Multi-omics atlas of combinatorial abiotic stress responses in wheat.
Ethylene-responsive element binding factor-associated amphiphilic repression motif
RNAseq
abiotic stress
metabolome
multi-environmental stresses
multi-omics
physiological traits
transcription factors
wheat (Triticum aestivum L.)
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
revised:
10
05
2023
received:
01
05
2022
accepted:
26
05
2023
medline:
10
11
2023
pubmed:
30
5
2023
entrez:
30
5
2023
Statut:
ppublish
Résumé
Field-grown crops rarely experience growth conditions in which yield can be maximized. Environmental stresses occur in combination, with advancements in crop tolerance further complicated by its polygenic nature. Strategic targeting of causal genes is required to meet future crop production needs. Here, we employed a systems biology approach in wheat (Triticum aestivum L.) to investigate physio-metabolic adjustments and transcriptome reprogramming involved in acclimations to heat, drought, salinity and all combinations therein. A significant shift in magnitude and complexity of plant response was evident across stress scenarios based on the agronomic losses, increased proline concentrations and 8.7-fold increase in unique differentially expressed transcripts (DETs) observed under the triple stress condition. Transcriptome data from all stress treatments were assembled into an online, open access eFP browser for visualizing gene expression during abiotic stress. Weighted gene co-expression network analysis revealed 152 hub genes of which 32% contained the ethylene-responsive element binding factor-associated amphiphilic repression (EAR) transcriptional repression motif. Cross-referencing against the 31 DETs common to all stress treatments isolated TaWRKY33 as a leading candidate for greater plant tolerance to combinatorial stresses. Integration of our findings with available literature on gene functional characterization allowed us to further suggest flexible gene combinations for future adaptive gene stacking in wheat. Our approach demonstrates the strength of robust multi-omics-based data resources for gene discovery in complex environmental conditions. Accessibility of such datasets will promote cross-validation of candidate genes across studies and aid in accelerating causal gene validation for crop resiliency.
Substances chimiques
Plant Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1118-1135Subventions
Organisme : Agriculture and Agri-Food Canada
ID : N/A
Organisme : National Research Council Canada through the Canadian Wheat Improvement Flagship Program
Organisme : Natural Sciences and Engineering Research Council of Canada
Informations de copyright
© 2023 His Majesty the King in Right of Canada and The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd. Reproduced with the permission of the Minister of Agriculture and Agri Food Canada.
Références
Abhinandan, K., Skori, L., Stanic, M., Hickerson, N.M.N., Jamshed, M. & Samuel, M.A. (2018) Abiotic stress signaling in wheat - an inclusive overview of hormonal interactions during abiotic stress responses in wheat. Frontiers in Plant Science, 9, 734. Available from: https://doi.org/10.3389/fpls.2018.00734
Acevedo, E., Silva, P. & Silva, H. (2002) Wheat growth and physiology. In: Bread wheat: Improvement and production. Rome, Italy: Food and Agriculture Organization of the United Nations. Plant Production and protection series No. 30, p. 567. Available from: http://www.fao.org/3/y4011e06.htm#bm06
Agarwal, P., Baranwal, V.K. & Khurana, P. (2019) Genome-wide analysis of bZIP transcription factors in wheat and functional characterization of a TabZIP under abiotic stress. Scientific Reports, 9, 4608. Available from: https://doi.org/10.1038/s41598-019-40659-7
Ashe, P., Shaterian, H., Akhov, L., Kulkarni, M. & Selvaraj, G. (2017) Contrasting root and photosynthesis traits in a large-acreage Canadian durum variety and its distant parent of algerian origin for assembling drought/heat tolerance attributes. Frontiers in Chemistry, 5, 121. Available from: https://doi.org/10.3389/fchem.2017.00121
Ashraf, M. (2010) Inducing drought tolerance in plants: recent advances. Biotechnology Advances, 28(1), 169-183. Available from: https://doi.org/10.1016/j.biotechadv.2009.11.005
Asseng, S., Ewert, F., Martre, P., Rötter, R.P., Lobell, D.B., Cammarano, D. et al. (2015) Rising temperatures reduce global wheat production. Nature Climate Change, 5, 143-147. Available from: https://doi.org/10.1038/nclimate2470
Batool, S., Uslu, V.V., Rajab, H., Ahmad, N., Waadt, R., Geiger, D. et al. (2018) Sulfate is incorporated into cysteine to trigger ABA production and stomatal closure. The Plant Cell, 30(12), 2973-2987. Available from: https://doi.org/10.1105/tpc.18.00612
Bheemanahalli, R., Sunoj, V.S.J., Saripalli, G., Prasad, P.V.V., Balyan, H.S., Gupta, P.K. et al. (2019) Quantifying the impact of heat stress on pollen germination, seed set, and grain filling in spring wheat. Crop Science, 59(2), 684-696. Available from: https://doi.org/10.2135/cropsci2018.05.0292
Biswal, A.K. & Kohli, A. (2013) Cereal flag leaf adaptations for grain yield under drought: knowledge status and gaps. Molecular Breeding, 31, 749-766. Available from: https://doi.org/10.1007/s11032-013-9847-7
Blake, N.K., Lanning, S.P., Martin, J.M., Sherman, J.D. & Talbert, L.E. (2007) Relationship of flag leaf characteristics to economically important traits in two spring wheat crosses. Crop Science, 47, 491-494. Available from: https://doi.org/10.2135/cropsci2006.05.0286
Bolger, A.M., Lohse, M. & Usadel, B. (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 30(15), 2114-2120. Available from: https://doi.org/10.1093/bioinformatics/btu170
Cai, H., Tian, S., Liu, C. & Dong, H. (2011) Identification of a MYB3R gene involved in drought, salt and cold stress in wheat (Triticum aestivum L.). Gene, 485(2), 146-152. Available from: https://doi.org/10.1016/j.gene.2011.06.026
Calabrese, E.J. & Mattson, M.P. (2017) How does hormesis impact biology, toxicology, and medicine? NPJ Aging and Mechanisms of Disease, 3, 1-8. Available from: https://doi.org/10.1038/s41514-017-0013-z
Cardoso, L., Freire, F. & Daloso, D. (2022) Plant metabolic networks under stress: a multi-species/stress condition meta-analysis. Journal of Soil Science and Plant Nutrition, 23, 4-21. Available from: https://doi.org/10.1007/s42729-022-01032-2
Davenport, R.J. & Tester, M. (2000) A weakly voltage-dependent, nonselective cation channel mediates toxic sodium influx in wheat. Plant Physiology, 122, 823-834. Available from: https://doi.org/10.1104/pp.122.3.823
DePauw, R.M., Knox, R.E., Clarke, F.R., Clarke, J.M. & McCaig, T.N. (2011) Stettler hard red spring wheat. Canadian Journal of Plant Science, 89, 945-951. Available from: https://doi.org/10.4141/CJPS08227
Dong, C.-J. & Liu, J.-Y. (2010) The Arabidopsis EAR-motif-containing protein RAP2.1 functions as an active transcriptional repressor to keep stress responses under tight control. BMC Plant Biology, 10, 47. Available from: https://doi.org/10.1186/1471-2229-10-47
Dong, W., Wang, M., Xu, F., Quan, T., Peng, K., Xiao, L. et al. (2013) Wheat oxophytodienoate reductase gene TaOPR1 confers salinity tolerance via enhancement of abscisic acid signaling and reactive oxygen species scavenging. Plant Physiology, 161, 1217-1228. Available from: https://doi.org/10.1104/pp.112.211854
Elferjani, R. & Soolanayakanahally, S. (2018) Canola responses to drought, heat and combined stress: shared and specific effects on carbon assimilation, seed yield, and oil composition. Frontiers in Plant Science, 9, 1124. Available from: https://doi.org/10.3389/fpls.2018.01224
Farooq, M., Bramley, H., Palta, J.A. & Siddique, K.H.M. (2011) Heat stress in wheat during reproductive and grain-filling phases. Critical Reviews in Plant Sciences, 30, 491-507. Available from: https://doi.org/10.1080/07352689.2011.615687
Farooq, M., Nawaz, A., Chaudhry, M.M., Indrasti, R. & Rehman, A. (2017) Improving resistance against terminal drought in bread wheat by exogenous application of proline and gamma-aminobutyric acid. Journal of Agronomy and Crop Science, 203, 464-472. Available from: https://doi.org/10.1111/jac.12222
Farquhar, G., Ehleringer, J. & Hubick, K. (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Biology, 40, 503-537.
Fucile, G., Di Biase, D., Nahal, H. et al. (2011) ePlant and the 3D data display initiative: integrative systems biology on the world wide web. PLoS One, 6, e15237. Available from: https://doi.org/10.1371/journal.pone.0015237
Gao, Z., He, X., Zhao, B., Zhou, C., Liang, Y., Ge, R. et al. (2010) Overexpressing a putative aquaporin gene from wheat, TaNIP, enhances salt tolerance in transgenic Arabidopsis. Plant and Cell Physiology, 51(5), 767-775. Available from: https://doi.org/10.1093/pcp/pcq036
Genc, Y., Mcdonald, G.K. & Tester, M. (2007) Reassessment of tissue Na+ concentration as a criterion for salinity tolerance in bread wheat. Plant, Cell & Environment, 30(11), 1486-1498. Available from: https://doi.org/10.1111/j.1365-3040.2007.01726.x
Hayat, S., Hayat, Q., Alyemeni, M.N., Wani, A.S., Pichtel, J. & Ahmad, A. (2012) Role of proline under changing environments. Plant Signaling & Behavior, 7(11), 1456-1466. Available from: https://doi.org/10.4161/psb.21949
He, G.H., Xu, J.Y., Wang, Y.X., Liu, J.M., Li, P.S., Chen, M. et al. (2016) Drought-responsive WRKY transcription factor genes TaWRKY1 and TaWRKY33 from wheat confer drought and/or heat resistance in Arabidopsis. BMC Plant Biology, 16, 116. Available from: https://doi.org/10.1186/s12870-016-0806-4
Hoagland, D.R. & Arnon, D.J. (1950) The water culture method for growing plants without soil. California Agriculture Experimental Station Circular No., 347, 1-32.
Hothorn, T., Bretz, F. & Westfall, P. (2008) Simultaneous inference in general parametric models. Biometrical Journal, 50(3), 346-363. Available from: https://doi.org/10.1002/bimj.200810425
Inaba, K., Fujiwara, T., Hayashi, H., Chino, M., Komeda, Y. & Naito, S. (1994) Isolation of an Arabidopsis thaliana mutant, mto1 that overaccumulates soluble methionine (temporal and spatial patterns of soluble methionine accumulation). Plant Physiology, 104(3), 881-887. Available from: https://doi.org/10.1104/pp.104.3.881
IWGSC, Appels, R., Eversole, K., Stein, N., Feuillet, C., Keller, B. et al. (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science, 361, eaar7191. Available from: https://doi.org/10.1126/science.aar7191
Joo, J., Choi, H.J., Lee, Y.H., Kim, Y.-K. & Song, S.I. (2013) A transcriptional repressor of the ERF family confers drought tolerance to rice and regulates genes preferentially located on chromosome 11. Planta, 238(1), 155-170. Available from: https://doi.org/10.1007/s00425-013-1880-6
Kagale, S., Links, M.G. & Rozwadowski, K. (2010) Genome-wide analysis of ethylene-responsive element binding factor-associated amphiphilic repression motif-containing transcriptional regulators in Arabidopsis. Plant Physiology, 152(3), 1109-1134. Available from: https://doi.org/10.1104/pp.109.151704
Kagale, S. & Rozwadowski, K. (2010) Small yet effective: the ethylene responsive element binding factor-associated amphiphilic repression (EAR) motif. Plant Signaling & Behavior, 5(6), 691-694. Available from: https://doi.org/10.4161/psb.5.6.11576
Kazan, K. (2006) Negative regulation of defence and stress genes by EAR-motif-containing repressors. Trends in Plant Science, 11(3), 109-112. Available from: https://doi.org/10.1016/j.tplants.2006.01.004
Khan, M.I., Iqbal, N., Masood, A., Per, T.S. & Khan, N.A. (2013) Salicylic acid alleviates adverse effects of heat stress on photosynthesis through changes in proline production and ethylene formation. Plant Signaling & Behavior, 8(11), e26374. Available from: https://doi.org/10.4161/psb.26374
Khatkar, D. & Kuhad, M.S. (2000) Short-term salinity induced changes in two wheat cultivars at different growth stages. Biologia Plantarum, 43(4), 629-632. Available from: https://doi.org/10.1023/A:1002868519779
Kumar, R., Goswami, S., Singh, K., Dubey, K. et al. (2018) Characterization of novel heat-responsive transcription factor (TaHSFA6e) gene involved in regulation of heat shock proteins (HSPs) - a key member of heat stress-tolerance network of wheat. Journal of Biotechnology, 279, 1-12. Available from: https://doi.org/10.1016/j.jbiotec.2018.05.008
Kumar, R., Masthigowda, M.H., Kaur, A., Bhusal, N., Pandey, A., Kumar, S. et al. (2020) Identification and characterization of multiple abiotic stress tolerance genes in wheat. Molecular Biology Reports, 47, 8629-8643. Available from: https://doi.org/10.1007/s11033-020-05906-5
Kumar, S., Beena, A.S., Awana, M. & Singh, A. (2017) Physiological, biochemical, epigenetic and molecular analyses of wheat (Triticum aestivum) genotypes with contrasting salt tolerance. Frontiers in Plant Science, 8, 1151. Available from: https://doi.org/10.3389/fpls.2017.01151
Langfelder, P. & Horvath, S. (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics, 9(1), 559. Available from: https://doi.org/10.1186/1471-2105-9-559
Lenth, R., Singmann, H., Love, J., Buerkner, P. & Herve, M. (2020) Emmeans: estimated marginal means. R package version 1.4. 4. The American Statistician, 34(4), 216-221.
Li, B. & Dewey, C.N. (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics, 12(1), 323. Available from: https://doi.org/10.1186/1471-2105-12-323
Li, B., Liu, D., Li, Q., Mao, X., Li, A., Wang, J. et al. (2016) Overexpression of wheat gene TaMOR improves root system architecture and grain yield in Oryza sativa. Journal of Experimental Botany, 67(14), 4155-4167. Available from: https://doi.org/10.1093/jxb/erw193
Li, G.Z., Li, H.X., Xu, M.J., Wang, P.F., Xiao, X.H. & Kang, G.Z. (2020) Functional characterization and regulatory mechanism of wheat CPK34 kinase in response to drought stress. BMC Genomics, 21, 577. Available from: https://doi.org/10.1186/s12864-020-06985-1
Li, Q., Wang, W., Wang, W., Zhang, G., Liu, Y., Wang, Y. et al. (2018) Wheat F-box protein gene TaFBA1 is involved in plant tolerance to heat stress. Frontiers in Plant Science, 9, 521. Available from: https://doi.org/10.3389/fpls.2018.00521
Li, Y. & Wei, K. (2020) Comparative functional genomics analysis of cytochrome P450 gene superfamily in wheat and maize. BMC Plant Biology, 20(1), 93. Available from: https://doi.org/10.1186/s12870-020-2288-7
Li, Z., Yu, J., Peng, Y. & Huang, B. (2016) Metabolic pathways regulated by abscisic acid, salicylic acid and γ-aminobutyric acid in association with improved drought tolerance in creeping bentgrass (Agrostis stolonifera). Physiologia Plantarum, 159(1), 42-58. Available from: https://doi.org/10.1111/ppl.12483
Liu, D., Liu, Y., Rao, J., Wang, G., Li, H., Ge, F. et al. (2013) Overexpression of the glutathione S-transferase gene from Pyrus pyrifolia fruit improves tolerance to abiotic stress in transgenic tobacco plants. Molecular Biology, 47(4), 515-523. Available from: https://doi.org/10.1134/S0026893313040109
Liu, Y., Mauve, C., Lamothe-Sibold, M., Guérard, F., Glab, N., Hodges, M. et al. (2019) Photorespiratory serine hydroxymethyltransferase 1 activity impacts abiotic stress tolerance and stomatal closure. Plant, Cell & Environment, 42(9), 2567-2583. Available from: https://doi.org/10.1111/pce.13595
Love, M.I., Huber, W. & Anders, S. (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15(12), 550. Available from: https://doi.org/10.1186/s13059-014-0550-8
Ma, X., Zhu, X., Li, C., Song, Y., Zhang, W., Xia, G. et al. (2015) Overexpression of wheat NF-YA10 gene regulates the salinity stress response in Arabidopsis thaliana. Plant Physiology and Biochemistry, 86, 34-43. Available from: https://doi.org/10.1016/j.plaphy.2014.11.011
Mustafa, G., Akhtar, M.S. & Abdullah, R. (2019) Global Concern for Salinity on Various Agro-Ecosystems. In: Akhtar, M.S. (Ed.) Salt Stress, Microbes, and Plant Interactions: Causes and Solution, Vol. 1. Singapore: Springer, pp. 1-19. Available from: https://doi.org/10.1007/978-981-13-8801-9_1
Nanjo, T., Fujita, M., Seki, M., Kato, T., Tabata, S. & Shinozaki, K. (2003) Toxicity of free proline revealed in an Arabidopsis T-DNA-tagged mutant deficient in proline dehydrogenase. Plant and Cell Physiology 15, 44, 541-548.
Niu, X., Luo, T., Zhao, H., Su, Y., Ji, W. & Li, H. (2020) Identification of wheat DREB genes and functional characterization of TaDREB3 in response to abiotic stresses. Gene, 740, 144514. Available from: https://doi.org/10.1016/j.gene.2020.144514
Preston, J., Tatematsu, K., Kanno, Y., Hobo, T., Kimura, M., Jikumaru, Y. et al. (2009) Temporal expression patterns of hormone metabolism genes during imbibition of Arabidopsis thaliana seeds: a comparative study on dormant and non-dormant accessions. Plant Cell & Physiology, 50, 1786-1800.
Qin, Y., Tian, Y. & Liu, X. (2015) A wheat salinity-induced WRKY transcription factor TaWRKY93 confers multiple abiotic stress tolerance in Arabidopsis thaliana. Biochemical and Biophysical Research Communications, 464(2), 428-433. Available from: https://doi.org/10.1016/j.bbrc.2015.06.128
R Core Team. (2019). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/
Ramirez-Gonzalez, R.H., Borrill, P., Lang, D., Harrington, S.A., Brinton, J., Venturini, L. et al. (2018) The transcriptional landscape of polyploid wheat. Science, 361, eaar6089. Available from: https://doi.org/10.1126/science.aar6089
Shaar-Moshe, L., Blumwald, E. & Peleg, Z. (2017) Unique physiological and transcriptional shifts under combinations of salinity, drought, and heat. Plant Physiology, 174(1), 421-434. Available from: https://doi.org/10.1104/pp.17.00030
Shaar-Moshe, L., Hayouka, R., Roessner, U. & Peleg, Z. (2019) Phenotypic and metabolic plasticity shapes life-history strategies under combinations of abiotic stresses. Plant Direct, 3(1), e00113. Available from: https://doi.org/10.1002/pld3.113
Shailani, A., Joshi, R., Singla-Pareek, S.L. & Pareek, A. (2020) Stacking for future: pyramiding genes to improve drought and salinity tolerance in rice. Physiologia Plantarum, 172, 1352-1362. Available from: https://doi.org/10.1111/ppl.13270
Spiertz, J.H.J., Hamer, R.J., Xu, H., Primo-Martin, C., Don, C. & van der Putten, P.E.L. (2006) Heat stress in wheat (Triticum aestivum L.): effects on grain growth and quality traits. European Journal of Agronomy, 25, 89-95. Available from: https://doi.org/10.1016/j.eja.2006.04.012
Suraj, H., SharathKumar, M. & van Kan, J. (2022) Too hot to defend: a tale of salicylic acid. Trends in Plant Science, 28, 4-6. Available from: https://doi.org/10.1016/j.tplants.2022.10.001
Thirsty work. (2021) Nature Plants, 7, 857. Available from: https://doi.org/10.1038/s41477-021-00978-y
Toufighi, K., Brady, S.M., Austin, R., Ly, E. & Provart, N.J. (2005) The botany array resource: e-northerns, expression angling, and promoter analyses. Plant Journal, 43, 153-163. Available from: https://doi.org/10.1111/j.1365-313X.2005.02437.x
Usadel, B., Poree, F., Nagel, A., Lohse, M., Czedik-Eysenberg, A. & Stitt, M. (2009) A guide to using MapMan to visualize and compare omics data in plants: a case study in the crop species, maize. Plant, Cell & Environment, 32(9), 1211-1229. Available from: https://doi.org/10.1111/j.1365-3040.2009.01978.x
Vendruscolo, E.C.G., Schuster, I., Pileggi, M., Scapim, C.A., Molinari, H.B.C., Marur, C.J. et al. (2007) Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat. Journal of Plant Physiology, 164(10), 1367-1376. Available from: https://doi.org/10.1016/j.jplph.2007.05.001
Waese, J., Fan, J., Pasha, A., Yu, H., Fucile, G., Shi, R. et al. (2017) ePlant: visualizing and exploring multiple levels of data for hypothesis generation in plant biology. Plant Cell, 29, 1806-1821. Available from: https://doi.org/10.1105/tpc.17.00073
Walkowiak, S., Gao, L., Monat, C., Haberer, G., Kassa, M.T., Brinton, J. et al. (2020) Multiple wheat genomes reveal global variation in modern breeding. Nature, 588, 277-283. Available from: https://doi.org/10.1038/s41586-020-2961-x
Xu, L., Wang, D., Liu, S., Fang, Z., Su, S., Guo, C. et al. (2020) Comprehensive atlas of wheat (Triticum aestivum L.) AUXIN RESPONSE FACTOR expression during male reproductive development and abiotic stress. Frontiers in Plant Science, 11, 586144. Available from: https://doi.org/10.3389/fpls.2020.586144
Xu, Z.S., Xia, L.Q., Chen, M., Cheng, X.G., Zhang, R.Y., Li, L.C. et al. (2007) Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant Molecular Biology, 65, 719-732. Available from: https://doi.org/10.1007/s11103-007-9237-9
Yang, J. & Zhang, J. (2006) Grain filling of cereals under soil drying. New Phytologist, 169(2), 223-236. Available from: https://doi.org/10.1111/j.1469-8137.2005.01597.x
Yang, M., Zhao, Y., Shi, S., Du, X., Gu, J. & Xiao, K. (2017) Wheat nuclear factor Y (NF-Y) B subfamily gene TaNF-YB3;l confers critical drought tolerance through modulation of the ABA-associated signaling pathway. Plant Cell, Tissue and Organ Culture, 128, 97-111. Available from: https://doi.org/10.1007/s11240-016-1088-0
Yang, T., Yao, S., Hao, L., Zhao, Y., Lu, W. & Xiao, K. (2016) Wheat bHLH-type transcription factor gene TabHLH1 is crucial in mediating osmotic stresses tolerance through modulating largely the ABA-associated pathway. Plant Cell Reports, 35, 2309-2323. Available from: https://doi.org/10.1007/s00299-016-2036-5
Yang, X., Zhu, X., Wei, J., Li, W., Wang, H., Xu, Y. et al. (2022) Primary root response to combined drought and heat stress is regulated via salicylic acid metabolism in maize. BMC Plant Biology, 22, 417. Available from: https://doi.org/10.1186/s12870-022-03805-4
Yu, Y., Ni, Z., Chen, Q. & Qu, Y. (2017) The wheat salinity-induced R2R3-MYB transcription factor TaSIM confers salt stress tolerance in Arabidopsis thaliana. Biochemical and Biophysical Research Communications, 491(3), 642-648. Available from: https://doi.org/10.1016/j.bbrc.2017.07.150
Zampieri, M., Ceglar, A., Dentener, F. & Toreti, A. (2017) Wheat yield loss attributable to heat waves, drought and water excess at the global, national and subnational scales. Environmental Research Letters, 12(6), 064008. Available from: https://doi.org/10.1088/1748-9326/aa723b
Zandalinas, S. & Mittler, R. (2022) Plant responses to multifactorial stress combination. New Phytologist, 234(4), 1161-1167. Available from: https://doi.org/10.1111/nph.18087
Zandalinas, S., Segupta, S., Fritschi, F., Azad, R., Nechushtai, R. & Mittler, R. (2021) The impact of multifactorial stress combination on plant growth and survival. New Phytologist, 230, 1034-1048. Available from: https://doi.org/10.1002/pld3.113
Zandalinas, S.I., Fritschi, F.B. & Mittler, R. (2020) Signal transduction networks during stress combination. Journal of Experimental Botany, 71(5), 1734-1741. Available from: https://doi.org/10.1093/jxb/erz486
Zhang, L., Zhang, L., Xia, C., Zhao, G., Jia, J. & Kong, X. (2016) The novel wheat transcription factor TaNAC47 enhances multiple abiotic stress tolerances in transgenic plants. Frontiers in Plant Science, 6, 1174. Available from: https://doi.org/10.3389/fpls.2015.01174
Zhang, L., Zhao, G., Xia, C., Jia, J., Liu, X. & Kong, X. (2012) Overexpression of a wheat MYB transcription factor gene, TaMYB56-B, enhances tolerances to freezing and salt stresses in transgenic Arabidopsis. Gene, 505(1), 100-107. Available from: https://doi.org/10.1016/j.gene.2012.05.033
Zhao, H., Dai, T., Jing, Q., Jiang, D. & Cao, W. (2007) Leaf senescence and grain filling affected by post-anthesis high temperatures in two different wheat cultivars. Plant Growth Regulation, 51, 149-158. Available from: https://doi.org/10.1007/s10725-006-9157-8
Zheng, J., Yang, Z., Madgwick, P.J., Carmo-Silva, E., Parry, M.A.J. & Hu, Y.-G. (2015) TaER expression is associated with transpiration efficiency traits and yield in bread wheat. PLoS One, 10(6), e0128415. Available from: https://doi.org/10.1371/journal.pone.0128415
Zhou, Y., Zhai, H., He, S., Zhu, H., Gao, S., Xing, S. et al. (2020) The sweetpotato BTB-TAZ protein gene, IbBT4, enhances drought tolerance in transgenic Arabidopsis. Frontiers in Plant Science, 11, 877. Available from: https://doi.org/10.3389/fpls.2020.00877
Zhou, Y., Zhou, B., Pache, L., Chang, M., Khodabakhshi, A.H., Tanaseichuk, O. et al. (2019) Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nature Communications, 10(1), 1523. Available from: https://doi.org/10.1038/s41467-019-09234-6