An Early Devonian actinostelic euphyllophyte with secondary growth from the Emsian of Gaspé (Canada) and the importance of tracheid wall thickening patterns in early euphyllophyte systematics

Abstract

Secondary growth is a tracheophyte structural feature whose earliest known occurrence dates to the late Pragianearly Emsian. Armoricaphyton, Franhueberia and an unnamed plant from eastern Canada represent the only instances of secondary growth documented to date for the Early Devonian. Here, we describe a new Early Devonian euphyllophyte exhibiting secondary growth, from the Emsian (c. 400-395 Ma) Battery Point Formation (Qu ebec, Canada): Gmujij tetraxylopteroides gen. et sp. nov., which is characterized by a mesarch actinostele with Psilophyton-type (P-type) tracheid wall thickening, and which exhibits a new type of anatomical organization in Early Devonian wood-producing euphyllophytes. Gmujij differs from coeval euphyllophytes, but lack of data on branching patterns, reproductive structures and other traditional diagnostic features precludes classification in previously recognized euphyllophyte groups. We experiment with a numerical approach to tracheid size distributions, to compare Gmujij with younger euphyllophytes exhibiting secondary growth. Comparisons indicate similarity between Gmujij and aneurophytalean progymnosperms, such as Tetraxylopteris. However, its plesiomorphic P-type tracheids set Gmujij apart from younger actinostelic euphyllophytes, questioning the importance of tracheid thickening patterns as diagnostic characters separating major lineages. Answers to this question hinge on whether transitions between wall thickening patterns require simple or complex changes in developmental regulation, a matter that requires improved understanding of regulatory programs that determine tracheid thickening patterns. Irrespective of these, Gmujij adds a new component to the diversity of anatomically preserved plants known in the Early Devonian, an incompletely explored interval of tracheophyte anatomical diversification, contributing information that will facilitate understanding of the evolutionary origins of secondary growth.

Complex wound response mechanisms and phellogen evolution – insights from Early Devonian euphyllophytes

“…Nevertheless, tangentially oriented tensional stress induced in outer plant layers (epidermis, cortex) by the increase in girth in deeper tissues from vascular cambial growth, results in tissue tearing, which is a form of wounding. In support of this tensional stress–response hypothesis, the oldest woody growth produced modest increases in thickness (Hoffman & Tomescu, 2013; Strullu‐Derrien et al ., 2014; Gerrienne & Gensel, 2016; Pfeiler & Tomescu, 2021) that resulted in low levels of tensional stress in the outermost layers of the axes, below the threshold that would elicit formation of canonical periderm. It is, thus, possible that early vascular plants that were deploying periderm as a wound response did not need canonical periderm because their vascular cambium did not produce significant increase in girth.…”

“…The fossil flora of the Battery Point Formation, studied ever since the mid‐19 th century (Dawson, 1859), has recently yielded a diversity of permineralized taxa that contribute to the understanding of early tracheophyte anatomy, phylogeny, and development (Bickner & Tomescu, 2019; Durieux et al ., 2021; Pfeiler & Tomescu, 2021; Toledo et al ., 2021; Tomescu & McQueen, 2022). Secondary growth, a major structural innovation in plants until recently thought to have evolved in the Middle Devonian, has been shown to have arisen much earlier (Gerrienne et al ., 2011) and has been documented in several plant types of the Gaspé flora that produced secondary xylem (Hoffman & Tomescu, 2013; Pfeiler & Tomescu, 2021; Toledo et al ., 2021).…”

Taxon sampling and alternative hypotheses of relationships in the euphyllophyte plexus that gave rise to seed plants: insights from an Early Devonian radiatopsid

“…Indeed, the accumulation curve of morphological diversity among Early Devonian plants has not plateaued yet; most newly discovered Early Devonian plants (e.g. Bickner & Tomescu, 2019; Pfeiler & Tomescu, 2021) possess novel combinations of the characters typical of multiple younger (Middle or Late Devonian) lineages. When added to phylogenetic matrices, each such new taxon alters character polarisation, and may act as a wildcard taxon (as does Kenrickia ), consequently affecting patterns of relationship.…”

A new phylogeny of the cladoxylopsid plexus: contribution of an early cladoxylopsid from the Lower Devonian (Emsian) of Quebec

“…These Early Devonian (Emsian; McGregor, 1977) deposits host plants preserved as carbonaceous compressions and permineralizations. The plant fossils of the Battery Point Formation have been studied ever since the first report by Dawson (1859) and represent the most diverse Early Devonian flora known in North America, including 12 species described to date based on anatomically preserved specimens: Crenaticaulis verruculosus Banks and Davis (1969); Psilophyton dawsonii Banks et al (1975); Psilophyton forbesii Gensel (1979); Drepanophycus spinaeformis Hartman (1981); Gensel's (1984) unnamed plant; Franhueberia gerriennei Hoffman and Tomescu (2013); Eddianna gaspiana Pfeiler and Tomescu (2018); Leptocentroxyla tetrarcha , Stenoloboxyla ambigua , Jowingera triloba , and Tainioxyla quebecana Bickner and Tomescu (2019); and Gmujij tetraxylopteroides Pfeiler and Tomescu (2020).…”