High-throughput phenotyping of physiological traits for wheat resilience to high temperature and drought stress
Jazyk angličtina Země Velká Británie, Anglie Médium print
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
EPPN2020
European Plant Phenotyping Network 2020
731013
European Union's Horizon 2020
PD65-2012
BioSys PhD Programme
Fundação para a Ciência e a Tecnologia
Ministry of Education
PubMed
35446418
PubMed Central
PMC9440435
DOI
10.1093/jxb/erac160
PII: 6572012
Knihovny.cz E-zdroje
- Klíčová slova
- Triticum aestivum, Carbohydrate metabolism, climate change, drought resilience, food security, high temperature, high-throughput plant phenotyping, multispectral imaging, water deficit, wheat,
- MeSH
- antioxidancia metabolismus MeSH
- fenotyp MeSH
- fyziologický stres MeSH
- období sucha * MeSH
- pšenice * fyziologie MeSH
- šlechtění rostlin MeSH
- teplota MeSH
- voda metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- antioxidancia MeSH
- voda MeSH
Interannual and local fluctuations in wheat crop yield are mostly explained by abiotic constraints. Heatwaves and drought, which are among the top stressors, commonly co-occur, and their frequency is increasing with global climate change. High-throughput methods were optimized to phenotype wheat plants under controlled water deficit and high temperature, with the aim to identify phenotypic traits conferring adaptative stress responses. Wheat plants of 10 genotypes were grown in a fully automated plant facility under 25/18 °C day/night for 30 d, and then the temperature was increased for 7 d (38/31 °C day/night) while maintaining half of the plants well irrigated and half at 30% field capacity. Thermal and multispectral images and pot weights were registered twice daily. At the end of the experiment, key metabolites and enzyme activities from carbohydrate and antioxidant metabolism were quantified. Regression machine learning models were successfully established to predict plant biomass using image-extracted parameters. Evapotranspiration traits expressed significant genotype-environment interactions (G×E) when acclimatization to stress was continuously monitored. Consequently, transpiration efficiency was essential to maintain the balance between water-saving strategies and biomass production in wheat under water deficit and high temperature. Stress tolerance included changes in carbohydrate metabolism, particularly in the sucrolytic and glycolytic pathways, and in antioxidant metabolism. The observed genetic differences in sensitivity to high temperature and water deficit can be exploited in breeding programmes to improve wheat resilience to climate change.
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Albacete A, Cantero-Navarro E, Großkinsky DK, et al. . 2015. Ectopic overexpression of the cell wall invertase gene CIN1 leads to dehydration avoidance in tomato. Journal of Experimental Botany 66, 863–878. PubMed PMC
Albacete AA, Großkinsky DK, Roitsch T.. 2011. Trick and treat: a review on the function and regulation of plant invertases in the abiotic stress response. Phyton 50, 181–204.
Araus JL. 2002. Plant breeding and drought in C3 cereals: what should we breed for? Annals of Botany 89, 925–940. PubMed PMC
Blackburn GA. 2007. Hyperspectral remote sensing of plant pigments. Journal of Experimental Botany 58, 855–867. PubMed
Bouslama M, Schapaugh WT.. 1984. Stress tolerance in soybeans. I. Evaluation of three screening techniques for heat and drought tolerance. Crop Science 24, 933–937.
Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Analytical Biochemistry 72, 248–254. PubMed
Carmo-Silva AE, Gore MA, Andrade-Sanchez P, French AN, Hunsaker DJ, Salvucci ME.. 2012. Decreased CO2 availability and inactivation of Rubisco limit photosynthesis in cotton plants under heat and drought stress in the field. Environmental and Experimental Botany 83, 1–11.
Catchpole WR, Wheeler CJ.. 1992. Estimating plant biomass: a review of techniques. Austral Ecology 17, 121–131.
Chaves MM, Maroco JP, Pereira JS.. 2003. Understanding plant responses to drought—from genes to the whole plant. Functional Plant Biology 30, 239. PubMed
Chen D, Fu LY, Hu D, Klukas C, Chen M, Kaufmann K.. 2018a. The HTPmod Shiny application enables modeling and visualization of large-scale biological data. Communications Biology 1, 1–8. PubMed PMC
Chen D, Neumann K, Friedel S, Kilian B, Chen M, Altmann T, Klukas C.. 2014. Dissecting the phenotypic components of crop plant growth and drought responses based on high-throughput image analysis. The Plant Cell 26, 4636–4655. PubMed PMC
Chen D, Shi R, Pape JM, Neumann K, Arend D, Graner A, Chen M, Klukas C.. 2018b. Predicting plant biomass accumulation from image-derived parameters. GigaScience 7, 1–13. PubMed PMC
Cobb JN, DeClerck G, Greenberg A, Clark R, McCouch S.. 2013. Next-generation phenotyping: requirements and strategies for enhancing our understanding of genotype–phenotype relationships and its relevance to crop improvement. Theoretical and Applied Genetics 126, 867–887. PubMed PMC
Correia PMP, Silva AB, Roitsch T, Carmo-Silva E, Marques da Silva J.. 2021. Photoprotection and optimization of sucrose usage contribute to faster recovery of photosynthesis after water deficit at high temperatures in wheat. Physiologia Plantarum 172, 615–628. PubMed
Costa JM, Grant OM, Chaves MM.. 2013. Thermography to explore plant–environment interactions. Journal of Experimental Botany 64, 3937–3949. PubMed
Cuesta-Seijo J, De Porcellinis AJ, Valente AH, et al. . 2019. Amylopectin chain length dynamics and activity signatures of key carbon metabolic enzymes highlight early maturation as culprit for yield reduction of barley endosperm starch after heat stress. Plant & Cell Physiology 60, 2692–2706. PubMed PMC
Deryng D, Conway D, Ramankutty N, Price J, Warren R.. 2014. Global crop yield response to extreme heat stress under multiple climate change futures. Environmental Research Letters 9, 034011.
Duque AS, de Almeida AM, Bernardes da Silva A, Marques da Silva J, Farinha AP, Santos D, Fevereiro P, de Sousa Araujo S.. 2013. Abiotic stress responses in plants: unraveling the complexity of genes and networks to survive. In: Vahdati K, Leslie C, eds. Abiotic stress—plant responses and applications in agriculture. InTech.
El Habti A, Fleury D, Jewell N, Garnett T, Tricker PJ.. 2020. Tolerance of combined drought and heat stress is associated with transpiration maintenance and water soluble carbohydrates in wheat grains. Frontiers in Plant Science 11, 1555. PubMed PMC
Fahlgren N, Gehan MA, Baxter I.. 2015. Lights, camera, action: high-throughput plant phenotyping is ready for a close-up. Current Opinion in Plant Biology 24, 93–99. PubMed
FAOSTAT. 2019. FAOSTAT statistical database. Rome: Food and Agriculture Organization of the United Nations.https://www.fao.org/faostat/en/#data
Fimognari L, Dölker R, Kaselyte G, Jensen CNG, Akhtar SS, Großkinsky DK, Roitsch T.. 2020. Simple semi-high throughput determination of activity signatures of key antioxidant enzymes for physiological phenotyping. Plant Methods 16, 42. PubMed PMC
Fiorani F, Schurr U.. 2013. Future scenarios for plant phenotyping. Annual Review of Plant Biology 64, 267–291. PubMed
Fischer RA, Maurer R.. 1978. Drought resistance in spring wheat cultivars. I. Grain yield responses. Australian Journal of Agricultural Research 29, 897–912.
Foyer CH, Noctor G.. 2005. Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant, Cell & Environment 28, 1056–1071.
Giusti MM, Wrolstad RE.. 2001. Characterization and measurement of anthocyanins by UV-visible spectroscopy. Current Protocols in Food Analytical Chemistry Unit F12. doi: 10.1002/0471142913.faf0102s00. DOI
Grubbs FE. 1950. Sample criteria for testing outlying observations. Annals of Mathematical Statistics 21, 27–58.
Grzesiak MT, Marcińska I, Janowiak F, Rzepka A, Hura T.. 2012. The relationship between seedling growth and grain yield under drought conditions in maize and triticale genotypes. Acta Physiologiae Plantarum 34, 1757–1764.
Guerreiro SB, Dawson RJ, Kilsby C, Lewis E, Ford A.. 2018. Future heat-waves, droughts and floods in 571 European cities Environmental Research Letters 13, 03409.
Jammer A, Gasperl A, Luschin-Ebengreuth N, et al. . 2015. Simple and robust determination of the activity signature of key carbohydrate metabolism enzymes for physiological phenotyping in model and crop plants. Journal of Experimental Botany 66, 5531–5542. PubMed
Joosen RV, Arends D, LiY, Willems LA, Keurentjes JJ, Ligterink W, Jansen RCHilhorst HW.. 2013. Identifying genotype-by-environment interactions in the metabolism of germinating arabidopsis seeds using generalized genetical genomics. Plant Physiology 162, 553–566. PubMed PMC
Junker A, Muraya MM, Weigelt-Fischer K, Arana-Ceballos F, Klukas C, Melchinger AE, Meyer RC, Riewe D, Altmann T.. 2015. Optimizing experimental procedures for quantitative evaluation of crop plant performance in high throughput phenotyping systems. Frontiers in Plant Science 5, 1–21. PubMed PMC
Koussevitzky S, Suzuki N, Huntington S, Armijo L, Sha W, Cortes D, Shulaev V, Mittler R.. 2008. Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. Journal of Biological Chemistry 283, 34197–34203. PubMed PMC
Kuhn M. 2008. Building predictive models in R using the caret package. Journal of Statistical Software 28, 1–26. PubMed
Lascano HR, Antonicelli GE, Luna CM, Melchiorre MN, Gómez LD, Racca RW, Trippi VS, Casano LM.. 2001. Antioxidant system response of different wheat cultivars under drought: field and in vitro studies. Australian Journal of Plant Physiology 28, 1095–1102.
Lawson T, Terashima I, Fujita T, Wang Y.. 2018. Coordination between photosynthesis and stomatal behavior. In: Adams W III, Terashima I, eds. The leaf: a platform for performing photosynthesis. Advances in Photosynthesis and Respiration, vol 44. Cham: Springer, 141–161.
Manès Y, Gomez HF, Puhl L, Reynolds M, Braun HJ, Trethowan R.. 2012. Genetic yield gains of the CIMMYT International semi-arid wheat yield trials from 1994 to 2010. Crop Science 52, 1543–1552.
Meade KA, Cooper M, Beavis WD.. 2013. Modeling biomass accumulation in maize kernels. Field Crops Research 151, 92–100.
Merzlyak MN, Gitelson AA, Chivkunova OB, Solovchenko AE, Pogosyan SI.. 2003. Application of reflectance spectroscopy for analysis of higher plant pigments. Russian Journal of Plant Physiology 50, 704–710.
Moore G. 2015. Strategic pre-breeding for wheat improvement. Nature Plants 1, 15018. PubMed
Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J.. 2003. Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300, 332–336. PubMed
Moshelion M. 2020. The dichotomy of yield and drought resistance. EMBO Reports 21, e51598. PubMed PMC
Nunes C, Araújo S, Silva JM, Fevereiro P, Silva AB.. 2009. Photosynthesis light curves: a method for screening water deficit resistance in the model legume Medicago truncatula. Annals of Applied Biology 155, 321–332.
Paine CET, Marthews TR, Vogt DR, Purves D, Rees M, Hector A, Turnbull LA.. 2012. How to fit nonlinear plant growth models and calculate growth rates: an update for ecologists. Methods in Ecology and Evolution 3, 245–256.
Parent B, Bonneau J, Maphosa L, Kovalchuk A, Langridge P, Fleury D.. 2017. Quantifying wheat sensitivities to environmental constraints to dissect genotype × environment interactions in the field. Plant Physiology 174, 1669–1682. PubMed PMC
Pennacchi JP, Carmo-Silva E, Andralojc PJ, Lawson T, Allen AM, Raines CA, Parry MAJ.. 2019. Stability of wheat grain yields over three field seasons in the UK. Food and Energy Security 8, e00147. PubMed PMC
Pinheiro C, Chaves MM.. 2011. Photosynthesis and drought: can we make metabolic connections from available data? Journal of Experimental Botany 62, 869–882. PubMed
Reynolds MP, Pask AJD, Hoppitt WJE, et al. . 2017. Strategic crossing of biomass and harvest index—source and sink—achieves genetic gains in wheat. Euphytica 213, 257. PubMed PMC
Reynolds MP, Saint PC, Saad ASI, Vargas M, Condon AG.. 2007. Evaluating potential genetic gains in wheat associated with stress-adaptive trait expression in elite genetic resources under drought and heat stress. Crop Science 47, S-172–S-189.
Rizhsky L, Liang H, Shuman J, S, hulaev V, Davletova S, Mittler R.. 2004. When defense pathways collide. The response of arabidopsis to a combination of drought and heat stress. Plant Physiology 134, 1683–1696. PubMed PMC
Roche D. 2015. Stomatal conductance is essential for higher yield potential of C3 crops. Critical Reviews in Plant Sciences 34, 429–453.
Rohart F, Gautier B, Singh A, Lê Cao K-A.. 2017. mixOmics: an R package for ‘omics feature selection and multiple data integration. PLoS Computational Biology 13, e1005752. PubMed PMC
Roitsch T, Cabrera-Bosquet L, Fournier A, Ghamkhar K, Jiménez-Berni J, Pinto F, Ober ES.. 2019. Review: new sensors and data-driven approaches—a path to next generation phenomics. Plant Science 282, 2–10. PubMed PMC
Roitsch T, González MC.. 2004. Function and regulation of plant invertases: sweet sensations. Trends in Plant Science 9, 606–613. PubMed
Sairam RK, Srivastava GC, Saxena DC.. 2000. Increased antioxidant activity under elevated temperatures: a mechanism of heat stress tolerance in wheat genotypes. Biologia Plantarum 43, 245–251.
Schoppach R, Taylor JD, Majerus E, Claverie E, Baumann U, Suchecki R, Fleury D, SadokW.. 2016. High resolution mapping of traits related to whole-plant transpiration under increasing evaporative demand in wheat. Journal of Experimental Botany 67, 2847–2860. PubMed PMC
Secchi F, Zwieniecki MA.. 2016. Accumulation of sugars in the xylem apoplast observed under water stress conditions is controlled by xylem pH. Plant, Cell & Environment 39, 2350–2360. PubMed
Seelig HD, Hoehn A, Stodieck LS, Klaus DM, Adams WW, Emery WJ.. 2008. The assessment of leaf water content using leaf reflectance ratios in the visible, near-, and short-wave-infrared. International Journal of Remote Sensing 29, 3701–3713.
Shahinnia F, Le Roy J, Laborde B, Sznajder B, Kalambettu P, Mahjourimajd S, Tilbrook J, Fleury D.. 2016. Genetic association of stomatal traits and yield in wheat grown in low rainfall environments. BMC Plant Biology 16, 150. PubMed PMC
Shokat S, Großkinsky DK, Roitsch T, Liu F.. 2020. Activities of leaf and spike carbohydrate-metabolic and antioxidant enzymes are linked with yield performance in three spring wheat genotypes grown under well-watered and drought conditions. BMC Plant Biology 20, 400. PubMed PMC
Singleton VL, Orthofer R, Lamuela-Raventós RM.. 1999. Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin–Ciocalteu reagent. Methods in Enzymology 299, 152–178.
Stekhoven DJ, Bühlmann P.. 2012. Missforest-non-parametric missing value imputation for mixed-type data. Bioinformatics 28, 112–118. PubMed
Tardieu F. 2012. Any trait or trait-related allele can confer drought tolerance: just design the right drought scenario. Journal of Experimental Botany 63, 25–31. PubMed
Tardieu F, Cabrera-Bosquet L, Pridmore T, Bennett M.. 2017. Plant phenomics, from sensors to knowledge. Current Biology 27, R770–R783. PubMed
Tessmer OL, Jiao Y, Cruz JA, Kramer DM, Chen J.. 2013. Functional approach to high-throughput plant growth analysis. BMC Systems Biology 7, 1–13. PubMed PMC
Tricker PJ, Elhabti A, Schmidt J, Fleury D.. 2018. The physiological and genetic basis of combined drought and heat tolerance in wheat. Journal of Experimental Botany 69, 3195–3210. PubMed
Whittaker A, Bochicchio A, Vazzana C, Lindsey G, Farrant J.. 2001. Changes in leaf hexokinase activity and metabolite levels in response to drying in the desiccation-tolerant species Sporobolus stapfianus and Xerophyta viscosa. Journal of Experimental Botany 52, 961–969. PubMed
Woodward FI, Hunt R.. 1983. Plant growth curves: the functional approach to plant growth analysis. Journal of Applied Ecology 20, 695.
Zampieri M, Ceglar A, Dentener F, Toreti A.. 2017. Wheat yield loss attributable to heat waves, drought and water excess at the global, national and subnational scales. Environmental Research Letters 12, 064008.
Zandalinas SI, Balfagón D, Arbona V, Gómez-Cadenas A.. 2017. Modulation of antioxidant defense system is associated with combined drought and heat stress tolerance in citrus. Frontiers in Plant Science 8, 953. PubMed PMC
Zhang G, Zhang M, Zhao Z, Ren Y, Li Q, Wang W.. 2017. Wheat TaPUB1 modulates plant drought stress resistance by improving antioxidant capability. Scientific Reports 7, 1–13. PubMed PMC
Zhishen J, Mengcheng T, Jianming W.. 1999. The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chemistry 64, 555–559.
Triticale field phenotyping using RGB camera for ear counting and yield estimation