Increased adaxial stomatal density is associated with greater mesophyll surface area exposed to intercellular air spaces and mesophyll conductance in diverse C 4 grasses
Abstract
Summary Mesophyll conductance ( g m ) is the diffusion of CO 2 from intercellular air spaces ( IAS ) to the first site of carboxylation in the mesophyll cells. In C 3 species, g m is influenced by diverse leaf structural and anatomical traits; however, little is known about traits affecting g m in C 4 species. To address this knowledge gap, we used online oxygen isotope discrimination measurements to estimate g m and microscopy techniques to measure leaf structural and anatomical traits potentially related to g m in 18 C 4 grasses. In this study, g m scaled positively with photosynthesis and intrinsic water‐use efficiency ( TE i ), but not with stomatal conductance. Also, g m was not determined by a single trait but was positively correlated with adaxial stomatal densities ( SD ada ), stomatal ratio ( SR ), mesophyll surface area exposed to IAS ( S mes ) and leaf thickness. However, g m was not related to abaxial stomatal densities ( SD aba ) and mesophyll cell wall thickness ( T CW ). Our study suggests that greater SD ada and SR increased g m by increasing S mes and creating additional parallel pathwaysmore »
- Authors:
-
[1];
[2];
[1]
- School of Biological Sciences Washington State University Pullman WA 99164‐4236 USA
- School of Biological Sciences Washington State University Pullman WA 99164‐4236 USA, Laboratory of Anatomy and Morphology V.L. Komarov Botanical Institute of the Russian Academy of Sciences 197376 St Petersburg Russia
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1560286
- Grant/Contract Number:
- DE‐SC0001685
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- New Phytologist
- Additional Journal Information:
- Journal Name: New Phytologist Journal Volume: 225 Journal Issue: 1; Journal ID: ISSN 0028-646X
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Pathare, Varsha S., Koteyeva, Nuria, and Cousins, Asaph B. Increased adaxial stomatal density is associated with greater mesophyll surface area exposed to intercellular air spaces and mesophyll conductance in diverse C 4 grasses. United Kingdom: N. p., 2019.
Web. doi:10.1111/nph.16106.
Pathare, Varsha S., Koteyeva, Nuria, & Cousins, Asaph B. Increased adaxial stomatal density is associated with greater mesophyll surface area exposed to intercellular air spaces and mesophyll conductance in diverse C 4 grasses. United Kingdom. https://doi.org/10.1111/nph.16106
Pathare, Varsha S., Koteyeva, Nuria, and Cousins, Asaph B. Wed .
"Increased adaxial stomatal density is associated with greater mesophyll surface area exposed to intercellular air spaces and mesophyll conductance in diverse C 4 grasses". United Kingdom. https://doi.org/10.1111/nph.16106.
@article{osti_1560286,
title = {Increased adaxial stomatal density is associated with greater mesophyll surface area exposed to intercellular air spaces and mesophyll conductance in diverse C 4 grasses},
author = {Pathare, Varsha S. and Koteyeva, Nuria and Cousins, Asaph B.},
abstractNote = {Summary Mesophyll conductance ( g m ) is the diffusion of CO 2 from intercellular air spaces ( IAS ) to the first site of carboxylation in the mesophyll cells. In C 3 species, g m is influenced by diverse leaf structural and anatomical traits; however, little is known about traits affecting g m in C 4 species. To address this knowledge gap, we used online oxygen isotope discrimination measurements to estimate g m and microscopy techniques to measure leaf structural and anatomical traits potentially related to g m in 18 C 4 grasses. In this study, g m scaled positively with photosynthesis and intrinsic water‐use efficiency ( TE i ), but not with stomatal conductance. Also, g m was not determined by a single trait but was positively correlated with adaxial stomatal densities ( SD ada ), stomatal ratio ( SR ), mesophyll surface area exposed to IAS ( S mes ) and leaf thickness. However, g m was not related to abaxial stomatal densities ( SD aba ) and mesophyll cell wall thickness ( T CW ). Our study suggests that greater SD ada and SR increased g m by increasing S mes and creating additional parallel pathways for CO 2 diffusion inside mesophyll cells. Thus, SD ada , SR and S mes are important determinants of C 4 ‐ g m and could be the target traits selected or modified for achieving greater g m and TE i in C 4 species.},
doi = {10.1111/nph.16106},
journal = {New Phytologist},
number = 1,
volume = 225,
place = {United Kingdom},
year = {Wed Sep 04 00:00:00 EDT 2019},
month = {Wed Sep 04 00:00:00 EDT 2019}
}
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Works referenced in this record:
Apparent Overinvestment in Leaf Venation Relaxes Leaf Morphological Constraints on Photosynthesis in Arid Habitats
journal, October 2016
- de Boer, Hugo J.; Drake, Paul L.; Wendt, Erin
- Plant Physiology, Vol. 172, Issue 4
The photosynthetic capacity in 35 ferns and fern allies: mesophyll CO 2 diffusion as a key trait
journal, October 2015
- Tosens, Tiina; Nishida, Keisuke; Gago, Jorge
- New Phytologist, Vol. 209, Issue 4
Stomatal conductance, mesophyll conductance, and transpiration efficiency in relation to leaf anatomy in rice and wheat genotypes under drought
journal, September 2017
- Ouyang, Wenjing; Struik, Paul C.; Yin, Xinyou
- Journal of Experimental Botany, Vol. 68, Issue 18
Making pore choices: repeated regime shifts in stomatal ratio
journal, August 2015
- Muir, Christopher D.
- Proceedings of the Royal Society B: Biological Sciences, Vol. 282, Issue 1813
Uncertainties and limitations of using carbon‐13 and oxygen‐18 leaf isotope exchange to estimate the temperature response of mesophyll CO 2 conductance in C 3 plants
journal, December 2018
- Sonawane, Balasaheb V.; Cousins, Asaph B.
- New Phytologist, Vol. 222, Issue 1
Mesophyll diffusion conductance to CO2: An unappreciated central player in photosynthesis
journal, September 2012
- Flexas, Jaume; Barbour, Margaret M.; Brendel, Oliver
- Plant Science, Vol. 193-194
Irradiance and phenotype: comparative eco-development of sun and shade leaves in relation to photosynthetic CO2 diffusion
journal, December 2005
- Terashima, Ichiro; Hanba, Yuko T.; Tazoe, Youshi
- Journal of Experimental Botany, Vol. 57, Issue 2
Photosynthesis at an extreme end of the leaf trait spectrum: how does it relate to high leaf dry mass per area and associated structural parameters?
journal, May 2010
- Hassiotou, Foteini; Renton, Michael; Ludwig, Martha
- Journal of Experimental Botany, Vol. 61, Issue 11
Resistances along the CO2 diffusion pathway inside leaves
journal, April 2009
- Evans, J. R.; Kaldenhoff, R.; Genty, B.
- Journal of Experimental Botany, Vol. 60, Issue 8
Cell-level anatomical characteristics explain high mesophyll conductance and photosynthetic capacity in sclerophyllous Mediterranean oaks
journal, January 2017
- Peguero-Pina, José Javier; Sisó, Sergio; Flexas, Jaume
- New Phytologist, Vol. 214, Issue 2
Improving water use in crop production
journal, July 2007
- Morison, J. I. L.; Baker, N. R.; Mullineaux, P. M.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1491
Diffusion of CO2 and other gases inside leaves
journal, March 1994
- Parkhurst, David F.
- New Phytologist, Vol. 126, Issue 3
Leaf responses to drought stress in Mediterranean accessions of Solanum lycopersicum : anatomical adaptations in relation to gas exchange parameters : Anatomical adaptations to water stress in tomato
journal, November 2012
- GalmÉS, Jeroni; OchogavÍA, Joan Manuel; Gago, Jorge
- Plant, Cell & Environment, Vol. 36, Issue 5
Physiological and structural tradeoffs underlying the leaf economics spectrum
journal, March 2017
- Onoda, Yusuke; Wright, Ian J.; Evans, John R.
- New Phytologist, Vol. 214, Issue 4
Mesophyll conductance to CO 2 and Rubisco as targets for improving intrinsic water use efficiency in C 3 plants : Gm and Rubisco: physiological traits driving WUEi
journal, December 2015
- Flexas, J.; Díaz-Espejo, A.; Conesa, M. A.
- Plant, Cell & Environment, Vol. 39, Issue 5
The Adaptive Significance of Stomatal Occurrence on One or Both Surfaces of Leaves
journal, July 1978
- Parkhurst, David F.
- The Journal of Ecology, Vol. 66, Issue 2
Importance of leaf anatomy in determining mesophyll diffusion conductance to CO2 across species: quantitative limitations and scaling up by models
journal, April 2013
- Tomás, Magdalena; Flexas, Jaume; Copolovici, Lucian
- Journal of Experimental Botany, Vol. 64, Issue 8
Extremely thick cell walls and low mesophyll conductance: welcome to the world of ancient living!
journal, March 2017
- Veromann-Jürgenson, Linda-Liisa; Tosens, Tiina; Laanisto, Lauri
- Journal of Experimental Botany, Vol. 68, Issue 7
Amphistomatic leaf surfaces independently regulate gas exchange in response to variations in evaporative demand
journal, June 2017
- Richardson, Freya; Brodribb, Timothy J.; Jordan, Gregory J.
- Tree Physiology, Vol. 37, Issue 7
Cell wall properties in Oryza sativa influence mesophyll CO 2 conductance
journal, April 2018
- Ellsworth, Patrícia V.; Ellsworth, Patrick Z.; Koteyeva, Nuria K.
- New Phytologist, Vol. 219, Issue 1
The influence of leaf thickness on the CO2 transfer conductance and leaf stable carbon isotope ratio for some evergreen tree species in Japanese warm-temperate forests
journal, October 1999
- Hanba, Y. T.; Miyazawa, S. -I.; Terashima, I.
- Functional Ecology, Vol. 13, Issue 5
Variable Mesophyll Conductance among Soybean Cultivars Sets a Tradeoff between Photosynthesis and Water-Use-Efficiency
journal, March 2017
- Tomeo, Nicholas J.; Rosenthal, David M.
- Plant Physiology, Vol. 174, Issue 1
FactoMineR : An R Package for Multivariate Analysis
journal, January 2008
- Lê, Sébastien; Josse, Julie; Husson, François
- Journal of Statistical Software, Vol. 25, Issue 1
Two sides to every leaf: water and CO 2 transport in hypostomatous and amphistomatous leaves
journal, January 2019
- Drake, Paul L.; Boer, Hugo J.; Schymanski, Stanislaus J.
- New Phytologist, Vol. 222, Issue 3
On the relationship between leaf anatomy and CO2 diffusion through the mesophyll of hypostomatous leaves
journal, February 1995
- Syvertsen, J. P.; Lloyd, J.; McCONCHIE, C.
- Plant, Cell and Environment, Vol. 18, Issue 2
Light and growth form interact to shape stomatal ratio among British angiosperms
journal, December 2017
- Muir, Christopher D.
- New Phytologist, Vol. 218, Issue 1
New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins
journal, November 2011
- Working Group, Grass Phylogeny
- New Phytologist, Vol. 193, Issue 2, p. 304-312
Online CO 2 and H 2 O oxygen isotope fractionation allows estimation of mesophyll conductance in C 4 plants, and reveals that mesophyll conductance decreases as leaves age in both C 4 and C 3 plants
journal, January 2016
- Barbour, Margaret M.; Evans, John R.; Simonin, Kevin A.
- New Phytologist, Vol. 210, Issue 3
Life history is a key factor explaining functional trait diversity among subtropical grasses, and its influence differs between C3 and C4 species
journal, February 2019
- Liu, Hui; Taylor, Samuel H.; Xu, Qiuyuan
- Journal of Experimental Botany, Vol. 70, Issue 5
Association genetics, geography and ecophysiology link stomatal patterning in Populus trichocarpa with carbon gain and disease resistance trade-offs
journal, November 2014
- McKown, Athena D.; Guy, Robert D.; Quamme, Linda
- Molecular Ecology, Vol. 23, Issue 23
The Application of Electronic Computers to Factor Analysis
journal, April 1960
- Kaiser, Henry F.
- Educational and Psychological Measurement, Vol. 20, Issue 1
Enhancement of leaf photosynthetic capacity through increased stomatal density in Arabidopsis
journal, February 2013
- Tanaka, Yu; Sugano, Shigeo S.; Shimada, Tomoo
- New Phytologist, Vol. 198, Issue 3
Leaf Functional Anatomy in Relation to Photosynthesis
journal, November 2010
- Terashima, Ichiro; Hanba, Yuko T.; Tholen, Danny
- Plant Physiology, Vol. 155, Issue 1
Ecological selection pressures for C 4 photosynthesis in the grasses
journal, February 2009
- Osborne, Colin P.; Freckleton, Robert P.
- Proceedings of the Royal Society B: Biological Sciences, Vol. 276, Issue 1663
Influence of stomatal distribution on transpiration in low-wind environments
journal, December 1986
- Foster, J. R.; Smith, W. K.
- Plant, Cell and Environment, Vol. 9, Issue 9
Evolution of a unique anatomical precision in angiosperm leaf venation lifts constraints on vascular plant ecology
journal, March 2014
- Zwieniecki, Maciej A.; Boyce, Charles K.
- Proceedings of the Royal Society B: Biological Sciences, Vol. 281, Issue 1779
The role of leaf width and conductances to CO 2 in determining water use efficiency in C 4 grasses
journal, May 2019
- Cano, Francisco Javier; Sharwood, Robert E.; Cousins, Asaph B.
- New Phytologist, Vol. 223, Issue 3
Diffusional conductances to CO2 as a target for increasing photosynthesis and photosynthetic water-use efficiency
journal, May 2013
- Flexas, Jaume; Niinemets, Ülo; Gallé, Alexander
- Photosynthesis Research, Vol. 117, Issue 1-3
Temperature response of mesophyll conductance in three C 4 species calculated with two methods: 18 O discrimination and in vitro V pmax
journal, December 2016
- Ubierna, Nerea; Gandin, Anthony; Boyd, Ryan A.
- New Phytologist, Vol. 214, Issue 1
Assessing the generality of global leaf trait relationships
journal, February 2005
- Wright, Ian J.; Reich, Peter B.; Cornelissen, Johannes H. C.
- New Phytologist, Vol. 166, Issue 2
Mesophyll conductance to CO 2 : current knowledge and future prospects
journal, May 2008
- Flexas, Jaume; Ribas-CarbÓ, Miquel; Diaz-Espejo, Antonio
- Plant, Cell & Environment, Vol. 31, Issue 5
Variability in mesophyll conductance between barley genotypes, and effects on transpiration efficiency and carbon isotope discrimination
journal, February 2010
- Barbour, Margaret M.; Warren, Charles R.; Farquhar, Graham D.
- Plant, Cell & Environment
Morphological and anatomical determinants of mesophyll conductance in wild relatives of tomato ( Solanum sect. Lycopersicon , sect. Lycopersicoides ; Solanaceae) : Mesophyll conductance in wild tomatoes
journal, December 2013
- Muir, Christopher D.; Hangarter, Roger P.; Moyle, Leonie C.
- Plant, Cell & Environment, Vol. 37, Issue 6
Anatomical basis of variation in mesophyll resistance in eastern Australian sclerophylls: news of a long and winding path
journal, August 2012
- Tosens, Tiina; Niinemets, Ülo; Westoby, Mark
- Journal of Experimental Botany, Vol. 63, Issue 14
Shifts in stomatal traits following the domestication of plant species
journal, July 2013
- Milla, Rubén; de Diego-Vico, Natalia; Martín-Robles, Nieves
- Journal of Experimental Botany, Vol. 64, Issue 11
Leaf hydraulic conductance is coordinated with leaf morpho-anatomical traits and nitrogen status in the genus Oryza
journal, November 2014
- Xiong, Dongliang; Yu, Tingting; Zhang, Tong
- Journal of Experimental Botany, Vol. 66, Issue 3
Photosynthetic pathway and ecological adaptation explain stomatal trait diversity amongst grasses
journal, November 2011
- Taylor, S. H.; Franks, P. J.; Hulme, S. P.
- New Phytologist, Vol. 193, Issue 2
Coordination of Leaf Photosynthesis, Transpiration, and Structural Traits in Rice and Wild Relatives (Genus Oryza)
journal, May 2013
- Giuliani, R.; Koteyeva, N.; Voznesenskaya, E.
- PLANT PHYSIOLOGY, Vol. 162, Issue 3
Mesophyll conductance in Zea mays responds transiently to CO 2 availability: implications for transpiration efficiency in C 4 crops
journal, December 2017
- Kolbe, Allison R.; Cousins, Asaph B.
- New Phytologist, Vol. 217, Issue 4
The Relationship Between CO2 Transfer Conductance and Leaf Anatomy in Transgenic Tobacco With a Reduced Content of Rubisco
journal, January 1994
- Evans, Jr; Caemmerer, Sv; Setchell, Ba
- Functional Plant Biology, Vol. 21, Issue 4
Estimating Mesophyll Conductance from Measurements of C 18 OO Photosynthetic Discrimination and Carbonic Anhydrase Activity
journal, August 2018
- Ogée, Jérôme; Wingate, Lisa; Genty, Bernard
- Plant Physiology, Vol. 178, Issue 2
Stomatal Behavior and CO 2 Exchange Characteristics in Amphistomatous Leaves
journal, January 1984
- Mott, Keith A.; O'Leary, James W.
- Plant Physiology, Vol. 74, Issue 1
Leaf anatomy mediates coordination of leaf hydraulic conductance and mesophyll conductance to CO 2 in Oryza
journal, September 2016
- Xiong, Dongliang; Flexas, Jaume; Yu, Tingting
- New Phytologist, Vol. 213, Issue 2
Carbon Dioxide Diffusion inside Leaves
journal, February 1996
- Evans, J. R.; von Caemmerer, S.
- Plant Physiology, Vol. 110, Issue 2