A model of stomatal control strategies in response to [CO2] characterized by a trade-off between short-term physiological behavior and longer-term morphological response

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一种气孔控制策略模型，用于响应 [CO2]，其特征是在短期生理行为和长期形态响应之间进行权衡

Um modelo de estratégias de controle estomático em resposta ao [CO2], caracterizado por um equilíbrio entre o comportamento fisiológico de curto prazo e a resposta morfológica de longo prazo

Un modelo de estrategias de control estomático en respuesta a [CO2], caracterizado por una compensación entre el comportamiento fisiológico a corto plazo y la respuesta morfológica a largo plazo.

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Coordination of stomatal physiological behavior and morphology with carbon dioxide determines stomatal control

Haworth M., Killi D., Materassi A., Raschi A. (2015)

Matthew Haworth, Dilek Killi, Alessandro Materassi, Antonio Raschi,

CNR—Tree and Timber Institute (IVALSA), Presso Area di Ricerca CNR, Via Madonna del Piano 10, Sesto Fiorentino, 50019 Florence, Italy

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American Journal of Botany 102(5): 677-688 – https://doi.org/10.3732/ajb.1400508 –

https://bsapubs.onlinelibrary.wiley.com/doi/full/10.3732/ajb.1400508

Abstract

• Premise of the study: Stomatal control is determined by the ability to alter stomatal aperture and/or the number of stomata on the surface of new leaves in response to growth conditions. The development of stomatal control mechanisms to the concentration of CO₂ within the atmosphere ([CO₂]) is fundamental to our understanding of plant evolutionary history and the prediction of gas exchange responses to future [CO₂].

• Methods: In a controlled environment, fern and angiosperm species were grown in atmospheres of ambient (400 ppm) and elevated (2000 ppm) [CO₂]. Physiological stomatal behavior was compared with the stomatal morphological response to [CO₂].

• Key results: An increase in [CO₂] or darkness induced physiological stomatal responses ranging from reductions (active) to no change (passive) in stomatal conductance. Those species with passive stomatal behavior exhibited pronounced reductions of stomatal density in new foliage when grown in elevated [CO₂], whereas species with active stomata showed little morphological response to [CO₂]. Analysis of the physiological and morphological stomatal responses of a wider range of species suggests that patterns of stomatal control to [CO₂] do not follow a phylogenetic pattern associated with plant evolution.

• Conclusions: Selective pressures may have driven the development of divergent stomatal control strategies to increased [CO₂]. Those species that are able to actively regulate guard cell turgor are more likely to respond to [CO₂] through a change in stomatal aperture than stomatal number. We propose a model of stomatal control strategies in response to [CO₂] characterized by a trade-off between short-term physiological behavior and longer-term morphological response.

The cycad species analysed showed no significant stomatal density, stomatal index or pore-length response to changes in [CO2] or [O2].

Cycads show no stomatal-density and index response to elevated carbon dioxide and subambient oxygen

Haworth M., Fitzgerald A., McElwain J. C. (2011)

Matthew Haworth, Annmarie Fitzgerald, Jennifer C Mcelwain,

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Australian Journal of Botany 59: 629–638 – DOI: 10.1071/BT11009 –

https://www.researchgate.net/publication/263030608_Cycads_show_no_stomataldensity_and_index_response_to_elevated_carbon_dioxide_and_subambient_oxygen

Abstract

The stomatal density (SD) and index (SI) of fossil plants are widely used in reconstructing palaeo-atmospheric CO2 concentration (palaeo-[CO2]). These stomatal reconstructions depend on the inverse relationship between atmospheric CO2 concentration ([CO2]) and SD and/or SI. Atmospheric oxygen concentration ([O2]) has also varied throughout earth history, influencing photosynthesis via the atmospheric CO2 : O2 ratio, and possibly affecting both SD and SI.

Cycads formed a major component of Mesozoic floras, and may serve as suitable proxies of palaeo-[CO2]. However, little is known regarding SD and SI responses of modern cycads to [CO2] and [O2]. SD, SI and pore length were measured in six cycad species (Cycas revoluta, Dioon merolae, Lepidozamia hopei, Lepidozamia peroffskyana, Macrozamia miquelii and Zamia integrifolia) grown under elevated [CO2] (1500 ppm) and subambient [O2] (13.0%) in combination and separately, and compared with SD, SI and pore length under control atmospheric conditions of 380 ppm [CO2] and 20.9% [O2].

The cycad species analysed showed no significant SD, SI or pore-length response to changes in [CO2] or [O2].

Stomatal reconstructions of palaeo-[CO(2)] during past episodes of global-scale volcanism probably reflect atmospheric [CO(2)] and not [SO(2)]

Stomatal index responses of Agrostis canina to carbon dioxide and sulphur dioxide: implications for palaeo-[CO₂] using the stomatal proxy

Haworth M., Gallagher A., Elliott-Kingston C., Raschi A., Marandola D., McElwain J. C. (2010)

Matthew Haworth, Angela Gallagher, Caroline Elliott-Kingston, Antonio Raschi, Danilo Marandola, Jennifer C McElwain,

School of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland

New Phytologist 188: 845–855 – doi: 10.1111/j.1469-8137.2010.03403.x – PMID: 20704659 –

https://pubmed.ncbi.nlm.nih.gov/20704659/

Abstract

• Stomatal index values of fossil plants are widely used in reconstructing palaeo-[CO(2)]. This depends upon the assumption that the stomatal index is determined by the atmospheric concentration of CO(2) ([CO(2)]). This study investigates whether fumigation with, and resistance to, sulphur dioxide (SO(2)) induces a reduction in the stomatal index that may affect stomatal reconstructions of palaeo-[CO(2)] coinciding with episodes of global-scale volcanism. • Agrostis canina from Mefite di Ansanto, Italy, grow in atmospheres of elevated-[CO(2)], SO(2) and hydrogen sulphide (H(2)S). Mefite A. canina were compared with a control population in a ‘common-garden’ experiment and a controlled-environment study under elevated-[CO(2)] and SO(2) fumigation. • In A. canina, resistance to toxic volcanic gases is not associated with reduced stomatal index, and fumigation with SO(2) does not cause a decrease in stomatal initiation. The two populations of A. canina analyzed in this study exhibit different stomatal index-[CO(2)] ‘responses’, with control plants showing a reduction in stomatal index and Mefite plants showing no response. • Stomatal reconstructions of palaeo-[CO(2)] during past episodes of global-scale volcanism probably reflect atmospheric [CO(2)] and not [SO(2)]. The lack of a reduction in the stomatal index in response to elevated [CO(2)] in the Mefite plants, suggests that resistance to toxic gases and/or long-term growth at high [CO(2)] reduces, or negates, sensitivity of the stomatal index-[CO(2)] relationship, or that stomatal index-[CO(2)] in the Mefite plants is attuned to [CO(2)] fluctuations at much higher concentrations.

The interaction between stomatal morphology and physiology

Example stomatal morphologies and distributions alongside stomatal closing (a, b) and opening (c, d) kinetics expressed as absolute and relative values for a cycad (Cycas sinanensis), a basal angiosperm (Magnolia grandiflora), a eudicot angiosperm (Chenopodium quinoa) and a monocot (Arundo donax). The key for identification of species is given on the left-hand y-axis. The rate of change of stomatal conductance, G_s, during stomatal opening or closing (G_s50%) is determined from the initial 50% of the G_s response

Integrating stomatal physiology and morphology: evolution of stomatal control and development of future crops

Haworth M., Marino G., Loreto F., Centritto M. (2021)

Matthew Haworth, Giovanni Marino, Francesco Loreto, Mauro Centritto,

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Oecologia 197: 867–883  – https://doi.org/10.1007/s00442-021-04857-3 –

https://link.springer.com/article/10.1007/s00442-021-04857-3

Abstract

Stomata are central players in the hydrological and carbon cycles, regulating the uptake of carbon dioxide (CO₂) for photosynthesis and transpirative loss of water (H₂O) between plants and the atmosphere. The necessity to balance water-loss and CO₂-uptake has played a key role in the evolution of plants, and is increasingly important in a hotter and drier world. The conductance of CO₂ and water vapour across the leaf surface is determined by epidermal and stomatal morphology (the number, size, and spacing of stomatal pores) and stomatal physiology (the regulation of stomatal pore aperture in response to environmental conditions). The proportion of the epidermis allocated to stomata and the evolution of amphistomaty are linked to the physiological function of stomata. Moreover, the relationship between stomatal density and [CO₂] is mediated by physiological stomatal behaviour; species with less responsive stomata to light and [CO₂] are most likely to adjust stomatal initiation. These differences in the sensitivity of the stomatal density—[CO₂] relationship between species influence the efficacy of the ‘stomatal method’ that is widely used to infer the palaeo-atmospheric [CO₂] in which fossil leaves developed. Many studies have investigated stomatal physiology or morphology in isolation, which may result in the loss of the ‘overall picture’ as these traits operate in a coordinated manner to produce distinct mechanisms for stomatal control. Consideration of the interaction between stomatal morphology and physiology is critical to our understanding of plant evolutionary history, plant responses to on-going climate change and the production of more efficient and climate-resilient food and bio-fuel crops.

Mid-Cretaceous pCO2 based on stomata of an extinct conifer

Mid-Cretaceous pCO2 based on stomata of the extinct conifer Pseudofrenelopsis (Cheirolepidaceae)

by Haworth M., Hesselbo S. P., McElwain J. C., Robinson S. A., Brunt J. W. (2005)

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In Geology 33: 749-752 – doi: 10.1130/G21736.1 – 

https://www.academia.edu/31865286/Mid-Cretaceous_pCO2_based_on_stomata_of_the_extinct_conifer_Pseudofrenelopsis_Cheirolepidiaceae_

Abstract

Stomatal characteristics of an extinct Cretaceous conifer, Pseudofrenelopsis parceramosa</em> (Fontaine) Watson, are used to reconstruct atmospheric carbon dioxide (p</em>CO₂) over a time previously inferred to exhibit major fluctuations in this greenhouse gas.

Samples are from nonmarine to marine strata of the Wealden and Lower Greensand Groups of England and the Potomac Group of the eastern United States, of Hauterivian to Albian age (136 100 Ma).

Atmospheric p</em>CO₂ is estimated from the ratios between stomatal indices of fossil cuticles and those from four modern analogs (nearest living equivalent plants).

Using this approach, and two calibration methods to explore ranges, results show relatively low and only slightly varying p</em>CO₂ over the Hauterivian Albian interval: a low of ˜560 960 ppm in the early Barremian and a high of ˜620 1200 ppm in the Albian.

Data from the Barremian Wealden Group yield p</em>CO₂ values indistinguishable from a soil-carbonate based estimate from the same beds. The new p</em>CO₂ estimates are compatible with sedimentological and oxygen-isotope evidence for relatively cool mid-Cretaceous climates.

The SD/SI ratios of fossil plants may serve as indicators of the effectiveness of stomatal reconstructions of palaeo-[CO2]

 

 

Sulphur dioxide fumigation effects on stomatal density and index of non-resistant plants: implications for the stomatal palaeo-[CO2] proxy method

by Haworth M., Elliott-Kingston C., Gallagher A., Fitzgerald A., McElwain J. C. (2012)

Matthew Haworth, ^a Caroline Elliott-Kingston, ^b Angela Gallagher, ^c Annmarie Fitzgerald, ^b Jennifer C. McElwain, ^b

^a CNR – Istituto di Biometeorologia (IBIMET), Via Giovanni Caproni 8, 50145 Firenze Italy

^b School of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland

^c Department of Hydrology and Geo-environmental Sciences, Vrije Universiteit, De Boelelaan 1085–1087, 1081 HV Amsterdam, The Netherlands

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in Review of Palaeobotany and Palynology 182: 44-54 – https://doi.org/10.1016/j.revpalbo.2012.06.006 – 

https://www.sciencedirect.com/science/article/pii/S0034666712001546

Abstract

The inverse relationship between the number of stomata on the surface of a leaf and the atmospheric concentration of carbon dioxide ([CO₂]) in which it developed permits the use of fossil plants as indicators of palaeo-atmospheric [CO₂] level (palaeo-[CO₂]).

This “stomatal method” to reconstruct palaeo-[CO₂] is dependant upon stomatal initiation being determined by [CO₂]. However, global perturbations to the carbon cycle and climate system throughout earth history are not only characterised by fluctuations in the level of atmospheric [CO₂], but also by the release of large volumes of toxic gases such as sulphur dioxide (SO₂) into the atmosphere.

Recent studies have raised uncertainties into the efficacy of stomatal palaeo-[CO₂] proxies during episodes of SO₂ fumigation. This study aims to assess the effect of exposure to 0.2 ppm SO₂ on the stomatal frequencies of plant species with no evolutionarily acquired resistance to toxic gases in comparison to individuals grown under control conditions and atmospheres of elevated [CO₂].

Fumigation with SO₂ resulted in a general pattern of increased stomatal density (SD) values, but induced variability in the stomatal index (SI) responses of the plant species studied. Ginkgo biloba exhibited an increase in SI, whereas the araucariacean conifers Agathis australis and Araucaria bidwillii displayed reductions in SI that were indistinguishable from values observed under [CO₂] enrichment.

These results suggest that the presence of atmospheric SO₂ may reduce the effectiveness of stomatal reconstructions of palaeo-[CO₂] during intervals characterised by the release of large volumes of toxic gases into the atmosphere.

However, exposure to SO₂induced significant increases in the SD/SI ratios of six of the seven species studied. Calculation of the SD/SI ratios of fossil plants may identify any stratigraphic horizons where the stomatal initiation responses of the fossil flora were affected by sudden fumigation with toxic gases, and thus influence palaeo-[CO₂] estimates. Therefore the SD/SI ratios of fossil plants may serve as indicators of the effectiveness of stomatal reconstructions of palaeo-[CO₂].

Highlights

► Stomatal densities of fossil plants can be used to reconstruction past CO₂ levels.

► SO₂ may also affect stomatal development and therefore estimates of CO₂.

► Seven plants with no resistance to SO₂ were grown in controlled environments.

► SO₂ resulted in an increase in the ratio of stomatal density to index.

► This ratio may be employed to differentiate between SO₂ and CO₂ effects on stomata.

 

The high photosynthesis is underpinned by highly effective stomatal control

 

 

Increased free abscisic acid during drought enhances stomatal sensitivity and modifies stomatal behaviour in fast growing giant reed (Arundo donax L.)

by Haworth M., Marino G., Cosentino S. L., Brunetti C., Riggi,E., Avola G., Loreto F., Centritto M. (2018)

Matthew Haworth, ^a Giovanni Marino, ^a Salvatore  Luciano Cosentino, ^b Cecilia Brunetti, ^ac Anna De Carlo, ^a Giovanni Avola, ^a Ezio Riggi, ^a Francesco Loreto, ^d Mauro Centritto, ^a

^a National Research Council of Italy − Tree and Timber Institute, (CNR − IVALSA), Via Madonna del Piano 10 Sesto Fiorentino, 50019 Firenze, Italy

^b Dipartimento di Agricoltura, Alimentazione e Ambiente (Di3A), Università degli Studi di Catania, via Valdisavoia 5, 95123 Catania, Italy

^c Department of Agrifood Production and Environmental Sciences (DiSPAA), University of Florence, Viale delle Idee 30, 50019 Sesto Fiorentino, Firenze, Italy

^d National Research Council of Italy − Department of Biology, Agriculture and Food Sciences (CNR-DISBA), Rome, Italy

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in Environ. Exp. Bot. 147: 116–124 – DOI: 10.1016/j.envexpbot.2017.11.002 –

https://www.sciencedirect.com/science/article/abs/pii/S0098847217302733

Highlights

• Giant reed (Arundo donax) grows well in drought-prone marginal lands with a warm to hot climate.

* Effective stomatal control underpins rapid growth and tolerance of drought.

• Drought induced an increase in free-abscisic acid (ABA) in the leaves of A. donax.

• ABA increased stomatal sensitivity to CO₂ and light, but not vapour pressure deficit.

• Modification of stomatal behaviour allows A. donax to optimise water use efficiency.

Abstract

The rapid growth of the giant reed (Arundo donax L.) is sustained by high rates of photosynthesis (P_N) and stomatal conductance (G_s).

High rates of G_s would render A. donax vulnerable to desiccation during episodes of high evapotranspirative demand and/or low water availability if not accompanied by effective stomatal control. Stomatal control involves the adjustment of stomatal pore aperture to the prevailing environmental conditions and physiological status of the plant to optimise water use efficiency.

We assessed stomatal response to environmental signals (light intensity, [CO₂] and leaf to air vapour pressure deficit − VPD) and the foliar concentration of abscisic acid ([ABA]) of field grown A. donax under irrigated (control) and rain-fed (drought) conditions.

Drought-stressed A. donax showed more rapid reductions in G_s to lower light intensity/darkness, a slower rise in G_s following increased light and enhanced sensitivity to variations in [CO₂]. The stomatal response to leaf to air VPD was unaffected by the water status of the plant.

The rates of stomatal response to light/dark and [CO₂] were strongly correlated with the concentration of free-ABA within the cytosol but not with the relative water content of the leaves. When exposed to drought, stomata became increasingly sensitive to [CO₂] in comparison to PAR and leaf to air VPD.

This pronounced increase in stomatal sensitivity to [CO₂] was replicated by supplying exogenous ABA to cut leaves from a well-watered control plant.

The results of this study indicate that the high P_N of A. donax is underpinned by highly effective stomatal control.

The stomata of A. donax respond rapidly to changes in environmental conditions and their behaviour is sensitive to the concentration of ABA within the leaf. The high potential for gas exchange and stomatal control observed in A. donax makes it a suitable model species for enhanced stomatal control of P_N and the optimisation of stomatal behaviour.

 

The Impact of Heat Stress and Water Deficit on Stomatal Physiology of Olive

 

 

The Impact of Heat Stress and Water Deficit on the Photosynthetic and Stomatal Physiology of Olive (Olea europaea L.)—A Case Study of the 2017 Heat Wave

by Haworth M., Marino G., Brunetti C., Killi D., De Carlo A., Centritto M. (2018)

Matthew Haworth ^1,* ,

Giovanni Marino ¹

,Cecilia Brunetti ^1,2

,Dilek Killi ³

,Anna De Carlo ¹

Mauro Centritto ¹

¹

Tree and Timber Institute, National Research Council of Italy (CNR-IVALSA), Via Madonna del Piano 10, 50019 Firenze, Italy

²

Department of Agrifood Production and Environmental Sciences (DiSPAA), University of Florence, Viale delle Idee 30, 50019 Firenze, Italy

³

Institute of Biometeorology, National Research Council of Italy (CNR-IBIMET), Via Giovanni Caproni 8, 50145 Firenze, Italy

 

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in Plants 7(4): 76 – https://doi.org/10.3390/plants7040076 –

http://www.mdpi.com/2223-7747/7/4/76

Abstract

Heat waves are predicted to increase in frequency and duration in many regions as global temperatures rise. These transient increases in temperature above normal average values will have pronounced impacts upon the photosynthetic and stomatal physiology of plants.

During the summer of 2017, much of the Mediterranean experienced a severe heat wave. Here, we report photosynthetic leaf gas exchange and chlorophyll fluorescence parameters of olive (Olea europaea cv. Leccino) grown under water deficit and full irrigation over the course of the heat wave as midday temperatures rose over 40 °C in Central Italy.

Heat stress induced a decline in the photosynthetic capacity of the olives consistent with reduced ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO) activity. Damage to photosystem II was more apparent in plants subject to water deficit. In contrast to previous studies, higher temperatures induced reductions in stomatal conductance.

Heat stress adversely affected the carbon efficiency of olive. The selection of olive varieties with enhanced tolerance to heat stress and/or strategies to mitigate the impact of higher temperatures will become increasingly important in developing sustainable agriculture in the Mediterranean as global temperatures rise.

Stomatal factors involved in the evolutionary diversification of the angiosperms

 

 

Allocation of the epidermis to stomata relates to stomatal physiological control: Stomatal factors involved in the evolutionary diversification of the angiosperms and development of amphistomaty

by Haworth M., Scutt C. P., Douthe C., Marino G., Gaudio T., Loreto F., Flexas J. Centritto M. (2018)

Matthew Haworth, Charles P. Scutt, Cyril Douthe, Giovanni Marino, Thiago Gaudio, Francesco Loreto, Jaume Flexas, Mauro Centritto,

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in Environmental and Experimental Botany 151 – DOI: 10.1016/j.envexpbot.2018.04.010 –

https://www.researchgate.net/publication/324682498_Allocation_of_the_epidermis_to_stomata_relates_to_stomatal_physiological_control_Stomatal_factors_involved_in_the_evolutionary_diversification_of_the_angiosperms_and_development_of_amphistomaty

Abstract and figures

The proportion of the leaf epidermis allocated to stomata (EP%) and stomatal function (the capacity to adjust stomatal pore area to regulate stomatal conductance: Gs) are key components in leaf gas exchange, and have likely played a major role in plant evolution. We examined the velocity of change in Gs (Gs50%) during a transition from steady state conditions in the light to darkness and EP% in 31 vascular plants with diverse evolutionary origins. Across all species, EP% correlated to Gs50% and the magnitude of Gs reduction (GsLIGHT-GsDARK) after the cessation of illumination.

Those species with higher absolute and relative Gs50% values tended to distribute stomata more evenly over the abaxial and adaxial leaf surfaces, whereas species with lower Gs50% utilised only one leaf surface for gas exchange. Groups that diverged at relatively early stages in plant phylogeny, including ferns, gymnosperms and basal angiosperms, exhibited lower EP% and Gs50%, and took longer to achieve the initial 50% reduction in Gs (T50%) than the more recently diverging angiosperms; in particular, the amphistomatous monocot grasses, which also showed higher absolute rates of photosynthesis and Gs.

We propose that selective pressures induced by declining [CO2] over the past 100 Myr have favoured greater allocation of the epidermis to stomata, increased amphistomaty (the presence of stomata on the abaxial and adaxial surfaces) and faster control of Gs in the more recently derived angiosperm groups.

Modification of photosynthesis to enhance the carbon and water use efficiencies of C3 crops may therefore require concurrent increases in stomatal density and in the capacity of stomata to react quickly to environmental pressures.

Impaired stomatal control may increase the vulnerability of plants to water deficit and high temperatures

 

 

Impaired Stomatal Control Is Associated with Reduced Photosynthetic Physiology in Crop Species Grown at Elevated [CO₂]

by Haworth M., Killi D.,  Materassi A.,  Raschi A., Centritto M. (2016)

Matthew Haworth,^1,* Dilek Killi,² Alessandro Materassi,³ Antonio Raschi,³ and Mauro Centritto¹

¹ National Research Council – Tree and Timber Institute, Florence, Italy

² Department of Agrifood Production and Environmental Sciences, University of Florence, Florence, Italy

³ National Research Council – Institute of Biometeorology, Florence, Italy

 

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in Front Plant Sci. 7: 1568 – doi:  10.3389/fpls.2016.01568 – 

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5078776/

Abstract

Physiological control of stomatal conductance (G_s) permits plants to balance CO₂-uptake for photosynthesis (P_N) against water-loss, so optimizing water use efficiency (WUE). An increase in the atmospheric concentration of carbon dioxide ([CO₂]) will result in a stimulation of P_N and reduction of G_s in many plants, enhancing carbon gain while reducing water-loss.

It has also been hypothesized that the increase in WUE associated with lower G_s at elevated [CO₂] would reduce the negative impacts of drought on many crops. Despite the large number of CO₂-enrichment studies to date, there is relatively little information regarding the effect of elevated [CO₂] on stomatal control. Five crop species with active physiological stomatal behavior were grown at ambient (400 ppm) and elevated (2000 ppm) [CO₂].

We investigated the relationship between stomatal function, stomatal size, and photosynthetic capacity in the five species, and then assessed the mechanistic effect of elevated [CO₂] on photosynthetic physiology, stomatal sensitivity to [CO₂] and the effectiveness of stomatal closure to darkness.

We observed positive relationships between the speed of stomatal response and the maximum rates of P_N and G_s sustained by the plants; indicative of close co-ordination of stomatal behavior and P_N. In contrast to previous studies we did not observe a negative relationship between speed of stomatal response and stomatal size.

The sensitivity of stomata to [CO₂] declined with the ribulose-1,5-bisphosphate limited rate of P_N at elevated [CO₂]. The effectiveness of stomatal closure was also impaired at high [CO₂].

Growth at elevated [CO₂] did not affect the performance of photosystem II indicating that high [CO₂] had not induced damage to the photosynthetic physiology, and suggesting that photosynthetic control of G_s is either directly impaired at high [CO₂], sensing/signaling of environmental change is disrupted or elevated [CO₂] causes some physical effect that constrains stomatal opening/closing.

This study indicates that while elevated [CO₂] may improve the WUE of crops under normal growth conditions, impaired stomatal control may increase the vulnerability of plants to water deficit and high temperatures.