The initiation of stomata, microscopic valves in the epidermis of higher plants that control of gas exchange, requires a co-ordinated sequence of asymmetric and symmetric divisions, which is under tight environmental and developmental control. Arabidopsis leaves grown under elevated photosynthetic photon flux density have a higher density of stomata. STOMAGEN encodes an epidermal patterning factor produced in the mesophyll, and our observations indicated that elevated photosynthetic irradiation stimulates STOMAGEN expression. Our analysis of gain and loss of function of STOMAGEN further detailed its function as a positive regulator of stomatal formation on both sides of the leaf, not only in terms of stomatal density across the leaf surface but also in terms of their stomatal index. STOMAGEN function was rate limiting for the light response of the stomatal lineage in the adaxial epidermis. Mutants in pathways that regulate stomatal spacing in the epidermis and have elevated stomatal density, such as stomatal density and distribution (sdd1) and too many mouth alleles, displayed elevated STOMAGEN expression, suggesting that STOMAGEN is either under the direct control of these pathways or is indirectly affected by stomatal patterning, suggestive of a feedback mechanism. These observations support a model in which changes in levels of light irradiation are perceived in the mesophyll and control the production of stomata in the epidermis by mesophyll-produced STOMAGEN, and whereby, conversely, stomatal patterning, either directly or indirectly, influences STOMAGEN levels.
- MeSH
- Arabidopsis genetics growth & development metabolism radiation effects MeSH
- Photosynthesis MeSH
- Plant Leaves growth & development metabolism radiation effects MeSH
- Arabidopsis Proteins genetics metabolism MeSH
- Plant Stomata genetics growth & development metabolism radiation effects MeSH
- Gene Expression Regulation, Plant radiation effects MeSH
- Signal Transduction MeSH
- Light MeSH
- Gene Expression Regulation, Developmental radiation effects MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Conifers growing at high elevations need to optimize their stomatal conductance (gs ) for maximizing photosynthetic yield while minimizing water loss under less favourable thermal conditions. Yet the ability of high-elevation conifers to adjust their gs sensitivity to environmental drivers remains largely unexplored. We used 4 years of sap flow measurements to elucidate intraspecific and interspecific variability of gs in Larix decidua Mill. and Picea abies (L.) Karst along an elevational gradient and contrasting soil moisture conditions. Site- and species-specific gs response to main environmental drivers were examined, including vapour pressure deficit, air temperature, solar irradiance, and soil water potential. Our results indicate that maximum gs of L. decidua is >2 times higher, shows a more plastic response to temperature, and down-regulates gs stronger during atmospheric drought compared to P. abies. These differences allow L. decidua to exert more efficient water use, adjust to site-specific thermal conditions, and reduce water loss during drought episodes. The stronger plasticity of gs sensitivity to temperature and higher conductance of L. decidua compared to P. abies provide new insights into species-specific water use strategies, which affect species' performance and should be considered when predicting terrestrial water dynamics under future climatic change.
- MeSH
- Pinus physiology MeSH
- Tracheophyta * physiology MeSH
- Adaptation, Physiological MeSH
- Larix physiology MeSH
- Droughts MeSH
- Plant Stomata physiology MeSH
- Soil MeSH
- Temperature MeSH
- Plant Transpiration physiology MeSH
- Water physiology MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Occurrence of stomata on both leaf surfaces (amphistomaty) promotes higher stomatal conductance and photosynthesis while simultaneously increasing exposure to potential disease agents in black cottonwood (Populus trichocarpa). A genome-wide association study (GWAS) with 2.2M single nucleotide polymorphisms generated through whole-genome sequencing found 280 loci associated with variation in adaxial stomatal traits, implicating genes regulating stomatal development and behavior. Strikingly, numerous loci regulating plant growth and response to biotic and abiotic stresses were also identified. The most significant locus was a poplar homologue of SPEECHLESS (PtSPCH1). Individuals possessing PtSPCH1 alleles associated with greater adaxial stomatal density originated primarily from environments with shorter growing seasons (e.g. northern latitudes, high elevations) or with less precipitation. PtSPCH1 was expressed in developing leaves but not developing stem xylem. In developing leaves, RNA sequencing showed patterns of coordinated expression between PtSPCH1 and other GWAS-identified genes. The breadth of our GWAS results suggests that the evolution of amphistomaty is part of a larger, complex response in plants. Suites of genes underpin this response, retrieved through genetic association to adaxial stomata, and show coordinated expression during development. We propose that the occurrence of amphistomaty in P. trichocarpa involves PtSPCH1 and reflects selection for supporting rapid growth over investment in immunity.
- MeSH
- Alleles MeSH
- Genome-Wide Association Study MeSH
- Species Specificity MeSH
- Phenotype MeSH
- Genotype MeSH
- Plant Immunity genetics MeSH
- Polymorphism, Single Nucleotide genetics MeSH
- Quantitative Trait, Heritable MeSH
- Climate MeSH
- Populus genetics growth & development immunology physiology MeSH
- Plant Stomata genetics physiology MeSH
- Gene Expression Regulation, Plant MeSH
- Genes, Plant MeSH
- Plant Proteins genetics metabolism MeSH
- Body Patterning * MeSH
- Plant Development MeSH
- Geography MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Understanding the response of a crop to drought is the first step in the breeding of tolerant genotypes. In our study, two maize (Zea mays L.) genotypes with contrasting sensitivity to dehydration were subjected to moderate drought conditions. The subsequent analysis of their physiological parameters revealed a decreased stomatal conductance accompanied by a slighter decrease in the relative water content in the sensitive genotype. In contrast, the tolerant genotype maintained open stomata and active photosynthesis, even under dehydration conditions. Drought-induced changes in the leaf proteome were analyzed by two independent approaches, 2D gel electrophoresis and iTRAQ analysis, which provided compatible but only partially overlapping results. Drought caused the up-regulation of protective and stress-related proteins (mainly chaperones and dehydrins) in both genotypes. The differences in the levels of various detoxification proteins corresponded well with the observed changes in the activities of antioxidant enzymes. The number and levels of up-regulated protective proteins were generally lower in the sensitive genotype, implying a reduced level of proteosynthesis, which was also indicated by specific changes in the components of the translation machinery. Based on these results, we propose that the hypersensitive early stomatal closure in the sensitive genotype leads to the inhibition of photosynthesis and, subsequently, to a less efficient synthesis of the protective/detoxification proteins that are associated with drought tolerance.
- MeSH
- Electrophoresis, Gel, Two-Dimensional MeSH
- Antioxidants metabolism MeSH
- Dehydration MeSH
- Adaptation, Physiological MeSH
- Genotype MeSH
- Glutathione Reductase metabolism MeSH
- Catalase metabolism MeSH
- Zea mays enzymology genetics physiology MeSH
- Droughts MeSH
- Proteomics MeSH
- Plant Stomata physiology MeSH
- Superoxide Dismutase metabolism MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Stomatal conductance directly modifies plant water relations and photosynthesis. Many environmental factors affecting the stomatal conductance have been intensively studied but temperature has been largely neglected, even though it is one of the fastest changing environmental variables and it is rising due to climate change. In this study, we describe how stomata open when the temperature increases. Stomatal conductance increased by ca 40% in a broadleaf and a coniferous species, poplar (Populus deltoides x nigra) and loblolly pine (Pinus taeda) when temperature was increased by 10 °C, from 30 °C to 40 °C at a constant vapor pressure deficit of 1 kPa. The mechanism of regulating stomatal conductance by temperature was, at least partly, independent of other known mechanisms linked to water status and carbon metabolism. Stomatal conductance increased with rising temperature despite the decrease in leaf water potential, increase in transpiration, increase in intercellular CO2 concentration and was decoupled from photosynthesis. Increase in xylem and mesophyll hydraulic conductance coming from lower water viscosity may to some degree explain temperature dependent opening of stomata. The direct stomatal response to temperature allows plants to benefit from increased evaporative cooling during the heat waves and from lower stomatal limitations to photosynthesis but they may be jeopardized by faster depletion of soil water.
- MeSH
- Pinus physiology MeSH
- Populus physiology MeSH
- Plant Stomata physiology MeSH
- Temperature * MeSH
- Vapor Pressure MeSH
- Water MeSH
- Publication type
- Journal Article MeSH
Cytokinins (CKs) are phytohormones regulating plant growth and development as well as response to the environment. In order to evaluate their function in heat stress (HS) responses, the effect of CK elevation was determined during three types of HS - targeted to shoots, targeted to roots and applied to the whole plant. The early (30min) and longer term (3h) responses were followed at the hormonal, transcriptomic and proteomic levels in Arabidopsis transformants with dexamethasone-inducible expression of the CK biosynthetic gene isopentenyltransferase (ipt) and the corresponding wild-type (Col-0). Combination of hormonal and phenotypic analyses showed transient up-regulation of the CK/abscisic acid ratio, which controls stomatal aperture, to be more pronounced in the transformant. HS responses of the root proteome and Rubisco-immunodepleted leaf proteome were followed using 2-D gel electrophoresis and MALDI-TOF/TOF. More than 100 HS-responsive proteins were detected, most of them being modulated by CK increase. Proteome and transcriptome analyses demonstrated that CKs have longer term positive effects on the stress-related proteins and transcripts, as well as on the photosynthesis-related ones. Transient accumulation of CKs and stimulation of their signal transduction in tissue(s) not exposed to HS indicate that they are involved in plant stress responses.
- MeSH
- Alkyl and Aryl Transferases physiology MeSH
- Arabidopsis drug effects metabolism physiology MeSH
- Cytokinins physiology MeSH
- Dexamethasone pharmacology MeSH
- Plant Roots metabolism physiology MeSH
- Abscisic Acid physiology MeSH
- Proteomics MeSH
- Heat-Shock Response physiology MeSH
- Gene Expression Regulation, Plant physiology MeSH
- Plant Growth Regulators physiology MeSH
- Signal Transduction drug effects physiology MeSH
- Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization MeSH
- Gene Expression Profiling MeSH
- Plant Shoots metabolism physiology MeSH
- Hot Temperature MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
BACKGROUND AND AIMS: Stomatal density (SD) generally decreases with rising atmospheric CO2 concentration, Ca. However, SD is also affected by light, air humidity and drought, all under systemic signalling from older leaves. This makes our understanding of how Ca controls SD incomplete. This study tested the hypotheses that SD is affected by the internal CO2 concentration of the leaf, Ci, rather than Ca, and that cotyledons, as the first plant assimilation organs, lack the systemic signal. METHODS: Sunflower (Helianthus annuus), beech (Fagus sylvatica), arabidopsis (Arabidopsis thaliana) and garden cress (Lepidium sativum) were grown under contrasting environmental conditions that affected Ci while Ca was kept constant. The SD, pavement cell density (PCD) and stomatal index (SI) responses to Ci in cotyledons and the first leaves of garden cress were compared. (13)C abundance (δ(13)C) in leaf dry matter was used to estimate the effective Ci during leaf development. The SD was estimated from leaf imprints. KEY RESULTS: SD correlated negatively with Ci in leaves of all four species and under three different treatments (irradiance, abscisic acid and osmotic stress). PCD in arabidopsis and garden cress responded similarly, so that SI was largely unaffected. However, SD and PCD of cotyledons were insensitive to Ci, indicating an essential role for systemic signalling. CONCLUSIONS: It is proposed that Ci or a Ci-linked factor plays an important role in modulating SD and PCD during epidermis development and leaf expansion. The absence of a Ci-SD relationship in the cotyledons of garden cress indicates the key role of lower-insertion CO2 assimilation organs in signal perception and its long-distance transport.
- MeSH
- Arabidopsis cytology drug effects MeSH
- Fagus cytology drug effects MeSH
- Dehydration MeSH
- Helianthus cytology drug effects MeSH
- Cotyledon drug effects physiology MeSH
- Lepidium cytology drug effects MeSH
- Carbon Dioxide pharmacology MeSH
- Cell Count MeSH
- Plant Stomata cytology drug effects MeSH
- Environment MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Stomatal ontogenesis, patterning, and function are hallmarks of environmental plant adaptation, especially to conditions limiting plant growth, such as elevated temperatures and reduced water availability. The specification and distribution of a stomatal cell lineage and its terminal differentiation into guard cells require a master regulatory protein phosphorylation cascade involving the YODA mitogen-activated protein kinase kinase kinase. YODA signaling results in the activation of MITOGEN-ACTIVATED PROTEIN KINASEs (MPK3 and MPK6), which regulate transcription factors, including SPEECHLESS (SPCH). Here, we report that acute heat stress affects the phosphorylation and deactivation of SPCH and modulates stomatal density. By using complementary molecular, genetic, biochemical, and cell biology approaches, we provide solid evidence that HEAT SHOCK PROTEINS 90 (HSP90s) play a crucial role in transducing heat-stress response through the YODA cascade. Genetic studies revealed that YODA and HSP90.1 are epistatic, and they likely function linearly in the same developmental pathway regulating stomata formation. HSP90s interact with YODA, affect its cellular polarization, and modulate the phosphorylation of downstream targets, such as MPK6 and SPCH, under both normal and heat-stress conditions. Thus, HSP90-mediated specification and differentiation of the stomatal cell lineage couples stomatal development to environmental cues, providing an adaptive heat stress response mechanism in plants.
- MeSH
- Arabidopsis physiology MeSH
- Cell Differentiation MeSH
- Cell Division MeSH
- Cell Lineage MeSH
- Epigenesis, Genetic MeSH
- Phosphorylation MeSH
- Cotyledon cytology MeSH
- MAP Kinase Kinase Kinases genetics metabolism MeSH
- Mitogen-Activated Protein Kinase Kinases metabolism MeSH
- Mitogen-Activated Protein Kinases metabolism MeSH
- Mutation MeSH
- Arabidopsis Proteins genetics metabolism MeSH
- HSP90 Heat-Shock Proteins genetics metabolism MeSH
- Plant Stomata cytology growth & development metabolism MeSH
- Heat-Shock Response * MeSH
- Gene Expression Regulation, Plant MeSH
- Signal Transduction MeSH
- Basic Helix-Loop-Helix Transcription Factors metabolism MeSH
- Protein Binding MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
