Pipe Cavitation Parameters Reveal Bubble Embolism Dynamics in Maize Xylem Vessels across Water Potential Gradients
Abstract
:1. Introduction
2. Materials and Methods
2.1. Materials
2.2. Theory
2.3. Sample Processing
2.3.1. Physiological Indicators
2.3.2. Measurement of Stem Flow Rate and Leaf Water Potential in Maize
2.3.3. Quantifying Hydraulic Conductivity Loss for Xylem Vulnerability-Curve Generation
2.4. Small Flow Method
3. Results
3.1. Physiological Parameters of Maize
3.2. Establishing the Bubble Radius–Sap Flow Rate–Water Potential Model
3.3. Comparison of Cavitation Emergence in Leaf PLC and Model Predictions
3.4. Observations of Leaf Conditions at Different Water Potentials during Cavitation
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
References
- Erenstein, O.; Jaleta, M.; Sonder, K.; Mottaleb, K.; Prasanna, B.M. Global Maize Production, Consumption and Trade: Trends and R&D Implications. Food Sec. 2022, 14, 1295–1319. [Google Scholar] [CrossRef]
- Shiferaw, B.; Prasanna, B.M.; Hellin, J.; Bänziger, M. Crops That Feed the World 6. Past Successes and Future Challenges to the Role Played by Maize in Global Food Security. Food Sec. 2011, 3, 307–327. [Google Scholar] [CrossRef]
- Jones-Garcia, E.; Krishna, V.V. Farmer Adoption of Sustainable Intensification Technologies in the Maize Systems of the Global South. A Review. Agron. Sustain. Dev. 2021, 41, 8. [Google Scholar] [CrossRef]
- Ranum, P.; Peña-Rosas, J.P.; Garcia-Casal, M.N. Global Maize Production, Utilization, and Consumption. Ann. N. Y. Acad. Sci. 2014, 1312, 105–112. [Google Scholar] [CrossRef]
- Farooq, M.; Wahid, A.; Kobayashi, N.; Fujita, D.; Basra, S.M.A. Plant Drought Stress: Effects, Mechanisms and Management. Agron. Sustain. Dev. 2009, 29, 185–212. [Google Scholar] [CrossRef]
- Sun, Y.; Chen, S.S.; Ning, J.F.; Han, W.T.; Weckler, P.R. Prediction of Moisture Content in Corn Leaves Based on Hyperspectral Imaging and Chemometric Analysis. Trans. ASABE 2015, 58, 531–537. [Google Scholar] [CrossRef]
- Katerji, N. Comparison of Corn Yield Response to Plant Water Stress Caused by Salinity and by Drought. Agric. Water Manag. 2003, 65, 95–101. [Google Scholar] [CrossRef]
- Nilahyane, A.; Islam, M.A.; Mesbah, A.O.; Herbert, S.K.; Garcia y Garcia, A. Growth, Water Productivity, Nutritive Value, and Physiology Responses of Silage Corn to Water Stress. Agron. J. 2020, 112, 1625–1635. [Google Scholar] [CrossRef]
- Mahmoud, M.A.B.; Sharp, R.E.; Oliver, M.J.; Finke, D.L.; Ellersieck, M.R.; Hibbard, B.E. The Effect of Western Corn Rootworm (Coleoptera: Chrysomelidae) and Water Deficit on Maize Performance under Controlled Conditions. J. Econ. Entomol. 2016, 109, 684–698. [Google Scholar] [CrossRef] [PubMed]
- Jansen, S.; Schenk, H.J. On the Ascent of Sap in the Presence of Bubbles. Am. J. Bot. 2015, 102, 1561–1563. [Google Scholar] [CrossRef]
- Ponomarenko, A.; Vincent, O.; Pietriga, A.; Cochard, H.; Badel, E.; Marmottant, P. Ultrasonic Emissions Reveal Individual Cavitation Bubbles in Water-Stressed Wood. J. R. Soc. Interface 2014, 11, 20140480. [Google Scholar] [CrossRef]
- Torres-Ruiz, J.M.; Diaz-Espejo, A.; Morales-Sillero, A.; Martin-Palomo, M.J.; Mayr, S.; Beikircher, B.; Fernandez, J.E. Shoot Hydraulic Characteristics, Plant Water Status and Stomatal Response in Olive Trees under Different Soil Water Conditions. Plant Soil 2013, 373, 77–87. [Google Scholar] [CrossRef]
- Miyashita, K.; Tanakamaru, S.; Maitani, T.; Kimura, K. Recovery Responses of Photosynthesis, Transpiration, and Stomatal Conductance in Kidney Bean Following Drought Stress. Environ. Exp. Bot. 2005, 53, 205–214. [Google Scholar] [CrossRef]
- Tyree, M.T.; Sperry, J.S. Vulnerability of Xylem to Cavitation and Embolism. Annu. Rev. Plant Biol. 1989, 40, 19–36. [Google Scholar] [CrossRef]
- Schenk, H.J.; Steppe, K.; Jansen, S. Nanobubbles: A New Paradigm for Air-Seeding in Xylem. Trends Plant Sci. 2015, 20, 199–205. [Google Scholar] [CrossRef]
- Tognettit, R.; Borghett, M. Formation and Seasonaloccurrence of Xylem Embolism in Alms Cordata. Tree Physiol. 1994, 14, 241–250. [Google Scholar] [CrossRef]
- Pratt, R.B.; Ewers, F.W.; Lawson, M.C.; Jacobsen, A.L.; Brediger, M.M.; Davis, S.D. Mechanisms for Tolerating Freeze–Thaw Stress of Two Evergreen Chaparral Species: Rhus Ovata and Malosma Laurina (Anacardiaceae). Am. J. Bot. 2005, 92, 1102–1113. [Google Scholar] [CrossRef]
- Umebayashi, T.; Fukuda, K. Seasonal Changes in the Occurrence of Embolisms among Broad-Leaved Trees in a Temperate Region. Botany 2018, 96, 873–881. [Google Scholar] [CrossRef]
- Ghosh, S.K.; Slot, J.C.; Visser, E.; Naidoo, S.; Sovic, M.; Conrad, A.O.; Bonello, P. How Abiotic Stress Plays Ally to Pathogenic Attack in Trees. In Proceedings of the Phytopathology; Amer Phytopathological SOC: Saint Paul, MN, USA, 2021; Volume 111, p. 63. [Google Scholar]
- Simova-Stoilova, L.; Vassileva, V.; Feller, U. Selection and Breeding of Suitable Crop Genotypes for Drought and Heat Periods in a Changing Climate: Which Morphological and Physiological Properties Should Be Considered? Agriculture 2016, 6, 26. [Google Scholar] [CrossRef]
- Torres-Ruiz, J.M.; Cochard, H.; Mencuccini, M.; Delzon, S.; Badel, E. Direct Observation and Modelling of Embolism Spread between Xylem Conduits: A Case Study in Scots Pine. Plant Cell Environ. 2016, 39, 2774–2785. [Google Scholar] [CrossRef] [PubMed]
- Holtta, T.; Juurola, E.; Lindfors, L.; Porcar-Castell, A. Cavitation Induced by a Surfactant Leads to a Transient Release of Water Stress and Subsequent “run Away” Embolism in Scots Pine (Pinus Sylvestris) Seedlings. J. Exp. Bot. 2012, 63, 1057–1067. [Google Scholar] [CrossRef] [PubMed]
- Omelyanyuk, M.; Ukolov, A.; Pakhlyan, I.; Bukharin, N.; El Hassan, M. Experimental and Numerical Study of Cavitation Number Limitations for Hydrodynamic Cavitation Inception Prediction. Fluids 2022, 7, 198. [Google Scholar] [CrossRef]
- Özçelik, M.S.; Tomášková, I.; Surový, P.; Modlinger, R. Effect of Forest Edge Cutting on Transpiration Rate in Picea abies (L.) H. Karst. Forests 2022, 13, 1238. Available online: https://www.mdpi.com/1999-4907/13/8/1238 (accessed on 27 August 2023). [CrossRef]
- Cutforth, H.W.; Wall, K.G. Water Stress, Sap Flow and Transpiration for Medium and Highly Drought Resistant Poplars Grown in the Semiarid Canadian Prairie. Can. J. Plant Sci. 2020, 100, 456–458. [Google Scholar] [CrossRef]
- Angadi, S.V.; Cutforth, H.W.; McConkey, B.G. Determination of the Water Use and Water Use Response of Canola to Solar Radiation and Temperature by Using Heat Balance Stem Flow Gauges. Can. J. Plant Sci. 2003, 83, 31–38. [Google Scholar] [CrossRef]
- Gebhardt, T.; Hesse, B.D.; Hikino, K.; Kolovrat, K.; Hafner, B.D.; Grams, T.E.E.; Häberle, K.-H. Repeated Summer Drought Changes the Radial Xylem Sap Flow Profile in Mature Norway Spruce but Not in European Beech. Agric. For. Meteorol. 2023, 329, 109285. [Google Scholar] [CrossRef]
- Zhao, L.; He, Z.; Zhao, W.; Yang, Q. Extensive Investigation of the Sap Flow of Maize Plants in an Oasis Farmland in the Middle Reach of the Heihe River, Northwest China. J. Plant Res. 2016, 129, 841–851. [Google Scholar] [CrossRef]
- Wason, J.; Bouda, M.; Lee, E.F.; McElrone, A.J.; Phillips, R.J.; Shackel, K.A.; Matthews, M.A.; Brodersen, C. Xylem Network Connectivity and Embolism Spread in Grapevine (Vitis vinifera L.). Plant Physiol. 2021, 186, 373–387. [Google Scholar] [CrossRef]
- Lee, H.; Taenaka, Y.; Kitamura, S. Cavitation Phenomenon in Monoleaflet Mechanical Heart Valves with Electrohydraulic Total Artificial Heart. Int. J. Artif. Organs 2004, 27, 779–786. [Google Scholar] [CrossRef] [PubMed]
- Singh, R.; Peles, Y. The Effects of Fluid Properties on Cavitation in a Micro Domain. J. Micromech. Microeng. 2009, 19, 025009. [Google Scholar] [CrossRef]
- Bibi, F.; Rahman, A. An Overview of Climate Change Impacts on Agriculture and Their Mitigation Strategies. Agriculture 2023, 13, 1508. [Google Scholar] [CrossRef]
- Lens, F.; Gleason, S.M.; Bortolami, G.; Brodersen, C.; Delzon, S.; Jansen, S. Functional Xylem Characteristics Associated with Drought-Induced Embolism in Angiosperms. New Phytol. 2022, 236, 2019–2036. [Google Scholar] [CrossRef]
- Rodriguez-Dominguez, C.M.; Carins Murphy, M.R.; Lucani, C.; Brodribb, T.J. Mapping Xylem Failure in Disparate Organs of Whole Plants Reveals Extreme Resistance in Olive Roots. New Phytol. 2018, 218, 1025–1035. [Google Scholar] [CrossRef]
- Tardieu, F.; Simonneau, T.; Parent, B. Modelling the Coordination of the Controls of Stomatal Aperture, Transpiration, Leaf Growth, and Abscisic Acid: Update and Extension of the Tardieu–Davies Model. J. Exp. Bot. 2015, 66, 2227–2237. [Google Scholar] [CrossRef] [PubMed]
- Venturas, M.D.; Sperry, J.S.; Love, D.M.; Frehner, E.H.; Allred, M.G.; Wang, Y.; Anderegg, W.R.L. A Stomatal Control Model Based on Optimization of Carbon Gain versus Hydraulic Risk Predicts Aspen Sapling Responses to Drought. New Phytol. 2018, 220, 836–850. [Google Scholar] [CrossRef] [PubMed]
- Sperry, J.S.; Venturas, M.D.; Anderegg, W.R.L.; Mencuccini, M.; Mackay, D.S.; Wang, Y.; Love, D.M. Predicting Stomatal Responses to the Environment from the Optimization of Photosynthetic Gain and Hydraulic Cost: A Stomatal Optimization Model. Plant Cell Environ. 2017, 40, 816–830. [Google Scholar] [CrossRef] [PubMed]
- Mencuccini, M. Modelling Water Fluxes in Plants: From Tissues to Biosphere. New Phytol. 2019, 222, 1207–1222. [Google Scholar] [CrossRef] [PubMed]
- Fan, D.-Y.; Dang, Q.-L.; Xu, C.-Y.; Jiang, C.-D.; Zhang, W.-F.; Xu, X.-W.; Yang, X.-F.; Zhang, S.-R. Stomatal Sensitivity to Vapor Pressure Deficit and the Loss of Hydraulic Conductivity Are Coordinated in Populus Euphratica, a Desert Phreatophyte Species. Front. Plant Sci. 2020, 11, 1248. [Google Scholar] [CrossRef]
- Sperry, J.S.; Donnelly, J.R.; Tyree, M.T. A Method for Measuring Hydraulic Conductivity and Embolism in Xylem. Plant Cell Environ. 1988, 11, 35–40. [Google Scholar] [CrossRef]
- Phillips, N.G.; Oren, R.; Licata, J.; Linder, S. Time Series Diagnosis of Tree Hydraulic Characteristics. Tree Physiol. 2004, 24, 879–890. [Google Scholar] [CrossRef]
- Giles, A.L.; Rowland, L.; Bittencourt, P.R.L.; Bartholomew, D.C.; Coughlin, I.; Costa, P.B.; Domingues, T.; Miatto, R.C.; Barros, F.V.; Ferreira, L.V.; et al. Small Understorey Trees Have Greater Capacity than Canopy Trees to Adjust Hydraulic Traits Following Prolonged Experimental Drought in a Tropical Forest. Tree Physiol. 2022, 42, 537–556. [Google Scholar] [CrossRef] [PubMed]
- Zhang, L.; Chen, Y.; Ma, K.; Bongers, F.; Sterck, F.J. Fully Exposed Canopy Tree and Liana Branches in a Tropical Forest Differ in Mechanic Traits but Are Similar in Hydraulic Traits. Tree Physiol. 2019, 39, 1713–1724. [Google Scholar] [CrossRef]
- Shen, F. Analysis of Cavitation Processes in Xylem. J. Appl. Math. Phys. 2020, 8, 1767–1778. [Google Scholar] [CrossRef]
- Shen, F.; Gao, R.; Liu, W.; Zhang, W. Physical Analysis of the Process of Cavitation in Xylem Sap. Tree Physiol. 2002, 22, 655–659. [Google Scholar] [CrossRef] [PubMed]
- Shen, F.; Cheng, Y.; Zhang, L.; Gao, R.; Shao, X. Experimental Study of the Types of Cavitation by Air Seeding Using Light Microscopy. Tree Physiol. 2015, 35, 1325–1332. [Google Scholar] [CrossRef] [PubMed]
- Jitang, H. Principles and Applications of Cavitation and Cavitation; Tsinghua University Press: Beijing, China, 1991; ISBN 7-302-00670-9. [Google Scholar]
- Sperry, J.S.; Wang, Y.; Wolfe, B.T.; Mackay, D.S.; Anderegg, W.R.L.; McDowell, N.G.; Pockman, W.T. Pragmatic Hydraulic Theory Predicts Stomatal Responses to Climatic Water Deficits. New Phytol. 2016, 212, 577–589. [Google Scholar] [CrossRef]
- Brennen, C.E. Cavitation and Bubble Dynamics; Oxford University Press: Oxford, UK, 1995. [Google Scholar]
- Borghetti, M.; Grace, J.; Raschi, A. Water Transport in Plants under Climatic Stress; Cambridge University Press: Cambridge, UK, 1993; ISBN 0-521-44219-2. [Google Scholar]
- Goldman, S.; Solano-Altamirano, J.M. An Explicitly Multi-Component Arterial Gas Embolus Dissolves Much More Slowly than Its One-Component Approximation. Math. Biosci. 2020, 326, 108393. [Google Scholar] [CrossRef]
- Tyree, M.T.; Salleo, S.; Nardini, A.; Assunta Lo Gullo, M.; Mosca, R. Refilling of Embolized Vessels in Young Stems of Laurel. Do We Need a New Paradigm? Plant Physiol. 1999, 120, 11–22. [Google Scholar] [CrossRef] [PubMed]
- Yang, S.; Tyree, M.T. A Theoretical Model of Hydraulic Conductivity Recovery from Embolism with Comparison to Experimental Data on Acer Saccharum. Plant Cell Environ. 1992, 15, 633–643. [Google Scholar] [CrossRef]
- Stohr, A.; Losch, R. Xylem Sap Flow and Drought Stress of Fraxinus Excelsior Saplings. Tree Physiol. 2004, 24, 169–180. [Google Scholar] [CrossRef] [PubMed]
- Gao, Y.; Duan, A.; Qiu, X.; Zhang, J.; Sun, J.; Wang, H. Plant Transpiration in a Maize/Soybean Intercropping System Measured with Heat Balance Method. Yingyong Shengtai Xuebao 2010, 21, 1283–1288. [Google Scholar]
- Ozier-Lafontaine, H.; Lafolie, F.; Bruckler, L.; Tournebize, R.; Mollier, A. Modelling Competition for Water in Intercrops: Theory and Comparison with Field Experiments. Plant Soil 1998, 204, 183–201. [Google Scholar] [CrossRef]
- Cohen, Y.; Huck, M.G.; Hesketh, J.D.; Frederick, J.R. Sap Flow in the Stem of Water Stressed Soybean and Maize Plants. Irrig. Sci. 1990, 11, 45–50. [Google Scholar] [CrossRef]
- Tyree, M.T.; Fiscus, E.L.; Wullschleger, S.; Dixon, M. Detection of Xylem Cavitation in Corn under Field Conditions. Plant Physiol. 1986, 82, 597–599. [Google Scholar] [CrossRef] [PubMed]
- McCully, M.; Huang, C.; Ling, L. Daily Embolism and Refilling of Xylem Vessels in the Roots of Field-Grown Maize. New Phytol. 1998, 138, 327–342. [Google Scholar] [CrossRef]
- Taiz, L.; Zeiger, E.; Møller, I.; Murphy, A. Plant Physiology and Development; Sinauer Associates, Inc., Publishers: Sunderland, Massachusetts, 2014; ISBN 978-1-60535-255-8. [Google Scholar]
- Xiong, D.; Nadal, M. Linking Water Relations and Hydraulics with Photosynthesis. Plant J. 2020, 101, 800–815. [Google Scholar] [CrossRef]
- McCully, M.E. Root Xylem Embolisms and Refilling. Relation to Water Potentials of Soil, Roots, and Leaves, and Osmotic Potentials of Root Xylem Sap. Plant Physiol. 1999, 119, 1001–1008. [Google Scholar] [CrossRef] [PubMed]
- Jones, H.G.; Sutherland, R.A. Stomatal Control of Xylem Embolism. Plant Cell Environ. 1991, 14, 607–612. [Google Scholar] [CrossRef]
- Cochard, H.; Delzon, S.; Badel, E. X-Ray Microtomography (Micro-CT): A Reference Technology for High-Resolution Quantification of Xylem Embolism in Trees: A Reference Method for Xylem Embolism. Plant Cell Environ. 2015, 38, 201–206. [Google Scholar] [CrossRef]
- van Ieperen, W.; van Meeteren, U.; van Gelder, H. Fluid Ionic Composition Influences Hydraulic Conductance of Xylem Conduits. J. Exp. Bot. 2000, 51, 769–776. [Google Scholar] [CrossRef]
- Mrad, A.; Domec, J.-C.; Huang, C.-W.; Lens, F.; Katul, G. A Network Model Links Wood Anatomy to Xylem Tissue Hydraulic Behaviour and Vulnerability to Cavitation. Plant Cell Environ. 2018, 41, 2718–2730. [Google Scholar] [CrossRef] [PubMed]
- Jia, Y.; Xiao, W.; Ye, Y.; Wang, X.; Liu, X.; Wang, G.; Li, G.; Wang, Y. Response of Photosynthetic Performance to Drought Duration and Re-Watering in Maize. Agronomy 2020, 10, 533. [Google Scholar] [CrossRef]
- Jiang, J.; Feng, S.; Ma, J.; Huo, Z.; Zhang, C. Irrigation Management for Spring Maize Grown on Saline Soil Based on SWAP Model. Field Crop. Res. 2016, 196, 85–97. [Google Scholar] [CrossRef]
Month | Mean Month Air Temperature (°C) | Humidity Range (%) | Precipitation (mm) | Mean Daily Net Radiation (W m−2) | |
---|---|---|---|---|---|
2021 | March | 21.91 | 18.1–99.9 | 1.39 | 259.3 |
2022 | March | 23.12 | 25.4–99.9 | 79.33 | 206.1 |
2023 | March | 20.69 | 23.1–99.9 | 0.13 | 197.4 |
Year | Number of Leaves | Number of Veins | Diameter of Xylem Vessels (μm) | Maize Leaf Length (cm) |
---|---|---|---|---|
2021 | 12 | 45 | 43.01 ± 0.35 | 74.95 ± 1.21 |
9 | 38 | 28.01 ± 1.27 | 56.50 ± 0.53 | |
11 | 43 | 36.13 ± 0.98 | 64.40 ± 3.18 | |
6 | 35 | 32.74 ± 2.77 | 47.90 ± 2.26 | |
9 | 39 | 34.29 ± 1.3 | 67.40 ± 1.30 | |
15 | 53 | 64.8 ± 1.43 | 93.70 ± 2.11 | |
12 | 48 | 41.57 ± 2.36 | 66.40 ± 1.57 | |
Average value | 10.57 | 43 | 40.08 | 67.30 |
2022 | 11 | 45 | 46.02 ± 2.78 | 78.40 ± 0.43 |
7 | 34 | 18.43 ± 1.24 | 41.55 ± 3.53 | |
8 | 35 | 22.65 ± 0.74 | 49.60 ± 1.73 | |
10 | 38 | 23.79 ± 2.1 | 56.10 ± 3.12 | |
12 | 47 | 46.19 ± 2.33 | 75.35 ± 1.83 | |
7 | 29 | 19.41 ± 0.69 | 40.75 ± 0.86 | |
10 | 40 | 35.43 ± 1.45 | 62.75 ± 1.48 | |
Average value | 9.29 | 38.29 | 30.27 | 57.80 |
2023 | 12 | 49 | 49 ± 1.26 | 72.5 ± 1.32 |
11 | 46 | 21.86 ± 2.10 | 59.05 ± 1.2 | |
7 | 36 | 23.2 ± 1.56 | 49.40 ± 2.10 | |
12 | 41 | 35.67 ± 1.43 | 66.70 ± 1.63 | |
8 | 37 | 27.81 ± 2.43 | 49.30 ± 3.41 | |
10 | 27 | 27.53 ± 1.15 | 78.15 ± 0.76 | |
9 | 35 | 25.67 ± 0.89 | 56.20 ± 0.84 | |
Average value | 9.86 | 38.71 | 30.51 | 62.20 |
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Ren, Y.; Zhang, Y.; Guo, S.; Wang, B.; Wang, S.; Gao, W. Pipe Cavitation Parameters Reveal Bubble Embolism Dynamics in Maize Xylem Vessels across Water Potential Gradients. Agriculture 2023, 13, 1867. https://doi.org/10.3390/agriculture13101867
Ren Y, Zhang Y, Guo S, Wang B, Wang S, Gao W. Pipe Cavitation Parameters Reveal Bubble Embolism Dynamics in Maize Xylem Vessels across Water Potential Gradients. Agriculture. 2023; 13(10):1867. https://doi.org/10.3390/agriculture13101867
Chicago/Turabian StyleRen, Yangjie, Yitong Zhang, Shiyang Guo, Ben Wang, Siqi Wang, and Wei Gao. 2023. "Pipe Cavitation Parameters Reveal Bubble Embolism Dynamics in Maize Xylem Vessels across Water Potential Gradients" Agriculture 13, no. 10: 1867. https://doi.org/10.3390/agriculture13101867