Evidence linking life-form to a major shift in diversification rate in Crassula

Premise Plants have evolved different ecological strategies in response to environmental challenges, and a higher lability of such strategies is more common in plant groups that adapt to various niches. Crassula (Crassulaceae), occurring in varied mesic to xeric habitats, exhibits a remarkable diversity of life-forms. However, whether any particular life-form trait has shaped species diversification in Crassula has remained unexplored. This study aims to investigate diversification patterns within Crassula and identify potential links to its life-form evolution. Methods A phylogenetic tree of 140 Crassula taxa was reconstructed using plastid and nuclear loci and dated based on the nuclear DNA information only. We reconstructed ancestral life-form characters to estimate the evolutionary trends of ecophysiological change, and subsequently estimated net diversification rates. Multiple diversification models were applied to examine the association between certain life-forms and net diversification rates. Results Our findings confirm a radiation within Crassula in the last 10 million years. A configuration of net diversification rate shifts was detected, which coincides with the emergence of a speciose lineage during the late Miocene. The results of ancestral state reconstruction demonstrate a high lability of life-forms in Crassula, and the trait-dependent diversification analyses revealed that the increased diversification is strongly associated with a compact growth form. Conclusions Transitions between life-forms in Crassula seem to have driven adaptation and shaped diversification of this genus across various habitats. The diversification patterns we inferred are similar to those observed in other major succulent lineages, with the most-speciose clades originating in the late Miocene

Defining the scope for altering rice leaf anatomy to improve photosynthesis: a modelling approach.

Leaf structure plays an important role in photosynthesis. However, the causal relationship and the quantitative importance of any single structural parameter to the overall photosynthetic performance of a leaf remains open to debate. In this paper, we report on a mechanistic model, eLeaf, which successfully captures rice leaf photosynthetic performance under varying environmental conditions of light and CO2. We developed a 3D reaction-diffusion model for leaf photosynthesis parameterised using a range of imaging data and biochemical measurements from plants grown under ambient and elevated CO2 and then interrogated the model to quantify the importance of these elements. The model successfully captured leaf-level photosynthetic performance in rice. Photosynthetic metabolism underpinned the majority of the increased carbon assimilation rate observed under elevated CO2 levels, with a range of structural elements making positive and negative contributions. Mesophyll porosity could be varied without any major outcome on photosynthetic performance, providing a theoretical underpinning for experimental data. eLeaf allows quantitative analysis of the influence of morphological and biochemical properties on leaf photosynthesis. The analysis highlights a degree of leaf structural plasticity with respect to photosynthesis of significance in the context of attempts to improve crop photosynthesis

Elastic and collapsible:current understanding of cell walls in succulent plants

Succulent plants represent a large functional group of drought-resistant plants which store water in specialized tissues. Several co-adaptive traits accompany water-storage capacity to constitute the succulent syndrome. A widely reported anatomical adaptation of cell walls in succulent tissues allows them to fold in a regular fashion during extended drought, thus preventing irreversible damage and allowing for reversible volume changes. Although ongoing research on crop and model species continuously reports the importance of cell walls and their dynamics in drought resistance, cell walls of succulent plants have received relatively little attention to date, despite the potential of succulents as natural capital to mitigate the effects of climate change. In this review, we summarize the current knowledge of cell walls in drought-avoiding succulents and their effects on tissue biomechanics, water relations and photosynthesis. We also highlight the existing knowledge gaps and propose a hypothetical model for regulated cell wall folding in succulent tissues upon dehydration. Future perspectives of methodological development in succulent cell wall characterization, including the latest technological advances in molecular and imaging techniques, are also presented

Cell wall polysaccharide and glycoprotein content tracks growth‐form diversity and an aridity gradient in the leaf‐succulent genus.

Cell wall traits are believed to be a key component of the succulent syndrome, an adaptive syndrome to drought, yet the variability of such traits remains largely unknown. In this study, we surveyed the leaf polysaccharide and glycoprotein composition in a wide sampling of species that occur naturally along an aridity gradient in southern Africa, and we interpreted its adaptive significance in relation to growth form and arid adaptation. To study the glycomic diversity, we sampled leaf material from 56 taxa and performed comprehensive microarray polymer profiling to obtain the relative content of cell wall polysaccharides and glycoproteins. This analysis was complemented by the determination of monosaccharide composition and immunolocalization in leaf sections using glycan‐targeting antibodies. We found that compact and non‐compact species occupy distinct phenotypic spaces in terms of leaf glycomics, particularly in regard to rhamnogalacturonan I, its arabinan side chains, and arabinogalactan proteins (AGPs). Moreover, these cell wall components also correlated positively with increasing aridity, which suggests that they are likely advantageous in terms of arid adaptation. These differences point to compact species having more elastic cell walls with plasticizing properties, which can be interpreted as an adaptation toward increased drought resistance. Furthermore, we report an intracellular pool of AGPs associated with oil bodies and calcium oxalate crystals, which could be a peculiarity of and could be linked to increased drought resistance. Our results indicate that glycomics may be underlying arid adaptation and drought resistance in succulent plants

Evolutionary success in arid habitats: Morpho-anatomy of succulent leaves of Crassula species from southern Africa

Succulence is widely interpreted as an adaptation to drought, usually associated with CAM and xeromorphic features among arid-adapted plants. However, this syndrome can also be observed in species typical of mesic and even hydric environments. The leaf-succulent genus Crassula (Crassulaceae) occurs in contrasting habitats in all nine biomes of southern Africa. This study represents the first to compare leaf traits in Crassula species which in nature are confined to diverse habitats in southern Africa. To determine their potential adaptive significance, we investigated leaf succulence and several morpho-anatomical traits of five southern African Crassula species (C. ausensis, C. brevifolia, C. multicava, C. nudicaulis, C. tecta), which occur naturally in habitats of differing aridity; all plants were grown under glasshouse conditions. For each species, we recorded water content, leaf anatomy, and leaf surface structure and hydrophobicity. We found that water content is relatively consistent in Crassula regardless of natural habitat. In contrast, most leaf morpho-anatomical traits examined here are related to macroclimatic conditions. We hypothesize that differences in mesophyll traits in Crassula are potentially linked to water storage and CAM performance, while differences in leaf surface properties are more closely related to water conservation and probably also to water uptake through hydathodes

Evidence linking life-form to a major shift in diversification rate in <i>Crassula</i>

Premise Plants have evolved different ecological strategies in response to environmental challenges, and a higher lability of such strategies is more common in plant groups that adapt to various niches. Crassula (Crassulaceae), occurring in varied mesic to xeric habitats, exhibits a remarkable diversity of life-forms. However, whether any particular life-form trait has shaped species diversification in Crassula has remained unexplored. This study aims to investigate diversification patterns within Crassula and identify potential links to its life-form evolution. Methods A phylogenetic tree of 140 Crassula taxa was reconstructed using plastid and nuclear loci and dated based on the nuclear DNA information only. We reconstructed ancestral life-form characters to estimate the evolutionary trends of ecophysiological change, and subsequently estimated net diversification rates. Multiple diversification models were applied to examine the association between certain life-forms and net diversification rates. Results Our findings confirm a radiation within Crassula in the last 10 million years. A configuration of net diversification rate shifts was detected, which coincides with the emergence of a speciose lineage during the late Miocene. The results of ancestral state reconstruction demonstrate a high lability of life-forms in Crassula, and the trait-dependent diversification analyses revealed that the increased diversification is strongly associated with a compact growth form. Conclusions Transitions between life-forms in Crassula seem to have driven adaptation and shaped diversification of this genus across various habitats. The diversification patterns we inferred are similar to those observed in other major succulent lineages, with the most-speciose clades originating in the late Miocene

Revisiting an ecophysiological oddity: Hydathode‐mediated foliar water uptake in Crassula species from southern Africa.

Hydathodes are usually associated with water exudation in plants. However, foliar water uptake (FWU) through the hydathodes has long been suspected in the leaf‐succulent genus (Crassulaceae), a highly diverse group in southern Africa, and, to our knowledge, no empirical observations exist in the literature that unequivocally link FWU to hydathodes in this genus. FWU is expected to be particularly beneficial on the arid western side of southern Africa, where up to 50% of species occur and where periodically high air humidity leads to fog and/or dew formation. To investigate if hydathode‐mediated FWU is operational in different species, we used the apoplastic fluorescent tracer Lucifer Yellow in combination with different imaging techniques. Our images of dye‐treated leaves confirm that hydathode‐mediated FWU does indeed occur in and that it might be widespread across the genus. Hydathodes in serve as moisture‐harvesting structures, besides their more common purpose of guttation, an adaptation that has likely played an important role in the evolutionary history of the genus. Our observations suggest that ability for FWU is independent of geographical distribution and not restricted to arid environments under fog influence, as FWU is also operational in species from the rather humid eastern side of southern Africa. Our observations point towards no apparent link between FWU ability and overall leaf surface wettability in . Instead, the hierarchically sculptured leaf surfaces of several species may facilitate FWU due to hydrophilic leaf surface microdomains, even in seemingly hydrophobic species. Overall, these results confirm the ecophysiological relevance of hydathode‐mediated FWU in and reassert the importance of atmospheric humidity for some arid‐adapted plant groups. This study demonstrates that foliar water uptake (FWU) through hydathodes, previously suspected but unconfirmed, is indeed operational in most species. This phenomenon occurs across different habitats and highlights the ecophysiological relevance of atmospheric humidity for these plants

Are cell wall traits a component of the succulent syndrome?

Succulence is an adaptation to low water availability characterised by the presence of water-storage tissues that alleviate water stress under low water availability. The succulent syndrome has evolved convergently in over 80 plant families and is associated with anatomical, physiological and biochemical traits. Despite the alleged importance of cell wall traits in drought responses, their significance in the succulent syndrome has long been overlooked. Here, by analyzing published pressure–volume curves, we show that elastic adjustment, whereby plants change cell wall elasticity, is uniquely beneficial to succulents for avoiding turgor loss. In addition, we used comprehensive microarray polymer profiling (CoMPP) to assess the biochemical composition of cell walls in leaves. Across phylogenetically diverse species, we uncover several differences in cell wall biochemistry between succulent and non-succulent leaves, pointing to the existence of a ‘succulent glycome’. We also highlight the glycomic diversity among succulent plants, with some glycomic features being restricted to certain succulent lineages. In conclusion, we suggest that cell wall biomechanics and biochemistry should be considered among the characteristic traits that make up the succulent syndrome

Mesophyll porosity is modulated by the presence of functional stomata

The formation of stomata and leaf mesophyll airspace must be coordinated to establish an efficient and robust network that facilitates gas exchange for photosynthesis, however the mechanism by which this coordinated development occurs remains unclear. Here, we combine microCT and gas exchange analyses with measures of stomatal size and patterning in a range of wild, domesticated and transgenic lines of wheat and Arabidopsis to show that mesophyll airspace formation is linked to stomatal function in both monocots and eudicots. Our results support the hypothesis that gas flux via stomatal pores influences the degree and spatial patterning of mesophyll airspace formation, and indicate that this relationship has been selected for during the evolution of modern wheat. We propose that the coordination of stomata and mesophyll airspace pattern underpins water use efficiency in crops, providing a target for future improvement