Genetic factors controlling nTiO2 nanoparticles stress tolerance in barley (Hordeum vulgare) during seed germination and seedling development
Samar G. Thabet
A * , Ahmed Sallam B , Yasser S. Moursi A , Mohamed A. Karam A and Ahmad M. Alqudah C *
+ Author Affiliations
- Author Affiliations
A Department of Botany, Faculty of Science, University of Fayoum, 63514 Fayoum, Egypt.
B Department of Genetics, Faculty of Agriculture, Assiut University, 71526 Assiut, Egypt.
C Department of Agroecology, Aarhus University, Flakkebjerg, 4200 Slagelse, Denmark.
Handling Editor: Honghong Wu
Functional Plant Biology 48(12) 1288-1301 https://doi.org/10.1071/FP21129
Submitted: 5 May 2021 Accepted: 30 September 2021 Published: 28 October 2021
© 2021 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Titanium dioxide nanoparticle (nTiO2) is one of the most produced nanoparticles worldwide. Its mechanism on crop development and performance is unclear as it is hard to predict their toxicity or benefit. Therefore, understanding the genetics of crop development under nTiO2 is a prerequisite for their applications in agriculture and crop improvement. Here, we aimed to examine the influnce of 300 ppm nTiO2 on seed germination, seedling morphology, root-related traits in 121 worldwide spring barley (Hordeum vulgare L.) accessions. Results show that nTiO2 significantley affected all traits scored in this study. Response to nTiO2 treatment, clear wide natural variation among accesions was detected. Remarkably, 10 genotypes showed increased root length under nTiO2 at the seedling stage indicating that nTiO2 enhanced the root elongation. Genome-wide association scan (GWAS) was applied using 9K single nucleotide polymorphism (SNPs) in a mixed-linear model that revealed 86 significant marker-trait associations with all traits scored in this study. Many significant SNPs were physically located near candidate genes, of which 191 genes were detected within the linkage disequilibrium and distributed over all barley chromosomes. Mostly, the genes harboured by chromosome 2H, specially calcium-binding genes family, regulate the variation of seedling length-related traits. Candidate genes on 7H encode zinc finger protein that controls the rate of germination. Therefore, these genomic regions at 2H and 7H can be targeted to select for improved seedling development and seed germination under nTiO2 stress in soils. These results improve understanding the genetic control of seed germination and seedling development under high levels of nTiO2 that can support plant breeding and crop improvement programmes.
Keywords: abiotic stress, barley, candidate genes, crop improvement, germination, GWAS, nanoparticles, nTiO2, root length, seedling.
References
Abdul-Baki AA, Anderson JD (1973) Vigor determination in soybean seed by multiple criteria. Crop Science 13, 630–633.| Vigor determination in soybean seed by multiple criteria.Crossref | GoogleScholarGoogle Scholar |
Alqudah AM, Sallam A, Stephen Baenziger P, Börner A (2020) GWAS: fast-forwarding gene identification and characterization in temperate Cereals: lessons from Barley – a review. Journal of Advanced Research 22, 119–135.
| GWAS: fast-forwarding gene identification and characterization in temperate Cereals: lessons from Barley – a review.Crossref | GoogleScholarGoogle Scholar | 31956447PubMed |
Andersen CP, King G, Plocher M, Storm M, Pokhrel LR, Johnson MG, Rygiewicz PT (2016) Germination and early plant development of ten plant species exposed to titanium dioxide and cerium oxide nanoparticles. Environmental Toxicology and Chemistry 35, 2223–2229.
| Germination and early plant development of ten plant species exposed to titanium dioxide and cerium oxide nanoparticles.Crossref | GoogleScholarGoogle Scholar | 26773270PubMed |
Ba C (2010) Study on the uptake, transport, and accumulation of nano-TiO2 in plants and its protein mechanism. Master dissertation, Hebei University, Hebei, China.
Barford D (2004) The role of cysteine residues as redox-sensitive regulatory switches. Current Opinion in Structural Biology 14, 679–686.
| The role of cysteine residues as redox-sensitive regulatory switches.Crossref | GoogleScholarGoogle Scholar | 15582391PubMed |
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.
| Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |
Beffagna N, Buffoli B, Busi C (2005) Modulation of reactive oxygen species production during osmotic stress in Arabidopsis thaliana cultured cells: involvement of the plasma membrane Ca2+-ATPase and H+-ATPase. Plant and Cell Physiology 46, 1326–1339.
| Modulation of reactive oxygen species production during osmotic stress in Arabidopsis thaliana cultured cells: involvement of the plasma membrane Ca2+-ATPase and H+-ATPase.Crossref | GoogleScholarGoogle Scholar | 15937326PubMed |
Boonyanitipong P, Kositsup B, Kumar P, Baruah S, Dutta J (2011) Toxicity of ZnO and TiO2 nanoparticles on germinating rice seed Oryza sativa L. International Journal of Bioscience, Biochemistry and Bioinformatics 1, 282–285.
| Toxicity of ZnO and TiO2 nanoparticles on germinating rice seed Oryza sativa L.Crossref | GoogleScholarGoogle Scholar |
Bose J, Pottosin II, Shabala SS, Palmgren MG, Shabala S (2011) Calcium efflux systems in stress signaling and adaptation in plants. Frontiers in Plant Science 2, 85
| Calcium efflux systems in stress signaling and adaptation in plants.Crossref | GoogleScholarGoogle Scholar | 22639615PubMed |
Burke DJ, Pietrasiak N, Situ SF, Abenojar EC, Porche M, Kraj P, Lakliang Y, Samia AC (2015) Iron oxide and titanium dioxide nanoparticle effects on plant performance and root associated microbes. International Journal of Molecular Sciences 16, 23630–23650.
| Iron oxide and titanium dioxide nanoparticle effects on plant performance and root associated microbes.Crossref | GoogleScholarGoogle Scholar | 26445042PubMed |
Chen Y, Wu N, Mao H, Zhou J, Su Y, Zhang Z, Zhang H, Yuan S (2019) Different toxicities of nanoscale titanium dioxide particles in the roots and leaves of wheat seedlings. RSC Advances 9, 19243–19252.
| Different toxicities of nanoscale titanium dioxide particles in the roots and leaves of wheat seedlings.Crossref | GoogleScholarGoogle Scholar |
Clément L, Hurel C, Marmier N (2013) Toxicity of TiO2 nanoparticles to cladocerans, algae, rotifers and plants – effects of size and crystalline structure. Chemosphere 90, 1083–1090.
| Toxicity of TiO2 nanoparticles to cladocerans, algae, rotifers and plants – effects of size and crystalline structure.Crossref | GoogleScholarGoogle Scholar | 23062945PubMed |
Cox A, Venkatachalam P, Sahi S, Sharma N (2016) Silver and titanium dioxide nanoparticle toxicity in plants: a review of current research. Plant Physiology and Biochemistry 107, 147–163.
| Silver and titanium dioxide nanoparticle toxicity in plants: a review of current research.Crossref | GoogleScholarGoogle Scholar | 27288991PubMed |
Davletova S, Schlauch K, Coutu J, Mittler R (2005) The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiology 139, 847–856.
| The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 16183833PubMed |
Du W, Sun Y, Ji R, Zhu J, Wu J, Guo H (2011) TiO2 and ZnO nanoparticles negatively affect wheat growth and soil enzyme activities in agricultural soil. Journal of Environmental Monitoring 13, 822–828.
| TiO2 and ZnO nanoparticles negatively affect wheat growth and soil enzyme activities in agricultural soil.Crossref | GoogleScholarGoogle Scholar | 21267473PubMed |
Fan W, Lou HQ, Gong YL, Liu MY, Cao MJ, Liu Y, Yang JL, Zheng SJ (2015) Characterization of an inducible C2H2-type zinc finger transcription factor Vu STOP 1 in rice bean (Vigna umbellata) reveals differential regulation between low pH and aluminum tolerance mechanisms. New Phytologist 208, 456–468.
| Characterization of an inducible C2H2-type zinc finger transcription factor Vu STOP 1 in rice bean (Vigna umbellata) reveals differential regulation between low pH and aluminum tolerance mechanisms.Crossref | GoogleScholarGoogle Scholar |
FAOSTAT (2016) Food and agriculture organization of the united nations, satatistical database. Italy.
Finkel T (2000) Redox-dependent signal transduction. FEBS Letters 476, 52–54.
| Redox-dependent signal transduction.Crossref | GoogleScholarGoogle Scholar | 10878249PubMed |
Foyer CH, Descourvieres P, Kunert KJ (1994) Protection against oxygen radicals – an important defense-mechanism studied in transgenic plants. Plant, Cell and Environment 17, 507–523.
| Protection against oxygen radicals – an important defense-mechanism studied in transgenic plants.Crossref | GoogleScholarGoogle Scholar |
Frazier TP, Burklew CE, Zhang B (2014) Titanium dioxide nanoparticles affect the growth and microRNA expression of tobacco (Nicotiana tabacum. Functional and Integrative Genomics 14, 75–83.
| Titanium dioxide nanoparticles affect the growth and microRNA expression of tobacco (Nicotiana tabacum.Crossref | GoogleScholarGoogle Scholar | 24132512PubMed |
Gohari G, Mohammadi A, Akbari A, Panahirad S, Dadpour MR, Fotopoulos V, Kimura S (2020) Titanium dioxide nanoparticles (TiO2 NPs) promote growth and ameliorate salinity stress effects on essential oil profile and biochemical attributes of Dracocephalum moldavica. Scientific Reports 10, 912
| Titanium dioxide nanoparticles (TiO2 NPs) promote growth and ameliorate salinity stress effects on essential oil profile and biochemical attributes of Dracocephalum moldavica.Crossref | GoogleScholarGoogle Scholar | 31969653PubMed |
Haghighi M, da Silva JAT (2014) The effect of N-TiO2 on tomato, onion, and radish seed germination. Journal of Crop Science and Biotechnology 17, 221–227.
| The effect of N-TiO2 on tomato, onion, and radish seed germination.Crossref | GoogleScholarGoogle Scholar |
Hetz W, Hochholdinger F, Schwall M, Feix G (1996) Isolation and characterization of rtcs, a maize mutant deficient in the formation of nodal roots. The Plant Journal 10, 845–857.
| Isolation and characterization of rtcs, a maize mutant deficient in the formation of nodal roots.Crossref | GoogleScholarGoogle Scholar |
Huda KMK, Banu MSA, Garg B, Tula S, Tuteja R, Tuteja N (2013) OsACA6, a P-type IIB Ca2+ ATPase promotes salinity and drought stress tolerance in tobacco by ROS scavenging and enhancing the expression of stress-responsive genes. The Plant Journal 76, 997–1015.
| OsACA6, a P-type IIB Ca2+ ATPase promotes salinity and drought stress tolerance in tobacco by ROS scavenging and enhancing the expression of stress-responsive genes.Crossref | GoogleScholarGoogle Scholar |
Hudson M, Ringli C, Boylan MT, Quail PH (1999) The FAR1 locus encodes a novel nuclear protein specific to phytochrome A signaling. Genes & Development 13, 2017–2027.
| The FAR1 locus encodes a novel nuclear protein specific to phytochrome A signaling.Crossref | GoogleScholarGoogle Scholar |
Keller AA, McFerran S, Lazareva A, Suh S (2013) Global life cycle releases of engineered nanomaterials. Journal of Nanoparticle Research 15, 1692
| Global life cycle releases of engineered nanomaterials.Crossref | GoogleScholarGoogle Scholar |
Kim E, Kim S-H, Kim H-C, Lee SG, Lee SJ, Jeong SW (2011) Growth inhibition of aquatic plant caused by silver and titanium oxide nanoparticles. Toxicology and Environmental Health Sciences 3, 1–6.
| Growth inhibition of aquatic plant caused by silver and titanium oxide nanoparticles.Crossref | GoogleScholarGoogle Scholar |
Kobayashi T, Nishizawa NK (2012) Iron uptake, translocation, and regulation in higher plants. Annual Review of Plant Biology 63, 131–152.
| Iron uptake, translocation, and regulation in higher plants.Crossref | GoogleScholarGoogle Scholar | 22404471PubMed |
Kolukisaoglu Ü, Weinl S, Blazevic D, Batistic O, Kudla J (2004) Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL-CIPK signaling networks. Plant Physiology 134, 43–58.
| Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL-CIPK signaling networks.Crossref | GoogleScholarGoogle Scholar | 14730064PubMed |
Larue C, Laurette J, Herlin-Boime N, Khodja H, Fayard B, Flank A-M, Brisset F, Carriere M (2012) Accumulation, translocation and impact of TiO2 nanoparticles in wheat (Triticum aestivum spp.): influence of diameter and crystal phase. Science of The Total Environment 431, 197–208.
| Accumulation, translocation and impact of TiO2 nanoparticles in wheat (Triticum aestivum spp.): influence of diameter and crystal phase.Crossref | GoogleScholarGoogle Scholar |
Li D, Fu X, Guo L, Huang Z, Li Y, Liu Y, He Z, Cao X, Ma X, Zhao M, Zhu G, Xiao L, Wang H, Chen X, Liu R, Liu X (2016) FAR-RED ELONGATED HYPOCOTYL3 activates SEPALLATA2 but inhibits CLAVATA3 to regulate meristem determinacy and maintenance in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 113, 9375–9380.
| FAR-RED ELONGATED HYPOCOTYL3 activates SEPALLATA2 but inhibits CLAVATA3 to regulate meristem determinacy and maintenance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 27469166PubMed |
Lin R, Ding L, Casola C, Ripoll DR, Feschotte C, Wang H (2007) Transposase-Derived transcription factors regulate light signaling in Arabidopsis. Science 318, 1302–1305.
| Transposase-Derived transcription factors regulate light signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 18033885PubMed |
Lipka AE, Tian F, Wang Q, Peiffer J, Li M, Bradbury PJ, Gore MA, Buckler ES, Zhang Z (2012) GAPIT: genome association and prediction integrated tool. Bioinformatics 28, 2397–2399.
| GAPIT: genome association and prediction integrated tool.Crossref | GoogleScholarGoogle Scholar | 22796960PubMed |
Liu RQ, Lal R (2015) Potentials of engineered nanoparticles as fertilizers for increasing agronomic productions. Science of The Total Environment 514, 131–139.
| Potentials of engineered nanoparticles as fertilizers for increasing agronomic productions.Crossref | GoogleScholarGoogle Scholar |
Lyu S, Wei X, Chen J, Wang C, Wang X, Pan D (2017) Titanium as a beneficial element for crop production. Frontiers in Plant Science 8, 597
| Titanium as a beneficial element for crop production.Crossref | GoogleScholarGoogle Scholar | 28487709PubMed |
Ma L, Li G (2018) FAR1-RELATED SEQUENCE (FRS) and FRS-RELATED FACTOR (FRF) family proteins in Arabidopsis growth and development. Frontiers in Plant Science 9, 692
| FAR1-RELATED SEQUENCE (FRS) and FRS-RELATED FACTOR (FRF) family proteins in Arabidopsis growth and development.Crossref | GoogleScholarGoogle Scholar | 29930561PubMed |
Ma Y, Kuang L, He X, Bai W, Ding Y, Zhang Z, Zhao Y, Chai Z (2010) Effects of rare earth oxide nanoparticles on root elongation of plants. Chemosphere 78, 273–279.
| Effects of rare earth oxide nanoparticles on root elongation of plants.Crossref | GoogleScholarGoogle Scholar | 19897228PubMed |
Ma L, Tian T, Lin R, Deng XW, Wang H, Li G (2016) Arabidopsis FHY3 and FAR1 regulate light-induced myo-inositol biosynthesis and oxidative stress responses by transcriptional activation of MIPS1. Molecular Plant 9, 541–557.
| Arabidopsis FHY3 and FAR1 regulate light-induced myo-inositol biosynthesis and oxidative stress responses by transcriptional activation of MIPS1.Crossref | GoogleScholarGoogle Scholar | 26714049PubMed |
Mahmoodzadeh H, Nabavi M, Kashefi H (2013) Effect of nanoscale titanium dioxide particles on the germination and growth of canola (Brassica napus. Journal of Ornamental plants 3, 25–32.
Marcec MJ, Gilroy S, Poovaiah BW, Tanaka K (2019) Mutual interplay of Ca2+ and ROS signaling in plant immune response. Plant Science 283, 343–354.
| Mutual interplay of Ca2+ and ROS signaling in plant immune response.Crossref | GoogleScholarGoogle Scholar | 31128705PubMed |
Mattiello A, Filippi A, Poscic F, Musetti R, Salvatici MC, Giordano C, Vischi M, Bertolini A, Marchiol L (2015) Evidence of phytotoxicity and genotoxicity in Hordeum vulgare L. exposed to CeO2 and TiO2 nanoparticles. Frontiers in Plant Science 6, 1043
| Evidence of phytotoxicity and genotoxicity in Hordeum vulgare L. exposed to CeO2 and TiO2 nanoparticles.Crossref | GoogleScholarGoogle Scholar | 26635858PubMed |
Mazars C, Thuleau P, Lamotte O, Bourque S (2010) Cross-talk between ROS and calcium in regulation of nuclear activities. Molecular Plant 3, 706–718.
| Cross-talk between ROS and calcium in regulation of nuclear activities.Crossref | GoogleScholarGoogle Scholar | 20522524PubMed |
MG J-JP (1962) ‘Falconer DS—Introduction to quantitative genetics. vol. 17’, pp. 152–153.
Moll J, Gogos A, Bucheli TD, Widmer F, van der Heijden MGA (2016a) Effect of nanoparticles on red clover and its symbiotic microorganisms. Journal of Nanobiotechnology 14, 36
| Effect of nanoparticles on red clover and its symbiotic microorganisms.Crossref | GoogleScholarGoogle Scholar | 27161241PubMed |
Moll J, Okupnik A, Gogos A, Knauer K, Bucheli TD, van der Heijden MGA, Widmer F (2016b) Effects of titanium dioxide nanoparticles on red clover and its rhizobial symbiont. PLoS One 11, e0155111
| Effects of titanium dioxide nanoparticles on red clover and its rhizobial symbiont.Crossref | GoogleScholarGoogle Scholar | 27171465PubMed |
Nhan L, Ma C, Rui Y, Liu S, Li X, Xing B, Liu L (2015) Phytotoxic mechanism of nanoparticles: destruction of chloroplasts and vascular bundles and alteration of nutrient absorption. Scientific Reports 5, 11618
| Phytotoxic mechanism of nanoparticles: destruction of chloroplasts and vascular bundles and alteration of nutrient absorption.Crossref | GoogleScholarGoogle Scholar | 26108166PubMed |
Reddy ASN, Ali GS, Celesnik H, Day IS (2011) Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. The Plant Cell 23, 2010–2032.
| Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression.Crossref | GoogleScholarGoogle Scholar |
Riaz A, Kanwal F, Börner A, Pillen K, Dai F, Alqudah AM (2021) Advances in genomics-based breeding of barley: molecular tools and genomic databases. Agronomy-Basel 11, 894
| Advances in genomics-based breeding of barley: molecular tools and genomic databases.Crossref | GoogleScholarGoogle Scholar |
Romani G, Bonza MC, Filippini I, Cerana M, Beffagna N, De Michelis MI (2004) Involvement of the plasma membrane Ca2+-ATPase in the short-term response of Arabidopsis thaliana cultured cells to oligogalacturonides. Plant Biology 6, 192–200.
| Involvement of the plasma membrane Ca2+-ATPase in the short-term response of Arabidopsis thaliana cultured cells to oligogalacturonides.Crossref | GoogleScholarGoogle Scholar | 15045671PubMed |
Ruffini Castiglione M, Giorgetti L, Geri C, Cremonini R (2011) The effects of nano-TiO2 on seed germination, development and mitosis of root tip cells of Vicia narbonensis L. and Zea mays L. Journal of Nanoparticle Research 13, 2443–2449.
| The effects of nano-TiO2 on seed germination, development and mitosis of root tip cells of Vicia narbonensis L. and Zea mays L.Crossref | GoogleScholarGoogle Scholar |
Samarah NH, Alqudah AM, Amayreh JA, McAndrews GM (2009) The effect of late-terminal drought stress on yield components of four barley cultivars. Journal of Agronomy and Crop Science 195, 427–441.
| The effect of late-terminal drought stress on yield components of four barley cultivars.Crossref | GoogleScholarGoogle Scholar |
Siddiqi KS, Husen A (2017) Plant response to engineered metal oxide nanoparticles. Nanoscale Research Letters 12, 92
| Plant response to engineered metal oxide nanoparticles.Crossref | GoogleScholarGoogle Scholar | 28168616PubMed |
Song G, Gao Y, Wu H, Hou W, Zhang C, Ma H (2012) Physiological effect of anatase TiO2 nanoparticles on Lemna minor. Environmental Toxicology and Chemistry 31, 2147–2152.
| Physiological effect of anatase TiO2 nanoparticles on Lemna minor.Crossref | GoogleScholarGoogle Scholar | 22760594PubMed |
Song U, Jun H, Waldman B, Roh J, Kim Y, Yi J, Lee EJ (2013a) Functional analyses of nanoparticle toxicity: a comparative study of the effects of TiO2 and Ag on tomatoes (Lycopersicon esculentum. Ecotoxicology and Environmental Safety 93, 60–67.
| Functional analyses of nanoparticle toxicity: a comparative study of the effects of TiO2 and Ag on tomatoes (Lycopersicon esculentum.Crossref | GoogleScholarGoogle Scholar | 23651654PubMed |
Song U, Shin M, Lee G, Roh J, Kim Y, Lee EJ (2013b) Functional analysis of TiO2 nanoparticle toxicity in three plant species. Biological Trace Element Research 155, 93–103.
| Functional analysis of TiO2 nanoparticle toxicity in three plant species.Crossref | GoogleScholarGoogle Scholar | 23900645PubMed |
Stirnberg P, Zhao S, Williamson L, Ward S, Leyser O (2012) FHY3 promotes shoot branching and stress tolerance in Arabidopsis in an AXR1-dependent manner. The Plant Journal 71, 907–920.
| FHY3 promotes shoot branching and stress tolerance in Arabidopsis in an AXR1-dependent manner.Crossref | GoogleScholarGoogle Scholar | 22540368PubMed |
Sun SJ, Guo SQ, Yang X, Bao YM, Tang HJ, Sun H, Huang J, Zhang HS (2010) Functional analysis of a novel Cys2/His2-type zinc finger protein involved in salt tolerance in rice. Journal of Experimental Botany 61, 2807–2818.
| Functional analysis of a novel Cys2/His2-type zinc finger protein involved in salt tolerance in rice.Crossref | GoogleScholarGoogle Scholar | 20460361PubMed |
Sun TY, Gottschalk F, Hungerbühler K, Nowack B (2014) Comprehensive probabilistic modelling of environmental emissions of engineered nanomaterials. Environmental Pollution 185, 69–76.
| Comprehensive probabilistic modelling of environmental emissions of engineered nanomaterials.Crossref | GoogleScholarGoogle Scholar | 24220022PubMed |
Szymańska R, Kołodziej K, Ślesak I, Zimak-Piekarczyk P, Orzechowska A, Gabruk M, Żądło A, Habina I, Knap W, Burda K, Kruk J (2016) Titanium dioxide nanoparticles (100–1000 mg/l) can affect vitamin E response in Arabidopsis thaliana. Environmental Pollution 213, 957–965.
| Titanium dioxide nanoparticles (100–1000 mg/l) can affect vitamin E response in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 27060280PubMed |
Tang W, Ji Q, Huang Y, Jiang Z, Bao M, Wang H, Lin R (2013) FAR-RED ELONGATED HYPOCOTYL3 and FAR-RED IMPAIRED RESPONSE1 transcription factors integrate light and abscisic acid signaling in Arabidopsis. Plant Physiology 163, 857–866.
| FAR-RED ELONGATED HYPOCOTYL3 and FAR-RED IMPAIRED RESPONSE1 transcription factors integrate light and abscisic acid signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 23946351PubMed |
Thabet SG, Alqudah AM (2019) Crops and drought. In ‘eLS’. pp. 1–8. (John Wiley & Sons Ltd: Hoboken, NJ, USA)
| Crossref |
Thabet SG, Moursi YS, Karam MA, Graner A, Alqudah AM (2018) Genetic basis of drought tolerance during seed germination in barley. PLoS One 13, e0206682
| Genetic basis of drought tolerance during seed germination in barley.Crossref | GoogleScholarGoogle Scholar | 30388157PubMed |
Thabet SG, Moursi YS, Karam MA, Börner A, Alqudah AM (2020) Natural variation uncovers candidate genes for barley spikelet number and grain yield under drought stress. Genes 11, 533
| Natural variation uncovers candidate genes for barley spikelet number and grain yield under drought stress.Crossref | GoogleScholarGoogle Scholar |
Thabet SG, Alomari DZ, Alqudah AM (2021a) Exploring natural diversity reveals alleles to enhance antioxidant system in barley under salt stress. Plant Physiology and Biochemistry 166, 789–798.
| Exploring natural diversity reveals alleles to enhance antioxidant system in barley under salt stress.Crossref | GoogleScholarGoogle Scholar | 34218207PubMed |
Thabet SG, Moursi YS, Sallam A, Karam MA, Alqudah AM (2021b) Genetic associations uncover candidate SNP markers and genes associated with salt tolerance during seedling developmental phase in barley. Environmental and Experimental Botany 188, 104499
| Genetic associations uncover candidate SNP markers and genes associated with salt tolerance during seedling developmental phase in barley.Crossref | GoogleScholarGoogle Scholar |
Tripathi DK Tripathi DK Tripathi DK (2017) An overview on manufactured nanoparticles in plants: uptake, translocation, accumulation and phytotoxicity. Plant Physiology and Biochemistry 110, 2–12.
| An overview on manufactured nanoparticles in plants: uptake, translocation, accumulation and phytotoxicity.Crossref | GoogleScholarGoogle Scholar |
Utz H (2011) PLABSTAT A computer program for statistical analysis of plant breeding experiments Version 3A. Institute of Plant Breeding, Seed Science and Population Genetics, University Hohenheim, Stuttgart.
Wang H, Deng XW (2002) Arabidopsis FHY3 defines a key phytochrome A signaling component directly interacting with its homologous partner FAR1. The EMBO Journal 21, 1339–1349.
| Arabidopsis FHY3 defines a key phytochrome A signaling component directly interacting with its homologous partner FAR1.Crossref | GoogleScholarGoogle Scholar |
Wang H, Kou X, Pei Z, Xiao JQ, Shan X, Xing B (2011) Physiological effects of magnetite (Fe3O4) nanoparticles on perennial ryegrass (Lolium perenne L.) and pumpkin (Cucurbita mixta) plants. Nanotoxicology 5, 30–42.
| Physiological effects of magnetite (Fe3O4) nanoparticles on perennial ryegrass (Lolium perenne L.) and pumpkin (Cucurbita mixta) plants.Crossref | GoogleScholarGoogle Scholar |
Wang W, Tang W, Ma T, Niu D, Jin JB, Wang H, Lin R (2016) A pair of light signaling factors FHY3 and FAR1 regulates plant immunity by modulating chlorophyll biosynthesis. Journal of Integrative Plant Biology 58, 91–103.
| A pair of light signaling factors FHY3 and FAR1 regulates plant immunity by modulating chlorophyll biosynthesis.Crossref | GoogleScholarGoogle Scholar |
Zhang H, Liu YP, Wen F, Yao DM, Wang L, Guo J, Ni L, Zhang A, Tan MP, Jiang MY (2014) A novel rice C2H2-type zinc finger protein, ZFP36, is a key player involved in abscisic acid-induced antioxidant defence and oxidative stress tolerance in rice. Journal of Experimental Botany 65, 5795–5809.
| A novel rice C2H2-type zinc finger protein, ZFP36, is a key player involved in abscisic acid-induced antioxidant defence and oxidative stress tolerance in rice.Crossref | GoogleScholarGoogle Scholar |
Zheng L, Hong F, Lu S, Liu C (2005) Effect of nano-TiO(2) on strength of naturally aged seeds and growth of spinach. Biological Trace Element Research 104, 83–92.
| Effect of nano-TiO(2) on strength of naturally aged seeds and growth of spinach.Crossref | GoogleScholarGoogle Scholar |
