On the origin of euphyllophyte roots - hypotheses from an Early Devonian Psilophyton.

Background and aims: Rooting structures have been documented in different Early Devonian plants, including rhyniophytes and zosterophylls. However, the basal euphyllophytes - the plexus from which modern ferns, equisetophytes and seed plants evolved - are the only group with no known rooting structures in Early Devonian representatives. We revisit the early euphyllophyte Psilophyton crenulatum whose emergences have implications for rooting structure evolution within the clade.

Methods: Well preserved Early Devonian (earliest Emsian) material from the Val d'Amour Formation in New Brunswick (Canada) was freed from the rock matrix using acid. Over 2000 emergences from 28 randomly selected P. crenulatum axes were characterized qualitatively and quantitatively in terms of morphology and distribution.

Key results: The features of the emergences are more consistent with a rooting function than with any other possible role: irregular morphology, including forms with complex branching; anatomy involving external layers of thin-walled cells; apical meristematic growth that allowed for branching; terminations in filiform rhizoid-sized tips; and vertically polarized distribution, with nearly twice as many emergences on the lower sides of axes compared to the upper sides. The absence of any other potential rooting structures associated with P. crenulatum also supports a rooting function for the emergences.

Conclusions: If the emergences of P. crenulatum had a rooting function, they are the oldest euphyllophyte rooting structures. They are also a novel, sui generis type of such structures among Early Devonian plants. They also provide the oldest direct evidence for gravity-induced morphological features in euphyllophytes. If they evolved from emergences like those of P. crenulatum, then euphyllophyte roots probably inherited from them apical growth and branching, and gene networks responsible for production of tip-growing filamentous cells. Progressive increase in size of such emergences could have increased auxin fluxes, leading to specification of vascular connections to subtending axes.