<i>Callitriche</i> as a potential model system for evolutionary studies on the dorsiventral distribution of stomata

Doll, Yuki; Koga, Hisao; Tsukaya, Hirokazu

doi:10.1080/15592324.2021.1978201

Cited by 7 publications

(4 citation statements)

References 27 publications

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“…Even in resupinate leaves where the abaxial surface faces up toward the sky, stomata develop on the lower adaxial surface (Lyshede, 2002). Exceptions to this general pattern include some arid woody plants which typically have vertically oriented, isobilateral leaves (Wood, 1934; Jordan et al, 2014; Boer et al, 2016; Drake et al, 2019) and floating/amphibious leaves of aquatic plants (Kaul, 1976; Doll et al, 2021). The dearth of amphistomatous leaves should be quite surprising and has been described as one of the most important unsolved problems in the study of leaf structure-function relations despite some recent progress (Grubb, 1977, 2020).…”

Section: Introductionmentioning

confidence: 99%

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

Triplett,

Buckley,

Muir

2023

Preprint

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Premise of the studyThe adaptive significance of stomata on both upper and lower leaf surfaces, called amphistomy, 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 why amphistomy evolves can inform its potential as a target for crop improvement and paleoenvironment reconstruction.MethodsWe developed a new method to quantify “amphistomy advantage”, AA, as the log-ratio of photosynthesis in an amphistomatous leaf to that of the same leaf but with gas exchange blocked through the upper (adaxial) surface, which we term “pseudohypostomy”. We used humidity to modulate stomatal conductance and thus compare photosynthetic rates at the same total stomatal conductance. We estimated AA and related physiological and anatomical traits in 12 populations, six coastal (open, sunny) and six montane (closed, shaded), of the indigenous Hawaiian species ‘ilima (Sida fallax).Key resultsCoastal ‘ilima leaves benefit 4.04 times more from amphistomy compared to their montane counterparts. Our evidence was equivocal with respect to two hypotheses – that coastal leaves benefit more because 1) they are thicker and therefore have lower CO2conductance through the internal airspace, and 2) that they benefit more because they have similar conductance on each surface, as opposed to most of the conductance being on the lower (abaxial) surface.ConclusionsThis is the first direct experimental evidence that amphistomyper seincreases photosynthesis, consistent with the hypothesis that parallel pathways through upper and lower mesophyll increase the supply of CO2to chloroplasts. The prevalence of amphistomatous leaves in open, sunny habitats can partially be explained the increased benefit of amphistomy in ‘sun’ leaves, but the mechanistic basis of this observation is an area for future research.

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Section: Introductionmentioning

confidence: 99%

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

Triplett,

Buckley,

Muir

2023

Preprint

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“…Callitriche is an ecologically diverse genus comprising not only terrestrial and aquatic species but also amphibious species that can grow both in water and on land ( Ito et al ., 2017 ). Accordingly, Callitriche species exhibit diversity in various aspects of stomatal development regulation, such as response to submergence ( Koga et al ., 2020 , 2021 ), dorsiventral stomatal distribution ( Doll et al ., 2021b ), and meristemoid behaviors ( Doll et al ., 2021a ). We found that meristemoids in terrestrial Callitriche species underwent multiple rounds of division before differentiating into stomata in a similar way to species with anisocytic stomata.…”

Section: Introductionmentioning

confidence: 99%

Experimental validation of the mechanism of stomatal development diversification

Doll

Koga

Tsukaya

2023

Journal of Experimental Botany

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Stomata are the structures responsible for gas exchange in plants. The established framework for stomatal development is based on the model plant Arabidopsis, but diverse patterns of stomatal development have been observed in other plant lineages and species. The molecular mechanisms behind these diversified patterns are still poorly understood. We recently proposed a model for the molecular mechanisms of the diversification of stomatal development based on the genus Callitriche (Plantaginaceae), according to which a temporal shift in the expression of key stomatal transcription factors SPEECHLESS and MUTE leads to changes in the behavior of meristemoids (stomatal precursor cells). In the present study, we genetically manipulated Arabidopsis to test this model. By altering the timing of MUTE expression, we successfully generated Arabidopsis plants with early differentiation or prolonged divisions of meristemoids, as predicted by the model. The epidermal morphology of the generated lines resembled that of species with prolonged or no meristemoid divisions. Thus, the evolutionary process can be reproduced by varying the SPEECHLESS to MUTE transition. We also observed unexpected phenotypes, which indicated the participation of additional factors in the evolution of the patterns observed in nature. This study provides novel experimental insights into the diversification of meristemoid behaviors.

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“…Even in resupinate leaves where the abaxial surface faces the sky, stomata develop on the lower adaxial surface (Lyshede, 2002). Exceptions to this general pattern include some arid woody plants that typically have vertically oriented, isobilateral leaves (Wood, 1934;Jordan et al, 2014;de Boer et al, 2016;Drake et al, 2019) and floating/amphibious leaves of aquatic plants (Kaul, 1976;Doll et al, 2021). The dearth of amphistomatous leaves should be quite surprising and has been described as one of the most important unsolved problems in the study of leaf structure-function relations despite some recent progress (Grubb, 1977(Grubb, , 2020.…”

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confidence: 99%

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.

show abstract

Callitriche as a potential model system for evolutionary studies on the dorsiventral distribution of stomata

Cited by 7 publications

References 27 publications

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

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

Experimental validation of the mechanism of stomatal development diversification

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

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