Drought stress triggers alterations of adaxial and abaxial stomatal development in basil leaves increasing water-use efficiency

Elisa Driesen , Maurice De Proft , Wouter Saeys

Horticulture Research ›› 2023, Vol. 10 ›› Issue (6) : 075

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Horticulture Research ›› 2023, Vol. 10 ›› Issue (6) :075 DOI: 10.1093/hr/uhad075
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Drought stress triggers alterations of adaxial and abaxial stomatal development in basil leaves increasing water-use efficiency
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Abstract

The physiological control of stomatal opening by which plants adjust for water availability has been extensively researched. However, the impact of water availability on stomatal development has not received as much attention, especially for amphistomatic plants. Therefore, the acclimation of stomatal development in basil (Ocimum basilicum L.) leaves was investigated. Our results show that leaves developed under water-deficit conditions possess higher stomatal densities and decreased stomatal length for both the adaxial and abaxial leaf sides. Although the stomatal developmental reaction to water deficit was similar for the two leaf surfaces, it was proven that adaxial stomata are more sensitive to water stress than abaxial stomata, with more closed adaxial stomata under water-deficit conditions. Furthermore, plants with leaves containing smaller stomata at higher densities possessed a higher water use efficiency. Our findings highlight the importance of stomatal development as a tool for long-term acclimation to limit water loss, with minimal reduction in biomass production. This highlights the central role that stomata play in both the short (opening) and long-term (development) reaction of plants to water availability, making them key tools for efficient resource use and anticipation of future environmental changes.

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Elisa Driesen, Maurice De Proft, Wouter Saeys. Drought stress triggers alterations of adaxial and abaxial stomatal development in basil leaves increasing water-use efficiency. Horticulture Research, 2023, 10 (6) : 075 DOI:10.1093/hr/uhad075

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Acknowledgements

The authors would like to thank Ir. Arthur Lauwers (Vegobel, Duffel, Belgium) for providing the growth chambers to conduct the experiments. This research was funded by Flanders Innovation & Entrepreneurship (Belgium) through project number HBC.2018.2070.

Author contribution

ED: conceptualization, methodology, formal analysis, investigation, writing – original draft, writing – review and editing, visualization funding acquisition. MDP and WS: conceptualization, methodology, writing – review & editing, funding acquisition. All authors reviewed and approved the final manuscript.

Data availability

All data can be obtained from the corresponding author upon request.

Conflict of interest statement

None declared.

References

[1]

Bertolino LT, Caine RS, Gray JE . Impact of stomatal density and morphology on water-use efficiency in a changing world. Front Plant Sci. 2019; 10: 225.

[2]

Chaerle L, Saibo N, Van Der Straeten D . Tuning the pores: towards engineering plants for improved water use efficiency. Trends Biotechnol. 2005; 23: 308-15.

[3]

Driesen E, De Proft M, Saeys W . Soil moisture levels affect the anatomy and mechanical properties of basil stems (Ocimum basilicum L.). Plan Theory. 2021; 10: 1-18.

[4]

Driesen E, Van den Ende W, De Proft M et al. Influence of environmental factors light, CO2, temperature, and relative humidity on Stomatal opening and development: a review . Agronomy. 2020; 10: 12.

[5]

Bucher SF, Auerswald K, Grün-Wenzel C et al. Stomatal traits relate to habitat preferences of herbaceous species in a temperate climate. Flora. 2017; 229: 107-15.

[6]

Mott KA, Leary JWO . Stomatal behavior and CO2 exchange characteristics in Amphistomatous leaves . Plant Physiol. 1984; 74: 47-51.

[7]

Richardson F, Brodribb TJ, Jordan GJ . Amphistomatic leaf surfaces independently regulate gas exchange in response to variations in evaporative demand. Tree Physiol. 2017; 37: 869-78.

[8]

Soares AS, Driscoll SP, Olmos E et al. Adaxial/abaxial specification in the regulation of photosynthesis and stomatal opening with respect to light orientation and growth with CO2 enrichment in the C4 species Paspalum dilatatum. New Phytol. 2008; 177: 186-98.

[9]

Aston M. Differences in the behaviour of Adaxial and Abaxial stomata of Amphistomatous sunflower leaves: inherent or environmental? Funct Plant Biol. 1978; 5: 211.

[10]

Driscoll SP, Prins A, Olmos E et al. Specification of adaxial and abaxial stomata, epidermal structure and photosynthesis to CO2 enrichment in maize leaves . J Exp Bot. 2006; 57: 381-90.

[11]

Wang Y, Noguchi K, Terashima I . Distinct light responses of the adaxial and abaxial stomata in intact leaves of Helianthus annuus L. Plant Cell Environ. 2008; 31: 1307-16.

[12]

Xu Z, Zhou G . Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. J Exp Bot. 2008; 59: 3317-25.

[13]

Hamanishi ET, Thomas BR, Campbell MM . Drought induces alterations in the stomatal development program in Populus. J Exp Bot. 2012; 63: 4959-71.

[14]

Jones HG . Breeding for stomatal characters. In: Zeiger E, Farquar G, eds. Stomatal Function. Standford University Press: Standford, CA, 1987, 431-43.

[15]

Milla R, De Diego-Vico N, Martín-Robles N . Shifts in stomatal traits following the domestication of plant species. J Exp Bot. 2013; 64: 3137-46.

[16]

Muir CD . Light and growth form interact to shape stomatal ratio among British angiosperms. New Phytol. 2018; 218: 242-52.

[17]

Muir CD . Making pore choices: repeated regime shifts in Stomatal ratio. Proc R Soc B Biol Sci. 2015; 282: 1-9.

[18]

Mott KA, Gibson AC, O’Leary JW . The adaptive significance of amphistomatic leaves. Plant Cell Environ. 1982; 5: 455-60.

[19]

Parkhurst DF . The adaptive significance of Stomatal occurrence on one or both surfaces of leaves. J Ecol. 1978; 66: 367-83.

[20]

Xiong D, Flexas J . From one side to two sides: the effects of stomatal distribution on photosynthesis. New Phytol. 2020; 228: 1754-66.

[21]

Drake PL, de Boer HJ, Schymanski SJ et al. Two sides to every leaf: water and CO2 transport in hypostomatous and amphistomatous leaves . New Phytol. 2019; 222: 1179-87.

[22]

Terashima I, Miyazawa SI, Hanba YT . Why are sun leaves thicker than shade leaves? - consideration based on analyses of CO2 diffusion in the leaf . J Plant Res. 2001; 114: 93-105.

[23]

Muir CD . Is Amphistomy an adaptation to high light? Optimality models of Stomatal traits along light gradients. Integr Comp Biol. 2019; 59: 571-84.

[24]

Richardson F, Jordan GJ, Brodribb TJ . Leaf hydraulic conductance is linked to leaf symmetry in bifacial, amphistomatic leaves of sunflower. J Exp Bot. 2020; 71: 2808-16.

[25]

Haworth M, Scutt CP, Douthe C et al. 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. Environ Exp Bot. 2018; 151: 55-63.

[26]

Buckley TN, John GP, Scoffoni C et al. The sites of evaporation within leaves. Plant Physiol. 2017; 173: 1763-82.

[27]

Haworth M, Marino G, Loreto F et al. Integrating stomatal physiology and morphology: evolution of stomatal control and development of future crops. Oecologia. 2021; 197: 867-83.

[28]

Raviv M, Blom TJ . The effect of water availability and quality on photosynthesis and productivity of soilless-grown cut roses. Sci Hortic. 2001; 88: 257-76.

[29]

Montesano FF, van Iersel MW, Boari F et al. Sensor-based irrigation management of soilless basil using a new smart irrigation system: effects of set-point on plant physiological responses and crop performance. Agric Water Manag. 2018; 203: 20-9.

[30]

de Boodt M, Verdonck O . The physical properties of the substrates in horticulture. Acta Hortic. 1972; 26: 37-44.

[31]

Yin Q, Tian T, Kou M et al. The relationships between photosynthesis and stomatal traits on the loess plateau. Glob Ecol Conserv. 2020; 23: e01146.

[32]

Franks PJ, Beerling DJ . Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time . Proc Natl Acad Sci U S A. 2009; 106: 10343-7.

[33]

Aguirrezabal L, Bouchier-Combaud S, Radziejwoski A et al. Plasticity to soil water deficit in Arabidopsis thaliana: dissection of leaf development into underlying growth dynamic and cellular variables reveals invisible phenotypes. Plant Cell Environ. 2006; 29: 2216-27.

[34]

Sadras VO, Milroy SP . Soil-water thresholds for the responses of leaf expansion and gas exchange: a review. Field Crops Res. 1996; 47: 253-66.

[35]

Soltani A, Khooie FR, Ghassemi-Golezani K et al. Thresholds for chickpea leaf expansion and transpiration response to soil water deficit. Field Crop Res. 2000; 68: 205-10.

[36]

Passioura JB . Soil conditions and plant growth. Plant Cell Environ. 2002; 25: 311-8.

[37]

Begum FA, Paul NK . Influence of soil moisture on growth, water use and yield of mustard. J Agron Crop Sci. 1993; 170: 136-41.

[38]

Clauw P, Coppens F, De Beuf K et al. Leaf responses to mild drought stress in natural variants of Arabidopsis. Plant Physiol. 2015; 167: 800-16.

[39]

Copolovici L, Lupitu A, Moisa C et al. The effect of antagonist abiotic stress on bioactive compounds from basil (Ocimum basilicum). Appl Sci. 2021; 11: 9282.

[40]

Galmés J, Flexas J, Savé R et al. Water relations and stomatal characteristics of Mediterranean plants with different growth forms and leaf habits: responses to water stress and recovery. Plant Soil. 2007; 290: 139-55.

[41]

Bergmann DC, Sack FD . Stomatal development. Annu Rev Plant Biol. 2007; 58: 163-81.

[42]

Quarrie SA, Jones HG . Effects of abscisic acid and water stress on development and morphology of wheat. J Exp Bot. 1977; 28: 192-203.

[43]

Pyankov VI, Voznesenskaya EV, Kuz’min AN et al. Occurrence of C3 and C4 photosynthesis in cotyledons and leaves of Salsola species (Chenopodiaceae). Photosynth Res. 2000; 63: 69-84.

[44]

Shi Y, Chen J, Hou X . Similarities and differences of photosynthesis establishment related mRNAs and novel lncRNAs in early seedlings (coleoptile/cotyledon vs. true leaf) of Rice and Arabidopsis. Front Genet. e2020; 11: 1-18.

[45]

Hetherington AM, Woodward FI . The role of stomata in sensing and driving environmental change. Nature. 2003; 424: 901-8.

[46]

Drake PL, Froend RH, Franks PJ . Smaller, faster stomata: scaling of stomatal size, rate of response, and stomatal conductance. J Exp Bot. 2013; 64: 495-505.

[47]

Franks PJ, Drake PL, Beerling DJ . Plasticity in maximum stomatal conductance constrained by negative correlation between stomatal size and density: an analysis using Eucalyptus globulus. Plant Cell Environ. 2009; 32: 1737-48.

[48]

Raven JA . Speedy small stomata? J Exp Bot. 2014; 65: 1415-24.

[49]

Wang Y, Noguchi K, Terashima I . Photosynthesis-dependent and -independent responses of stomata to blue, red and green monochromatic light: differences between the normally oriented and inverted leaves of sunflower. Plant Cell Physiol. 2011; 52: 479-89.

[50]

Mott KA . Leaf hydraulic conductivity and stomatal responses to humidity in amphistomatous leaves. Plant Cell Environ. 2007; 30: 1444-9.

[51]

McKown AD, Guy RD, Quamme L et al. Association genetics, geography and ecophysiology link stomatal patterning in Populus trichocarpa with carbon gain and disease resistance trade-offs . Mol Ecol. 2014; 23: 5771-90.

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