Quantitative mesophyll parameters rather than whole‐leaf traits predict response of C₃ steppe plants to aridity

Abstract

We studied the impact of aridity on leaf and mesophyll traits in dominant and very abundant plant species of Eurasian steppe plant communities. We covered a 500-km latitudinal gradient across three vegetation zones in the Volga region of southern European Russia. Whole-leaf traits, volumetric fractions of leaf tissues, quantitative parameters of photosynthetic cells and chloroplasts, and chlorophyll, carbon (C) and nitrogen (N) contents were analyzed and related to plant functional type (PFT), type of mesophyll anatomy, phylogeny and climate aridity. The proportions of prevailing PFTs in the communities, such as C monocots, C dicots with dorsiventral and isopalisade anatomy and C dicots, changed with increasing aridity which influenced the whole-leaf parameters and tissue composition in the leaf. Leaf mass per unit area and leaf thickness slightly increased along the aridity gradient, but the most significant changes were observed in the mesophyll. Mesophyll cell surface area, chloroplast number and chloroplast surface area per unit leaf area were higher in C plants growing in the desert steppe compared with those of the forest steppe, while chlorophyll content per single chloroplast and per unit N content as well chlorophyll a/b ratio decreased. Our results identify a suite of mesophyll traits as a typical 'syndrome' of increasingly drought-adapted steppe plants.

Leaf traits of C3- and C4-plants indicating climatic adaptation along a latitudinal gradient in Southern Siberia and Mongolia

“…Cell projection area and perimeter were measured separately for each type of photosynthetic tissue (palisade and spongy mesophyll for C 3 -plants, mesophyll and bundle sheath cells for C 4 -plants, simple and segmented mesophyll cells for grasses) with a light microscope (Axiostar plus, Zeiss, Germany) and the image analysis system SIAMS Mesoplant (SIAMS, Yekaterinburg, Russia). The mesophyll cell volume (V cel , 10 3 μm 3 ) and the chloroplast volume (V chl, μm 3 ) as well as their surface areas (S cel , 10 3 μm 2 , and S chl , μm 2 ) were calculated by the projection method described in detail by Ivanova and Pyankov (2002) and Ivanova et al (2018). Chloroplast number per cell (Chl per cell) was determined in 30 replicates per sample in the same cells that were measured for cell sizes.…”

“…Instead of individual parameters of cells or chloroplasts, the most promising traits are integral parameters of photosynthetic tissues as the total chloroplast number per leaf area (N chl /A) and the total surface area of chloroplasts (A chl /A) and cells (A mes /A) per leaf area. These functional leaf traits were shown to predict the response of C 3plants to climate in different climatic zones inside Russia-European steppes (Ivanova et al, 2018). The site-mean values of N chl /A, A chl /A and A mes /A were higher in steppe than in boreal plants, and in C 3 -plants growing in the desert steppe compared with those of the forest steppe.…”

“…High abundance of plants with C 4 -type photosynthesis in arid climates is attributed to high water use efficiency, high photosynthetic temperature optimum, a stable quantum yield at high temperatures and other favorable physiological peculiarities (Black, 1971(Black, , 1973Ehleringer, 1978;Ehleringer et al, 1997;Pyankov et al, 2000). Photosynthetic functioning of C 3 -plants is tightly linked to spatial mesophyll structure in mature leaves (Laisk et al, 1970;Nobel and Walker, 1985;Terashima et al, 2001Terashima et al, , 2011Evans et al, 2009;Tosens et al, 2012;Flexas et al, 2013), therefore quantitative mesophyll parameters are considered to be good indicators of C 3 -plants response to climate (Mokronosov, 1981;Pyankov and Mokronosov, 1993;Ivanova et al, 2018). Instead of individual parameters of cells or chloroplasts, the most promising traits are integral parameters of photosynthetic tissues as the total chloroplast number per leaf area (N chl /A) and the total surface area of chloroplasts (A chl /A) and cells (A mes /A) per leaf area.…”

A role for ecophysiology in the ’omics’ era

“…This diffusion pathway is complex, as it involves air, aqueous and lipid phases; namely intercellular air spaces, cell walls, plasma membrane, cytosol, chloroplast membrane, and stroma. In a recent study, Ivanova et al (2018) quantitatively analyzed the internal structures of leaves from many C3 steppe plant species using only chemical and microscopy techniques. They concluded that larger mesophyll and chloroplast surface areas per total leaf area (S c /S) were very indicative of plant adaptation to increasing aridity, speculating on the relationship between these characters and g m , photosynthesis, etc.…”

Interactive effect of leaf age and ozone on mesophyll conductance in Siebold's beech

“…Mesophyll conductance is generally lower in leaves with thicker cell walls and greater leaf density (Adachi et al 2013, Ivanova et al 2018) that are conditions limiting the diffusion of CO 2 in the leaf liquid phase (Tomás et al 2013, Onoda et al 2017). Ozone may affect leaf morphology, which is likely to modify the CO 2 diffusion inside leaves (Heath 1994, Moura et al 2018).…”