Analysis of chlorophyll fluorescence parameters as predictors of biomass accumulation and tolerance to heat and drought stress of wheat (Triticum aestivum) plants
Oksana Sherstneva
A , Andrey Khlopkov A , Ekaterina Gromova A , Lyubov Yudina A , Yana Vetrova A , Anna Pecherina A , Darya Kuznetsova A , Elena Krutova B , Vladimir Sukhov A and Vladimir Vodeneev A *
+ Author Affiliations
- Author Affiliations
A Department of Biophysics, Lobachevsky State University of Nizhny Novgorod, Nizhny Novgorod 603950, Russia.
B Agronomic Faculty, Nizhny Novgorod State Agricultural Academy, Nizhny Novgorod 603107, Russia.
Functional Plant Biology 49(2) 155-169 https://doi.org/10.1071/FP21209
Submitted: 20 July 2021 Accepted: 3 November 2021 Published: 24 November 2021
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Agricultural technologies aimed at increasing yields require the development of highly productive and stress-tolerant cultivars. Phenotyping can significantly accelerate breeding; however, no reliable markers have been identified to select the most promising cultivars at an early stage. In this work, we determined the light-induced dynamic of chlorophyll fluorescence (ChlF) parameters in young seedlings of 10 wheat (Triticum aestivum L.) cultivars and evaluated potency of these parameters as predictors of biomass accumulation and stress tolerance. Dry matter accumulation positively correlated with the effective quantum efficiency of photosystem II (ΦPSIIef) and negatively correlated with the half-time of ΦPSIIef reaching (t1/2(ΦPSIIef)). There was a highly significant correlation between t1/2(ΦPSIIef) and dry matter accumulation with increasing prediction period. Short-term heating and drought caused an inhibition of biomass accumulation and photosynthetic activity depending on the stressor intensity. The positive correlation between the ΦPSII dark level (ΦPSIId) in young seedlings and tolerance to a rapidly increasing short-term stressor (heating) was shown. In the case of a long-term stressor (drought), we revealed a strong negative relationship between tolerance and the level of non-photochemical fluorescence quenching (NPQ). In general, the results show the potency of the ChlF parameters of young seedlings as predictors of biomass accumulation and stress tolerance.
Keywords: chlorophyll fluorescence, drought, heat stress, phenotyping, plant breeding, prediction, Triticum aestivum, wheat.
References
Abid M, Tian Z, Ata-Ul-Karim ST, Liu Y, Cui Y, Zahoor R, Jiang D, Dai T (2016) Improved tolerance to post-anthesis drought stress by pre-drought priming at vegetative stages in drought-tolerant and -sensitive wheat cultivars. Plant Physiology and Biochemistry 106, 218–227.| Improved tolerance to post-anthesis drought stress by pre-drought priming at vegetative stages in drought-tolerant and -sensitive wheat cultivars.Crossref | GoogleScholarGoogle Scholar | 27179928PubMed |
Aliyeva DR, Aydinli LM, Pashayeva AN, Zulfugarov IS, Huseynova IM (2020) Photosynthetic machinery and antioxidant status of wheat genotypes under drought stress followed by rewatering. Photosynthetica 58, 1217–1225.
| Photosynthetic machinery and antioxidant status of wheat genotypes under drought stress followed by rewatering.Crossref | GoogleScholarGoogle Scholar |
Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynthesis Research 98, 541–550.
| Heat stress: an overview of molecular responses in photosynthesis.Crossref | GoogleScholarGoogle Scholar | 18649006PubMed |
Andersson I (2008) Catalysis and regulation in Rubisco. Journal of Experimental Botany 59, 1555–1568.
| Catalysis and regulation in Rubisco.Crossref | GoogleScholarGoogle Scholar | 18417482PubMed |
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annual Review of Plant Biology 59, 89–113.
| Chlorophyll fluorescence: a probe of photosynthesis in vivo.Crossref | GoogleScholarGoogle Scholar | 18444897PubMed |
Bano H, Athar HUR, Zafar ZU, Ogbaga CC, Ashraf M (2021) Peroxidase activity and operation of photo-protective component of NPQ play key roles in drought tolerance of mung bean [Vigna radiata (L.) Wilcziek]. Physiologia Plantarum 172, 603–614.
| Peroxidase activity and operation of photo-protective component of NPQ play key roles in drought tolerance of mung bean [Vigna radiata (L.) Wilcziek].Crossref | GoogleScholarGoogle Scholar | 33491210PubMed |
Bekkering CS, Huang J, Tian L (2020) Image-based organ-level plant phenotyping for wheat improvement. Agronomy 10, 1287
| Image-based organ-level plant phenotyping for wheat improvement.Crossref | GoogleScholarGoogle Scholar |
Brestic M, Zivcak M, Kunderlikova K, Allakhverdiev SI (2016) High temperature specifically affects the photoprotective responses of chlorophyll b-deficient wheat mutant lines. Photosynthesis Research 130, 251–266.
| High temperature specifically affects the photoprotective responses of chlorophyll b-deficient wheat mutant lines.Crossref | GoogleScholarGoogle Scholar | 27023107PubMed |
Chovancek E, Zivcak M, Botyanszka L, Hauptvogel P, Yang X, Misheva S, Hussain S, Brestic M (2019) Transient heat waves may affect the photosynthetic capacity of susceptible wheat genotypes due to insufficient photosystem I photoprotection. Plants 8, 282
| Transient heat waves may affect the photosynthetic capacity of susceptible wheat genotypes due to insufficient photosystem I photoprotection.Crossref | GoogleScholarGoogle Scholar |
Chovancek E, Zivcak M, Brestic M, Hussain S, Allakhverdiev SI (2021) The different patterns of post-heat stress responses in wheat genotypes: the role of the transthylakoid proton gradient in efficient recovery of leaf photosynthetic capacity. Photosynthesis Research 150, 179–193.
| The different patterns of post-heat stress responses in wheat genotypes: the role of the transthylakoid proton gradient in efficient recovery of leaf photosynthetic capacity.Crossref | GoogleScholarGoogle Scholar | 33393064PubMed |
Crafts-Brandner SJ, Salvucci ME (2000) Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proceedings of the National Academy of Sciences of the United States of America 97, 13430–13435.
| Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2.Crossref | GoogleScholarGoogle Scholar |
Daryanto S, Wang L, Jacinthe PA (2016) Global synthesis of drought effects on maize and wheat production. PLoS ONE 11, e0156362
| Global synthesis of drought effects on maize and wheat production.Crossref | GoogleScholarGoogle Scholar | 27223810PubMed |
Degen GE, Orr DJ, Carmo-Silva E (2021) Heat-induced changes in the abundance of wheat Rubisco activase isoforms. New Phytologist 229, 1298–1311.
| Heat-induced changes in the abundance of wheat Rubisco activase isoforms.Crossref | GoogleScholarGoogle Scholar |
Demidchik VV, Shashko AY, Bandarenka UY, Smolikova GN, Przhevalskaya DA, Charnysh MA, Pozhvanov GA, Barkosvkyi AV, Smolich II, Sokolik AI, Yu M, Medvedev SS (2020) Plant phenomics: fundamental bases, software and hardware platforms, and machine learning. Russian Journal of Plant Physiology 67, 397–412.
| Plant phenomics: fundamental bases, software and hardware platforms, and machine learning.Crossref | GoogleScholarGoogle Scholar |
Djanaguiraman M, Narayanan S, Erdayani E, Prasad PVV (2020) Effects of high temperature stress during anthesis and grain filling periods on photosynthesis, lipids and grain yield in wheat. BMC Plant Biology 20, 268
| Effects of high temperature stress during anthesis and grain filling periods on photosynthesis, lipids and grain yield in wheat.Crossref | GoogleScholarGoogle Scholar | 32517754PubMed |
Ferguson JN, Tidy AC, Murchie EH, Wilson ZA (2021) The potential of resilient carbon dynamics for stabilizing crop reproductive development and productivity during heat stress. Plant, Cell & Environment 44, 2066–2089.
| The potential of resilient carbon dynamics for stabilizing crop reproductive development and productivity during heat stress.Crossref | GoogleScholarGoogle Scholar |
Gautam A, Agrawal D, SaiPrasad SV, Jajoo A (2014) A quick method to screen high and low yielding wheat cultivars exposed to high temperature. Physiology and Molecular Biology of Plants 20, 533–537.
| A quick method to screen high and low yielding wheat cultivars exposed to high temperature.Crossref | GoogleScholarGoogle Scholar | 25320477PubMed |
Goltsev VN, Kalaji HM, Paunov M, Bąba W, Horaczek T, Mojski J, Kociel H, Allakhverdiev SI (2016) Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus. Russian Journal of Plant Physiology 63, 869–893.
| Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus.Crossref | GoogleScholarGoogle Scholar |
Grieco M, Roustan V, Dermendjiev G, Rantala S, Jain A, Leonardelli M, Neumann K, Berger V, Engelmeier D, Bachmann G, Ebersberger I, Aro E-M, Weckwerth W, Teige M (2020) Adjustment of photosynthetic activity to drought and fluctuating light in wheat. Plant, Cell & Environment 43, 1484–1500.
| Adjustment of photosynthetic activity to drought and fluctuating light in wheat.Crossref | GoogleScholarGoogle Scholar |
Guidi L, Degl’Innocenti E (2011) Imaging of chlorophyll a fluorescence: a tool to study abiotic stress in plants. In ‘Abiotic stress in plants: mechanisms and adaptations’. (ed. A Shanker) pp. 1–20. (InTech)
Harbinson J, Prinzenberg AE, Kruijer W, Aarts MGM (2012) High throughput screening with chlorophyll fluorescence imaging and its use in crop improvement. Current Opinion in Biotechnology 23, 221–226.
| High throughput screening with chlorophyll fluorescence imaging and its use in crop improvement.Crossref | GoogleScholarGoogle Scholar | 22054643PubMed |
Heyneke E, Fernie AR (2018) Metabolic regulation of photosynthesis. Biochemical Society Transactions 46, 321–328.
| Metabolic regulation of photosynthesis.Crossref | GoogleScholarGoogle Scholar | 29523770PubMed |
Hickey LT, Hafeez AN, Robinson H, Jackson SA, Leal-Bertioli SCM, Tester M, Gao C, Godwin ID, Hayes BJ, Wulff BBH (2019) Breeding crops to feed 10 billion. Nature Biotechnology 37, 744–754.
| Breeding crops to feed 10 billion.Crossref | GoogleScholarGoogle Scholar | 31209375PubMed |
Ibrahimova U, Zivcak M, Gasparovic K, Rastogi A, Allakhverdiev SI, Yang X, Brestic M (2021) Electron and proton transport in wheat exposed to salt stress: is the increase of the thylakoid membrane proton conductivity responsible for decreasing the photosynthetic activity in sensitive genotypes? Photosynthesis Research 150, 195–211.
| Electron and proton transport in wheat exposed to salt stress: is the increase of the thylakoid membrane proton conductivity responsible for decreasing the photosynthetic activity in sensitive genotypes?Crossref | GoogleScholarGoogle Scholar | 34125427PubMed |
Kalaji HM, Rastogi A, Živčák M, Brestic M, Daszkowska-Golec A, Sitko K, Alsharafa KY, Lotfi R, Stypiński P, Samborska IA, Cetner MD (2018) Prompt chlorophyll fluorescence as a tool for crop phenotyping: an example of barley landraces exposed to various abiotic stress factors. Photosynthetica 56, 953–961.
| Prompt chlorophyll fluorescence as a tool for crop phenotyping: an example of barley landraces exposed to various abiotic stress factors.Crossref | GoogleScholarGoogle Scholar |
Khan A, Ahmad M, Ahmed M, Iftikhar Hussain M (2021) Rising atmospheric temperature impact on wheat and thermotolerance strategies. Plants 10, 43
| Rising atmospheric temperature impact on wheat and thermotolerance strategies.Crossref | GoogleScholarGoogle Scholar |
Keleş Y, Öncel I (2002) Response of antioxidative defence system to temperature and water stress combinations in wheat seedlings. Plant Science 163, 783–790.
| Response of antioxidative defence system to temperature and water stress combinations in wheat seedlings.Crossref | GoogleScholarGoogle Scholar |
Kruger EL, Volin JC (2006) Reexamining the empirical relation between plant growth and leaf photosynthesis. Functional Plant Biology 33, 421–429.
| Reexamining the empirical relation between plant growth and leaf photosynthesis.Crossref | GoogleScholarGoogle Scholar | 32689249PubMed |
Langridge P, Reynolds M (2021) Breeding for drought and heat tolerance in wheat. Theoretical and Applied Genetics 134, 1753–1769.
| Breeding for drought and heat tolerance in wheat.Crossref | GoogleScholarGoogle Scholar | 33715017PubMed |
Leipner J, Fracheboud Y, Stamp P (1999) Effect of growing season on the photosynthetic apparatus and leaf antioxidative defenses in two maize genotypes of different chilling tolerance. Environmental and Experimental Botany 42, 129–139.
| Effect of growing season on the photosynthetic apparatus and leaf antioxidative defenses in two maize genotypes of different chilling tolerance.Crossref | GoogleScholarGoogle Scholar |
Marutani Y, Yamauchi Y, Higashiyama M, Miyoshi A, Akimoto S, Inoue K, Ikeda K-I, Mizutani M, Sugimoto Y (2017) Essential role of the PSI–LHCII supercomplex in photosystem acclimation to light and/or heat conditions by state transitions. Photosynthesis Research 131, 41–50.
| Essential role of the PSI–LHCII supercomplex in photosystem acclimation to light and/or heat conditions by state transitions.Crossref | GoogleScholarGoogle Scholar | 27432175PubMed |
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence: a practical guide. Journal of Experimental Botany 51, 659–668.
| Chlorophyll fluorescence: a practical guide.Crossref | GoogleScholarGoogle Scholar | 10938857PubMed |
McAusland L, Atkinson JA, Lawson T, Murchie EH (2019) High throughput procedure utilising chlorophyll fuorescence imaging to phenotype dynamic photosynthesis and photoprotection in leaves under controlled gaseous conditions. Plant Methods 15, 109
| High throughput procedure utilising chlorophyll fuorescence imaging to phenotype dynamic photosynthesis and photoprotection in leaves under controlled gaseous conditions.Crossref | GoogleScholarGoogle Scholar | 31548849PubMed |
Medina E, Kim S-H, Yun M, Choi W-G (2021) Recapitulation of the function and role of ROS generated in response to heat stress in plants. Plants 10, 371
| Recapitulation of the function and role of ROS generated in response to heat stress in plants.Crossref | GoogleScholarGoogle Scholar | 33671904PubMed |
Mendanha T, Rosenqvist E, Hyldgaard BN, Doonan JH, Ottosen CO (2020) Drought priming effects on alleviating the photosynthetic limitations of wheat cultivars (Triticum aestivum L.) with contrasting tolerance to abiotic stresses. Journal of Agronomy and Crop Science 206, 651–664.
| Drought priming effects on alleviating the photosynthetic limitations of wheat cultivars (Triticum aestivum L.) with contrasting tolerance to abiotic stresses.Crossref | GoogleScholarGoogle Scholar |
Mir RR, Reynolds M, Pinto F, Khan MA, Bhat MA (2019) High-throughput phenotyping for crop improvement in the genomics era. Plant Science 282, 60–72.
| High-throughput phenotyping for crop improvement in the genomics era.Crossref | GoogleScholarGoogle Scholar | 31003612PubMed |
Montesinos-López A, Montesinos-López OA, Cuevas J, Mata-López WA, Burgueño J, Mondal S, Huerta J, Singh R, Autrique E, González-Pérez L, Crossa J (2017) Genomic Bayesian functional regression models with interactions for predicting wheat grain yield using hyper-spectral image data. Plant Methods 13, 62
| Genomic Bayesian functional regression models with interactions for predicting wheat grain yield using hyper-spectral image data.Crossref | GoogleScholarGoogle Scholar | 28769997PubMed |
Moore CE, Meacham-Hensold K, Lemonnier P, Slattery RA, Benjamin C, Bernacchi CJ, Lawson T, Cavanagh AP (2021) The effect of increasing temperature on crop photosynthesis: from enzymes to ecosystems. Journal of Experimental Botany 72, 2822–2844.
| The effect of increasing temperature on crop photosynthesis: from enzymes to ecosystems.Crossref | GoogleScholarGoogle Scholar | 33619527PubMed |
Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. Journal of Experimental Botany 64, 3983–3998.
| Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications.Crossref | GoogleScholarGoogle Scholar | 23913954PubMed |
Nezhadahmadi A, Prodhan ZH, Faruq G (2013) Drought tolerance in wheat. The Scientific World Journal 2013, 610721
| Drought tolerance in wheat.Crossref | GoogleScholarGoogle Scholar | 24319376PubMed |
Nowicka B, Ciura J, Szymańska R, Kruk J (2018) Improving photosynthesis, plant productivity and abiotic stress tolerance – current trends and future perspectives. Journal of Plant Physiology 231, 415–433.
| Improving photosynthesis, plant productivity and abiotic stress tolerance – current trends and future perspectives.Crossref | GoogleScholarGoogle Scholar | 30412849PubMed |
Okuyama LA, Federizzi LC, Neto JFB (2004) Correlation and path analysis of yield and its components and plant traits in wheat. Ciência Rural 34, 1701–1708.
| Correlation and path analysis of yield and its components and plant traits in wheat.Crossref | GoogleScholarGoogle Scholar |
Paul K, Pauk J, Deák Z, Sass L, Vass I (2016) Contrasting response of biomass and grain yield to severe drought in Cappelle Desprez and Plainsman V wheat cultivars. PeerJ 4, e1708
| Contrasting response of biomass and grain yield to severe drought in Cappelle Desprez and Plainsman V wheat cultivars.Crossref | GoogleScholarGoogle Scholar | 27047703PubMed |
Perdomo JA, Conesa MÀ, Medrano H, Ribas-Carbó M, Galmés J (2015) Effects of long-term individual and combined water and temperature stress on the growth of rice, wheat and maize: relationship with morphological and physiological acclimation. Physiologia Plantarum 155, 149–165.
| Effects of long-term individual and combined water and temperature stress on the growth of rice, wheat and maize: relationship with morphological and physiological acclimation.Crossref | GoogleScholarGoogle Scholar | 25348109PubMed |
Prasad PVV, Pisipati SR, Momčilovič I, Ristic Z (2011) Independent and combined effects of high temperature and drought stress during grain filling on plant yield and chloroplast EF-Tu expression in spring wheat. Journal of Agronomy and Crop Science 197, 430–441.
| Independent and combined effects of high temperature and drought stress during grain filling on plant yield and chloroplast EF-Tu expression in spring wheat.Crossref | GoogleScholarGoogle Scholar |
Qi X, Xu W, Zhang J, Guo R, Zhao M, Hu L, Wang H, Dong H, Li Y (2017) Physiological characteristics and metabolomics of transgenic wheat containing the maize C4 phosphoenolpyruvate carboxylase (PEPC) gene under high temperature stress. Protoplasma 254, 1017–1030.
| Physiological characteristics and metabolomics of transgenic wheat containing the maize C4 phosphoenolpyruvate carboxylase (PEPC) gene under high temperature stress.Crossref | GoogleScholarGoogle Scholar | 27491550PubMed |
Rich SM, Christopher J, Richards R, Watt M (2020) Root phenotypes of young wheat plants grown in controlled environments show inconsistent correlation with mature root traits in the field. Journal of Experimental Botany 71, 4751–4762.
| Root phenotypes of young wheat plants grown in controlled environments show inconsistent correlation with mature root traits in the field.Crossref | GoogleScholarGoogle Scholar | 32347952PubMed |
Salvucci ME, Osteryoung KW, Crafts-Brandner SJ, Vierling E (2001) Exceptional sensitivity of Rubisco activase to thermal denaturation in vitro and in vivo. Plant Physiology 127, 1053–1064.
| Exceptional sensitivity of Rubisco activase to thermal denaturation in vitro and in vivo.Crossref | GoogleScholarGoogle Scholar | 11706186PubMed |
Sankarana S, Khot LR, Espinoza CZ, Jarolmasjed S, Sathuvalli VR, Vandemark GJ, Miklase PN, Carter AH, Pumphrey MO, Knowles NR, Pavek MJ (2015) Low-altitude, high-resolution aerial imaging systems for row and field crop phenotyping: a review. European Journal of Agronomy 70, 112–123.
| Low-altitude, high-resolution aerial imaging systems for row and field crop phenotyping: a review.Crossref | GoogleScholarGoogle Scholar |
Sattar A, Sher A, Ijaz M, Ul-Allah S, Rizwan MS, Hussain M, Jabran K, Cheema MA (2020) Terminal drought and heat stress alter physiological and biochemical attributes in flag leaf of bread wheat. PLoS One 15, e0232974
| Terminal drought and heat stress alter physiological and biochemical attributes in flag leaf of bread wheat.Crossref | GoogleScholarGoogle Scholar | 32401803PubMed |
Schreiber U, Klughammer C, Schansker G (2019) Rapidly reversible chlorophyll fluorescence quenching induced by pulses of supersaturating light in vivo. Photosynthesis Research 142, 35–50.
| Rapidly reversible chlorophyll fluorescence quenching induced by pulses of supersaturating light in vivo.Crossref | GoogleScholarGoogle Scholar | 31090015PubMed |
Sharma DK, Andersen SB, Ottosen C-O, Rosenqvist E (2012) Phenotyping of wheat cultivars for heat tolerance using chlorophyll a fluorescence. Functional Plant Biology 39, 936–947.
| Phenotyping of wheat cultivars for heat tolerance using chlorophyll a fluorescence.Crossref | GoogleScholarGoogle Scholar | 32480843PubMed |
Sharma DK, Andersen SB, Ottosen C-O, Rosenqvist E (2015) Wheat cultivars selected for high FvFm under heat stress maintain high photosynthesis, total chlorophyll, stomatal conductance, transpiration and dry matter. Physiologia Plantarum 153, 284–298.
| Wheat cultivars selected for high FvFm under heat stress maintain high photosynthesis, total chlorophyll, stomatal conductance, transpiration and dry matter.Crossref | GoogleScholarGoogle Scholar | 24962705PubMed |
Sharmin S, Hasan MA, Sikder S (2020) Physiological evaluation of wheat genotypes for high temperature tolerance. The Agriculturists 18, 112–125.
Song P, Wang J, Guo X, Yang W, Zhao C (2021) High-throughput phenotyping: breaking through the bottleneck in future crop breeding. The Crop Journal 9, 633–645.
| High-throughput phenotyping: breaking through the bottleneck in future crop breeding.Crossref | GoogleScholarGoogle Scholar |
Sukhov V, Sukhova E, Khlopkov A, Yudina L, Ryabkova A, Telnykh A, Sergeeva E, Vodeneev V, Turchin I (2021) Proximal imaging of changes in photochemical reflectance index in leaves based on using pulses of green-yellow light. Remote Sensing 13, 1762
| Proximal imaging of changes in photochemical reflectance index in leaves based on using pulses of green-yellow light.Crossref | GoogleScholarGoogle Scholar |
Sukhova E, Yudina L, Gromova E, Ryabkova A, Kior D, Sukhov V (2021) Complex analysis of the efficiency of difference reflectance indices on the basis of 400–700 nm wavelengths for revealing the influences of water shortage and heating on plant seedlings. Remote Sensing 13, 962
| Complex analysis of the efficiency of difference reflectance indices on the basis of 400–700 nm wavelengths for revealing the influences of water shortage and heating on plant seedlings.Crossref | GoogleScholarGoogle Scholar |
Terletskaya NV, Stupko VY, Altayeva NA, Kudrina NO, Blavachinskaya IV, Kurmanbayeva MS, Erezhetova U (2021) Photosynthetic activity of Triticum dicoccum × Triticum aestivum alloplasmic lines during vegetation in connection with productivity traits under varying moister conditions. Photosynthetica 59, 74–83.
| Photosynthetic activity of Triticum dicoccum × Triticum aestivum alloplasmic lines during vegetation in connection with productivity traits under varying moister conditions.Crossref | GoogleScholarGoogle Scholar |
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.
| The physiological and genetic basis of combined drought and heat tolerance in wheat.Crossref | GoogleScholarGoogle Scholar | 29562265PubMed |
van Bezouw RFHM, Keurentjes JJB, Harbinson J, Aarts MGM (2019) Converging phenomics and genomics to study natural variation in plant photosynthetic efficiency. The Plant Journal 97, 112–133.
| Converging phenomics and genomics to study natural variation in plant photosynthetic efficiency.Crossref | GoogleScholarGoogle Scholar | 30548574PubMed |
Wang X, Wang L, Shangguan Z (2016) Leaf gas exchange and fluorescence of two winter wheat varieties in response to drought stress and nitrogen supply. PLoS ONE 11, e0165733
| Leaf gas exchange and fluorescence of two winter wheat varieties in response to drought stress and nitrogen supply.Crossref | GoogleScholarGoogle Scholar | 27802318PubMed |
Wang X, Zhang X, Chen J, Wang X, Cai J, Zhou Q, Dai T, Cao W, Jiang D (2018) Parental drought-priming enhances tolerance to post-anthesis drought in offspring of wheat. Frontiers in Plant Science 9, 261
| Parental drought-priming enhances tolerance to post-anthesis drought in offspring of wheat.Crossref | GoogleScholarGoogle Scholar | 29545817PubMed |
White EM, Wilson FEA (2006) Responses of grain yield, biomass and harvest index and their rates of genetic progress to nitrogen availability in ten winter wheat varieties. Irish Journal of Agricultural and Food Research 45, 85–101.
Yang W, Feng H, Zhang X, Zhang J, Doonan JH, Batchelor W D, Xiong L, Yan J (2020) Crop phenomics and high-throughput phenotyping: past decades, current challenges, and future perspectives. Molecular Plant 13, 187–214.
| Crop phenomics and high-throughput phenotyping: past decades, current challenges, and future perspectives.Crossref | GoogleScholarGoogle Scholar | 31981735PubMed |
Yudina L, Sukhova E, Gromova E, Nerush V, Vodeneev V, Sukhov V (2020) A light-induced decrease in the photochemical reflectance index (PRI) can be used to estimate the energy-dependent component of non-photochemical quenching under heat stress and soil drought in pea, wheat, and pumpkin. Photosynthesis Research 146, 175–187.
| A light-induced decrease in the photochemical reflectance index (PRI) can be used to estimate the energy-dependent component of non-photochemical quenching under heat stress and soil drought in pea, wheat, and pumpkin.Crossref | GoogleScholarGoogle Scholar | 32043219PubMed |
Zandalinas SI, Mittler R, Balfagón D, Arbona V, Gómez-Cadenas A (2018) Plant adaptations to the combination of drought and high temperatures. Physiologia Plantarum 162, 2–12.
| Plant adaptations to the combination of drought and high temperatures.Crossref | GoogleScholarGoogle Scholar | 28042678PubMed |
Zhang J, Zhang S, Cheng M, Jiang H, Zhang X, Peng C, Lu X, Zhang M, Jin J (2018) Effect of drought on agronomic traits of rice and wheat: a meta-analysis. International Journal of Environmental Research and Public Health 15, 839
| Effect of drought on agronomic traits of rice and wheat: a meta-analysis.Crossref | GoogleScholarGoogle Scholar |
Zhao C, Liu B, Piao S, Wang X, Lobell DB, Huang Y, Huang M, Yao Y, Bassu S, Ciais P, Durand J-L, Elliott J, Ewert F, Janssens IA, Li T, Lin E, Liu Q, Martre P, Müller C, Peng S, Peñuelas J, Ruane AC, Wallach D, Wang T, Wu D, Liu Z, Zhu Y, Zhu Z, Asseng S (2017) Temperature increase reduces global yields of major crops in four independent estimates. Proceedings of the National Academy of Sciences of the United States of America 114, 9326–9331.
| Temperature increase reduces global yields of major crops in four independent estimates.Crossref | GoogleScholarGoogle Scholar | 28811375PubMed |
Zivcak M, Kalaji HM, Shao H-B, Olsovska K, Brestic M (2014) Photosynthetic proton and electron transport in wheat leaves under prolonged moderate drought stress. Journal of Photochemistry and Photobiology B: Biology 137, 107–115.
| Photosynthetic proton and electron transport in wheat leaves under prolonged moderate drought stress.Crossref | GoogleScholarGoogle Scholar |
