Parental drought priming enhances tolerance to low temperature in wheat (Triticum aestivum) offspring
Junhong Guo A E , Hongyan Wang B , Shengqun Liu A , Yongjun Wang C , Fulai Liu D and Xiangnan Li
A E F *
+ Author Affiliations
- Author Affiliations
A Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun 130102, China.
B Laboratory of Plant Epigenetics and Evolution, School of Life Science, Liaoning University, Shenyang 110036, China.
C Institute of Agricultural Resources and Environment, Jilin Academy of Agriculture Sciences/State Engineering Laboratory of Maize, Changchun 130033, China.
D University of Copenhagen, Faculty of Science, Department of Plant and Environmental Sciences, Højbakkegård Allé 13, Tåstrup DK-2630, Denmark.
E University of Chinese Academy of Sciences, Beijing 100049, China.
F CAS Engineering Laboratory for Eco-agriculture in Water Source of Liaoheyuan, Chinese Academy of Science, Changchun 130102, China.
Functional Plant Biology 49(11) 946-957 https://doi.org/10.1071/FP22043
Submitted: 20 February 2022 Accepted: 28 June 2022 Published: 25 July 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Low temperature is one of the major environmental stresses that limit crop growth and grain yield in wheat (Triticum aestivum L.). Drought priming at the vegetative stage could enhance wheat tolerance to later cold stress; however, the transgenerational effects of drought priming on wheat offspring’s cold stress tolerance remains unclear. Here, the low temperature responses of offspring were tested after the parental drought priming treatment at grain filling stage. The offspring plants from parental drought priming treatment had a higher abscisic acid (ABA) level and lower osmotic potential (Ψo) than the control plants under cold conditions. Moreover, parental drought priming increased the antioxidant enzyme activities and decreased hydrogen peroxide (H2O2) accumulation in offspring. In comparison to control plants, parental drought priming plants had a higher ATP concentration and higher activities of ATPase and the enzymes involved in sucrose biosynthesis and starch metabolism. The results indicated that parental drought priming induced low temperature tolerance in offspring by regulating endogenous ABA levels and maintaining the redox homeostasis and the balance of carbohydrate metabolism, which provided a potential approach for cold resistant cultivation in wheat.
Keywords: antioxidant capacity, carbohydrate metabolism, drought priming, low temperature, osmotic adjustment, photosynthesis, transgenerational effects, Triticum aestivum.
References
Allen RD (1995) Dissection of oxidative stress tolerance using transgenic plants. Plant Physiology 107, 1049–1054.| Dissection of oxidative stress tolerance using transgenic plants.Crossref | GoogleScholarGoogle Scholar |
AOAC (1984) ‘Official methods of analysis.’ 14th edn. (Association of official analytical chemists: Arlington, VA)
Baier M, Bittner A, Prescher A, van Buer J (2019) Preparing plants for improved cold tolerance by priming. Plant, Cell & Environment 42, 782–800.
| Preparing plants for improved cold tolerance by priming.Crossref | GoogleScholarGoogle Scholar |
Benincasa P, Bravi E, Marconi O, Lutts S, Tosti G, Falcinelli B (2021) Transgenerational effects of salt stress imposed to rapeseed (Brassica napus var. oleifera Del.) plants involve greater phenolic content and antioxidant activity in the edible sprouts obtained from offspring seeds. Plants (Basel) 10, 932
| Transgenerational effects of salt stress imposed to rapeseed (Brassica napus var. oleifera Del.) plants involve greater phenolic content and antioxidant activity in the edible sprouts obtained from offspring seeds.Crossref | GoogleScholarGoogle Scholar |
Bilska-Kos A, Mytych J, Suski S, Magon J, Ochodzki P, Zebrowski J (2020) Sucrose phosphate synthase (SPS), sucrose synthase (SUS) and their products in the leaves of Miscanthus x giganteus and Zea mays at low temperature. Planta 252, 23
| Sucrose phosphate synthase (SPS), sucrose synthase (SUS) and their products in the leaves of Miscanthus x giganteus and Zea mays at low temperature.Crossref | GoogleScholarGoogle Scholar |
Bittner A, van Buer J, Baier M (2020) Cold priming uncouples light- and cold-regulation of gene expression in Arabidopsis thaliana. BMC Plant Biology 20, 281
| Cold priming uncouples light- and cold-regulation of gene expression in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Annals of Botany 91, 179–194.
| Antioxidants, oxidative damage and oxygen deprivation stress: a review.Crossref | GoogleScholarGoogle Scholar |
Boyko A, Kovalchuk I (2014) Transgenerational response to stress in Arabidopsis thaliana. Plant Signaling & Behavior 5, 995–998.
| Transgenerational response to stress in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Bracher A, Whitney SM, Hartl FU, Hayer-Hartl M (2017) Biogenesis and metabolic maintenance of rubisco. Annual Review of Plant Biology 68, 29–60.
| Biogenesis and metabolic maintenance of rubisco.Crossref | GoogleScholarGoogle Scholar |
Burns JG, Mery F (2010) Transgenerational memory effect of ageing in Drosophila. Journal of Evolutionary Biology 23, 678–686.
| Transgenerational memory effect of ageing in Drosophila.Crossref | GoogleScholarGoogle Scholar |
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Molecular Plant 13, 1194–1202.
| TBtools: an integrative toolkit developed for interactive analyses of big biological data.Crossref | GoogleScholarGoogle Scholar |
Ciereszko I, Johansson H, Kleczkowski LA (2001) Sucrose and light regulation of a cold-inducible UDP-glucose pyrophosphorylase gene via a hexokinase-independent and abscisic acid-insensitive pathway in Arabidopsis. Biochemical Journal 354, 67–72.
| Sucrose and light regulation of a cold-inducible UDP-glucose pyrophosphorylase gene via a hexokinase-independent and abscisic acid-insensitive pathway in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Cong W, Miao Y, Xu L, Zhang Y, Yuan C, Wang J, Zhuang T, Lin X, Jiang L, Wang N, Ma J, Sanguinet KA, Liu B, Rustgi S, Ou X (2019) Transgenerational memory of gene expression changes induced by heavy metal stress in rice (Oryza sativa L.). BMC Plant Biology 19, 282
| Transgenerational memory of gene expression changes induced by heavy metal stress in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |
Cui Y, Tian Z, Hu J, Shao Y, Liu R, Jiang D, Yuan J, Dai T (2019) Drought priming during the vegetative stage can enhance post-anthesis drought tolerance by improving photosynthetic capacity in winter wheat. Arid Land Research and Management 33, 183–199.
| Drought priming during the vegetative stage can enhance post-anthesis drought tolerance by improving photosynthetic capacity in winter wheat.Crossref | GoogleScholarGoogle Scholar |
da-Silva WS, Rezende GL, Galina A (2001) Subcellular distribution and kinetic properties of cytosolic and non-cytosolic hexokinases in maize seedling roots: implications for hexose phosphorylation. Journal of Experimental Botany 52, 1191–1201.
| Subcellular distribution and kinetic properties of cytosolic and non-cytosolic hexokinases in maize seedling roots: implications for hexose phosphorylation.Crossref | GoogleScholarGoogle Scholar |
Devireddy AR, Tschaplinski TJ, Tuskan GA, Muchero W, Chen J-G (2021) Role of reactive oxygen species and hormones in plant responses to temperature changes. International Journal of Molecular Sciences 22, 8843
| Role of reactive oxygen species and hormones in plant responses to temperature changes.Crossref | GoogleScholarGoogle Scholar |
Fábián A, Jäger K, Rakszegi M, Barnabás B (2011) Embryo and endosperm development in wheat (Triticum aestivum L.) kernels subjected to drought stress. Plant Cell Reports 30, 551–563.
| Embryo and endosperm development in wheat (Triticum aestivum L.) kernels subjected to drought stress.Crossref | GoogleScholarGoogle Scholar |
Gibbs J, Greenway H (2003) Review: Mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism. Functional Plant Biology 30, 1–47.
| Review: Mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism.Crossref | GoogleScholarGoogle Scholar |
González APR, Chrtek J, Dobrev PI, Dumalasova V, Fehrer J, Mraz P, Latzel V (2016) Stress-induced memory alters growth of clonal offspring of white clover (Trifolium repens). American Journal of Botany 103, 1567–1574.
| Stress-induced memory alters growth of clonal offspring of white clover (Trifolium repens).Crossref | GoogleScholarGoogle Scholar |
Iwasaki M, Paszkowski J (2014) Identification of genes preventing transgenerational transmission of stress-induced epigenetic states. Proceedings of the National Academy of Sciences of the United States of America 111, 8547–8552.
| Identification of genes preventing transgenerational transmission of stress-induced epigenetic states.Crossref | GoogleScholarGoogle Scholar |
Jammer A, Gasperl A, Luschin-Ebengreuth N, Heyneke E, Chu H, Cantero-Navarro E, Grosskinsky DK, Albacete AA, Stabentheiner E, Franzaring J, Fangmeier A, van der Graaff E, Roitsch T (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.
| Simple and robust determination of the activity signature of key carbohydrate metabolism enzymes for physiological phenotyping in model and crop plants.Crossref | GoogleScholarGoogle Scholar |
Jurczyk B, Grzesiak M, Pociecha E, Wlazlo M, Rapacz M (2019) Diverse stomatal behaviors mediating photosynthetic acclimation to low temperatures in Hordeum vulgare. Frontiers in Plant Science 9, 1963
| Diverse stomatal behaviors mediating photosynthetic acclimation to low temperatures in Hordeum vulgare.Crossref | GoogleScholarGoogle Scholar |
Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiology 136, 4159–4168.
| Exploring the temperature-stress metabolome of Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Lawlor DW (2002) Limitation to photosynthesis in water-stressed leaves: stomata vs. metabolism and the role of ATP. Annals of Botany 89, 871–885.
| Limitation to photosynthesis in water-stressed leaves: stomata vs. metabolism and the role of ATP.Crossref | GoogleScholarGoogle Scholar |
León-Chan RG, López-Meyer M, Osuna-Enciso T, Sañudo-Barajas JA, Heredia JB, León-Félix J (2017) Low temperature and ultraviolet-B radiation affect chlorophyll content and induce the accumulation of UV-B-absorbing and antioxidant compounds in bell pepper (Capsicum annuum) plants. Environmental and Experimental Botany 139, 143–151.
| Low temperature and ultraviolet-B radiation affect chlorophyll content and induce the accumulation of UV-B-absorbing and antioxidant compounds in bell pepper (Capsicum annuum) plants.Crossref | GoogleScholarGoogle Scholar |
Leuendorf JE, Frank M, Schmülling T (2020) Acclimation, priming and memory in the response of Arabidopsis thaliana seedlings to cold stress. Scientific Reports 10, 689
| Acclimation, priming and memory in the response of Arabidopsis thaliana seedlings to cold stress.Crossref | GoogleScholarGoogle Scholar |
Li X, Cai J, Liu F, Dai T, Cao W, Jiang D (2014) Physiological, proteomic and transcriptional responses of wheat to combination of drought or waterlogging with late spring low temperature. Functional Plant Biology 41, 690–703.
| Physiological, proteomic and transcriptional responses of wheat to combination of drought or waterlogging with late spring low temperature.Crossref | GoogleScholarGoogle Scholar |
Li X, Hao C, Zhong J, Liu F, Cai J, Wang X, Zhou Q, Dai T, Cao W, Jiang D (2015a) Mechano-stimulated modifications in the chloroplast antioxidant system and proteome changes are associated with cold response in wheat. BMC Plant Biology 15, 219
| Mechano-stimulated modifications in the chloroplast antioxidant system and proteome changes are associated with cold response in wheat.Crossref | GoogleScholarGoogle Scholar |
Li X, Topbjerg HB, Jiang D, Liu F (2015b) Drought priming at vegetative stage improves the antioxidant capacity and photosynthesis performance of wheat exposed to a short-term low temperature stress at jointing stage. Plant and Soil 393, 307–318.
| Drought priming at vegetative stage improves the antioxidant capacity and photosynthesis performance of wheat exposed to a short-term low temperature stress at jointing stage.Crossref | GoogleScholarGoogle Scholar |
Li X, Tan D-X, Jiang D, Liu F (2016) Melatonin enhances cold tolerance in drought-primed wild-type and abscisic acid-deficient mutant barley. Journal of Pineal Research 61, 328–339.
| Melatonin enhances cold tolerance in drought-primed wild-type and abscisic acid-deficient mutant barley.Crossref | GoogleScholarGoogle Scholar |
Li X, Brestic M, Tan D-X, Zivcak M, Zhu X, Liu S, Song F, Reiter RJ, Liu F (2018) Melatonin alleviates low PS I-limited carbon assimilation under elevated CO2 and enhances the cold tolerance of offspring in chlorophyll b-deficient mutant wheat. Journal of Pineal Research 64, e12453
| Melatonin alleviates low PS I-limited carbon assimilation under elevated CO2 and enhances the cold tolerance of offspring in chlorophyll b-deficient mutant wheat.Crossref | GoogleScholarGoogle Scholar |
Li H, Li S, Wang Z, Liu S, Zhou R, Li X (2020) Abscisic acid-mimicking ligand AMF4 induced cold tolerance in wheat by altering the activities of key carbohydrate metabolism enzymes. Plant Physiology and Biochemistry 157, 284–290.
| Abscisic acid-mimicking ligand AMF4 induced cold tolerance in wheat by altering the activities of key carbohydrate metabolism enzymes.Crossref | GoogleScholarGoogle Scholar |
Liu H, Able AJ, Able JA (2021) Small RNA, transcriptome and degradome analysis of the transgenerational heat stress response network in durum wheat. International Journal of Molecular Sciences 22, 5532
| Small RNA, transcriptome and degradome analysis of the transgenerational heat stress response network in durum wheat.Crossref | GoogleScholarGoogle Scholar |
Lukaszuk E, Ciereszko I (2010) Plant’s UDP-glucose pyrophosphorylase - an underestimated enzyme. Postepy Biologii Komorki 37, 279–295.
McWilliam JR, Naylor AW (1967) Temperature and plant adaptation. I. Interaction of temperature and light in the synthesis of chlorophyll in corn. Plant Physiology 42, 1711–1715.
| Temperature and plant adaptation. I. Interaction of temperature and light in the synthesis of chlorophyll in corn.Crossref | GoogleScholarGoogle Scholar |
Meng M, Geisler M, Johansson H, Mellerowicz EJ, Karpinski S, Kleczkowski LA (2007) Differential tissue/organ-dependent expression of two sucrose- and cold-responsive genes for UDP-glucose pyrophosphorylase in Populus. Gene 389, 186–195.
| Differential tissue/organ-dependent expression of two sucrose- and cold-responsive genes for UDP-glucose pyrophosphorylase in Populus.Crossref | GoogleScholarGoogle Scholar |
Meng F-Z, Hu L-P, Wang S-H, Sui X-L, Wei L, Wei Y-X, Sun J-L, Zhang Z-X (2008) Effects of exogenous abscisic acid (ABA) on cucumber seedling leaf carbohydrate metabolism under low temperature. Plant Growth Regulation 56, 233–244.
| Effects of exogenous abscisic acid (ABA) on cucumber seedling leaf carbohydrate metabolism under low temperature.Crossref | GoogleScholarGoogle Scholar |
Migicovsky Z, Kovalchuk I (2014) Transgenerational changes in plant physiology and in transposon expression in response to UV-C stress in Arabidopsis thaliana. Plant Signaling & Behavior 9, e976490
| Transgenerational changes in plant physiology and in transposon expression in response to UV-C stress in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Nosalewicz A, Siecińska J, Śmiech M, Nosalewicz M, Wiącek D, Pecio A, Wach D (2016) Transgenerational effects of temporal drought stress on spring barley morphology and functioning. Environmental and Experimental Botany 131, 120–127.
| Transgenerational effects of temporal drought stress on spring barley morphology and functioning.Crossref | GoogleScholarGoogle Scholar |
Oliver SN, Van Dongen JT, Alfred SC, Mamun EA, Zhao X, Saini HS, Fernandes SF, Blanchard CL, Sutton BG, Geigenberger P, Dennis ES, Dolferus R (2005) Cold-induced repression of the rice anther-specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility. Plant, Cell & Environment 28, 1534–1551.
| Cold-induced repression of the rice anther-specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility.Crossref | GoogleScholarGoogle Scholar |
Ou X, Zhang Y, Xu C, Lin X, Zang Q, Zhuang T, Jiang L, von Wettstein D, Liu B (2012) Transgenerational inheritance of modified DNA methylation patterns and enhanced tolerance induced by heavy metal stress in rice (Oryza sativa L.). PLoS ONE 7, e41143
| Transgenerational inheritance of modified DNA methylation patterns and enhanced tolerance induced by heavy metal stress in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |
Pearce RS (2001) Plant freezing and damage. Annals of Botany 87, 417–424.
| Plant freezing and damage.Crossref | GoogleScholarGoogle Scholar |
Pei Z-M, Murata Y, Benning G, Thomine S, Klüsener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406, 731–734.
| Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells.Crossref | GoogleScholarGoogle Scholar |
Price AH (1990) A possible role for calcium in oxidative plant stress. Free Radical Research Communications 10, 345–349.
| A possible role for calcium in oxidative plant stress.Crossref | GoogleScholarGoogle Scholar |
Racette K, Zurweller B, Tillman B, Rowland D (2020) Transgenerational stress memory of water deficit in peanut production. Field Crops Research 248, 107712
| Transgenerational stress memory of water deficit in peanut production.Crossref | GoogleScholarGoogle Scholar |
Rahavi MR, Migicovsky Z, Titov V, Kovalchuk I (2011) Transgenerational adaptation to heavy metal salts in Arabidopsis. Frontiers in Plant Science 2, 91
| Transgenerational adaptation to heavy metal salts in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Ritonga FN, Chen S (2020) Physiological and molecular mechanism involved in cold stress tolerance in plants. Plants 9, 560
| Physiological and molecular mechanism involved in cold stress tolerance in plants.Crossref | GoogleScholarGoogle Scholar |
Sage RF (2002) Variation in the kcat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature. Journal of Experimental Botany 53, 609–620.
| Variation in the kcat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature.Crossref | GoogleScholarGoogle Scholar |
Saini R, Adhikary A, Nayyar H, Kumar S (2019) Cross-priming accentuates key biochemical and molecular indicators of defense and improves cold tolerance in chickpea (Cicer arietinum L.). Acta Physiologiae Plantarum 41, 181
| Cross-priming accentuates key biochemical and molecular indicators of defense and improves cold tolerance in chickpea (Cicer arietinum L.).Crossref | GoogleScholarGoogle Scholar |
Savitch LV, Gray GR, Huner NPA (1997) Feedback-limited photosynthesis and regulation of sucrose-starch accumulation during cold acclimation and low-temperature stress in a spring and winter wheat. Planta 201, 18–26.
| Feedback-limited photosynthesis and regulation of sucrose-starch accumulation during cold acclimation and low-temperature stress in a spring and winter wheat.Crossref | GoogleScholarGoogle Scholar |
Scheumann V, Schoch S, Rüdiger W (1998) Chlorophyll a formation in the chlorophyll breductase reaction requires reduced ferredoxin. Journal of Biological Chemistry 273, 35102–35108.
| Chlorophyll a formation in the chlorophyll breductase reaction requires reduced ferredoxin.Crossref | GoogleScholarGoogle Scholar |
Shi K, Fu L-J, Zhang S, Li X, Liao Y-W-K, Xia X-J, Zhou Y-H, Wang R-Q, Chen Z-X, Yu J-Q (2013) Flexible change and cooperation between mitochondrial electron transport and cytosolic glycolysis as the basis for chilling tolerance in tomato plants. Planta 237, 589–601.
| Flexible change and cooperation between mitochondrial electron transport and cytosolic glycolysis as the basis for chilling tolerance in tomato plants.Crossref | GoogleScholarGoogle Scholar |
Smallwood M, Bowles DJ (2002) Plants in a cold climate. Philosophical Transactions of the Royal Society B: Biological Sciences 357, 831–847.
| Plants in a cold climate.Crossref | GoogleScholarGoogle Scholar |
Sturm A, Tang G-Q (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends in Plant Science 4, 401–407.
| The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning.Crossref | GoogleScholarGoogle Scholar |
Tabassum T, Farooq M, Ahmad R, Zohaib A, Wahid A (2017) Seed priming and transgenerational drought memory improves tolerance against salt stress in bread wheat. Plant Physiology and Biochemistry 118, 362–369.
| Seed priming and transgenerational drought memory improves tolerance against salt stress in bread wheat.Crossref | GoogleScholarGoogle Scholar |
Tan W, Liu J, Dai T, Jing Q, Cao W, Jiang D (2008) Alterations in photosynthesis and antioxidant enzyme activity in winter wheat subjected to post-anthesis water-logging. Photosynthetica 46, 21–27.
| Alterations in photosynthesis and antioxidant enzyme activity in winter wheat subjected to post-anthesis water-logging.Crossref | GoogleScholarGoogle Scholar |
Vaultier M-N, Cantrel C, Vergnolle C, Justin A-M, Demandre C, Benhassaine-Kesri G, Çiçek D, Zachowski A, Ruelland E (2006) Desaturase mutants reveal that membrane rigidification acts as a cold perception mechanism upstream of the diacylglycerol kinase pathway in Arabidopsis cells. FEBS Letters 580, 4218–4223.
| Desaturase mutants reveal that membrane rigidification acts as a cold perception mechanism upstream of the diacylglycerol kinase pathway in Arabidopsis cells.Crossref | GoogleScholarGoogle Scholar |
Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu J, Zhu J-K (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. The Plant Journal 45, 523–539.
| Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status.Crossref | GoogleScholarGoogle Scholar |
Wan Q-L, Meng X, Wang C, Dai W, Luo Z, Yin Z, Ju Z, Fu X, Yang J, Ye Q, Zhang Z-H, Zhou Q (2022) Histone H3K4me3 modification is a transgenerational epigenetic signal for lipid metabolism in Caenorhabditis elegans. Nature Communications 13, 768
| Histone H3K4me3 modification is a transgenerational epigenetic signal for lipid metabolism in Caenorhabditis elegans.Crossref | GoogleScholarGoogle Scholar |
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 |
Wang Z, Baskin JM, Baskin CC, Yang X, Liu G, Ye X, Huang Z, Cornelissen JHC (2021) Great granny still ruling from the grave: phenotypical response of plant performance and seed functional traits to salt stress affects multiple generations of a halophyte. Journal of Ecology 110, 117–128.
| Great granny still ruling from the grave: phenotypical response of plant performance and seed functional traits to salt stress affects multiple generations of a halophyte.Crossref | GoogleScholarGoogle Scholar |
Welti R, Li W, Li M, Sang Y, Biesiada H, Zhou H-E, Rajashekar CB, Williams TD, Wang X (2002) Profiling membrane lipids in plant stress responses. Role of phospholipase D alpha in freezing-induced lipid changes in Arabidopsis. Journal of Biological Chemistry 277, 31994–32002.
| Profiling membrane lipids in plant stress responses. Role of phospholipase D alpha in freezing-induced lipid changes in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Xu P, Chen H, Hu J, Cai W (2021) Potential evidence for transgenerational epigenetic memory in Arabidopsis thaliana following spaceflight. Communications Biology 4, 835
| Potential evidence for transgenerational epigenetic memory in Arabidopsis thaliana following spaceflight.Crossref | GoogleScholarGoogle Scholar |
Yamasaki T, Yamakawa T, Yamane Y, Koike H, Satoh K, Katoh S (2002) Temperature acclimation of photosynthesis and related changes in photosystem II electron transport in winter wheat. Plant Physiology 128, 1087–1097.
| Temperature acclimation of photosynthesis and related changes in photosystem II electron transport in winter wheat.Crossref | GoogleScholarGoogle Scholar |
Yang S-H, Wang L-J, Li S-H (2007) Ultraviolet-B irradiation-induced freezing tolerance in relation to antioxidant system in winter wheat (Triticum aestivum L.) leaves. Environmental and Experimental Botany 60, 300–307.
| Ultraviolet-B irradiation-induced freezing tolerance in relation to antioxidant system in winter wheat (Triticum aestivum L.) leaves.Crossref | GoogleScholarGoogle Scholar |
Yang Y-J, Chang W, Huang W, Zhang S-B, Hu H (2017) The effects of chilling-light stress on photosystems I and II in three Paphiopedilum species. Botanical Studies 58, 53
| The effects of chilling-light stress on photosystems I and II in three Paphiopedilum species.Crossref | GoogleScholarGoogle Scholar |
Zhang X, Miao YC, An GY, Zhou Y, Shangguan ZP, Gao JF, Song CP (2001a) K+ channels inhibited by hydrogen peroxide mediate abscisic acid signaling in Vicia guard cells. Cell Research 11, 195–202.
| K+ channels inhibited by hydrogen peroxide mediate abscisic acid signaling in Vicia guard cells.Crossref | GoogleScholarGoogle Scholar |
Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song C-P (2001b) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiology 126, 1438–1448.
| Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba.Crossref | GoogleScholarGoogle Scholar |
Zhang X, Wang X, Zhong J, Zhou Q, Wang X, Cai J, Dai T, Cao W, Jiang D (2016) Drought priming induces thermo-tolerance to post-anthesis high-temperature in offspring of winter wheat. Environmental and Experimental Botany 127, 26–36.
| Drought priming induces thermo-tolerance to post-anthesis high-temperature in offspring of winter wheat.Crossref | GoogleScholarGoogle Scholar |
Zhang H, Liu L, Wang Z, Feng G, Gao Q, Li X (2021) Induction of low temperature tolerance in wheat by pre-soaking and parental treatment with melatonin. Molecules 26, 1192
| Induction of low temperature tolerance in wheat by pre-soaking and parental treatment with melatonin.Crossref | GoogleScholarGoogle Scholar |
Zhao H, Dai T, Jiang D, Cao W (2008) Effects of high temperature on key enzymes involved in starch and protein formation in grains of two wheat cultivars. Journal of Agronomy and Crop Science 194, 47–54.
| Effects of high temperature on key enzymes involved in starch and protein formation in grains of two wheat cultivars.Crossref | GoogleScholarGoogle Scholar |
Zheng C, Jiang D, Liu F, Dai T, Jing Q, Cao W (2009) Effects of salt and waterlogging stresses and their combination on leaf photosynthesis, chloroplast ATP synthesis, and antioxidant capacity in wheat. Plant Science 176, 575–582.
| Effects of salt and waterlogging stresses and their combination on leaf photosynthesis, chloroplast ATP synthesis, and antioxidant capacity in wheat.Crossref | GoogleScholarGoogle Scholar |
