Apparent Overinvestment in Leaf Venation Relaxes Leaf Morphological Constraints on Photosynthesis in Arid Habitats

Boer, Hugo J. de; Drake, Paul L.; Wendt, Erin; Price, Charles A.; Schulze, Ernst Detlef; Turner, Neil C.; Nicolle, Dean; Veneklaas, Erik J.

doi:10.1104/pp.16.01313

Cited by 61 publications

(61 citation statements)

References 54 publications

(108 reference statements)

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“…PPFD, Photosynthetic photon flux density. 2005de Boer et al, 2016;McElwain et al, 2016;McElwain and Steinthorsdottir, 2017). Fiorin et al (2016) recently supported the hydraulic limitation theory, showing that uniformity of spatial patterning demonstrates an organization of veins and stomata that ensures a constant mesophyll hydraulic resistance throughout the leaf in woody angiosperm species, which agrees with the functional models of leaf hydraulic supply of Brodribb et al (2007) and Buckley et al (2015).…”

Section: Influence Of Stomatal Patterning On Leaf-level Gas Exchangesupporting

confidence: 54%

Diurnal Variation in Gas Exchange: The Balance between Carbon Fixation and Water Loss

2017

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Stomatal control of transpiration is critical for maintaining important processes, such as plant water status, leaf temperature, as well as permitting sufficient CO 2 diffusion into the leaf to maintain photosynthetic rates (A). Stomatal conductance often closely correlates with A and is thought to control the balance between water loss and carbon gain. It has been suggested that a mesophyll-driven signal coordinates A and stomatal conductance responses to maintain this relationship; however, the signal has yet to be fully elucidated. Despite this correlation under stable environmental conditions, the responses of both parameters vary spatially and temporally and are dependent on species, environment, and plant water status. Most current models neglect these aspects of gas exchange, although it is clear that they play a vital role in the balance of carbon fixation and water loss. Future efforts should consider the dynamic nature of whole-plant gas exchange and how it represents much more than the sum of its individual leaf-level components, and they should take into consideration the long-term effect on gas exchange over time.As the waxy surface of most leaves makes them virtually impermeable to CO 2 and water, nearly all CO 2 absorbed by the plant and water lost pass through the stomatal pores (Cowan and Troughton, 1971;Caird et al., 2007;Jones, 2013). Although these pores represent only a small fraction of the leaf surface, stomatal behavior has major consequences for photosynthetic CO 2 fixation and water loss from leaf to canopy levels, influencing carbon and hydrological cycles at global scales (Hetherington and Woodward, 2003;Keenan et al., 2013). Guard cells that surround the stomatal pore open and close in response to environmental stimuli, controlling the flux of gas between the leaf interior and the bulk atmosphere. Stomatal conductance (g s ) appears to be closely linked with mesophyll demands for CO 2 , and a strong correlation between photosynthetic rate (A) and g s is often observed (Wong et al., 1979;Farquhar and Sharkey, 1982;Mansfield et al., 1990;Buckley and Mott, 2013), and although conserved, it is not always constant (Lawson and Morison, 2004;Bonan et al., 2014). However, the A and properties of each leaf may not be identical and depend on acclimation to the surrounding microclimatic conditions; therefore, each leaf could be considered unique (Niinemets, 2016).In order to maintain an appropriate water status, plants must balance water loss between leaves with different properties depending on the availability of soil water, which raises the question about the regulation of g s at the whole-plant level. Early experiments by Meinzer and Grantz (1990) showed that the balance between water loss and water transport capacity enables the maintenance of a constant leaf water status over a wide range of plant sizes and growing conditions. Therefore, plants regulate the transpiration of each leaf independently in response to variations in microclimate by constantly adjusting stomatal aperture. The sto...

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Section: Influence Of Stomatal Patterning On Leaf-level Gas Exchangesupporting

confidence: 54%

Diurnal Variation in Gas Exchange: The Balance between Carbon Fixation and Water Loss

2017

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“…Although there are costs to developing thick amphistomatous leaves capable of high rates of water transport and gas exchange (such as a longer and potentially more tortuous path for water and a high carbon content), there is also a benefit of reduced heat stress (Schymanski et al ., ). As a high VLA can partially compensate for a reduction in K leaf caused by a large d y (de Boer et al ., ), this may explain the low d x : d y values observed here. An alternative morphology not considered in our analysis is the presence of two layers of veins, common in Acacia phyllodes, which may enable leaves to achieve a higher d x : d y .…”

Section: Inter‐vein and Vein‐epidermal Pathwaysmentioning

confidence: 47%

“…Thick eucalypt leaves, which tend to be amphistomatous (Fig. b), exhibit a very low d x : d y (down to 0.2) by combining a high VLA with a long outside‐xylem path length (de Boer et al ., ) (Fig. c).…”

Section: Inter‐vein and Vein‐epidermal Pathwaysmentioning

confidence: 83%

“…Many derived angiosperms achieve a (presumed) optimal vein placement by combining a relatively high VLA with relatively thin leaves (Zwieniecki & Boyce, ). In other phylogenetic clades, however, d x : d y is significantly greater than unity (Zwieniecki & Boyce, ) or less than unity (de Boer et al ., ).…”

Section: Inter‐vein and Vein‐epidermal Pathwaysmentioning

confidence: 97%

“…Amphistomaty is often observed in fast‐growing crops (Metcalfe & Chalk, ), in which high light and access to a continuous supply of water can provide an adaptive advantage from high leaf conductance (Mott et al ., ). Paradoxically, amphistomatous species can also be slow growing and are common in arid environments (Parkhurst, ), for example many arid‐zone eucalypts (Wood, ; de Boer et al ., ). When considering the functional benefits and costs of amphistomaty, it is important to distinguish leaves with a dorsiventral anatomy from those with an isobilateral anatomy (Fig.…”

Section: Introductionmentioning

confidence: 97%

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Two sides to every leaf: water and CO₂ transport in hypostomatous and amphistomatous leaves

et al. 2019

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Summary Leaves with stomata on both upper and lower surfaces, termed amphistomatous, are relatively rare compared with hypostomatous leaves with stomata only on the lower surface. Amphistomaty occurs predominantly in fast‐growing herbaceous annuals and in slow‐growing perennial shrubs and trees. In this paper, we present the current understanding and hypotheses on the costs and benefits of amphistomaty related to water and CO2 transport in contrasting leaf morphologies. First, there is no evidence that amphistomatous species achieve higher stomatal densities on a projected leaf area basis than hypostomatous species, but two‐sided gas exchange is less limited by boundary layer effects. Second, amphistomaty may provide a specific advantage in thick leaves by shortening the pathway for CO2 transport between the atmosphere and the chloroplasts. In thin leaves of fast‐growing herbaceous annuals, in which both the adaxial and abaxial pathways are already short, amphistomaty enhances leaf–atmosphere gas‐exchange capacity. Third, amphistomaty may help to optimise the leaf‐interior water status for CO2 transport by reducing temperature gradients and so preventing the condensation of water that could limit CO2 diffusion. Fourth, a potential cost of amphistomaty is the need for additional investments in leaf water transport tissue to balance the water loss through the adaxial surface.

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Amphistomy increases leaf photosynthesis more in coastal than montane plants of Hawaiian ʻilima (Sida fallax)

Triplett,

Buckley,

Muir

2024

American J of Botany

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PremiseThe adaptive significance of amphistomy (stomata on both upper and lower leaf surfaces) is unresolved. A widespread association between amphistomy and open, sunny habitats suggests the adaptive benefit of amphistomy may be greatest in these contexts, but this hypothesis has not been tested experimentally. Understanding amphistomy informs its potential as a target for crop improvement and paleoenvironment reconstruction.MethodsWe developed a method to quantify “amphistomy advantage” () as the log‐ratio of photosynthesis in an amphistomatous leaf to that of the same leaf but with gas exchange blocked through the upper surface (pseudohypostomy). Humidity modulated stomatal conductance and thus enabled comparing photosynthesis at the same total stomatal conductance. We estimated and leaf traits in six coastal (open, sunny) and six montane (closed, shaded) populations of the indigenous Hawaiian species ʻilima (Sida fallax).ResultsCoastal ʻilima leaves benefit 4.04 times more from amphistomy than montane leaves. Evidence was equivocal with respect to two hypotheses: (1) that coastal leaves benefit more because they are thicker and have lower CO2 conductance through the internal airspace and (2) that they benefit more because they have similar conductance on each surface, as opposed to most conductance being through the lower surface.ConclusionsThis is the first direct experimental evidence that amphistomy increases photosynthesis, consistent with the hypothesis that parallel pathways through upper and lower mesophyll increase CO2 supply to chloroplasts. The prevalence of amphistomatous leaves in open, sunny habitats can partially be explained by the increased benefit of amphistomy in “sun” leaves, but the mechanistic basis remains uncertain.

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Apparent Overinvestment in Leaf Venation Relaxes Leaf Morphological Constraints on Photosynthesis in Arid Habitats

Cited by 61 publications

References 54 publications

Diurnal Variation in Gas Exchange: The Balance between Carbon Fixation and Water Loss

Diurnal Variation in Gas Exchange: The Balance between Carbon Fixation and Water Loss

Two sides to every leaf: water and CO₂ transport in hypostomatous and amphistomatous leaves

Amphistomy increases leaf photosynthesis more in coastal than montane plants of Hawaiian ʻilima (Sida fallax)

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Apparent Overinvestment in Leaf Venation Relaxes Leaf Morphological Constraints on Photosynthesis in Arid Habitats

Cited by 61 publications

References 54 publications

Diurnal Variation in Gas Exchange: The Balance between Carbon Fixation and Water Loss

Diurnal Variation in Gas Exchange: The Balance between Carbon Fixation and Water Loss

Two sides to every leaf: water and CO2 transport in hypostomatous and amphistomatous leaves

Amphistomy increases leaf photosynthesis more in coastal than montane plants of Hawaiian ʻilima (Sida fallax)

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Two sides to every leaf: water and CO₂ transport in hypostomatous and amphistomatous leaves