Harboured cation/proton antiporters modulate stress response to integrated heat and salt via up-regulating KIN1 and GOLS1 in double transgenic Arabidopsis
Nihal Kahraman A and Necla Pehlivan A *A Recep Tayyip Erdogan University, Biology Department, Rize, Turkey.
Functional Plant Biology 49(12) 1070-1084 https://doi.org/10.1071/FP21334
Submitted: 12 November 2021 Accepted: 2 August 2022 Published: 29 August 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Recent research has pointed to improved salt tolerance by co-overexpression of Arabidopsis thaliana NHX1 (Na+/H+ antiporter) and SOS1 (Salt Overly Sensitive1). However, functionality under salt stress accompanying heat is less understood in double transgenics. To further advance possible co-operational interactions of AtNHX1 (N) and AtSOS1 (S) under combined stress, modulation of osmolyte, redox, energy, and abscisic acid metabolism genes was analysed. The expression of the target BIP3, KIN1, GOLS1, OHP2, and CYCA3;2 in transgenic Arabidopsis seedlings were significantly regulated towards a dramatic suppression by ionic, osmotic, and heat stresses. AtNHX1 and AtSOS1 co-overexpression (NS) outpaced the single transgenics and control in terms of membrane disorganisation and the electrolyte leakage of the cell damage caused by heat and salt stress in seedlings. While NaCl slightly induced CYCA3;2 in transgenics, combined stress up-regulated KIN1 and GOLS1, not other genes. Single N and S transgenics overexpressing AtNHX1 and AtSOS1 only appeared similar in their growth and development; however, different to WT and NS dual transgenics under heat + salt stress. Seed germination, cotyledon survival, and hypocotyl length were less influenced by combined stress in NS double transgenic lines than in single N and S and wild type. Stress combination caused significant reprogramming of gene expression profiles, mainly towards downregulation, possibly as a trade-off strategy. Analysing phenotypic, cellular, and transcriptional responses regulating growth facets of tolerant transgenic genotypes may support the ongoing efforts to achieve combined salt and heat tolerance.
Keywords: Arabidopsis thailana Schur, AtNHX1, AtSOS1, basal thermotolerance, Brassicaceae, combined heat and salt, sodium/proton antiporter, stress.
References
Anwar K, Joshi R, Dhankher OP, Singla-Pareek SL, Pareek A (2021) Elucidating the response of crop plants towards individual, combined and sequentially occurring abiotic stresses. International Journal of Molecular Sciences 22, 6119| Elucidating the response of crop plants towards individual, combined and sequentially occurring abiotic stresses.Crossref | GoogleScholarGoogle Scholar |
Beck J, Lohscheider JN, Albert S, Andersson U, Mendgen KW, Rojas-Stütz MC, et al. (2017) Small one-helix proteins are essential for photosynthesis in Arabidopsis. Frontiers in Plant Science 8, 7
| Small one-helix proteins are essential for photosynthesis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Bhardwaj A, Devi P, Chaudhary S, Rani A, Jha UC, Kumar S, et al. (2021) ‘Omics’ approaches in developing combined drought and heat tolerance in food crops. Plant Cell Reports 41, 699–739.
| ‘Omics’ approaches in developing combined drought and heat tolerance in food crops.Crossref | GoogleScholarGoogle Scholar |
Brestic M, Zivcak M, Kalaji HM, Carpentier R, Allakhverdiev SI (2012) Photosystem II thermostability in situ: environmentally induced acclimation and genotype-specific reactions in Triticum aestivum L. Plant Physiology and Biochemistry 57, 93–105.
| Photosystem II thermostability in situ: environmentally induced acclimation and genotype-specific reactions in Triticum aestivum L.Crossref | GoogleScholarGoogle Scholar |
Chen L, Xia W, Song J, Wu M, Xu Z, Hu X, Zhang W (2020) Enhanced thermotolerance of Arabidopsis by chitooligosaccharides-induced CERK1n-ERc fusion gene. Plant Signaling & Behavior 15, 1816322
| Enhanced thermotolerance of Arabidopsis by chitooligosaccharides-induced CERK1n-ERc fusion gene.Crossref | GoogleScholarGoogle Scholar |
Christou A, Filippou P, Manganaris GA, Fotopoulos V (2014) Sodium hydrosulfide induces systemic thermotolerance to strawberry plants through transcriptional regulation of heat shock proteins and aquaporin. BMC Plant Biology 14, 42
| Sodium hydrosulfide induces systemic thermotolerance to strawberry plants through transcriptional regulation of heat shock proteins and aquaporin.Crossref | GoogleScholarGoogle Scholar |
Colmenero Flores JM, Rosales Villegas MÁ (2014) Interaction between salt and heat stress: when two wrongs make a right. Plant, Cell & Environment 37, 1042–1045.
| Interaction between salt and heat stress: when two wrongs make a right.Crossref | GoogleScholarGoogle Scholar |
Esmaeili N, Yang X, Cai Y, Sun L, Zhu X, Shen G, et al. (2019) Co-overexpression of AVP1 and OsSIZ1 in Arabidopsis substantially enhances plant tolerance to drought, salt, and heat stresses. Scientific Reports 9, 7642
| Co-overexpression of AVP1 and OsSIZ1 in Arabidopsis substantially enhances plant tolerance to drought, salt, and heat stresses.Crossref | GoogleScholarGoogle Scholar |
Fauset S, Oliveira L, Buckeridge MS, Foyer CH, Galbraith D, Tiwari R, Gloor M (2019) Contrasting responses of stomatal conductance and photosynthetic capacity to warming and elevated CO2 in the tropical tree species Alchornea glandulosa under heatwave conditions. Environmental and Experimental Botany 158, 28–39.
| Contrasting responses of stomatal conductance and photosynthetic capacity to warming and elevated CO2 in the tropical tree species Alchornea glandulosa under heatwave conditions.Crossref | GoogleScholarGoogle Scholar |
Fernández-Bautista N, Fernández-Calvino L, Muñoz A, Castellano MM (2017) HOP3 a new regulator of the ER stress response in Arabidopsis with possible implications in plant development and response to biotic and abiotic stresses. Plant Signaling & Behavior 12, e1317421
| HOP3 a new regulator of the ER stress response in Arabidopsis with possible implications in plant development and response to biotic and abiotic stresses.Crossref | GoogleScholarGoogle Scholar |
Ferreira-Silva SL, Voigt EL, Silva EN, Maia JM, de Vasconcelos Fontenele A, Silveira JAG (2011) High temperature positively modulates oxidative protection in salt-stressed cashew plants. Environmental and Experimental Botany 74, 162–170.
| High temperature positively modulates oxidative protection in salt-stressed cashew plants.Crossref | GoogleScholarGoogle Scholar |
Flowers TJ, Muscolo A (2015) Introduction to the special issue: halophytes in a changing world. AoB Plants 7, plv020
| Introduction to the special issue: halophytes in a changing world.Crossref | GoogleScholarGoogle Scholar |
Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Current Opinion in Plant Biology 9, 436–442.
| Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks.Crossref | GoogleScholarGoogle Scholar |
Georgii E, Jin M, Zhao J, Kanawati B, Schmitt-Kopplin P, Albert A, et al. (2017) Relationships between drought, heat and air humidity responses revealed by transcriptome-metabolome co-analysis. BMC Plant Biology 17, 120
| Relationships between drought, heat and air humidity responses revealed by transcriptome-metabolome co-analysis.Crossref | GoogleScholarGoogle Scholar |
Guan P, Wang J, Li H, Xie C, Zhang S, Wu C, Zheng C (2018) SENSITIVE TO SALT1, an endoplasmic reticulum-localized chaperone, positively regulates salt resistance. Plant Physiology 178, 1390–1405.
| SENSITIVE TO SALT1, an endoplasmic reticulum-localized chaperone, positively regulates salt resistance.Crossref | GoogleScholarGoogle Scholar |
Hajihashemi S, Skalicky M, Brestic M, Pavla V (2020) Cross-talk between nitric oxide, hydrogen peroxide and calcium in salt-stressed Chenopodium quinoa Willd. At seed germination stage. Plant Physiology and Biochemistry 154, 657–664.
| Cross-talk between nitric oxide, hydrogen peroxide and calcium in salt-stressed Chenopodium quinoa Willd. At seed germination stage.Crossref | GoogleScholarGoogle Scholar |
Henriquez-Valencia C, Moreno AA, Sandoval-Ibañez O, Mitina I, Blanco-Herrera F, Cifuentes-Esquivel N, Orellana A (2015) bZIP17 and bZIP60 regulate the expression of BIP3 and other salt stress responsive genes in an UPR-independent manner in Arabidopsis thaliana. Journal of Cellular Biochemistry 116, 1638–1645.
| bZIP17 and bZIP60 regulate the expression of BIP3 and other salt stress responsive genes in an UPR-independent manner in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Hey D, Grimm B (2018) ONE-HELIX PROTEIN2 (OHP2) is required for the stability of OHP1 and assembly factor HCF244 and is functionally linked to PSII biogenesis. Plant Physiology 177, 1453–1472.
| ONE-HELIX PROTEIN2 (OHP2) is required for the stability of OHP1 and assembly factor HCF244 and is functionally linked to PSII biogenesis.Crossref | GoogleScholarGoogle Scholar |
Huang J, Wang H, Wang Y, Copenhaver GP (2021) Comparative transcriptomic analysis of thermally stressed Arabidopsis thaliana meiotic recombination mutants. BMC Genomics 22, 181
| Comparative transcriptomic analysis of thermally stressed Arabidopsis thaliana meiotic recombination mutants.Crossref | GoogleScholarGoogle Scholar |
Huo L, Sun X, Guo Z, Jia X, Che R, Sun Y, et al. (2020) MdATG18a overexpression improves basal thermotolerance in transgenic apple by decreasing damage to chloroplasts. Horticulture Research 7, 21
| MdATG18a overexpression improves basal thermotolerance in transgenic apple by decreasing damage to chloroplasts.Crossref | GoogleScholarGoogle Scholar |
Jansson S, Andersson J, Jung Kim S, Jackowski G (2000) An Arabidopsis thaliana protein homologous to cyanobacterial high-light-inducible proteins. Plant Molecular Biology 42, 345–351.
| An Arabidopsis thaliana protein homologous to cyanobacterial high-light-inducible proteins.Crossref | GoogleScholarGoogle Scholar |
Ji H, Pardo JM, Batelli G, Van Oosten MJ, Bressan RA, Li X (2013) The salt overly sensitive (SOS) pathway: established and emerging roles. Molecular Plant 6, 275–286.
| The salt overly sensitive (SOS) pathway: established and emerging roles.Crossref | GoogleScholarGoogle Scholar |
Jiang Y, Zheng Q, Chen L, Liang Y, Wu J (2018) Ectopic overexpression of maize heat shock transcription factor gene ZmHsf04 confers increased thermo and salt-stress tolerance in transgenic Arabidopsis. Acta Physiologiae Plantarum 40, 9
| Ectopic overexpression of maize heat shock transcription factor gene ZmHsf04 confers increased thermo and salt-stress tolerance in transgenic Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Jiang Z, Zhou X, Tao M, Yuan F, Liu L, Wu F, et al. (2019) Plant cell-surface GIPC sphingolipids sense salt to trigger Ca2+ influx. Nature 572, 341–346.
| Plant cell-surface GIPC sphingolipids sense salt to trigger Ca2+ influx.Crossref | GoogleScholarGoogle Scholar |
Kaleem F, Shabir G, Aslam K, Rasul S, Manzoor H, Shah SM, Khan AR (2018) An overview of the genetics of plant response to salt stress: present status and the way forward. Applied Biochemistry and Biotechnology 186, 306–334.
| An overview of the genetics of plant response to salt stress: present status and the way forward.Crossref | GoogleScholarGoogle Scholar |
Li W, Zhang C, Lu Q, Wen X, Lu C (2011) The combined effect of salt stress and heat shock on proteome profiling in Suaeda salsa. Journal of Plant Physiology 168, 1743–1752.
| The combined effect of salt stress and heat shock on proteome profiling in Suaeda salsa.Crossref | GoogleScholarGoogle Scholar |
Li Q, Wang W, Wang W, Zhang G, Liu Y, Wang Y, Wang W (2018) Wheat F-box protein gene TaFBA1 is involved in plant tolerance to heat stress. Frontiers in Plant Science 9, 521
| Wheat F-box protein gene TaFBA1 is involved in plant tolerance to heat stress.Crossref | GoogleScholarGoogle Scholar |
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method.Crossref | GoogleScholarGoogle Scholar |
Ma Z-X, Leng Y-J, Chen G-X, Zhou P-M, Ye D, Chen L-Q (2015) The thermosensitive male sterile 1 interacts with the BiPs via DnaJ domain and stimulates their ATPase enzyme activities in Arabidopsis. PLoS One 10, e0132500
| The thermosensitive male sterile 1 interacts with the BiPs via DnaJ domain and stimulates their ATPase enzyme activities in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Ma J, Cirillo V, Zhang D, Maggio A, Wang L, Xiao X, Yao Y (2020) Regulation of ammonium cellular levels is an important adaptive trait for the euhalophytic behavior of Salicornia europaea. Plants 9, 257
| Regulation of ammonium cellular levels is an important adaptive trait for the euhalophytic behavior of Salicornia europaea.Crossref | GoogleScholarGoogle Scholar |
Mian A, Oomen RJFJ, Isayenkov S, Sentenac H, Maathuis FJM, Véry A-A (2011) Over-expression of an Na+- and K+-permeable HKT transporter in barley improves salt tolerance. The Plant Journal 68, 468–479.
| Over-expression of an Na+- and K+-permeable HKT transporter in barley improves salt tolerance.Crossref | GoogleScholarGoogle Scholar |
Mishra RK, Singhal GS (1992) Function of photosynthetic apparatus of intact wheat leaves under high light and heat stress and its relationship with peroxidation of thylakoid lipids. Plant Physiology 98, 1–6.
| Function of photosynthetic apparatus of intact wheat leaves under high light and heat stress and its relationship with peroxidation of thylakoid lipids.Crossref | GoogleScholarGoogle Scholar |
Mishra N, Srivastava AP, Esmaeili N, Hu W, Shen G (2018) Overexpression of the rice gene OsSIZ1 in Arabidopsis improves drought-, heat-, and salt-tolerance simultaneously. PLoS One 13, e0201716
| Overexpression of the rice gene OsSIZ1 in Arabidopsis improves drought-, heat-, and salt-tolerance simultaneously.Crossref | GoogleScholarGoogle Scholar |
Mittler R, Blumwald E (2015) The roles of ROS and ABA in systemic acquired acclimation. The Plant Cell 27, 64–70.
| The roles of ROS and ABA in systemic acquired acclimation.Crossref | GoogleScholarGoogle Scholar |
Niu Y, Xiang Y (2018) An overview of biomembrane functions in plant responses to high-temperature stress. Frontiers in Plant Science 9, 915
| An overview of biomembrane functions in plant responses to high-temperature stress.Crossref | GoogleScholarGoogle Scholar |
Park C-J, Seo Y-S (2015) Heat shock proteins: a review of the molecular chaperones for plant immunity. The Plant Pathology Journal 31, 323
| Heat shock proteins: a review of the molecular chaperones for plant immunity.Crossref | GoogleScholarGoogle Scholar |
Pehlivan N, Sun L, Jarrett P, Yang X, Mishra N, Chen L, et al. (2016) Co-overexpressing a plasma membrane and a vacuolar membrane sodium/proton antiporter significantly improves salt tolerance in transgenic Arabidopsis plants. Plant and Cell Physiology 57, 1069–1084.
| Co-overexpressing a plasma membrane and a vacuolar membrane sodium/proton antiporter significantly improves salt tolerance in transgenic Arabidopsis plants.Crossref | GoogleScholarGoogle Scholar |
Pehlivan N, Sun L, Mishra N (2020) Defensive manoeuvres of NHX1 and SOS1 co/overexpression in plant salt tolerance. Turkish Journal of Botany 44, 367–376.
| Defensive manoeuvres of NHX1 and SOS1 co/overexpression in plant salt tolerance.Crossref | GoogleScholarGoogle Scholar |
Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta (BBA) - Bioenergetics 975, 384–394.
| Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy.Crossref | GoogleScholarGoogle Scholar |
Rani S, Kumar P, Suneja P (2021) Biotechnological interventions for inducing abiotic stress tolerance in crops. Plant Gene 27, 100315
| Biotechnological interventions for inducing abiotic stress tolerance in crops.Crossref | GoogleScholarGoogle Scholar |
Rasmussen S, Barah P, Suarez-Rodriguez MC, Bressendorff S, Friis P, Costantino P, et al. (2013) Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiology 161, 1783–1794.
| Transcriptome responses to combinations of stresses in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Rivero RM, Mestre TC, Mittler R, Rubio F, Garcia-Sanchez F, Martinez V (2014) The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant, Cell & Environment 37, 1059–1073.
| The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants.Crossref | GoogleScholarGoogle Scholar |
Rodríguez-Rosales MP, Gálvez FJ, Huertas R, Aranda MN, Baghour M, Cagnac O, Venema K (2009) Plant NHX cation/proton antiporters. Plant Signaling & Behavior 4, 265–276.
| Plant NHX cation/proton antiporters.Crossref | GoogleScholarGoogle Scholar |
Saidi Y, Finka A, Goloubinoff P (2011) Heat perception and signalling in plants: a tortuous path to thermotolerance. New Phytologist 190, 556–565.
| Heat perception and signalling in plants: a tortuous path to thermotolerance.Crossref | GoogleScholarGoogle Scholar |
Sairam RK, Shukla DS, Saxena DC (1997) Stress induced injury and antioxidant enzymes in relation to drought tolerance in wheat genotypes. Biologia Plantarum 39, 357–364.
| Stress induced injury and antioxidant enzymes in relation to drought tolerance in wheat genotypes.Crossref | GoogleScholarGoogle Scholar |
Scholes RJ (2020) The future of semi-arid regions: a weak fabric unravels. Climate 8, 43
| The future of semi-arid regions: a weak fabric unravels.Crossref | GoogleScholarGoogle Scholar |
Sewelam N, Brilhaus D, Bräutigam A, Alseekh S, Fernie AR, Maurino VG (2020) Molecular plant responses to combined abiotic stresses put a spotlight on unknown and abundant genes. Journal of Experimental Botany 71, 5098–5112.
| Molecular plant responses to combined abiotic stresses put a spotlight on unknown and abundant genes.Crossref | GoogleScholarGoogle Scholar |
Shaar-Moshe L, Blumwald E, Peleg Z (2017) Unique physiological and transcriptional shifts under combinations of salinity, drought, and heat. Plant Physiology 174, 421–434.
| Unique physiological and transcriptional shifts under combinations of salinity, drought, and heat.Crossref | GoogleScholarGoogle Scholar |
Shi Y, Sun H, Wang X, Jin W, Chen Q, Yuan Z, Yu H (2019) Physiological and transcriptomic analyses reveal the molecular networks of responses induced by exogenous trehalose in plant. PLoS One 14, e0217204–5.
| Physiological and transcriptomic analyses reveal the molecular networks of responses induced by exogenous trehalose in plant.Crossref | GoogleScholarGoogle Scholar |
Shukla MK, Llansola-Portoles MJ, Tichý M, Pascal AA, Robert B, Sobotka R (2018) Binding of pigments to the cyanobacterial high-light-inducible protein HliC. Photosynthesis Research 137, 29–39.
| Binding of pigments to the cyanobacterial high-light-inducible protein HliC.Crossref | GoogleScholarGoogle Scholar |
Silva-Correia J, Freitas S, Tavares RM, Lino-Neto T, Azevedo H (2014) Phenotypic analysis of the Arabidopsis heat stress response during germination and early seedling development. Plant Methods 10, 7
| Phenotypic analysis of the Arabidopsis heat stress response during germination and early seedling development.Crossref | GoogleScholarGoogle Scholar |
Singhal RK, Saha D, Skalicky M, Mishra UN, Chauhan J, Behera LP, Lenka D, Chand S, Kumar V, Dey P, Pandey S, Vachova P, Gupta A, Brestic M, El Sabagh A (2021) Crucial cell signaling compounds crosstalk and integrative multi-omics techniques for salinity stress tolerance in plants. Frontiers in Plant Science 12, 670369
| Crucial cell signaling compounds crosstalk and integrative multi-omics techniques for salinity stress tolerance in plants.Crossref | GoogleScholarGoogle Scholar |
Song P, Jia Q, Xiao X, Tang Y, Liu C, Li W, et al. (2021) HSP70-3 interacts with phospholipase Dδ and participates in heat stress defense. Plant Physiology 185, 1148–1165.
| HSP70-3 interacts with phospholipase Dδ and participates in heat stress defense.Crossref | GoogleScholarGoogle Scholar |
Sun L, Pehlivan N, Esmaeili N, Jiang W, Yang X, Jarrett P, et al. (2018) Co-overexpression of AVP1 and PP2A-C5 in Arabidopsis makes plants tolerant to multiple abiotic stresses. Plant Science 274, 271–283.
| Co-overexpression of AVP1 and PP2A-C5 in Arabidopsis makes plants tolerant to multiple abiotic stresses.Crossref | GoogleScholarGoogle Scholar |
Suzuki N, Bassil E, Hamilton JS, Inupakutika MA, Zandalinas SI, Tripathy D, et al. (2016) ABA is required for plant acclimation to a combination of salt and heat stress. PLoS One 11, e0147625
| ABA is required for plant acclimation to a combination of salt and heat stress.Crossref | GoogleScholarGoogle Scholar |
Takahashi I, Kojima S, Sakaguchi N, Umeda-Hara C, Umeda M (2010) Two Arabidopsis cyclin A3s possess G1 cyclin-like features. Plant Cell Reports 29, 307–315.
| Two Arabidopsis cyclin A3s possess G1 cyclin-like features.Crossref | GoogleScholarGoogle Scholar |
Takatsuka H, Ohno R, Umeda M (2009) The Arabidopsis cyclin-dependent kinase-activating kinase CDKF;1 is a major regulator of cell proliferation and cell expansion but is dispensable for CDKA activation. The Plant Journal 59, 475–487.
| The Arabidopsis cyclin-dependent kinase-activating kinase CDKF;1 is a major regulator of cell proliferation and cell expansion but is dispensable for CDKA activation.Crossref | GoogleScholarGoogle Scholar |
Thabet SG, Moursi YS, Sallam A, Karam MA, Alqudah AM (2021) 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 |
Turan S, Cornish K, Kumar S (2012) Salinity tolerance in plants: breeding and genetic engineering. Australian Journal of Crop Science 6, 1337–1348.
Uchida A, Jagendorf AT, Hibino T, Takabe T, Takabe T (2002) Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Science 163, 515–523.
| Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice.Crossref | GoogleScholarGoogle Scholar |
Wijewardene I, Mishra N, Sun L, Smith J, Zhu X, Payton P, et al. (2020) Improving drought-, salinity-, and heat-tolerance in transgenic plants by co-overexpressing Arabidopsis vacuolar pyrophosphatase gene AVP1 and Larrea Rubisco activase gene RCA. Plant Science 296, 110499
| Improving drought-, salinity-, and heat-tolerance in transgenic plants by co-overexpressing Arabidopsis vacuolar pyrophosphatase gene AVP1 and Larrea Rubisco activase gene RCA.Crossref | GoogleScholarGoogle Scholar |
Witcombe JR, Hollington PA, Howarth CJ, Reader S, Steele KA (2008) Breeding for abiotic stresses for sustainable agriculture. Philosophical Transactions of the Royal Society B: Biological Sciences 363, 703–716.
| Breeding for abiotic stresses for sustainable agriculture.Crossref | GoogleScholarGoogle Scholar |
Xu D, Leister D, Kleine T (2017) Arabidopsis thaliana mTERF10 and mTERF11, but not mTERF12, are involved in the response to salt stress. Frontiers in Plant Science 8, 1213
| Arabidopsis thaliana mTERF10 and mTERF11, but not mTERF12, are involved in the response to salt stress.Crossref | GoogleScholarGoogle Scholar |
Zhang X, Wang X, Zhuang L, Gao Y, Huang B (2019) Abscisic acid mediation of drought priming-enhanced heat tolerance in tall fescue (Festuca arundinacea) and Arabidopsis. Physiologia Plantarum 167, 488–501.
| Abscisic acid mediation of drought priming-enhanced heat tolerance in tall fescue (Festuca arundinacea) and Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Zhao F-Y, Zhang X-J, Li P-H, Zhao Y-X, Zhang H (2006) Co-expression of the Suaeda salsa SsNHX1 and Arabidopsis AVP1 confer greater salt tolerance to transgenic rice than the single SsNHX1. Molecular Breeding 17, 341–353.
| Co-expression of the Suaeda salsa SsNHX1 and Arabidopsis AVP1 confer greater salt tolerance to transgenic rice than the single SsNHX1.Crossref | GoogleScholarGoogle Scholar |
Zhu J-K (2003) Regulation of ion homeostasis under salt stress. Current Opinion in Plant Biology 6, 441–445.
| Regulation of ion homeostasis under salt stress.Crossref | GoogleScholarGoogle Scholar |