Stomatal evolution and plant adaptation to future climate.

Global climate change is affecting plant photosynthesis and transpiration processes, as well as increasing weather extremes impacting socio-political and environmental events and decisions for decades to come. One major research challenge in plant biology and ecology is the interaction of photosynthesis with the environment. Stomata control plant gas exchange and their evolution was a crucial innovation that facilitated the earliest land plants to colonize terrestrial environments. Stomata couple homoiohydry, together with cuticles, intercellular gas space, with the endohydric water-conducting system, enabling plants to adapt and diversify across the planet. Plants control stomatal movement in response to environmental change through regulating guard cell turgor mediated by membrane transporters and signaling transduction. However, the origin, evolution, and active control of stomata remain controversial topics. We first review stomatal evolution and diversity, providing fossil and phylogenetic evidence of their origins. We summarize functional evolution of guard cell membrane transporters in the context of climate changes and environmental stresses. Our analyses show that the core signaling elements of stomatal movement are more ancient than stomata, while genes involved in stomatal development co-evolved de novo with the earliest stomata. These results suggest that novel stomatal development-specific genes were acquired during plant evolution, whereas genes regulating stomatal movement, especially cell signaling pathways, were inherited ancestrally and co-opted by dynamic functional differentiation. These two processes reflect the different adaptation strategies during land plant evolution.

Molecular evolution and interaction of 14-3-3 proteins with H+-ATPases in plant abiotic stresses.

Environmental stresses severely affect plant growth and crop productivity. Regulated by 14-3-3 proteins (14-3-3s), H+-ATPases (AHAs) are important proton pumps that can induce diverse secondary transport via channels and co-transporters for the abiotic stress response of plants. Many studies demonstrated the roles of 14-3-3s and AHAs in coordinating the processes of plant growth, phytohormone signaling, and stress responses. However, the molecular evolution of 14-3-3s and AHAs has not been summarized in parallel with evolutionary insights across multiple plant species. Here, we comprehensively review the roles of 14-3-3s and AHAs in cell signaling to enhance plant responses to diverse environmental stresses. We analyzed the molecular evolution of key proteins and functional domains that are associated with 14-3-3s and AHAs in plant growth and hormone signaling. The results revealed evolution, duplication, contraction, and expansion of 14-3-3s and AHAs in green plants. We also discussed the stress-specific expression of those 14-3-3and AHA genes in a eudicotyledon (Arabidopsis thaliana), a monocotyledon (Hordeum vulgare), and a moss (Physcomitrium patens) under abiotic stresses. We propose that 14-3-3s and AHAs respond to abiotic stresses through many important targets and signaling components of phytohormones, which could be promising to improve plant tolerance to single or multiple environmental stresses.

Allene oxide synthase 1 contributes to limiting grain arsenic accumulation and seedling detoxification in rice.

Arsenic (As) is a cancerogenic metalloid ubiquitously distributed in the environment, which can be easily accumulated in food crops like rice. Jasmonic acid (JA) and its derivatives play critical roles in plant growth and stress response. However, the role of endogenous JA in As accumulation and detoxification is still poorly understood. In this study, we found that JA biosynthesis enzymes Allene Oxide Synthases, OsAOS1 and OsAOS2, regulate As accumulation and As tolerance in rice. Evolutionary bioinformatic analysis indicated that AOS1 and AOS2 have evolved from streptophyte algae (e.g. the basal lineage Klebsormidium flaccidum) - sister clade of land plants. Compared to other two AOSs, OsAOS1 and OsAOS2 were highly expressed in all examined rice tissues and their transcripts were highly induced by As in root and shoot. Loss-of-function of OsAOS1 (osaos1-1) showed elevated As concentration in grains, which was likely attributed to the increased As translocation from root to shoot when the plants were subjected to arsenate [As(V)] but not arsenite [As (III)]. However, the mutation of OsAOS2 (osaos2-1) showed no such effect. Moreover, osaos1-1 and osaos2-1 increased the sensitivity of rice plants to both As(V) and As(III). Disrupted expression of genes involved in As accumulation and detoxification, such as OsPT4, OsNIP3;2, and OsOASTL-A1, was observed in both osaos1-1 and osaos2-1 mutant lines. In addition, a As(V)-induced significant decrease in Reactive Oxygen Species (ROS) production was observed in the root of osaos1-1 but not in osaos2-1. Taken together, our results indicate OsAOS1 modulates both As allocation and detoxification, which could be partially attributed to the altered gene expression profiling and ROS homeostasis in rice while OsAOS2 is important for As tolerance.

A vacuolar transporter plays important roles in zinc and cadmium accumulation in rice grain.

Rice grain is a poor dietary source of zinc (Zn) but the primary source of cadmium (Cd) for humans; however, the molecular mechanisms for their accumulation in rice grain remain incompletely understood. This study functionally characterized a tonoplast-localized transporter, OsMTP1. OsMTP1 was preferentially expressed in the roots, aleurone layer, and embryo of seeds. OsMTP1 knockout decreased Zn concentration in the root cell sap, roots, aleurone layer and embryo, and subsequently increased Zn concentration in shoots and polished rice (endosperm) without yield penalty. OsMTP1 haplotype analysis revealed elite alleles associated with increased Zn level in polished rice, mostly because of the decreased OsMTP1 transcripts. OsMTP1 expression in yeast enhanced Zn tolerance but did not affect that of Cd. While OsMTP1 knockout resulted in decreased uptake, translocation and accumulation of Cd in plant and rice grain, which could be attributed to the indirect effects of altered Zn accumulation. Our results suggest that rice OsMTP1 primarily functions as a tonoplast-localized transporter for sequestrating Zn into vacuole. OsMTP1 knockout elevated Zn concentration but prevented Cd deposition in polished rice without yield penalty. Thus, OsMTP1 is a candidate gene for enhancing Zn level and reducing Cd level in rice grains.

Hydrogen peroxide reduces root cadmium uptake but facilitates root-to-shoot cadmium translocation in rice through modulating cadmium transporters.

Cadmium (Cd) contamination in agricultural soils has become a serious worldwide environmental problem threatening crop production and human health. Hydrogen peroxide (H2O2) is a critical second messenger in plant response to Cd exposure. However, its role in Cd accumulation in various organs of plants and the mechanistic basis of this regulation remains to be elucidated. In this study, we used electrophysiological and molecular approaches to understand how H2O2 regulates Cd uptake and translocation in rice plants. Our results showed that the pretreatment of H2O2 significantly reduced Cd uptake by rice roots, which was associated with the downregulation of OsNRAMP1 and OsNRAMP5. On the other hand, H2O2 promoted the root-to-shoot translocation of Cd, which might be attributed to the upregulation of OsHMA2 critical for Cd2+ phloem loading and the downregulation of OsHMA3 involved in the vacuolar compartmentalization of Cd2+, leading to the increased Cd accumulation in rice shoots. Furthermore, such regulatory effects of H2O2 on Cd uptake and translocation were notably amplified by the elevated level of exogenous calcium (Ca). Collectively, our results suggest that H2O2 can inhibit Cd uptake but increase root to shoot translocation through modulating the transcriptional levels of genes encoding Cd transporters, furthermore, application of Ca can amplify this effect. These findings will broaden our understanding of the regulatory mechanisms of Cd transport in rice plants and provide theoretical foundation for breeding rice for low Cd accumulation.

Physiological and transcriptomic evidence of antioxidative system and ion transport in chromium detoxification in germinating seedlings of soybean.

Chromium (Cr) toxicity impairs the productivity of crops and is a major threat to food security worldwide. However, the effect of Cr toxicity on seed germination and transcriptome of germinating seedlings of soybean crop has not been fully explored. In this study, two Cr-tolerant lines (J82, S125) and two Cr-sensitive ones (LD1, RL) were screened out of twenty-one soybean (Glycine max L.) genotypes based on seed germination rate, seed germinative energy, seed germination index, and growth of germinating seedlings under 50 mg L-1 Cr treatment. We found that Cr stress inhibits the growth of soybean seed germinating seedlings due to the Cr-induced overaccumulation of reactive oxygen species (ROS). Significantly different levels of element contents, antioxidant enzyme activities, malondialdehyde content were observed in the four soybean genotypes with contrasting Cr tolerance. Further, a total of 13,777 differentially expressed genes (DEGs) were identified in transcriptomic sequencing and 1298 DEGs in six gene modules were found highly correlated with the physiological traits by weighted correlation network analysis (WGCNA) analysis. The DEGs encoding antioxidant enzymes, transcription factors, and ion transporters are proposed to confer Cr tolerance in soybean germinating seedlings by reducing the uptake and translocation of Cr, decreasing the level of ROS, and keeping the osmotic balance in soybean germinating seedings. In conclusion, our study provided a molecular regulation network on soybean Cr tolerance at seed germinating stage and identified candidate genes for molecular breeding of low Cr accumulation soybean cultivars.

Molecular Regulation and Evolution of Cytokinin Signaling in Plant Abiotic Stresses.

The sustainable production of crops faces increasing challenges from global climate change and human activities, which leads to increasing instances of many abiotic stressors to plants. Among the abiotic stressors, drought, salinity and excessive levels of toxic metals cause reductions in global agricultural productivity and serious health risks for humans. Cytokinins (CKs) are key phytohormones functioning in both normal development and stress responses in plants. Here, we summarize the molecular mechanisms on the biosynthesis, metabolism, transport and signaling transduction pathways of CKs. CKs act as negative regulators of both root system architecture plasticity and root sodium exclusion in response to salt stress. The functions of CKs in mineral-toxicity tolerance and their detoxification in plants are reviewed. Comparative genomic analyses were performed to trace the origin, evolution and diversification of the critical regulatory networks linking CK signaling and abiotic stress. We found that the production of CKs and their derivatives, pathways of signal transduction and drought-response root growth regulation are evolutionarily conserved in land plants. In addition, the mechanisms of CK-mediated sodium exclusion under salt stress are suggested for further investigations. In summary, we propose that the manipulation of CK levels and their signaling pathways is important for plant abiotic stress and is, therefore, a potential strategy for meeting the increasing demand for global food production under changing climatic conditions.

Molecular evidence for adaptive evolution of drought tolerance in wild cereals.

The considerable drought tolerance of wild cereal crop progenitors has diminished during domestication in the pursuit of higher productivity. Regaining this trait in cereal crops is essential for global food security but requires novel genetic insight. Here, we assessed the molecular evidence for natural variation of drought tolerance in wild barley (Hordeum spontaneum), wild emmer wheat (Triticum dicoccoides), and Brachypodium species collected from dry and moist habitats at Evolution Canyon, Israel (ECI). We report that prevailing moist vs dry conditions have differentially shaped the stomatal and photosynthetic traits of these wild cereals in their respective habitats. We present the genomic and transcriptomic evidence accounting for differences, including co-expression gene modules, correlated with physiological traits, and selective sweeps, driven by the xeric site conditions on the African Slope (AS) at ECI. Co-expression gene module 'circadian rhythm' was linked to significant drought-induced delay in flowering time in Brachypodium stacei genotypes. African Slope-specific differentially expressed genes are important in barley drought tolerance, verified by silencing Disease-Related Nonspecific Lipid Transfer 1 (DRN1), Nonphotochemical Quenching 4 (NPQ4), and Brassinosteroid-Responsive Ring-H1 (BRH1). Our results provide new genetic information for the breeding of resilient wheat and barley in a changing global climate with increasingly frequent drought events.

Molecular Evolution of Plant 14-3-3 Proteins and Function of Hv14-3-3A in Stomatal Regulation and Drought Tolerance.

Drought significantly affects stomatal regulation, leading to the reduced growth and productivity of plants. Plant 14-3-3 proteins were reported to participate in drought response by regulating the activities of a wide array of target proteins. However, the molecular evolution, expression pattern and physiological functions of 14-3-3s under drought stress remain unclear. In this study, a comparative genomic analysis and the tissue-specific expression of 14-3-3s revealed the highly conserved and early evolution of 14-3-3s in green plants and duplication and expansion of the 14-3-3s family members in angiosperms. Using barley (Hordeum vulgare) for the functional characterization of 14-3-3 proteins, the transcripts of five members out of six Hv14-3-3s were highly induced by drought in the drought-tolerant line, XZ141. Suppression of the expression of Hv14-3-3A through barley stripe mosaic virus-virus induced gene silencing resulted in significantly increased drought sensitivity and stomatal density as well as significantly reduced net CO2 assimilation (A) and stomatal conductance (gs) in barley. Moreover, we showed the functional interactions between Hv14-3-3s and key proteins in drought and stomatal responses in plants-such as Open Stomata 1 (HvOST1), Slow Anion Channel 1 (HvSLAC1), three Heat Shock Proteins (HvHSP90-1/2/5) and Dehydration-Responsive Element-Binding 3 (HvDREB3). Taken together, we propose that 14-3-3s are highly evolutionarily conserved proteins and that Hv14-3-3s represent a group of the core regulatory components for the rapid stomatal response to drought in barley. This study will provide important evolutionary and molecular evidence for future applications of 14-3-3 proteins in breeding drought-tolerant crops in a changing global climate.

Molecular Regulation and Evolution of Redox Homeostasis in Photosynthetic Machinery.

The recent advances in plant biology have significantly improved our understanding of reactive oxygen species (ROS) as signaling molecules in the redox regulation of complex cellular processes. In plants, free radicals and non-radicals are prevalent intra- and inter-cellular ROS, catalyzing complex metabolic processes such as photosynthesis. Photosynthesis homeostasis is maintained by thiol-based systems and antioxidative enzymes, which belong to some of the evolutionarily conserved protein families. The molecular and biological functions of redox regulation in photosynthesis are usually to balance the electron transport chain, photosystem II, photosystem I, mesophyll and bundle sheath signaling, and photo-protection regulating plant growth and productivity. Here, we review the recent progress of ROS signaling in photosynthesis. We present a comprehensive comparative bioinformatic analysis of redox regulation in evolutionary distinct photosynthetic cells. Gene expression, phylogenies, sequence alignments, and 3D protein structures in representative algal and plant species revealed conserved key features including functional domains catalyzing oxidation and reduction reactions. We then discuss the antioxidant-related ROS signaling and important pathways for achieving homeostasis of photosynthesis. Finally, we highlight the importance of plant responses to stress cues and genetic manipulation of disturbed redox status for balanced and enhanced photosynthetic efficiency and plant productivity.

Quantum anomalous Hall effect in M2X3honeycomb Kagome lattice.

The quantum anomalous Hall (QAH) effect has recently drawn great attention in spintronics with extraordinary property of chiral edge states without dissipation in absence of magnetic field. In M2X3honeycomb Kagome lattice, numerous two-dimensional materials are predicted to be QAH insulators including metal oxides/sulfides and metal organic lattice. In this work, we proposed a general model to explain the mechanism of Dirac half metal with absence of spin orbital coupling and the nontrivial topological property with spin orbital coupling, which could be induced by combination of electron counting rule, crystal field effect anddxz,dyzorbitals hybridization. Based on the mechanism, we further predict that triphenyl-metal lattice M2(C6H4)3(M= V, Nb, Ta) are all QAH insulators with high Curie temperature and large nontrivial band gap for triphenyl-Nb and triphenyl-Ta lattice.

Molecular evolution and functional modification of plant miRNAs with CRISPR.

Gene editing using clustered regularly interspaced short palindromic repeat/CRISPR-associated proteins (CRISPR/Cas) has revolutionized biotechnology and provides genetic tools for medicine and life sciences. However, the application of this technology to miRNAs, with the function as negative gene regulators, has not been extensively reviewed in plants. Here, we summarize the evolution, biogenesis, and structure of miRNAs, as well as their interactions with mRNAs and computational models for predicting target genes. In addition, we review current advances in CRISPR/Cas for functional analysis and for modulating miRNA genes in plants. Extending our knowledge of miRNAs and their manipulation with CRISPR will provide fundamental understanding of the functions of plant miRNAs and facilitate more sustainable and publicly acceptable genetic engineering of crops.

Molecular response and evolution of plant anion transport systems to abiotic stress.

KEY MESSAGE: We propose that anion channels are essential players for green plants to respond and adapt to the abiotic stresses associated changing climate via reviewing the literature and analyzing the molecular evolution, comparative genetic analysis, and bioinformatics analysis of the key anion channel gene families. Climate change-induced abiotic stresses including heatwave, elevated CO2, drought, and flooding, had a major impact on plant growth in the last few decades. This scenario could lead to the exposure of plants to various stresses. Anion channels are confirmed as the key factors in plant stress responses, which exist in the green lineage plants. Numerous studies on anion channels have shed light on their protein structure, ion selectivity and permeability, gating characteristics, and regulatory mechanisms, but a great quantity of questions remain poorly understand. Here, we review function of plant anion channels in cell signaling to improve plant response to environmental stresses, focusing on climate change related abiotic stresses. We investigate the molecular response and evolution of plant slow anion channel, aluminum-activated malate transporter, chloride channel, voltage-dependent anion channel, and mechanosensitive-like anion channel in green plant. Furthermore, comparative genetic and bioinformatic analysis reveal the conservation of these anion channel gene families. We also discuss the tissue and stress specific expression, molecular regulation, and signaling transduction of those anion channels. We propose that anion channels are essential players for green plants to adapt in a diverse environment, calling for more fundamental and practical studies on those anion channels towards sustainable food production and ecosystem health in the future.

Duplication of a manganese/cadmium transporter gene reduces cadmium accumulation in rice grain.

Global contamination of soils with toxic cadmium (Cd) is a serious health threat. Here we found that a tandem duplication of a gene encoding a manganese/Cd transporter, OsNramp5, was responsible for low-Cd accumulation in Pokkali, an old rice cultivar. This duplication doubled the expression of OsNramp5 gene but did not alter its spatial expression pattern and cellular localization. Higher expression of OsNramp5 increased uptake of Cd and Mn into the root cells but decreased Cd release to the xylem. Introgression of this allele into Koshihikari, an elite rice cultivar, through backcrossing significantly reduced Cd accumulation in the grain when cultivated in soil heavily contaminated with Cd but did not affect both grain yield and eating quality. This study not only reveals the molecular mechanism underlying low-Cd accumulation but also provides a useful target for breeding rice cultivars with low-Cd accumulation.

Molecular Evolution of Calcium Signaling and Transport in Plant Adaptation to Abiotic Stress.

Adaptation to unfavorable abiotic stresses is one of the key processes in the evolution of plants. Calcium (Ca2+) signaling is characterized by the spatiotemporal pattern of Ca2+ distribution and the activities of multi-domain proteins in integrating environmental stimuli and cellular responses, which are crucial early events in abiotic stress responses in plants. However, a comprehensive summary and explanation for evolutionary and functional synergies in Ca2+ signaling remains elusive in green plants. We review mechanisms of Ca2+ membrane transporters and intracellular Ca2+ sensors with evolutionary imprinting and structural clues. These may provide molecular and bioinformatics insights for the functional analysis of some non-model species in the evolutionarily important green plant lineages. We summarize the chronological order, spatial location, and characteristics of Ca2+ functional proteins. Furthermore, we highlight the integral functions of calcium-signaling components in various nodes of the Ca2+ signaling pathway through conserved or variant evolutionary processes. These ultimately bridge the Ca2+ cascade reactions into regulatory networks, particularly in the hormonal signaling pathways. In summary, this review provides new perspectives towards a better understanding of the evolution, interaction and integration of Ca2+ signaling components in green plants, which is likely to benefit future research in agriculture, evolutionary biology, ecology and the environment.

Molecular Interaction and Evolution of Jasmonate Signaling With Transport and Detoxification of Heavy Metals and Metalloids in Plants.

An increase in environmental pollution resulting from toxic heavy metals and metalloids [e.g., cadmium (Cd), arsenic (As), and lead (Pb)] causes serious health risks to humans and animals. Mitigation strategies need to be developed to reduce the accumulation of the toxic elements in plant-derived foods. Natural and genetically-engineered plants with hyper-tolerant and hyper-accumulating capacity of toxic minerals are valuable for phytoremediation. However, the molecular mechanisms of detoxification and accumulation in plants have only been demonstrated in very few plant species such as Arabidopsis and rice. Here, we review the physiological and molecular aspects of jasmonic acid and the jasmonate derivatives (JAs) in response to toxic heavy metals and metalloids. Jasmonates have been identified in, limiting the accumulation and enhancing the tolerance to the toxic elements, by coordinating the ion transport system, the activity of antioxidant enzymes, and the chelating capacity in plants. We also propose the potential involvement of Ca2+ signaling in the stress-induced production of jasmonates. Comparative transcriptomics analyses using the public datasets reveal the key gene families involved in the JA-responsive routes. Furthermore, we show that JAs may function as a fundamental phytohormone that protects plants from heavy metals and metalloids as demonstrated by the evolutionary conservation and diversity of these gene families in a large number of species of the major green plant lineages. Using ATP-Binding Cassette G (ABCG) transporter subfamily of six representative green plant species, we propose that JA transporters in Subgroup 4 of ABCGs may also have roles in heavy metal detoxification. Our paper may provide guidance toward the selection and development of suitable plant and crop species that are tolerant to toxic heavy metals and metalloids.

Changes in levels of coagulation parameters in different trimesters among Chinese pregnant women.

BACKGROUND: This article is to explore changes in levels of coagulation parameters in different trimesters among healthy pregnant women in China. METHODS: A total of 760 eligible women were enrolled (first-trimester group: n = 183, second-trimester group: n = 183, third-trimester group: n = 263, non-pregnant group: n = 131). Seven parameters including prothrombin time (PT), activated partial thromboplastin time (APTT), thrombin time (TT), fibrinogen (FIB), D-dimer (DD), fibrinogen degradation products (FDP), and antithrombin III (ATIII), of all participants were collected. The non-parametric 2.5th-97.5th percentiles reference intervals were calculated for each parameter. RESULTS: The reference intervals for FIB, PT, APTT, TT, FDP, DD, and ATIII at first trimester were 2.11-4.32 g/L, 10.90-13.85 s, 24.60-39.28 s, 12.95-15.88 s, 0.04-2.55 µg/mL, 0.03-1.15 µg/mL, and 75.57%-125.31%, respectively. The reference intervals at second trimester were 2.31-4.77 g/L, 9.70-12.64 s, 24.16-35.43 s, 12.95-15.88 s, 0.15-7.40 µg/mL, 0.08-2.13 µg/mL, and 74.35%-119.28%, respectively. For the third-trimester, the intervals were 2.39-4.96 g/L, 9.20-11.95 s, 23.90-35.51 s, 13.41-18.00 s, 0.55-13.43 µg/mL, 0.15-3.60 µg/mL, and 71.61%-118.29%, respectively. The third-trimester group showed decreased PT, APTT, and ATIII and increased FIB, TT, DD and FDP as compared with the other groups. CONCLUSION: In this study, level changes of coagulation parameters in different trimesters were observed. And the ranges for coagulation parameters were presented, which may provide some reference for clinicians to more accurately monitor the coagulation and fibrinolytic system in pregnant women.

Metalloid hazards: From plant molecular evolution to mitigation strategies.

Metalloids such as boron and silicon are key elements for plant growth and crop productivity. However, toxic metalloids such as arsenic are increasing in the environment due to inputs from natural sources and human activities. These hazardous metalloids can cause serious health risks to humans and animals if they enter the food chain. Plants have developed highly regulated mechanisms to alleviate the toxicity of metalloids during their 500 million years of evolution. A better understanding the molecular mechanisms underlying the transport and detoxification of toxic metalloids in plants will shed light on developing mitigation strategies. Key transporters and regulatory proteins responsive to toxic metalloids have been identified through evolutionary and molecular analyses. Moreover, knowledge of the regulatory proteins and their pathways can be used in the breeding of crops with lower accumulation of metalloids. These findings can also assist phytoremediation by the exploration of plants such as fern species that hyperaccumulate metalloids from soils and water, and can be used to engineer plants with elevated uptake and storage capacity of toxic metalloids. In summary, there are solutions to remediate contamination due to toxic metalloids by combining the research advances and industrial technologies with agricultural and environmental practices.