Environmental and Experimental Botany 187 (2021) 104495 Available online 26 April 2021 0098-8472/© 2021 Elsevier B.V. All rights reserved. Anatomical adaptations in aquatic and wetland dicot plants: Disentangling the environmental, morphological and evolutionary signals Jiˇrí Doleˇzal a, b, *, Andrea Kuˇcerov´ a a , Veronika Jandov´ a a , Adam Klimeˇs a, c , Pavel ˇ Ríha a , Lubomír Adamec a , Fritz Hans Schweingruber d a Institute of Botany of the Czech Academy of Science, Dukelsk´ a 135, CZ-379 01, Tˇreboˇ n, Czech Republic b Faculty of Science, University of South Bohemia, Braniˇsovsk´ a 31, CZ-370 05, ˇ Cesk´e Budˇejovice, Czech Republic c Faculty of Science, Charles University, Ovocný trh 560/5, CZ-116 36, Praha 1, Czech Republic d Swiss Federal Research Institute WSL, Birmensdorf, Switzerland A R T I C L E INFO Keywords: Comparative plant anatomy Evolutionary adaptation Gradient analysis Dicot forbs Europe ABSTRACT Understanding how plants adjust their internal structures to withstand adverse environmental conditions is vital for predicting their responses to ongoing environmental change. Plants have repeatedly evolved small water transporting conduits and large storage parenchyma tissues to cope with anoxia, freezing- or drought-induced damages. However, how these adaptations evolved in unrelated taxa across hydrological and thermal gradients, remains unclear. Here we show that stem anatomical variations in 212 European aquatic and wetland dicots are driven by thermal and hydrological constraints via control over plant size, growth form, and leaf traits, while phylogenetic constraints have only a weak effect. Phylogenetic comparative analyses controlling for confounding factors showed that both waterlogging (anoxia) and low-temperature promote smaller plants with reduced vessel conduits and limited lignification, but extended parenchyma and hence storage and tissue renewal capacity to secure resilience to biomass loss induced by running water or frost disturbances. Decreasing water depth and anoxia promote larger wetland plants with thick-walled libriform fibers, large vessels with simple perforation plates securing high hydraulic efficiency, and semi-ring porous xylem with wide earlywood vessels in spring and narrow latewood vessels in summer, providing both efficiency and safety in water transport. The aquatic envi- ronment promotes plants with a large cortex zone with photosynthetic chlorenchyma and starch-storing pa- renchyma cells along with extensive air spaces that provide aeration and buoyancy. Low temperatures promote short-stature forbs with smaller vessels, scalariform perforation plate, extended parenchyma, resulting in reduced embolism risk. Although most anatomical variation was explained by differences between aquatic and wet terrestrial growth forms, environmental gradients, plant size, and leaf properties exerted a significant control on plant tissue structures not confounded by phylogenetic inertia. Distinct habitats, spread across broad thermal and hydrological gradients, harbor unrelated species with different evolutionary histories that have converged to similar anatomical and hence morphological structures. 1. Introduction During their evolution, vascular plants have developed specific ad- aptations to withstand adverse environmental conditions and utilize to their maximal benefit the nutrients and other conditions prevailing therein. While plant strategies for coping with adverse conditions are usually characterized by morphological, ecophysiological, and repro- ductive adaptations (Kleyer et al., 2008), plant anatomy has been studied less frequently (Rascio, 2002; Schweingruber et al., 2020). Detailed knowledge of plant anatomical characteristics and their vari- ation across species and habitats is both rare and limited mainly to woody species (e.g. Greguss, 1945; Schweingruber, 1990; Neumann et al., 2001; Schweingruber et al., 2013). Anatomical analysis of herbs has recently become of interest (Schweingruber et al., 2013; Crivellaro and Schweingruber, 2015; Schweingruber and Berger, 2019), as many herbs also develop annual rings as they age. However, these studies * Corresponding author at: Institute of Botany of the Czech Academy of Science, Dukelsk´ a 135, CZ-379 01, Tˇreboˇ n, Czech Republic. E-mail addresses: Jiri.Dolezal@ibot.cas.cz (J. Doleˇzal), Andrea.Kucerova@ibot.cas.cz (A. Kuˇcerov´ a), VeronikaLangova@seznam.cz (V. Jandov´a), adam.klimes@ ibot.cas.cz (A. Klimeˇs), pavel.riha.cb@centrum.cz (P. ˇ Ríha), lubomir.adamec@ibot.cas.cz (L. Adamec), fritz.schweingruber@wsl.ch (F.H. Schweingruber). Contents lists available at ScienceDirect Environmental and Experimental Botany journal homepage: www.elsevier.com/locate/envexpbot https://doi.org/10.1016/j.envexpbot.2021.104495 Received 8 December 2020; Received in revised form 20 April 2021; Accepted 21 April 2021