Linking structure to function: the connection between mesophyll structure and intrinsic water use efficiency
Jeroen D. M. Schreel
A B * , Guillaume Théroux-Rancourt C and Adam B. Roddy A
A
B
C
Abstract
Climate change-driven drought events are becoming unescapable in an increasing number of areas worldwide. Understanding how plants are able to adapt to these changing environmental conditions is a non-trivial challenge. Physiologically, improving a plant’s intrinsic water use efficiency (WUEi) will be essential for plant survival in dry conditions. Physically, plant adaptation and acclimatisation are constrained by a plant’s anatomy. In other words, there is a strong link between anatomical structure and physiological function. Former research predominantly focused on using 2D anatomical measurements to approximate 3D structures based on the assumption of ideal shapes, such as spherical spongy mesophyll cells. As a result of increasing progress in 3D imaging technology, the validity of these assumptions is being assessed, and recent research has indicated that these approximations can contain significant errors. We suggest to invert the workflow and use the less common 3D assessments to provide corrections and functions for the more widely available 2D assessments. By combining these 3D and corrected 2D anatomical assessments with physiological measurements of WUEi, our understanding of how a plant’s physical adaptation affects its function will increase and greatly improve our ability to assess plant survival.
Keywords: functional plant anatomy, intercellular airspace, leaf anatomy, leaf functional traits, leaf structure, mesophyll, structure-function relations, water use efficiency.
References
Barbier de Reuille P, Routier-Kierzkowska A-L, Kierzkowski D, Bassel GW, Schüpbach T, Tauriello G, Bajpai N, Strauss S, Weber A, Kiss A, et al. (2015) MorphoGraphX: a platform for quantifying morphogenesis in 4D. eLife 4, e05864.
| Crossref | Google Scholar |
Borsuk AM, Roddy AB, Théroux-Rancourt G, Brodersen CR (2022) Structural organization of the spongy mesophyll. New Phytologist 234, 946-960.
| Crossref | Google Scholar | PubMed |
Brodersen CR, Roddy AB (2016) New frontiers in the three-dimensional visualization of plant structure and function. American Journal of Botany 103, 184-188.
| Crossref | Google Scholar | PubMed |
Bunce J (2016) Variation among soybean cultivars in mesophyll conductance and leaf water use efficiency. Plants 5, 44.
| Crossref | Google Scholar |
Corlett RT, Westcott DA (2013) Will plant movements keep up with climate change? Trends in Ecology & Evolution 28, 482-488.
| Crossref | Google Scholar | PubMed |
Earles JM, Théroux-Rancourt G, Roddy AB, Gilbert ME, McElrone AJ, Brodersen CR (2018) Beyond porosity: 3D leaf intercellular airspace traits that impact mesophyll conductance. Plant Physiology 178, 148-162.
| Crossref | Google Scholar | PubMed |
Earles JM, Buckley TN, Brodersen CR, Busch FA, Cano FJ, Choat B, Evans JR, Farquhar GD, Harwood R, Huynh M, et al. (2019) Embracing 3D complexity in leaf carbon–water exchange. Trends in Plant Science 24, 15-24.
| Crossref | Google Scholar | PubMed |
Evans JR, Kaldenhoff R, Genty B, Terashima I (2009) Resistances along the CO2 diffusion pathway inside leaves. Journal of Experimental Botany 60, 2235-2248.
| Crossref | Google Scholar | PubMed |
Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A, Sadia S, Nasim W, Adkins S, Saud S, et al. (2017) Crop production under drought and heat stress: plant responses and management options. Frontiers in Plant Science 8, 1147.
| Crossref | Google Scholar |
Feeley KJ, Bravo-Avila C, Fadrique B, Perez TM, Zuleta D (2020) Climate-driven changes in the composition of New World plant communities. Nature Climate Change 10, 965-970.
| Crossref | Google Scholar |
Fitzpatrick MC, Gove AD, Sanders NJ, Dunn RR (2008) Climate change, plant migration, and range collapse in a global biodiversity hotspot: the Banksia (Proteaceae) of Western Australia. Global Change Biology 14, 1337-1352.
| Crossref | Google Scholar |
Harwood R, Goodman E, Gudmundsdottir M, Huynh M, Musulin Q, Song M, Barbour MM (2020) Cell and chloroplast anatomical features are poorly estimated from 2D cross-sections. New Phytologist 225, 2567-2578.
| Crossref | Google Scholar | PubMed |
Harwood R, Théroux-Rancourt G, Barbour MM (2021) Understanding airspace in leaves: 3D anatomy and directional tortuosity. Plant, Cell & Environment 44, 2455-2465.
| Crossref | Google Scholar | PubMed |
Hentschel R, Hommel R, Poschenrieder W, Grote R, Holst J, Biernath C, Gessler A, Priesack E (2016) Stomatal conductance and intrinsic water use efficiency in the drought year 2003: a case study of European beech. Trees 30, 153-174.
| Crossref | Google Scholar |
Hogan KP, Smith AP, Aruis JL, Saavedra A (1994) Ecotypic differentiation of gas exchange responses and leaf anatomy in a tropical forest understory shrub from areas of contrasting rainfall regimes. Tree Physiology 14, 819-831.
| Crossref | Google Scholar | PubMed |
IPCC (2018) Global Warming of 1.5°C. An IPCC Special Report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty. IPCC.
Janová J, Kubásek J, Grams TEE, Zeisler-Diehl V, Schreiber L, Šantrůček J (2024) Effect of light-induced changes in leaf anatomy on intercellular and cellular components of mesophyll resistance for CO2 in Fagus sylvatica. Plant Biology 26, 842-854.
| Crossref | Google Scholar | PubMed |
Jordan GJ, Carpenter RJ, Holland BR, Beeton NJ, Woodhams MD, Brodribb TJ (2020) Links between environment and stomatal size through evolutionary time in Proteaceae. Proceedings of the Royal Society B: Biological Sciences 287, 20192876.
| Crossref | Google Scholar |
Lauteri M, Scartazza A, Guido MC, Brugnoli E (1997) Genetic variation in photosynthetic capacity, carbon isotope discrimination and mesophyll conductance in provenances of Castanea sativa adapted to different environments. Functional Ecology 11, 675-683.
| Crossref | Google Scholar |
Liu C, He N, Zhang J, Li Y, Wang Q, Sack L, Yu G (2018) Variation of stomatal traits from cold temperate to tropical forests and association with water use efficiency. Functional Ecology 32, 20-28.
| Crossref | Google Scholar |
Lundgren MR, Mathers A, Baillie AL, Dunn J, Wilson MJ, Hunt L, Pajor R, Fradera-Soler M, Rolfe S, Osborne CP, et al. (2019) Mesophyll porosity is modulated by the presence of functional stomata. Nature Communications 10, 2825.
| Crossref | Google Scholar |
Maggio A, Hasegawa PM, Bressan RA, Consiglio MF, Joly RJ (2001) Review: Unravelling the functional relationship between root anatomy and stress tolerance. Australian Journal of Plant Physiology 28, 999-1004.
| Crossref | Google Scholar |
Mathers AW, Hepworth C, Baillie AL, Sloan J, Jones H, Lundgren M, Fleming AJ, Mooney SJ, Sturrock CJ (2018) Investigating the microstructure of plant leaves in 3D with lab-based X-ray computed tomography. Plant Methods 14, 99.
| Crossref | Google Scholar |
Momayyezi M, Borsuk AM, Brodersen CR, Gilbert ME, Théroux-Rancourt G, Kluepfel DA, McElrone AJ (2022) Desiccation of the leaf mesophyll and its implications for CO2 diffusion and light processing. Plant, Cell & Environment 45, 1362-1381.
| Crossref | Google Scholar | PubMed |
Rippner DA, Raja PV, Earles JM, Momayyezi M, Buchko A, Duong FV, Forrestel EJ, Parkinson DY, Shackel KA, Neyhart JL, et al. (2022) A workflow for segmenting soil and plant X-ray computed tomography images with deep learning in Google’s Colaboratory. Frontiers in Plant Science 13, 893140.
| Crossref | Google Scholar |
Roddy AB, Théroux-Rancourt G, Abbo T, Benedetti JW, Brodersen CR, Castro M, Castro S, Gilbride AB, Jensen B, Jiang G-F, et al. (2020) The scaling of genome size and cell size limits maximum rates of photosynthesis with implications for ecological strategies. International Journal of Plant Sciences 181, 75-87.
| Crossref | Google Scholar |
Seibt U, Rajabi A, Griffiths H, Berry JA (2008) Carbon isotopes and water use efficiency: sense and sensitivity. Oecologia 155, 441-454.
| Crossref | Google Scholar | PubMed |
Shao H-B, Chu L-Y, Jaleel CA, Zhao C-X (2008) Water-deficit stress-induced anatomical changes in higher plants. Comptes Rendus. Biologies 331, 215-225.
| Crossref | Google Scholar | PubMed |
Théroux-Rancourt G, Gilbert ME (2017) The light response of mesophyll conductance is controlled by structure across leaf profiles. Plant, Cell & Environment 40, 726-740.
| Crossref | Google Scholar | PubMed |
Théroux-Rancourt G, Earles JM, Gilbert ME, Zwieniecki MA, Boyce CK, McElrone AJ, Brodersen CR (2017) The bias of a two-dimensional view: comparing two-dimensional and three-dimensional mesophyll surface area estimates using noninvasive imaging. New Phytologist 215, 1609-1622.
| Crossref | Google Scholar | PubMed |
Théroux-Rancourt G, Voggeneder K, Tholen D (2020a) Shape matters: the pitfalls of analyzing mesophyll anatomy. New Phytologist 225, 2239-2242.
| Crossref | Google Scholar | PubMed |
Théroux-Rancourt G, Jenkins MR, Brodersen CR, McElrone A, Forrestel EJ, Earles JM (2020b) Digitally deconstructing leaves in 3D using X-ray microcomputed tomography and machine learning. Applications in Plant Sciences 8, e11380.
| Crossref | Google Scholar |
Théroux-Rancourt G, Roddy AB, Earles JM, Gilbert ME, Zwieniecki MA, Boyce CK, Tholen D, McElrone AJ, Simonin KA, Brodersen CR (2021) Maximum CO2 diffusion inside leaves is limited by the scaling of cell size and genome size. Proceedings of the Royal Society B: Biological Sciences 288, 20203145.
| Crossref | Google Scholar |
Théroux-Rancourt G, Herrera JC, Voggeneder K, De Berardinis F, Luijken N, Nocker L, Savi T, Scheffknecht S, Schneck M, Tholen D (2023) Analyzing anatomy over three dimensions unpacks the differences in mesophyll diffusive area between sun and shade Vitis vinifera leaves. AoB Plants 15, plad001.
| Crossref | Google Scholar |
Trueba S, Théroux-Rancourt G, Earles JM, Buckley TN, Love D, Johnson DM, Brodersen C (2022) The three-dimensional construction of leaves is coordinated with water use efficiency in conifers. New Phytologist 233, 851-861.
| Crossref | Google Scholar | PubMed |
Vyas P, Bisht MS, Miyazawa S-I, Yano S, Noguchi K, Terashima I, Funayama-Noguchi S (2007) Effects of polyploidy on photosynthetic properties and anatomy in leaves of Phlox drummondii. Functional Plant Biology 34, 673-682.
| Crossref | Google Scholar | PubMed |
Warren CR (2008) Stand aside stomata, another actor deserves centre stage: the forgotten role of the internal conductance to CO2 transfer. Journal of Experimental Botany 59, 1475-1487.
| Crossref | Google Scholar | PubMed |
Wuyts N, Palauqui J-C, Conejero G, Verdeil J-L, Granier C, Massonnet C (2010) High-contrast three-dimensional imaging of the Arabidopsis leaf enables the analysis of cell dimensions in the epidermis and mesophyll. Plant Methods 6, 17.
| Crossref | Google Scholar |
