The influence of stomatal morphology and distribution on photosynthetic gas exchange

Harrison, Emily; Cubas, Lucía Arce; Gray, Julie E.; Hepworth, Christopher

doi:10.1111/tpj.14560

Cited by 169 publications

(150 citation statements)

References 104 publications

(163 reference statements)

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“…Stomatal density and size set the upper limit on gas exchange in leaves (Harrison et al, 2019) and is often closely related to operational stomatal conductance in nature (Murray et al, 2019). Despite the fact that many foliar pathogens infect through stomata, the relationship between stomatal anatomy and resistance to foliar pathogens is less clear than it is for gas exchange.…”

Section: Discussionmentioning

confidence: 99%

“…In summary, the physical relationship between stomatal size, density, and conductance is well-established (Harrison et al, 2019). Size and density also likely affect the probability of pathogen colonization, but we do not have a theoretical model that makes quantitative predictions.…”

Section: Introductionmentioning

confidence: 94%

“…The stomatal density and maximum pore area set an anatomical upper limit on stomatal conductance (Brown and Escombe, 1900;Parlange and Waggoner, 1970;Franks and Farquhar, 2001;Franks and Beerling, 2009b;Lehmann and Or, 2015;Sack and Buckley, 2016;Harrison et al, 2019), but stomatal shape, distribution, and patterning also affect gas exchange. Smaller guard cells and dumbbell-shaped stomata of grasses can respond faster to environmental changes (Drake et al, 2013), but responsiveness is further modulated by subsidiary cell anatomy and physiology (Franks and Farquhar, 2007;Raissig et al, 2017;Gray et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

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A Stomatal Model of Anatomical Tradeoffs Between Gas Exchange and Pathogen Colonization

Muir

2020

Front. Plant Sci.

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Stomatal pores control leaf gas exchange and are one route for infection of internal plant tissues by many foliar pathogens, setting up the potential for tradeoffs between photosynthesis and pathogen colonization. Anatomical shifts to lower stomatal density and/or size may also limit pathogen colonization, but such developmental changes could permanently reduce the gas exchange capacity for the life of the leaf. I developed and analyzed a spatially explicit model of pathogen colonization on the leaf as a function of stomatal size and density, anatomical traits which partially determine maximum rates of gas exchange. The model predicts greater stomatal size or density increases the probability of colonization, but the effect is most pronounced when the fraction of leaf surface covered by stomata is low. I also derived scaling relationships between stomatal size and density that preserves a given probability of colonization. These scaling relationships set up a potential anatomical conflict between limiting pathogen colonization and minimizing the fraction of leaf surface covered by stomata. Although a connection between gas exchange and pathogen defense has been suggested empirically, this is the first mathematical model connecting gas exchange and pathogen defense via stomatal anatomy. A limitation of the model is that it does not include variation in innate immunity and stomatal closure in response to pathogens. Nevertheless, the model makes predictions that can be tested with experiments and may explain variation in stomatal size and density among plants. The model is generalizable to many types of pathogens, but lacks significant biological realism that may be needed for precise predictions.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 94%

Section: Introductionmentioning

confidence: 99%

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A Stomatal Model of Anatomical Tradeoffs Between Gas Exchange and Pathogen Colonization

Muir

2020

Front. Plant Sci.

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“…It has been shown that changes to stomatal size and density can be correlated with g s , and so it follows that genetic manipulation of SD has the potential to increase photosynthetic gas exchange (Franks et al, 2012). However, as pointed out by Harrison et al (2019), such a coupling between SD and gas exchange does not always exist in practice. Nevertheless, Arabidopsis EPFL9overexpressing plants (with~600% increased SD) show enhanced A at both ambient and elevated CO 2 , probably due to a much increased g s (Tanaka et al, 2013).…”

Section: Can Increases To Stomatal Density Improve Photosynthetic Effmentioning

confidence: 99%

Pores for Thought: Can Genetic Manipulation of Stomatal Density Protect Future Rice Yields?

2020

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Rice (Oryza sativa L.) contributes to the diets of around 3.5 billion people every day and is consumed more than any other plant. Alarmingly, climate predictions suggest that the frequency of severe drought and high-temperature events will increase, and this is set to threaten the global rice supply. In this review, we consider whether water or heat stresses in cropsespecially ricecould be mitigated through alterations to stomata; minute pores on the plant epidermis that permit carbon acquisition and regulate water loss. In the short-term, water loss is controlled via alterations to the degree of stomatal "openness", or, in the longer-term, by altering the number (or density) of stomata that form. A range of molecular components contribute to the regulation of stomatal density, including transcription factors, plasma membrane-associated proteins and intercellular and extracellular signaling molecules. Much of our existing knowledge relating to stomatal development comes from research conducted on the model plant, Arabidopsis thaliana. However, due to the importance of cereal crops to global food supply, studies on grass stomata have expanded in recent years, with molecular-level discoveries underscoring several divergent developmental and morphological features. Cultivation of rice is particularly water-intensive, and there is interest in developing varieties that require less water yet still maintain grain yields. This could be achieved by manipulating stomatal development; a crop with fewer stomata might be more conservative in its water use and therefore more capable of surviving periods of water stress. However, decreasing stomatal density might restrict the rate of CO 2 uptake and reduce the extent of evaporative cooling, potentially leading to detrimental effects on yields. Thus, the extent to which crop yields in the future climate will be affected by increasing or decreasing stomatal density should be determined. Here, our current understanding of the regulation of stomatal development is summarised, focusing particularly on the genetic mechanisms that have recently been described for rice and other grasses. Application of this knowledge toward the creation of "climate-ready" rice is discussed, with attention drawn to the lesser-studied molecular elements whose contributions to the complexity of grass stomatal development must be understood to advance efforts.

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“…The triple MAPK BdYODA was shown to be involved in maintaining fate asymmetry, and bdyda mutant plants showed clustered stomata, prickle hair cells and silica cells within but never between cell files (Abrash et al, 2018). Furthermore, overexpression of EPF1 in barley, rice and wheat drastically reduced stomatal density and resulted in more drought-resistant plants (for review, see Hughes et al, 2017;Caine et al, 2018;Bertolino et al, 2019;Dunn et al, 2019;Harrison et al 2019;Lu et al, 2019). Similarly, CRISPR/Cas9-editing of the stomatal fate promoting OsEPFL9/OsSTOMAGEN lead to an eightfold decrease in stomatal density in rice leaves (Yin et al, 2017).…”

Section: The One-cell-spacing Rulecontrol Of Stomatal Patterning and mentioning

confidence: 99%

Form, development and function of grass stomata

2019

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Summary Stomata are cellular breathing pores on leaves that open and close to absorb photosynthetic carbon dioxide and to restrict water loss through transpiration, respectively. Grasses (Poaceae) form morphologically innovative stomata, which consist of two dumbbell‐shaped guard cells flanked by two lateral subsidiary cells (SCs). This ‘graminoid’ morphology is associated with faster stomatal movements leading to more water‐efficient gas exchange in changing environments. Here, we offer a genetic and mechanistic perspective on the unique graminoid form of grass stomata and the developmental innovations during stomatal cell lineage initiation, recruitment of SCs and stomatal morphogenesis. Furthermore, the functional consequences of the four‐celled, graminoid stomatal morphology are summarized. We compile the identified players relevant for stomatal opening and closing in grasses, and discuss possible mechanisms leading to cell‐type‐specific regulation of osmotic potential and turgor. In conclusion, we propose that the investigation of functionally superior grass stomata might reveal routes to improve water‐stress resilience of agriculturally relevant plants in a changing climate.

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The influence of stomatal morphology and distribution on photosynthetic gas exchange

Cited by 169 publications

References 104 publications

A Stomatal Model of Anatomical Tradeoffs Between Gas Exchange and Pathogen Colonization

A Stomatal Model of Anatomical Tradeoffs Between Gas Exchange and Pathogen Colonization

Pores for Thought: Can Genetic Manipulation of Stomatal Density Protect Future Rice Yields?

Form, development and function of grass stomata

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