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Acetabularia Acetabulum Plant Cell Physiol. 48(1): 122–133 (2007) doi:10.1093/pcp/pcl053, available online at www.pcp.oxfordjournals.org ß The Author 2006. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: [email protected] Spectroscopic and Biochemical Analysis of Regions of the Cell Wall of the Unicellular ‘Mannan Weed’, Acetabularia acetabulum Erin K. Dunn 1, 5, Douglas A. Shoue 2, 5, Xuemei Huang 3, Raymond E. Kline 4, Alex L. MacKay 3, Nicholas C. Carpita 2, Iain E.P. Taylor 4 and Dina F. Mandoli 1,Ã 1 Department of Biology, Center for Developmental Biology & Institute for Stem Cell and Regenerative Medicine, Box 35325, University of Washington, Seattle, WA 98195-5325, USA 2 Department of Botany and Plant Pathology, Purdue University, W. Lafayette, Indiana 47907-2054, USA 3 Department of Physics and Astronomy, University of British Columbia, Vancouver, BC, Canada V6T 1Z1 4 Department of Botany, University of British Columbia, Vancouver, BC, Canada V6T 1Z4 Downloaded from https://academic.oup.com/pcp/article/48/1/122/2469303 by guest on 29 September 2021 Although the Dasycladalean alga Acetabularia acetabulum Introduction has long been known to contain mannan-rich walls, it is not known to what extent wall composition varies as a function of The Mediterranean coralline alga Acetabularia the elaborate cellular differentiation of this cell, nor has it acetabulum (previously classified as A. mediterranea)isa been determined what other polysaccharides accompany the giant unicell with a precisely defined, intricate morphology. mannans. Cell walls were prepared from rhizoids, stalks, This diploid organism produces an upright stalk from which hairs, hair scars, apical septa, gametophores and gametangia, whorls of branched hairs emerge, a basal rhizoid composed subjected to nuclear magnetic resonance and Fourier trans- of multiple digits which houses the cell’s sole nucleus for form infrared spectroscopy, and analyzed for monosaccharide most of the life cycle, and later in development an elaborate composition and linkage, although material limitations reproductive structure or ‘cap’ at the apex, 3–4 cm away prevented some cell regions from being analyzed by some of from the rhizoid (Fig. 1). During reproduction, haploid the methods. In diplophase, walls contain a para-crystalline nuclei are generated, which migrate with the majority of the mannan, with other polysaccharides accounting for 10–20% parental cytoplasm into the cap. Once there, each nucleus of the wall mass; in haplophase, gametangia have a cellulosic along with some cytoplasm is surrounded by a new cell wall, wall, with mannans and other polymers representing about a creating the ‘gametangia’. The subsequently produced quarter of the mass. In the walls of the diplophase, the gametes lack a cell wall of any kind. Previous studies have mannan appears less crystalline than typical of cellulose. indicated that the vegetative wall of this organism consists The walls of both diploid and haploid phases contain little mostly of mannan, but that during reproduction the if any xyloglucan or pectic polysaccharides, but appear to gametangial wall is about 80% cellulose and about 20% contain small amounts of a homorhamnan, galactomannans mannan (Zetsche et al. 1970). and glucogalactomannans, and branched xylans. These There are three reasons why further investigation of the ancillary polysaccharides are approximately as abundant wall of A. acetabulum is of interest. First, the cell comprises in the cellulose-rich gametangia as in the mannan-rich more than stalk, cap and gametangia—prior studies ignored diplophase. In the diplophase, different regions of the cell the other distinct regions of the cell (e.g. rhizoid, hairs, differ modestly but reproducibly in the composition of the cell septa; Fig. 1). Indeed, the ‘stalk’ and ‘cap’ in previous wall. These results suggest unique cell wall architecture for studies are themselves heterogeneous (Fig. 1). It is reason- the mannan-rich cell walls of the Dasycladales. able that the morphological and physiological differentia- tion of the cell may be accompanied by differences in cell Keywords: Acetabularia acetabulum — Cellulose — wall composition and structure. However, such spatial Dasycladales — FTIR — Linkage analysis —Mannan differences in cell wall composition have been little studied weed. in any giant unicellular species. Here, we carefully dissected distinct regions of the cell for analysis. Abbreviations: FTIR, Fourier transform infrared spectro- Secondly, mannans in this type of cell wall have been scopy; GC–MS, gas chromatography–mass spectrometry; GalA, galacturonic acid; GlcA, glucuronic acid; ManA, mannuronic acid; poorly characterized compared with cellulose, leaving NMR, nuclear magnetic resonance; RG I, rhamnogalacturonan I; doubts about the form(s) of mannan present. In theory, TFA, trifluoracetic acid. a microfibril made from mannans would be all but identical 5Present address: c/o University of California San Diego, Biology Graduate Student Affairs, 0348, 9500 Gilman Drive, La Jolla, CA 92093-0348, USA. ÃCorresponding author: E-mail, [email protected]; Fax, þ1–206–685–1728. 122 Cell walls of Acetabularia 123 Gametophores Cap Gametangial wall encloses Cap septum each nucleus Mitoses (~9x) Whorl scar Downloaded from https://academic.oup.com/pcp/article/48/1/122/2469303 by guest on 29 September 2021 Hairs Stalk Interwhorl Gametophore Nucleus Rhizoid (2n) Meiosis (1x) then mitoses (~9x) followed by transport of haploid Gametangium nuclei into the cap Fig. 1 Anatomy of vegetative adult and reproductive individuals. Septa join the stalk to the cap and each hair to the stalk. Older hairs are normally shed during vegetative growth. When hairs separate from the stalk, they leave behind a ‘whorl scar’. Cap initiation marks reproductive onset. Later, during cap expansion, meiosis of the single diploid nucleus and subsequent rounds of mitosis generate thousands of haploid nuclei. For clarity, not all the nuclei, gametangia and gametes were drawn. Hairs are usually completely shed by the time that the cap bears gametangia. To clarify anatomy, images are drawn only roughly to scale. Cells average 3–4 cm tall, caps average 1 cm and stalks average 0.3 mm in diameter. Detailed dimensions of anatomical regions within cell populations can be found in Nishimura et al. (1992a, b) and also in Ngo et al. (2005). to cellulose; however, a cellulose-like high tensile strength is depends on the interactions between cellulose and pectin generally not ascribed to the mannan-rich walls of (Proseus and Boyer 2006), with xyloglucan being absent A. acetabulum or of other species with mannan-rich walls (Popper and Fry 2003). How the major mannan phase is (the so-called ‘mannan weeds’). Were the mannan sub- modified by the remaining cell wall matrix has been almost stituted to even a small extent, then this would undermine totally unexplored. its ability to form high tensile strength microfibrils, but Here, we have used Fourier transform infrared might enhance its ability to form a flexible network. spectroscopy (FTIR), nuclear magnetic resonance (NMR), Frei and Preston (1968), using X-ray diffraction, observed and sugar and methylation analyses to characterize each physical polymorphism within the mannan from whole region of the wall of A. acetabulum. We found that the A. acetabulum walls but did not find microfibrillar forms. mannan makes up almost 90% of the diplophase cell wall Chanzy (1984), using electron diffraction and microscopy, mass and that the diplophase contained small amounts of confirmed the existence of at least two forms of mannan hemicelluloses, resembling those described for other cells but after chemical extraction, but detected both granular and not including xyloglucan, and had essentially no recognizable microfibrillar domains. Neither author prepared cell walls pectin. The haplophase, although containing a majority of from defined regions of the cell. cellulose, had remaining cell wall material similar to that of the Thirdly, although the identity of the major cell wall diplophase rather than to the cellulosic walls of other algae. component of diplophase (rhizoid, stalk, cap) and haplo- phase (gametangia) has been identified as mannan and Results cellulose, respectively, there has been almost no analysis of the other polymers of the cell wall. Even algal orders that Regions of the vegetative and reproductive thalli dissected for contain cellulose-rich walls, such as charophytes, have non- analysis cellulosic components that differ from that found in the The anatomy of both vegetative and reproductive thalli type I or type II walls of angiosperms. It has recently of this unicell is complex. Fig. 1 is a labeled drawing of become clear, for example, that elongation in Chara corallina subcellular regions of the wall that are macroscopically 124 Cell walls of Acetabularia Table 1 Amino acid composition (mean% of totals) in stalk and cap walls of A. acetabulum Amino acid Asx Glx Lysine Leucine Totals of other amino acidsa Stalks 12.3 12.5 13.9 6.4 54.9 Caps 14.1 16.0 8.5 9.0 52.4 Values are expressed as a percentage of the total amino acids recovered in analysis of that region of the thallus wall. a Total other amino acids includes threonine, serine, glycine, alanine proline methionine, valine, isoleucine, tyrosine, phenylalanine, histidine and arginine, which each were always58% of the total amino acids recovered. Asx ¼ (Asn þ
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