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      Allometric relationships between leaf and petiole traits across 31 floating-leaved plants reveal a different adaptation pattern from terrestrial plants

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          Abstract

          Background and Aims

          Allometric scaling between stomata and xylem for terrestrial woody plants is a widely observed pattern that may be constrained by water transport. Floating-leaved plants, a particular life form of aquatic plants, have leaves in direct contact with both air and water and a poorly developed xylem that may not be limited by water supply as for terrestrial plants. However, whether such an allometric scaling relationship still exists in floating-leaved plants has not been explored.

          Methods

          We analysed 31 floating-leaved species/varieties with a range in leaf area covering six orders of magnitude. For all 31 floating-leaved plants, we studied the allometric relationships between leaf area and petiole transverse area, and between total stomatal area and petiole vascular area.

          Key Results

          The slopes of both relationships were similar to the slope of the allometric relationship (1.23) between total stomatal area and xylem area of 53 terrestrial plants. However, for ten of them with xylem that can be clearly defined, the strong positive relationship between total stomatal area and petiole xylem area had a significantly smaller slope than that of terrestrial plants (0.64 vs. 1.23). Furthermore, after considering phylogeny, the scaling relationships between total stomatal area and petiole traits in floating-leaved plants remained significant.

          Conclusions

          We speculated that for floating-leaved plants, the hyperallometric relationship (slope >1) between the construction of leaf/stoma and petiole was promoted by the high demand for photosynthesis and thus more leaves/stomata. While the hypoallometric relationship (slope <1) between stomatal and xylem area was related more to hydraulic processes, the selection pressure on stomata was lower than xylem of floating-leaved plants. Allometric relationships among the hydraulic traits on water transport of aquatic plants are the result of natural selection to achieve maximum carbon gain, which is similar to terrestrial plants.

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          Most cited references50

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          Testing for phylogenetic signal in comparative data: behavioral traits are more labile.

          The primary rationale for the use of phylogenetically based statistical methods is that phylogenetic signal, the tendency for related species to resemble each other, is ubiquitous. Whether this assertion is true for a given trait in a given lineage is an empirical question, but general tools for detecting and quantifying phylogenetic signal are inadequately developed. We present new methods for continuous-valued characters that can be implemented with either phylogenetically independent contrasts or generalized least-squares models. First, a simple randomization procedure allows one to test the null hypothesis of no pattern of similarity among relatives. The test demonstrates correct Type I error rate at a nominal alpha = 0.05 and good power (0.8) for simulated datasets with 20 or more species. Second, we derive a descriptive statistic, K, which allows valid comparisons of the amount of phylogenetic signal across traits and trees. Third, we provide two biologically motivated branch-length transformations, one based on the Ornstein-Uhlenbeck (OU) model of stabilizing selection, the other based on a new model in which character evolution can accelerate or decelerate (ACDC) in rate (e.g., as may occur during or after an adaptive radiation). Maximum likelihood estimation of the OU (d) and ACDC (g) parameters can serve as tests for phylogenetic signal because an estimate of d or g near zero implies that a phylogeny with little hierarchical structure (a star) offers a good fit to the data. Transformations that improve the fit of a tree to comparative data will increase power to detect phylogenetic signal and may also be preferable for further comparative analyses, such as of correlated character evolution. Application of the methods to data from the literature revealed that, for trees with 20 or more species, 92% of traits exhibited significant phylogenetic signal (randomization test), including behavioral and ecological ones that are thought to be relatively evolutionarily malleable (e.g., highly adaptive) and/or subject to relatively strong environmental (nongenetic) effects or high levels of measurement error. Irrespective of sample size, most traits (but not body size, on average) showed less signal than expected given the topology, branch lengths, and a Brownian motion model of evolution (i.e., K was less than one), which may be attributed to adaptation and/or measurement error in the broad sense (including errors in estimates of phenotypes, branch lengths, and topology). Analysis of variance of log K for all 121 traits (from 35 trees) indicated that behavioral traits exhibit lower signal than body size, morphological, life-history, or physiological traits. In addition, physiological traits (corrected for body size) showed less signal than did body size itself. For trees with 20 or more species, the estimated OU (25% of traits) and/or ACDC (40%) transformation parameter differed significantly from both zero and unity, indicating that a hierarchical tree with less (or occasionally more) structure than the original better fit the data and so could be preferred for comparative analyses.
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            The role of stomata in sensing and driving environmental change.

            Stomata, the small pores on the surfaces of leaves and stalks, regulate the flow of gases in and out of leaves and thus plants as a whole. They adapt to local and global changes on all timescales from minutes to millennia. Recent data from diverse fields are establishing their central importance to plant physiology, evolution and global ecology. Stomatal morphology, distribution and behaviour respond to a spectrum of signals, from intracellular signalling to global climatic change. Such concerted adaptation results from a web of control systems, reminiscent of a 'scale-free' network, whose untangling requires integrated approaches beyond those currently used.
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              Three keys to the radiation of angiosperms into freezing environments.

              Early flowering plants are thought to have been woody species restricted to warm habitats. This lineage has since radiated into almost every climate, with manifold growth forms. As angiosperms spread and climate changed, they evolved mechanisms to cope with episodic freezing. To explore the evolution of traits underpinning the ability to persist in freezing conditions, we assembled a large species-level database of growth habit (woody or herbaceous; 49,064 species), as well as leaf phenology (evergreen or deciduous), diameter of hydraulic conduits (that is, xylem vessels and tracheids) and climate occupancies (exposure to freezing). To model the evolution of species' traits and climate occupancies, we combined these data with an unparalleled dated molecular phylogeny (32,223 species) for land plants. Here we show that woody clades successfully moved into freezing-prone environments by either possessing transport networks of small safe conduits and/or shutting down hydraulic function by dropping leaves during freezing. Herbaceous species largely avoided freezing periods by senescing cheaply constructed aboveground tissue. Growth habit has long been considered labile, but we find that growth habit was less labile than climate occupancy. Additionally, freezing environments were largely filled by lineages that had already become herbs or, when remaining woody, already had small conduits (that is, the trait evolved before the climate occupancy). By contrast, most deciduous woody lineages had an evolutionary shift to seasonally shedding their leaves only after exposure to freezing (that is, the climate occupancy evolved before the trait). For angiosperms to inhabit novel cold environments they had to gain new structural and functional trait solutions; our results suggest that many of these solutions were probably acquired before their foray into the cold.
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                Author and article information

                Contributors
                Journal
                Ann Bot
                Ann Bot
                annbot
                Annals of Botany
                Oxford University Press (US )
                0305-7364
                1095-8290
                16 February 2023
                19 January 2023
                19 January 2023
                : 131
                : 3
                : 545-552
                Affiliations
                Aquatic Plants Research Center, Wuhan Botanical Garden, Chinese Academy of Sciences , Wuhan 430074, China
                University of Chinese Academy of Sciences , Beijing 100049, China
                Freshwater Biological Laboratory, Department of Biology, University of Copenhagen , Copenhagen 2100, Denmark
                Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystem, South China Botanical Garden, Chinese Academy of Sciences , Guangzhou 510650, China
                South China National Botanical Garden , Guangzhou 510650, China
                Freshwater Biological Laboratory, Department of Biology, University of Copenhagen , Copenhagen 2100, Denmark
                Aquatic Plants Research Center, Wuhan Botanical Garden, Chinese Academy of Sciences , Wuhan 430074, China
                Research Center for Ecology, College of Science, Tibet University , Lhasa 850000, China
                Aquatic Plants Research Center, Wuhan Botanical Garden, Chinese Academy of Sciences , Wuhan 430074, China
                Center for Plant Ecology, Core Botanical Gardens, Chinese Academy of Sciences , Wuhan 430074, China
                Horticulture and Conservation Centre, Wuhan Botanical Garden, Chinese Academy of Sciences , Wuhan 430074, China
                Aquatic Plants Research Center, Wuhan Botanical Garden, Chinese Academy of Sciences , Wuhan 430074, China
                Author notes
                Author information
                https://orcid.org/0000-0001-6208-7285
                https://orcid.org/0000-0003-4027-499X
                https://orcid.org/0000-0003-4310-2544
                https://orcid.org/0000-0003-2716-6580
                Article
                mcad007
                10.1093/aob/mcad007
                10072084
                36655615
                a6b7eaa1-6010-44ba-8858-41a0b8d6848e
                © The Author(s) 2023. Published by Oxford University Press on behalf of the Annals of Botany Company.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 03 October 2022
                : 17 December 2022
                : 13 January 2023
                : 06 January 2023
                : 31 March 2023
                Page count
                Pages: 8
                Funding
                Funded by: National Natural Science Foundation of China, DOI 10.13039/501100001809;
                Award ID: 31870345
                Funded by: China Scholarship Council, DOI 10.13039/501100004543;
                Award ID: 202104910381
                Funded by: Chinese Academy of Sciences, DOI 10.13039/501100002367;
                Award ID: 2019339
                Categories
                Original Articles
                AcademicSubjects/SCI01080
                AcademicSubjects/SCI01130
                AcademicSubjects/SCI01210

                Plant science & Botany
                stoma,xylem,vascular,water transport,phylogeny,evolution,aquatic plant
                Plant science & Botany
                stoma, xylem, vascular, water transport, phylogeny, evolution, aquatic plant

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