Sleep tight and wake-up early: nocturnal transpiration traits to increase wheat drought tolerance in a Mediterranean environment
Rémy Schoppach A , Thomas R. Sinclair
B and Walid Sadok A C
+ Author Affiliations
- Author Affiliations
A Department of Agronomy and Plant Genetics, University of Minnesota, St. Paul, MN 55108-6026, USA.
B Crop Science Department, North Carolina State University, Raleigh, NC 27695-7620, USA.
C Corresponding author. Email: msadok@umn.edu
Functional Plant Biology 47(12) 1117-1127 https://doi.org/10.1071/FP20044
Submitted: 9 February 2020 Accepted: 20 June 2020 Published: 20 July 2020
Abstract
In wheat, night-time transpiration rate (TRN) could amount to 14–55% of daytime transpiration rate (TR), depending on the cultivar and environment. Recent evidence suggests that TRN is much less responsive to soil drying than daytime TR, and that such ‘wasteful’ water losses would increase the impact of drought on yields. In contrast, other evidence indicates that pre-dawn, circadian increases in TRN may enable enhanced radiation use efficiency, resulting in increased productivity under water deficit. Until now, there have been no attempts to evaluate these seemingly conflicting hypotheses in terms of their impact on yields in any crop. Here, using the Mediterranean environment of Tunisia as a case study, we undertook a simulation modelling approach using SSM-Wheat to evaluate yield outcomes resulting from these TRN trait modifications. TRN represented 15% of daytime TR-generated yield penalties of up to 20%, and these worsened when TRN was not sensitive to soil drying TR. For the same TRN level (15%), simulating a predawn increase in TRN alleviated yield penalties, leading to yield gains of up to 25%. Overall, this work suggests that decreasing TRN but increasing pre-dawn circadian control would be a viable breeding target to increase drought tolerance in a Mediterranean environment.
Additional keywords: circadian clock, food security, physiological trade-offs, process-based crop model, water conservation.
References
Abaza K (2012) Dynamique de l’occupation des sols et risques environnementaux en milieux montagneux arides: le cas de la région de Ghomrassen et ses environs (Sud- Est de la Tunisie). Revue des Regions Arides 29, 77–101.Abdel-Aziz MH, Taylor SA, Ashcroft GL (1964) Influence of advective energy on transpiration. Agronomy Journal 56, 139–142.
| Influence of advective energy on transpiration.Crossref | GoogleScholarGoogle Scholar |
Alvarado-Barrientos MS, Holwerda F, Geissert DR, Muñoz-Villers LE, Gotsch SG, Asbjornsen H, Dawson TE (2015) Nighttime transpiration in a seasonally dry tropical montane cloud forest environment. Trees 29, 259–274.
| Nighttime transpiration in a seasonally dry tropical montane cloud forest environment.Crossref | GoogleScholarGoogle Scholar |
Bazié HR, Sanou J, Bayala J, Bargués-Tobella A, Zombré G, Ilstedt U (2018) Temporal variations in transpiration of Vitellaria paradoxa in West African agroforestry parklands. Agroforestry Systems 92, 1673–1686.
| Temporal variations in transpiration of Vitellaria paradoxa in West African agroforestry parklands.Crossref | GoogleScholarGoogle Scholar |
Benzarti Z (2003) La pluviométrie en Tunisie. Analyse Des Années Très Pluvieuses. ENS Editions, 2003.
Caird MA, Richards JH, Donovan LA (2007a) Night-time stomatal conductance and transpiration in C3 and C4 plants. Plant Physiology 143, 4–10.
| Night-time stomatal conductance and transpiration in C3 and C4 plants.Crossref | GoogleScholarGoogle Scholar | 17210908PubMed |
Caird MA, Richards JH, Hsiao TC (2007b) Significant transpirational water loss occurs throughout the night in field-grown tomato. Functional Plant Biology 34, 172–177.
| Significant transpirational water loss occurs throughout the night in field-grown tomato.Crossref | GoogleScholarGoogle Scholar |
Carter TE, Todd SM, Gillen AM (2016) Registration of ‘USDA-N8002’ soybean cultivar with high yield and abiotic stress resistance traits. Journal of Plant Registrations 10, 238–245.
| Registration of ‘USDA-N8002’ soybean cultivar with high yield and abiotic stress resistance traits.Crossref | GoogleScholarGoogle Scholar |
Claverie E, Meunier F, Javaux M, Sadok W (2018) Increased contribution of wheat nocturnal transpiration to daily water use under drought. Physiologia Plantarum 162, 290–300.
| Increased contribution of wheat nocturnal transpiration to daily water use under drought.Crossref | GoogleScholarGoogle Scholar | 28833246PubMed |
Coupel-Ledru A, Lebon E, Christophe A, Gallo A, Gago P, Pantin F, Doligez A, Simonneau T (2016) Reduced nighttime transpiration is a relevant breeding target for high water-use efficiency in grapevine. Proceedings of the National Academy of Sciences of the United States of America 113, 8963–8968.
| Reduced nighttime transpiration is a relevant breeding target for high water-use efficiency in grapevine.Crossref | GoogleScholarGoogle Scholar | 27457942PubMed |
Duursma RA, Blackman CJ, Lopéz R, Martin-StPaul NK, Cochard H, Medlyn BE (2019) On the minimum leaf conductance: its role in models of plant water use, and ecological and environmental controls. New Phytologist 221, 693–705.
| On the minimum leaf conductance: its role in models of plant water use, and ecological and environmental controls.Crossref | GoogleScholarGoogle Scholar | 30144393PubMed |
Émile M (1950) Les principales espèces et variétés de Blé cultivées en Afrique du Nord. In Revue internationale de botanique appliquée et d’agriculture tropicale, 30e année. Bulletin no. 327–328. Janvier-février 1950. pp. 16–38. (Muséum national d’histoire naturelle, Laboratoire d’agronomie colonial: Paris)
Even M, Sabo M, Meng D, Kreszies T, Schreiber L, Fricke W (2018) Night-time transpiration in barley (Hordeum vulgare) facilitates respiratory carbon dioxide release and is regulated during salt stress. Annals of Botany 122, 569–582.
| Night-time transpiration in barley (Hordeum vulgare) facilitates respiratory carbon dioxide release and is regulated during salt stress.Crossref | GoogleScholarGoogle Scholar | 29850772PubMed |
Fricke W (2019) Nighttime transpiration – favoring growth? Trends in Plant Science 24, 311–317.
| Nighttime transpiration – favoring growth?Crossref | GoogleScholarGoogle Scholar | 30770287PubMed |
Fuentes S, Mahadevan M, Bonada M, Skewes MA, Cox JW (2013) Night-time sap flow is parabolically linked to midday water potential for field-grown almond trees. Irrigation Science 31, 1265–1276.
| Night-time sap flow is parabolically linked to midday water potential for field-grown almond trees.Crossref | GoogleScholarGoogle Scholar |
Fuentes S, De Bei R, Collins MJ, Escalona JM, Medrano H, Tyerman S (2014) Night-time responses to water supply in grapevines (Vitis vinifera L.) under deficit irrigation and partial root-zone drying. Agricultural Water Management 138, 1–9.
| Night-time responses to water supply in grapevines (Vitis vinifera L.) under deficit irrigation and partial root-zone drying.Crossref | GoogleScholarGoogle Scholar |
Gaffney J, Schussler J, Löffler C, Cai W, Paszkiewicz S, Messina C, Groeteke J, Keaschall J, Cooper M (2015) Industry scale evaluation of maize hybrids selected for increased yield in drought stress conditions of the US Corn Belt. Crop Science 55, 1608–1618.
| Industry scale evaluation of maize hybrids selected for increased yield in drought stress conditions of the US Corn Belt.Crossref | GoogleScholarGoogle Scholar |
Ghanem ME, Kehel Z, Marrou H, Sinclair TR (2020) Seasonal and climatic variation of weighted VPD for transpiration T estimation. European Journal of Agronomy 113, 125966
| Seasonal and climatic variation of weighted VPD for transpiration T estimation.Crossref | GoogleScholarGoogle Scholar |
Gijsman AJ, Jagtap SS, Jones JW (2002) Wading through a swamp of complete confusion: how to choose a method for estimating soil water retention parameters for crop models. European Journal of Agronomy 18, 77–106.
| Wading through a swamp of complete confusion: how to choose a method for estimating soil water retention parameters for crop models.Crossref | GoogleScholarGoogle Scholar |
Green SR, McNaughton KG, Clothier BE (1989) Observations of night-time water use in kiwifruit vines and apple trees. Agricultural and Forest Meteorology 48, 251–261.
| Observations of night-time water use in kiwifruit vines and apple trees.Crossref | GoogleScholarGoogle Scholar |
Guiguitant J, Marrou H, Vadez V, Gupta P, Kumar S, Soltani A, Sinclair TR, Ghanem ME (2017) Relevance of limited-transpiration trait for lentil (Lens culinaris Medik.) in South Asia. Field Crops Research 209, 96–107.
| Relevance of limited-transpiration trait for lentil (Lens culinaris Medik.) in South Asia.Crossref | GoogleScholarGoogle Scholar |
HWSD (2012) HWSD ver. 1.2. FAO 2012. Available at https://daac.ornl.gov/SOILS/guides/HWSD.html [Verified 26 June 2020]
Latiri K, Lhomme JP, Annabi M, Setter TL (2010) Wheat production in Tunisia: progress, inter-annual variability and relation to rainfall. European Journal of Agronomy 33, 33–42.
| Wheat production in Tunisia: progress, inter-annual variability and relation to rainfall.Crossref | GoogleScholarGoogle Scholar |
Marks CO, Lechowicz MJ (2007) The ecological and functional correlates of nocturnal transpiration. Tree Physiology 27, 577–584.
| The ecological and functional correlates of nocturnal transpiration.Crossref | GoogleScholarGoogle Scholar | 17241999PubMed |
Messina CD, Sinclair TR, Hammer GL, Curan D, Thompson J, Oler Z, Gho C, Cooper M (2015) Limited-transpiration trait may increase maize drought tolerance in the US corn belt. Agronomy Journal 107, 1978–1986.
| Limited-transpiration trait may increase maize drought tolerance in the US corn belt.Crossref | GoogleScholarGoogle Scholar |
Neumann RB, Cardon ZG, Teshera-Levye J, Rockwell FE, Zwieniecki MA, Holbrook NM (2014) Modelled hydraulic redistribution by sunflower (Helianthus annuus L.) matches observed data only after including night-time transpiration. Plant, Cell & Environment 37, 899–910.
| Modelled hydraulic redistribution by sunflower (Helianthus annuus L.) matches observed data only after including night-time transpiration.Crossref | GoogleScholarGoogle Scholar |
Perrot E (1909) Les productions végétales de la Tunisie (Notes de botanique économique) Bulletin de la Société Botanique de France 56, CCCXVII–CCCLII.
| Les productions végétales de la Tunisie (Notes de botanique économique)Crossref | GoogleScholarGoogle Scholar |
R Core Team (2017) R: A language and environment for statistical computing. (R Foundation for Statistical Computing, Vienna, Austria) Available at http://www.R-project.org/ [Verified 26 June 2020]
Rawson HM, Clarke JM (1988) Nocturnal transpiration in wheat. Australian Journal of Plant Physiology 15, 397–406.
| Nocturnal transpiration in wheat.Crossref | GoogleScholarGoogle Scholar |
Resco de Dios V, Roy J, Ferrio JP, Alday JG, Landais D, Milcu A, Gessler A (2015) Processes driving nocturnal transpiration and implications for estimating land evapotranspiration. Scientific Reports 5, 10975
| Processes driving nocturnal transpiration and implications for estimating land evapotranspiration.Crossref | GoogleScholarGoogle Scholar |
Resco de Dios V, Loik ME, Smith R, Aspinwall MJ, Tissue DT (2016) Genetic variation in circadian regulation of nocturnal stomatal conductance enhances carbon assimilation and growth. Plant, Cell & Environment 39, 3–11.
| Genetic variation in circadian regulation of nocturnal stomatal conductance enhances carbon assimilation and growth.Crossref | GoogleScholarGoogle Scholar |
Resco de Dios V, Chowdhury FI, Granda E, Yao Y, Tissue DT (2019) Assessing the potential functions of nocturnal stomatal conductance in C3 and C4 plants. New Phytologist 223, 1696–1706.
| Assessing the potential functions of nocturnal stomatal conductance in C3 and C4 plants.Crossref | GoogleScholarGoogle Scholar | 31055839PubMed |
Richards RA, Rawson HM, Johnson DA (1986) Glaucousness in wheat: its development and effect on water-use efficiency, gas exchange and photosynthetic tissue temperatures. Australian Journal of Plant Physiology 13, 465–473.
| Glaucousness in wheat: its development and effect on water-use efficiency, gas exchange and photosynthetic tissue temperatures.Crossref | GoogleScholarGoogle Scholar |
Rogiers SY, Greer DH, Hutton RJ, Landsberg JJ (2009) Does night-time transpiration contribute to anisohydric behaviour in a Vitis vinifera cultivar? Journal of Experimental Botany 60, 3751–3763.
| Does night-time transpiration contribute to anisohydric behaviour in a Vitis vinifera cultivar?Crossref | GoogleScholarGoogle Scholar | 19584116PubMed |
Rogiers SY, Greer DH, Hatfield JM, Hutton RJ, Clarke SJ, Hutchinson PA, Somers A (2012) Stomatal response of an anisohydric grapevine cultivar to evaporative demand, available soil moisture and abscisic acid. Tree Physiology 32, 249–261.
| Stomatal response of an anisohydric grapevine cultivar to evaporative demand, available soil moisture and abscisic acid.Crossref | GoogleScholarGoogle Scholar | 22199014PubMed |
Sadok W, Jagadish SVK (2020) The hidden costs of nighttime warming on yields. Trends in Plant Science
| The hidden costs of nighttime warming on yields.Crossref | GoogleScholarGoogle Scholar | 32526169PubMed | In press
Sadok W, Tamang BG (2019) Diversity in daytime and night‐time transpiration dynamics in barley indicates adaptation to drought regimes across the Middle‐East. Journal Agronomy & Crop Science 205, 372–384.
| Diversity in daytime and night‐time transpiration dynamics in barley indicates adaptation to drought regimes across the Middle‐East.Crossref | GoogleScholarGoogle Scholar |
Sadok W, Schoppach R, Ghanem ME, Zucca C, Sinclair TR (2019) Wheat drought-tolerance to enhance food security in Tunisia, birthplace of the Arab Spring. European Journal of Agronomy 107, 1–9.
| Wheat drought-tolerance to enhance food security in Tunisia, birthplace of the Arab Spring.Crossref | GoogleScholarGoogle Scholar |
Schoppach R, Sadok W (2012) Differential sensitivities of transpiration to evaporative demand and soil water deficit among wheat elite cultivars indicate different strategies for drought tolerance. Environmental and Experimental Botany 84, 1–10.
| Differential sensitivities of transpiration to evaporative demand and soil water deficit among wheat elite cultivars indicate different strategies for drought tolerance.Crossref | GoogleScholarGoogle Scholar |
Schoppach R, Claverie E, Sadok W (2014) Genotype-dependent influence of night-time vapour pressure deficit on night-time transpiration and daytime gas exchange in wheat. Functional Plant Biology 41, 963–971.
| Genotype-dependent influence of night-time vapour pressure deficit on night-time transpiration and daytime gas exchange in wheat.Crossref | GoogleScholarGoogle Scholar | 32481049PubMed |
Schoppach R, Soltani A, Sinclair TR, Sadok W (2017) Yield comparison of simulated rainfed wheat and barley across Middle-East. Agricultural Systems 153, 101–108.
| Yield comparison of simulated rainfed wheat and barley across Middle-East.Crossref | GoogleScholarGoogle Scholar |
Sinclair TR, Amir J (1992) A model to assess nitrogen limitations on the growth and yield of spring wheat. Field Crops Research 30, 1–11.
| A model to assess nitrogen limitations on the growth and yield of spring wheat.Crossref | GoogleScholarGoogle Scholar |
Sinclair TR, Hammer GL, van Oosterom EJ (2005) Potential yield and water – use efficiency benefits in sorghum from limited maximum transpiration rate. Functional Plant Biology 32, 945–952.
| Potential yield and water – use efficiency benefits in sorghum from limited maximum transpiration rate.Crossref | GoogleScholarGoogle Scholar |
Sinclair TR, Messina CD, Beatty A, Samples M (2010) Assessment across the United States of the benefits of altered soybean drought traits. Agronomy Journal 102, 475–482.
| Assessment across the United States of the benefits of altered soybean drought traits.Crossref | GoogleScholarGoogle Scholar |
Sinclair TR, Marrou H, Soltani A, Vadez V, Chandolou KC (2014) Soybean production potential in Africa. Global Food Security 3, 31–40.
| Soybean production potential in Africa.Crossref | GoogleScholarGoogle Scholar |
Soltani A, Hoogenboom G (2007) Assessing crop management options with crop simulation models based on generated weather data. Field Crops Research 103, 198–207.
| Assessing crop management options with crop simulation models based on generated weather data.Crossref | GoogleScholarGoogle Scholar |
Soltani A, Sinclair TR (2012) ‘Modeling physiology of crop development, growth and yield.’ (CAB International: Wallingford, UK)
Soltani A, Maddaha V, Sinclair TR (2013) SSM-wheat: a simulation model for wheat development, growth and yield. International Journal of Plant Production 7, 714
Tamang BG, Schoppach R, Monnens D, Steffenson BJ, Anderson JA, Sadok W (2019) Variability in temperature-independent transpiration responses to evaporative demand correlate with nighttime water use and its circadian control across diverse wheat populations. Planta 250, 115–127.
| Variability in temperature-independent transpiration responses to evaporative demand correlate with nighttime water use and its circadian control across diverse wheat populations.Crossref | GoogleScholarGoogle Scholar | 30941570PubMed |
Tanner CB, Sinclair TR (1983) Efficient water use in crop production: research or re- search? In ‘Limitations to efficient water use in crop production’. (Eds HM Taylor, JR Wayne, SR Thomas) pp. 1–27. (American Society of Agronomy, Crop Science Society of America, Soil Science Society of America: Madison, WI, USA)
Tolk JA, Howell TA, Evett SR (2006) Night-time evapotranspiration from alfalfa and cotton in a semiarid climate. Agronomy Journal 98, 730–736.
| Night-time evapotranspiration from alfalfa and cotton in a semiarid climate.Crossref | GoogleScholarGoogle Scholar |
USDA-FAS (2005) Tunisia Grain and Feed Annual, 2005. GAIN Report Number: TS5004.
USDA-FAS (2007) Tunisia Grain and Feed Annual, 2007. GAIN Report Number: TS7006.
USDA-FAS (2009) Tunisia Grain and Feed Annual, 2009. GAIN Report Number: TS9003.
USDA-FAS (2011) Tunisia Grain and Feed Annual, 2011. GAIN Report Number: TS1102.
USDA-FAS (2013) Tunisia Grain and Feed Annual, 2013. GAIN Report Number: TS1303.
USDA-FAS (2016) Tunisia Grain and Feed Annual, 2016. GAIN Report Number: TS1604.
World Food Programme (WFP) (2011) Secondary data analysis of the food security situation in Tunisia. Available at https://documents.wfp.org/stellent/groups/public/documents/ena/wfp236106.pdf [Verified 2 July 2020]
Yu K, Goldsmith GR, Wang Y, Anderegg WRL (2019) Phylogenetic and biogeographic controls of plant nighttime stomatal conductance. New Phytologist 222, 1778–1788.
| Phylogenetic and biogeographic controls of plant nighttime stomatal conductance.Crossref | GoogleScholarGoogle Scholar | 30779147PubMed |
