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.

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.