BACKGROUND: Drought is a major environmental stress that affects crop productivity worldwide. Although previous research demonstrated links between strigolactones (SLs) and drought, here we used barley (Hordeum vulgare) SL-insensitive mutant hvd14 (dwarf14) to scrutinize the SL-dependent mechanisms associated with water deficit response. RESULTS: We have employed a combination of transcriptomics, proteomics, phytohormonomics analyses, and physiological data to unravel differences between wild-type and hvd14 plants under drought. Our research revealed that drought sensitivity of hvd14 is related to weaker induction of abscisic acid-responsive genes/proteins, lower jasmonic acid content, higher reactive oxygen species content, and lower wax biosynthetic and deposition mechanisms than wild-type plants. In addition, we identified a set of transcription factors (TFs) that are exclusively drought-induced in the wild-type barley. CONCLUSIONS: Critically, we resolved a comprehensive series of interactions between the drought-induced barley transcriptome and proteome responses, allowing us to understand the profound effects of SLs in alleviating water-limiting conditions. Several new avenues have opened for developing barley more resilient to drought through the information provided. Moreover, our study contributes to a better understanding of the complex interplay between genes, proteins, and hormones in response to drought, and underscores the importance of a multidisciplinary approach to studying plant stress response mechanisms.

Department of Biological Sciences University of Alberta 11455 Saskatchewan Drive Edmonton AB T6G 2E9 Canada

Institute of Biology Biotechnology and Environmental Protection Faculty of Natural Sciences University of Silesia in Katowice Jagiellonska 28 40 032 Katowice Poland

Laboratory of Growth Regulators Faculty of Science Palacký University and Institute of Experimental Botany The Czech Academy of Sciences Olomouc Czech Republic

Leibniz Institute of Plant Genetics and Crop Plant Research Gatersleben Seeland 06466 Gatersleben OT Germany

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Gupta A, Rico-Medina A, Caño-Delgado AI. The physiology of plant responses to drought. Science. 2020;368:266–269. PubMed

Waters MT, Gutjahr C, Bennett T, Nelson DC. Strigolactone Signaling and Evolution. Annu Rev Plant Biol. 2017;68:291–322. PubMed

Hamiaux C, Drummond RSM, Janssen BJ, Ledger SE, Cooney JM, Newcomb RD, et al. DAD2 is an α/β hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr Biol. 2012;22:2032–2036. PubMed

Stirnberg P, van de Sande K, Leyser HMO. MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development. 2002;129:1131–1141. PubMed

Yao R, Ming Z, Yan L, Li S, Wang F, Ma S, et al. DWARF14 is a non-canonical hormone receptor for strigolactone. Nature. 2016;536:469–473. PubMed

Soundappan I, Bennett T, Morffy N, Liang Y, Stanga JP, Abbas A, et al. SMAX1-LIKE/D53 Family Members Enable Distinct MAX2-Dependent Responses to Strigolactones and Karrikins in Arabidopsis. Plant Cell. 2015;27:3143–3159. PubMed PMC

Wang L, Wang B, Yu H, Guo H, Lin T, Kou L, et al. Transcriptional regulation of strigolactone signalling in Arabidopsis. Nature. 2020;583:277–281. PubMed

Bu Q, Lv T, Shen H, Luong P, Wang J, Wang Z, et al. Regulation of drought tolerance by the F-box protein MAX2 in Arabidopsis. Plant Physiol. 2014;164:424–439. PubMed PMC

Ha CV, Leyva-González MA, Osakabe Y, Tran UT, Nishiyama R, Watanabe Y, et al. Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc Natl Acad Sci USA. 2014;111:851–856. PubMed PMC

Sedaghat M, Tahmasebi-Sarvestani Z, Emam Y, Mokhtassi-Bidgoli A. Physiological and antioxidant responses of winter wheat cultivars to strigolactone and salicylic acid in drought. Plant Physiol Biochem. 2017;119:59–69. PubMed

Min Z, Li R, Chen L, Zhang Y, Li Z, Liu M, et al. Alleviation of drought stress in grapevine by foliar-applied strigolactones. Plant Physiol Biochem. 2019;135:99–110. PubMed

Waters MT, Nelson DC, Scaffidi A, Flematti GR, Sun YK, Dixon KW, et al. Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development. 2012;139:1285–1295. PubMed

Wang Y, Sun S, Zhu W, Jia K, Yang H, Wang X. Strigolactone/MAX2-Induced Degradation of Brassinosteroid Transcriptional Effector BES1 Regulates Shoot Branching. Dev Cell. 2013;27:681–688. PubMed

Scaffidi A, Waters MT, Sun YK, Skelton BW, Dixon KW, Ghisalberti EL, et al. Strigolactone Hormones and Their Stereoisomers Signal through Two Related Receptor Proteins to Induce Different Physiological Responses in Arabidopsis. Plant Physiol. 2014;165:1221–1232. PubMed PMC

Li S, Chen L, Li Y, Yao R, Wang F, Yang M, et al. Effect of GR24 Stereoisomers on Plant Development in Arabidopsis. Mol Plant. 2016;9:1432–1435. PubMed

Haider I, Andreo-Jimenez B, Bruno M, Bimbo A, Floková K, Abuauf H, et al. The interaction of strigolactones with abscisic acid during the drought response in rice. J Exp Bot. 2018;69:2403–2414. PubMed

Liu J, He H, Vitali M, Visentin I, Charnikhova T, Haider I, et al. Osmotic stress represses strigolactone biosynthesis in Lotus japonicus roots: exploring the interaction between strigolactones and ABA under abiotic stress. Planta. 2015;241:1435–1451. PubMed

Visentin I, Vitali M, Ferrero M, Zhang Y, Ruyter-Spira C, Novák O, et al. Low levels of strigolactones in roots as a component of the systemic signal of drought stress in tomato. New Phytol. 2016;212:954–963. PubMed

Marzec M, Daszkowska-Golec A, Collin A, Melzer M, Eggert K, Szarejko I. Barley strigolactone signaling mutant hvd14.d reveals the role of strigolactones in ABA-dependent response to drought. Plant Cell Environ. 2020. 10.1111/pce.13815. PubMed

Li W, Nguyen KH, Chu HD, Watanabe Y, Osakabe Y, Sato M, et al. Comparative functional analyses of DWARF14 and KARRIKIN INSENSITIVE 2 in drought adaptation of Arabidopsis thaliana. Plant J. 2020;103:111–127. PubMed

Visentin I, Pagliarani C, Deva E, Caracci A, Turečková V, Novák O, et al. A novel strigolactone-miR156 module controls stomatal behaviour during drought recovery. Plant Cell Environ. 2020;43:1613–1624. PubMed

Lv S, Zhang Y, Li C, Liu Z, Yang N, Pan L, et al. Strigolactone-triggered stomatal closure requires hydrogen peroxide synthesis and nitric oxide production in an abscisic acid-independent manner. New Phytol. 2018;217:290–304. PubMed

Marzec M, Gruszka D, Tylec P, Szarejko I. Identification and functional analysis of the HvD14 gene involved in strigolactone signaling in Hordeum vulgare. Physiol Plant. 2016;158:341–355. PubMed

Chwialkowska K, Nowakowska U, Mroziewicz A, Szarejko I, Kwasniewski M. Water-deficiency conditions differently modulate the methylome of roots and leaves in barley ( Hordeum vulgare L.) EXBOTJ. 2016;67:1109–21. PubMed PMC

Singh RK, Prasad M. Delineating the epigenetic regulation of heat and drought response in plants. Crit Rev Biotechnol. 2021;42:1–14. PubMed

Jacobsen JV, Pearce DW, Poole AT, Pharis RP, Mander LN. Abscisic acid, phaseic acid and gibberellin contents associated with dormancy and germination in barley. Physiol Plant. 2002;115:428–441. PubMed

Stintzi A, Browse J. The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc Natl Acad Sci. 2000;97:10625–10630. PubMed PMC

De Ollas C, Arbona V, Gómez-Cadenas A, Dodd IC. Attenuated accumulation of jasmonates modifies stomatal responses to water deficit. J Exp Bot. 2018;69:2103–2116. PubMed PMC

Reichholf B, Herzog VA, Fasching N, Manzenreither RA, Sowemimo I, Ameres SL. Time-Resolved Small RNA Sequencing Unravels the Molecular Principles of MicroRNA Homeostasis. Mol Cell. 2019;75:756–768.e7. PubMed PMC

Simeoni F, Skirycz A, Simoni L, Castorina G, de Souza LP, Fernie AR, et al. The AtMYB60 transcription factor regulates stomatal opening by modulating oxylipin synthesis in guard cells. Sci Rep. 2022;12:533. PubMed PMC

Kudo T, Kiba T, Sakakibara H. Metabolism and Long-distance Translocation of Cytokinins. J Integr Plant Biol. 2010;52:53–60. PubMed

Daszkowska-Golec A, Karcz J, Plociniczak T, Sitko K, Szarejko I. Cuticular waxes—A shield of barley mutant in CBP20 (Cap-Binding Protein 20) gene when struggling with drought stress. Plant Sci. 2020;300:110593. PubMed

Richardson A, Wojciechowski T, Franke R, Schreiber L, Kerstiens G, Jarvis M, et al. Cuticular permeance in relation to wax and cutin development along the growing barley (Hordeum vulgare) leaf. Planta. 2007;225:1471–1481. PubMed

Hu P, Tirelli N. Scavenging ROS: Superoxide Dismutase/Catalase Mimetics by the Use of an Oxidation-Sensitive Nanocarrier/Enzyme Conjugate. Bioconjugate Chem. 2012;23:438–449. PubMed

Daudi A, O’Brien JA. Detection of Hydrogen Peroxide by DAB Staining in Arabidopsis Leaves. Bio Protoc. 2012;2:e263. PubMed PMC

Yoshida T, Christmann A, Yamaguchi-Shinozaki K, Grill E, Fernie AR. Revisiting the Basal Role of ABA – Roles Outside of Stress. Trends Plant Sci. 2019;24:625–635. PubMed

Yin X, Bai Y-L, Ye T, Yu M, Wu Y, Feng Y-Q. Cinnamoyl coA:NADP oxidoreductase like 1 regulates abscisic acid response by modulating phaseic acid homeostasis in Arabidopsis thaliana. J Exp Bot. 2021;73:erab474. PubMed

Ferrero M, Pagliarani C, Novák O, Ferrandino A, Cardinale F, Visentin I, et al. Exogenous strigolactone interacts with abscisic acid-mediated accumulation of anthocyanins in grapevine berries. J Exp Bot. 2018;69:2391–2401. PubMed PMC

Yoshida K, Kondoh Y, Nakano T, Bolortuya B, Kawabata S, Iwahashi F, et al. New Abscisic Acid Derivatives Revealed Adequate Regulation of Stomatal, Transcriptional, and Developmental Responses to Conquer Drought. ACS Chem Biol. 2021;16:1566–1575. PubMed

Gosti F, Beaudoin N, Serizet C, Webb AAR, Vartanian N, Giraudat J. ABI1 Protein Phosphatase 2C Is a Negative Regulator of Abscisic Acid Signaling. Plant Cell. 1999;11:1897–1909. PubMed PMC

Saez A, Apostolova N, Gonzalez-Guzman M, Gonzalez-Garcia MP, Nicolas C, Lorenzo O, et al. Gain-of-function and loss-of-function phenotypes of the protein phosphatase 2C HAB1 reveal its role as a negative regulator of abscisic acid signalling. Plant J. 2004;37:354–369. PubMed

Xiong X, James VA, Zhang H, Altpeter F. Constitutive expression of the barley HvWRKY38 transcription factor enhances drought tolerance in turf and forage grass (Paspalum notatum Flugge) Mol Breeding. 2010;25:419–432.

Janiak A, Kwasniewski M, Sowa M, Kuczyńska A, Mikołajczak K, Ogrodowicz P, et al. Insights into Barley Root Transcriptome under Mild Drought Stress with an Emphasis on Gene Expression Regulatory Mechanisms. IJMS. 2019;20:6139. PubMed PMC

Daszkowska-Golec A, Collin A, Sitko K, Janiak A, Kalaji HM, Szarejko I. Genetic and Physiological Dissection of Photosynthesis in Barley Exposed to Drought Stress. IJMS. 2019;20:6341. PubMed PMC

Korwin Krukowski P, Visentin I, Russo G, Minerdi D, Bendahmane A, Schubert A, et al. Transcriptome Analysis Points to BES1 as a Transducer of Strigolactone Effects on Drought Memory in Arabidopsis thaliana. Plant Cell Physiol. 2023;63:1873–1889. PubMed

Wang T, Huang S, Zhang A, Guo P, Liu Y, Xu C, et al. JMJ17–WRKY40 and HY5–ABI5 modules regulate the expression of ABA-responsive genes in Arabidopsis. New Phytol. 2021;230:567–584. PubMed

Aarts MG, Keijzer CJ, Stiekema WJ, Pereira A. Molecular characterization of the CER1 gene of arabidopsis involved in epicuticular wax biosynthesis and pollen fertility. Plant Cell. 1995;7:2115–2127. PubMed PMC

Trasoletti M, Visentin I, Campo E, Schubert A, Cardinale F. Strigolactones as a hormonal hub for the acclimation and priming to environmental stress in plants. Plant, Cell Environ. 2022;45:3611–3630. PubMed PMC

Qiu C-W, Zhang C, Wang N-H, Mao W, Wu F. Strigolactone GR24 improves cadmium tolerance by regulating cadmium uptake, nitric oxide signaling and antioxidant metabolism in barley (Hordeum vulgare L.) Environmental Pollution. 2021;273:116486. PubMed

Koramutla MK, Negi M, Ayele BT. Roles of Glutathione in Mediating Abscisic Acid Signaling and Its Regulation of Seed Dormancy and Drought Tolerance. Genes. 2021;12:1620. PubMed PMC

Xu Y, Burgess P, Huang B. Transcriptional regulation of hormone-synthesis and signaling pathways by overexpressing cytokinin-synthesis contributes to improved drought tolerance in creeping bentgrass. Physiol Plant. 2017;161:235–256. PubMed

Jahan MS, Nozulaidi M, Khairi M, Mat N. Light-harvesting complexes in photosystem II regulate glutathione-induced sensitivity of Arabidopsis guard cells to abscisic acid. J Plant Physiol. 2016;195:1–8. PubMed

Halder T, Upadhyaya G, Basak C, Das A, Chakraborty C, Ray S. Dehydrins Impart Protection against Oxidative Stress in Transgenic Tobacco Plants. Front Plant Sci. 2018;9:136. PubMed PMC

Labhilili M, Joudrier P, Gautier M-F. Characterization of cDNAs encoding Triticum durum dehydrins and their expression patterns in cultivars that differ in drought tolerance. Plant Sci. 1995;112:219–230.

Choi D-W, Zhu B, Close TJ. The barley (Hordeum vulgare L.) dehydrin multigene family: sequences, allele types, chromosome assignments, and expression characteristics of 11 Dhn genes of cv Dicktoo. Theor Appl Genet. 1999;98:1234–47.

Bezerra-Neto JP, de Araújo FC, Ferreira-Neto JRC, da Silva MD, Pandolfi V, Aburjaile FF, et al. Plant Aquaporins: Diversity, Evolution and Biotechnological Applications. Curr Protein Pept Sci. 2019;20:368–395. PubMed

Kurowska MM, Wiecha K, Gajek K, Szarejko I. Drought stress and re-watering affect the abundance of TIP aquaporin transcripts in barley. PLoS ONE. 2019;14:e0226423. PubMed PMC

Dai M, Zhou N, Zhang Y, Zhang Y, Ni K, Wu Z, et al. Genome-wide analysis of the SBT gene family involved in drought tolerance in cotton. Front Plant Sci. 2023;13:1097732. PubMed PMC

Cui H, Zhou G, Ruan H, Zhao J, Hasi A, Zong N. Genome-Wide Identification and Analysis of the Maize Serine Peptidase S8 Family Genes in Response to Drought at Seedling Stage. Plants. 2023;12:369. PubMed PMC

Roberts IN, Veliz CG, Criado MV, Signorini A, Simonetti E, Caputo C. Identification and expression analysis of 11 subtilase genes during natural and induced senescence of barley plants. J Plant Physiol. 2017;211:70–80. PubMed

Sebastián D, Fernando FD, Raúl DG, Gabriela GM. Overexpression of Arabidopsis aspartic protease APA1 gene confers drought tolerance. Plant Sci. 2020;292:110406. PubMed

Szurman-Zubrzycka ME, Zbieszczyk J, Marzec M, Jelonek J, Chmielewska B, Kurowska MM, et al. HorTILLUS-A Rich and Renewable Source of Induced Mutations for Forward/Reverse Genetics and Pre-breeding Programs in Barley (Hordeum vulgare L.) Frontiers  Plant Science. 2018;9:216. PubMed PMC

Leutert M, Rodríguez‐Mias RA, Fukuda NK, Villén J. R2‐P2 rapid‐robotic phosphoproteomics enables multidimensional cell signaling studies. Mol Syst Biol. 2019;15:e9021. PubMed PMC

Tyanova S, Temu T, Cox J. The MaxQuant computational platform for mass spectrometry-based shotgun proteomics. Nat Protoc. 2016;11:2301–2319. PubMed

Tyanova S, Temu T, Sinitcyn P, Carlson A, Hein MY, Geiger T, et al. The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat Methods. 2016;13:731–740. PubMed

Šimura J, Antoniadi I, Široká J, Tarkowská D, Strnad M, Ljung K, et al. Plant Hormonomics: Multiple Phytohormone Profiling by Targeted Metabolomics. Plant Physiol. 2018;177:476–489. PubMed PMC

Kolano B, Plucienniczak A, Kwasniewski M, Maluszynska J. Chromosomal localization of a novel repetitive sequence in the Chenopodium quinoa genome. J Appl Genet. 2008;49:313–320. PubMed

Braszewska-Zalewska A, Bernas T, Maluszynska J. Epigenetic chromatin modifications in Brassica genomes. Genome. 2010;53:203–210. PubMed

Braszewska-Zalewska AJ, Wolny EA, Smialek L, Hasterok R. Tissue-Specific Epigenetic Modifications in Root Apical Meristem Cells of Hordeum vulgare. PLoS ONE. 2013;8:e69204. PubMed PMC

Wolny E, Braszewska-Zalewska A, Hasterok R. Spatial distribution of epigenetic modifications in Brachypodium distachyon embryos during seed maturation and germination. PLoS ONE. 2014;9:e101246. PubMed PMC