Distribution of cell‐wall xylans in bryophytes and tracheophytes: new insights into basal interrelationships of land plants

Abstract

Summary• Xylans are known to be major cellulose-linking polysaccharides in secondary cell walls in higher plants.• We used two monoclonal antibodies (LM10 and LM11) for a comparative immunocytochemical analysis of tissue and cell distribution of xylans in a number of taxa representative of all major tracheophyte and bryophyte lineages.• The results show that xylans containing the epitopes recognized by LM10 and LM11 are ubiquitous components of secondary cell walls in vascular and mechanical tissues in all present-living tracheophytes. In contrast, among the three bryophyte lineages, LM11 binding was detected in specific cell-wall layers in pseudoelaters and spores in the sporophyte of hornworts, while no binding was observed with either antibody in the gametophyte or sporophyte of liverworts and mosses.• The ubiquitous occurrence of xylans containing LM10 and LM11 epitopes in tracheophytes suggests that the appearance of these polysaccharides has been a pivotal event for the evolution of highly efficient vascular and mechanical tissues. LM11 binding in the sporophyte of hornworts, indicating the presence of relatively highly substituted xylans (possibly arabinoxylans), separates these from the other bryophytes and is consistent with recent molecular data indicating a sister relationship of the hornworts with tracheophytes.

How Have Plant Cell Walls Evolved?

“…While cellulose and RGII are highly conserved (although some nonseed tracheophytes have RGII in which a L-rhamnosyl residue is replaced by a 3-O-methylrhamnosyl), many other cell wall components exhibit phylogenetically correlated variability. For example, the presence of highly substituted xylan epitope recognized by antibody LM11 in hornworts but not other bryophytes supports molecular studies that indicate a sister relationship between the hornworts and tracheophytes (Carafa et al, 2005). Also, detailed biochemical studies of XyGs have revealed intriguing variations in the side chain structural motifs between taxa (Hoffman et al, 2005;Peñ a et al, 2008;Hsieh and Harris, 2009).…”

“…RGII can be cross-linked by boron, and it is significant that grasses, which have a lower requirement for boron than dicots, also have reduced levels of RGII in their walls. Xylans are ubiquitous and often highly abundant in vascular plants, and their evolution may have been an important aspect of the preadaptation that enabled the emergence of vascular and mechanical tissues (Carafa et al, 2005;Popper, 2008). Further layers of complexity are revealed when one considers the variations in fine structure within polysaccharide classes.…”

The deepest divergences in land plants inferred from phylogenomic evidence

“…Hornworts are unique among bryophytes in exhibiting several similar features on both gametophyte and sporophyte: persistent photosynthetic capacity, nutritional independence, as well as plant size and longevity (2,32,35,36). Also, there are similarities between sporophytes of hornworts and early vascular plants (2,15,(31)(32)(33)(34)(35)(36)(37). Hence, one might interpret that hornworts, among three extant bryophyte lineages, approach closest toward vascular plants in their sporophyte development in terms of achieving an independent free-living sporophyte generation.…”

“…These characters were not used in or available to earlier morphological cladistic analyses (5, 6). They include lack of ventral slime papillae, hairs, and͞or scales in prothalli (15); the embedded position of gametangia (31,32); intermingled͞interdigitate gametophyte-sporophyte junction (33); spiral thickening on cell walls in the columella (34); the persistently chlorophyllous and nutritionally largely independent sporophyte (32, 35, 36); rhizoid-like behavior of surface cells of the sporophyte foot (35); the longevity and large size of the sporophyte (32,35); and xylan content in cell walls of pseudoelaters and spores (37). It should be emphasized that, although some of these similarities between hornworts and vascular plants are controversial (5,6,15), our results suggest they should be critically reexamined to identify truly synapomorphic changes shared by hornworts and vascular plants.…”

Evolution of the cell wall components during terrestrialization

“…Xylans are ubiquitous hemicelluloses of vascular plants [68], present mainly in their secondary cell walls [69,70]. Therefore, it was suggested that the acquisition of xylan synthesis capabilities could have been an evolutionary innovation of this group of plants [49,68].…”