Secondary Phloem in Early Carboniferous Seed Plants: Anatomical Diversity and Evolutionary Implications

Abstract

Editor: Michael T. DunnPremise of research. Secondary phloem produced by a bifacial vascular cambium is the distinctive feature of lignophytes, the group that comprises the seed plants and the progymnosperms. Because secondary phloem is rarely well preserved in the fossil record, our knowledge of the evolution of this tissue remains incomplete.Methodology. We illustrate the secondary phloem anatomy of nine seed plants of Mississippian (Early Carboniferous) age that represent to date the oldest representatives of the group in which this tissue is well preserved. In addition, we review the information available on the secondary phloem anatomy of Devonian progymnosperms and Late Carboniferous-Permian seed plants.Pivotal results. Secondary phloem anatomy was already diversified in the Mississippian seed plants, in terms of cell composition and spatial organization of the different cell types. We propose four models of secondary phloem anatomy and organization in lignophytes of Devonian-Carboniferous age.Conclusions. The diversity of secondary phloem anatomy in Mississippian seed plants parallels what is observed for other parts of their vascular system; it is most likely linked to the Mississippian diversification of seed plant growth architectures and habitats. The accumulated fossil evidence also demonstrates that several characters that have been considered as advanced on the basis of the study of extant gymnosperms (e.g., the presence of fibers in the functional phloem and the arrangement in alternate tangential layers of a same cell type) were actually already present in some early representatives of the lignophytes.

Ahnetia, a new lignophyte stem from the Lower Carboniferous of southern Algeria

“…The secondary phloem of Mississippian lignophyte trees is a complex tissue containing sieve cells, axial and radial parenchyma, sclereids, and fibers. In this aspect it is similar to that of Devonian Aneurophytalean and Archaeopteridalean progymnosperms (Beck, 1957;Banks, 1971a, 1971b;Stein and Beck, 1983;Decombeix & Meyer-Berthaud, 2013;Decombeix et al, 2014). The organization observed in the specimen from Algeria, with tangential layers of fibers that are several cells thick alternating with bands of thin-walled cells is relatively unusual.…”

“…A drawing of a transverse section of the specimen and a picture of a general view have already been published (Galtier, 1988;Galtier and Meyer-Berthaud, 2006, "new taxon 3"), as well as a description of the secondary phloem (Decombeix et al, 2014). However, this paper is the first detailed anatomical and systematic treatment of the specimen.…”

“…It is quite similar to the organization seen in Middle Tournaisian trunks from Australia that have a Pitus/Eristophyton type of wood but an apparently more complex type of leaf trace emission (Decombeix at al., 2011b;Decombeix, 2013). It differs from the secondary phloem organization of all other Mississippian lignophytes in which this tissue is known, i.e., Bilignea, Calamopitys (and the other calamopityales Diichnia and Triichnia), Eristophyton fasciculare, Faironia, Lyginopitys, and Stanwoodia (Decombeix et al, 2014). Secondary phloem in Pitus is not well-known but Gordon (1935) only reported thin-walled cells in the poorly preserved phloem of P. dayi.…”

Una historia de éxito: biodiversidad a través de fósiles

“…La composición de la pared de las traqueidas de estas primeras plantas vasculares semeja la estructura obtenida de traqueidas de Huprezia y otras Molinofitas en el laboratorio (degradada o con poca pared secundaria; e. g., Friedmann & Cook, 2000;Kato, 2010). A esta interrogante hay que aumentar que no se ha documentado de forma convincente el floema (Decombeix et al, 2014(Decombeix et al, , 2016Taylor, 1990). Entonces la fisiología de este grupo de plantas vasculares (Figuras 2 -6) ¿sería distinta a la de sus descendientes?…”

“…Dos grupos son especialmente importantes después del dominio de las primeras hierbas (Figuras 2 -3, 6). Un grupo de plantas novedosas de ese tiempo continuó teniendo un solo meristemo primario, el apical, generador del crecimiento longitudinal, y desarrolla un meristemo secundario, el cambium vascular, que les permite crecer en diámetro, A diferencia de las plantas actuales cuyo cambium vascular es bifacial, produciendo xilema hacia el interior y floema hacia el exterior de la planta, en estas plantas del Paleozoico el cambium vascular es unifacial, sólo produce xilema hacia el interior (Figuras 3, 6 -7;Decombeix et al, 2014Decombeix et al, , 2016Taylor, 1990). Aunque se han interpretado algunas células como representantes del floema secundario, no se ha demostrado la presencia de un tejido que tuviera funciones de conducción de materiales elaborados (Taylor, 1990).…”