Vegetative and reproductive innovations of early land plants: implications for a unified phylogeny

Abstract

As the oldest extant lineages of land plants, bryophytes provide a living laboratory in which to evaluate morphological adaptations associated with early land existence. In this paper we examine reproductive and structural innovations in the gametophyte and sporophyte generations of hornworts, liverworts, mosses and basal pteridophytes. Reproductive features relating to spermatogenesis and the architecture of motile male gametes are overviewed and evaluated from an evolutionary perspective. Phylogenetic analyses of a data set derived from spermatogenesis and one derived from comprehensive morphogenetic data are compared with a molecular analysis of nuclear and mitochondrial small subunit rDNA sequences.Although relatively small because of a reliance on water for sexual reproduction, gametophytes of bryophytes are the most elaborate of those produced by any land plant. Phenotypic variability in gametophytic habit ranges from leafy to thalloid forms with the greatest diversity exhibited by hepatics. Appendages, including leaves, slime papillae and hairs, predominate in liverworts and mosses, while hornwort gametophytes are strictly thalloid with no organized external structures. Internalization of reproductive and vegetative structures within mucilage-¢lled spaces is an adaptive strategy exhibited by hornworts. The formative stages of gametangial development are similar in the three bryophyte groups, with the exception that in mosses apical growth is intercalated into early organogenesis, a feature echoed in moss sporophyte ontogeny.A monosporangiate, unbranched sporophyte typi¢es bryophytes, but developmental and structural innovations suggest the three bryophyte groups diverged prior to elaboration of this generation. Sporophyte morphogenesis in hornworts involves non-synchronized sporogenesis and the continued elongation of the single sporangium, features unique among archegoniates. In hepatics, elongation of the sporophyte seta and archegoniophore is rapid and requires instantaneous wall expandability and hydrostatic support. Unicellular, spiralled elaters and capsule dehiscence through the formation of four regular valves are autapomorphies of liverworts. Sporophytic sophistications in the moss clade include conducting tissue, stomata, an assimilative layer and an elaborate peristome for extended spore dispersal. Characters such as stomata and conducting cells that are shared among sporophytes of mosses, hornworts and pteridophytes are interpreted as parallelisms and not homologies.Our phylogenetic analysis of three di¡erent data sets is the most comprehensive to date and points to a single phylogenetic solution for the evolution of basal embryophytes. Hornworts are supported as the earliest divergent embryophyte clade with a moss/liverwort clade sister to tracheophytes. Among pteridophytes, lycophytes are monophyletic and an assemblage containing ferns, Equisetum and psilophytes is sister to seed plants. Congruence between morphological and molecular hypotheses indicates that these data sets are tracking the...

The deepest divergences in land plants inferred from phylogenomic evidence

“…In alternative topology test analyses of the multigene supermatrix, we were initially unable to reject the three competing hypotheses: mosses sister to vascular plants (5,6), hornworts basal (14,15), and bryophytes monophyletic (13,16,17), although the first two were close to the rejection threshold under ML (Tables 1 and 2, which are published as supporting information on the PNAS web site). We implemented a second constraint search in which relationships within the four major land plant clades were constrained based on the 50% majority BS trees obtained from ML and MP analyses.…”

“…In contrast, the placement of hornworts as sister to vascular plants is rather novel. Hornworts have been strongly argued to be sister to all other land plants (14,15). On the other hand, several other studies hinted they could be sister to vascular plants (8)(9)(10)(11)(12)(13), and three recent analyses of cp-genome sequences and genomic structural characters are particularly noteworthy in this regard, because BS values supporting this relationship range from 82% to 100% (10, 12, 13).…”

To concentrate or ventilate? Carbon acquisition, isotope discrimination and physiological ecology of early land plant life forms

“…Overall, none of the three groups have developed a significant degree of cuticularization, stomata and water transport tissues, and then only in specialized tissues in certain groups (e.g. stomata in sporophytes of mosses and hornworts: Edwards et al 1998;Renzaglia et al 2004Renzaglia et al , 2007Shaw & Renzaglia 2004).…”

Hormonal regulation in green plant lineage families

“…This lineage is believed to be monophyletic in origin (Graham, 1996). The phylogenetic relationships of different lineages of land plants -the embryophytes represented by green algae, bryophytes, pteridophytes and seed plants have been reviewed extensively (Karol et al, 2001;Kendric and Crane, 1997;Mishler et al, 1994;Renzaglia et al, 2000). Here, only the salient features of the most widely accepted viewpoint will be discussed.…”