Astelia is a key group with regard to these questions, because of special features of microstructure of its tracheary elements. Cheadle (1942) emphasized levels of specialization in monocotyledon xylem, even assigning numerical values to degree of specialization. These trends do occur, but the main determinants of vessel element presence and perforation plate type in monocotyledons are ecological and habital (Carlquist 1975) rather than position within a phylogenetic tree or clade. For example, in onions and allied genera (Alliaceae), there are vessels with simple perforation plates in roots but only tracheids in stems and leaves. This has been interpreted as an adaptation to rapid transport of water by roots, which are short-lived, during brief periods of moisture availability in combination with the conductive safety of tracheids, which restrict spread of air embolisms, within stems and leaves (Carlquist 1975). Orchid roots have longer duration than do the roots of bulbous monocotyledons. That fact may be correlated with the scalariform perforation plates in vessels and, more commonly, tracheids transitional to vessel elements in roots. One could say, in agreement with Cheadle (1942), that these tracheary element expressions are less specialized. One could even imagine that a lower degree of specialization in vessel types in such families as Orchidaceae is due to lack of selection for simple perforation plates because of the mesophytic habitats that these plants occupy. This probably is true in Acoraceae, the family that is a sister group to the remainder of the monocotyledons (Carlquist and Schneider 1997). However, the tracheary elements with scalariform perforation plates in orchids frequently have extensive pit membrane remnants in end walls (Carlquist and Schneider 2006). We see the context for our studies as being primarily of ecology and physiology, and only to a much less extent systematic or phylogenetic in nature. For example, Boryaceae are considered a family of Asparagales that may be close to Asteliaceae (Davis et al. 2004), although resolution is not high currently for branching in phylogenetic trees of Asparagales (APG III 2009). Borya is 608 PACIFIC SCIENCE . October 2010