Integrated transcriptome, proteome and metabolome analyses revealed secondary metabolites and auxiliary carbohydrate metabolism augmenting drought tolerance in rice

Abdel-Ghany, 2020, Transcriptome analysis of drought-resistant and drought-sensitive sorghum (Sorghum bicolor) genotypes in response to PEG-induced drought stress, Int. J. Mol. Sci., 21, 772, 10.3390/ijms21030772 Agrawal, 2016, Elucidation of complex nature of PEG induced drought-stress response in rice root using comparative proteomics approach, Front. Plant Sci., 7, 1466, 10.3389/fpls.2016.01466 Ahn, 2017, Transcriptional network analysis reveals drought resistance mechanisms of AP2/ERF transgenic rice, Front. Plant Sci., 8, 1044, 10.3389/fpls.2017.01044 Alqurashi, 2018, Early responses to severe drought stress in the Arabidopsis thaliana cell suspension culture proteome, Proteomes, 6, 38, 10.3390/proteomes6040038 Altuntas, 2019, Application of sucrose modulates the expressions of genes involved in proline and polyamine metabolism in maize seedlings exposed to drought, Biol. Plantarum., 63, 247, 10.32615/bp.2019.028 Anupama, 2019, Morphological, transcriptomic and proteomic responses of contrasting rice genotypes towards drought stress, Environ. Exp. Bot., 166, 10.1016/j.envexpbot.2019.06.008 Astorquiza, 2016, Diacylglycerol pyrophosphate binds and inhibits the glyceraldehyde-3-phosphate dehydrogenase in barley aleurone, Plant Physiol. Biochem., 101, 88, 10.1016/j.plaphy.2016.01.012 Baldoni, 2015, Plant MYB transcription factors: their role in drought response mechanisms, Int. J. Mol. Sci., 16, 15811, 10.3390/ijms160715811 Bandumula, 2018, Rice production in Asia: key to global food security, Proc. Natl. Acad. Sci. India B Biol. Sci., 88, 1323, 10.1007/s40011-017-0867-7 Batista-Silva, 2019, The role of amino acid metabolism during abiotic stress release, Plant Cell Environ., 42, 1630, 10.1111/pce.13518 Bisht, 2020, Bacillus amyloliquefaciens inoculation alters physiology of rice (Oryza sativa L. var. IR-36) through modulating carbohydrate metabolism to mitigate stress induced by nutrient starvation, Int. J. Biol. Macromol., 143, 937, 10.1016/j.ijbiomac.2019.09.154 Borah, 2017, Analysis of drought-responsive signalling network in two contrasting rice cultivars using transcriptome-based approach, Sci. Rep., 7, 10.1038/srep42131 Bowne, 2012, Drought responses of leaf tissues from wheat cultivars of differing drought tolerance at the metabolite level, Mol. Plant, 5, 418, 10.1093/mp/ssr114 Bross, 2017, Subcellular localization of Arabidopsis arogenate dehydratases suggests novel and non-enzymatic roles, J. Exp. Bot., 68, 1425, 10.1093/jxb/erx024 Cai, 2015, A key ABA catabolic gene, OsABA8ox3, is involved in drought stress resistance in rice, PLoS One, 10 Camisón, 2020, Changes in carbohydrates induced by drought and waterlogging in Castanea sativa, Trees (Berl.), 34, 579, 10.1007/s00468-019-01939-x Cao, 2018, Ammonium uptake and metabolism alleviate PEG-induced water stress in rice seedlings, Plant Physiol. Biochem., 132, 128, 10.1016/j.plaphy.2018.08.041 Casartelli, 2018, Exploring traditional aus-type rice for metabolites conferring drought tolerance, Rice, 11, 9, 10.1186/s12284-017-0189-7 Chang, 2017, Co-Overexpression of the constitutively active form of OsbZIP46 and ABA-activated protein kinase SAPK6 improves drought and temperature stress resistance in rice, Front. Plant Sci., 8, 1102, 10.3389/fpls.2017.01102 Chen, 2020, TBtools: an integrative toolkit developed for interactive analyses of big biological data, Mol. Plant, 13, 1194, 10.1016/j.molp.2020.06.009 Chen, 2016, Specific roles of tocopherols and tocotrienols in seed longevity and germination tolerance to abiotic stress in transgenic rice, Plant Sci., 244, 31, 10.1016/j.plantsci.2015.12.005 Chintakovid, 2017, Proteomic analysis of drought-responsive proteins in rice reveals photosynthesis-related adaptations to drought stress, Acta Physiol. Plant., 39, 240, 10.1007/s11738-017-2532-4 Cho, 2008, Integrated transcriptomics, proteomics, and metabolomics analyses to survey ozone responses in the leaves of rice seedling, J. Proteome Res., 7, 2980, 10.1021/pr800128q Cho, 2007, Phenylalanine biosynthesis in Arabidopsis thaliana. Identification and characterization of arogenate dehydratases, J. Biol. Chem., 282, 30827, 10.1074/jbc.M702662200 Chong, 2018, MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis, Nucleic Acids Res., 46, W486, 10.1093/nar/gky310 Chung, 2018, Genome-wide analyses of direct target genes of four rice NAC-domain transcription factors involved in drought tolerance, BMC Genom., 19, 40, 10.1186/s12864-017-4367-1 Cui, 2018, Comparative transcriptome analysis of seedling stage of two sorghum cultivars under salt stress, J. Plant Growth Regul., 37, 986, 10.1007/s00344-018-9796-9 Das, 2019, A unique bZIP transcription factor imparting multiple stress tolerance in Rice, Rice, 12, 58, 10.1186/s12284-019-0316-8 de Oliveira, 2020, The future of rice demand: quality beyond productivity, Springer Nature, 1-544 Ding, 2020, Highly dynamic, coordinated, and stage-specific profiles are revealed by a multi-omics integrative analysis during tuberous root development in cassava, J. Exp. Bot., 71, 7003, 10.1093/jxb/eraa369 Duan, 2012, OsMIOX, a myo-inositol oxygenase gene, improves drought tolerance through scavenging of reactive oxygen species in rice (Oryza sativa L.), Plant Sci., 196, 143, 10.1016/j.plantsci.2012.08.003 Du, 2011, Characterization of an inositol 1,3,4-trisphosphate 5/6-kinase gene that is essential for drought and salt stress responses in rice, Plant Mol. Biol., 77, 547, 10.1007/s11103-011-9830-9 Fernandes, 2008, Distinctive transcriptome responses to adverse environmental conditions in Zea mays L, Plant Biotechnol. J., 6, 782, 10.1111/j.1467-7652.2008.00360.x Ford, 2011, Quantitative proteomic analysis of wheat cultivars with differing drought stress tolerance, Front. Plant Sci., 2, 44, 10.3389/fpls.2011.00044 Foti, 2021, Metabolic responses of two contrasting lentil genotypes to PEG-induced drought stress, Agronomy, 11, 1190, 10.3390/agronomy11061190 Fu, 2017, OsJAZ1 attenuates drought resistance by regulating JA and ABA signaling in rice, Front. Plant Sci., 8, 2108, 10.3389/fpls.2017.02108 Gill, 2003, Changes in germination, growth and soluble sugar contents of Sorghum bicolor (L.) Moench seeds under various abiotic stresses, Plant Growth Regul., 40, 157, 10.1023/A:1024252222376 Guo, 2021, Current understanding of bHLH transcription factors in plant abiotic stress tolerance, Int. J. Mol. Sci., 22, 4921, 10.3390/ijms22094921 Guo, 2020, Growth and carbohydrate dynamic of perennial ryegrass seedlings during PEG-simulated drought and subsequent recovery, Plant Physiol. Biochem., 154, 85, 10.1016/j.plaphy.2020.06.008 Gupta, 2020, Identifying transcripts associated with efficient transport and accumulation of Fe and Zn in hexaploid wheat (T. aestivum L.), J. Biotechnol., 316, 46, 10.1016/j.jbiotec.2020.03.015 Gu, 2014, Circlize implements and enhances circular visualization in R, Bioinformatics, 30, 2811, 10.1093/bioinformatics/btu393 Harrell, 2019 Hirsch, 2014, Insights into the maize pan-genome and pan-transcriptome, Plant Cell, 26, 121, 10.1105/tpc.113.119982 Huang, 2010, Pleiotropic physiological consequences of feedback-insensitive phenylalanine biosynthesis in Arabidopsis thaliana, Plant J., 63, 823, 10.1111/j.1365-313X.2010.04287.x Hu, 2020, Drought-induced disturbance of carbohydrate metabolism in anthers and male abortion of two Gossypium hirsutum cultivars differing in drought tolerance, Plant Cell Rep., 39, 195, 10.1007/s00299-019-02483-1 Jagadish, 2010, Physiological and proteomic approaches to address heat tolerance during anthesis in rice (Oryza sativa L.), J. Exp. Bot., 61, 143, 10.1093/jxb/erp289 Jang, 2012, Increased polyamine biosynthesis enhances stress tolerance by preventing the accumulation of reactive oxygen species: T-DNA mutational analysis of Oryza sativa lysine decarboxylase-like protein 1, Mol. Cell., 34, 251, 10.1007/s10059-012-0067-5 Jarzyniak, 2014, Membrane transporters and drought resistance - a complex issue, Front. Plant Sci., 5, 687, 10.3389/fpls.2014.00687 Jiang, 2021, Multi-omics approach reveals the contribution of KLU to leaf longevity and drought tolerance, Plant Physiol., 185, 352, 10.1093/plphys/kiaa034 Khan, 2021, Improving drought tolerance in rice: ensuring food security through multi-dimensional approaches, Physiol. Plantarum, 172, 645, 10.1111/ppl.13223 Kim, 2013, TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions, Genome Biol., 14, R36, 10.1186/gb-2013-14-4-r36 Kumar, 2014, Breeding high-yielding drought-tolerant rice: genetic variations and conventional and molecular approaches, J. Exp. Bot., 65, 6265, 10.1093/jxb/eru363 Kumar, 2022, Unraveling the contribution of OsSOS2 in conferring salinity and drought tolerance in a high‐yielding rice, Physiol. Plantarum, 174, 10.1111/ppl.13638 Langmead, 2012, Fast gapped-read alignment with Bowtie 2, Nat. Methods, 9, 357, 10.1038/nmeth.1923 Lei, 2015, Ribosome profiling reveals dynamic translational landscape in maize seedlings under drought stress, Plant J., 84, 1206, 10.1111/tpj.13073 Lenka, 2011, Comparative analysis of drought-responsive transcriptome in Indica rice genotypes with contrasting drought tolerance, Plant Biotechnol. J., 9, 315, 10.1111/j.1467-7652.2010.00560.x Li, 2011, Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice, Planta, 234, 1007, 10.1007/s00425-011-1458-0 Liu, 2011, Reversible and irreversible drought-induced changes in the anther proteome of rice (Oryza sativa L.) genotypes IR64 and Moroberekan, Mol. Plant, 4, 59, 10.1093/mp/ssq039 Liu, 2020, Comparative non-targeted metabolomic analysis reveals insights into the mechanism of rice yellowing, Food Chem., 308, 10.1016/j.foodchem.2019.125621 Li, 2015, Metabolic and transcriptomic signatures of rice floral organs reveal sugar starvation as a factor in reproductive failure under heat and drought stress, Plant Cell Environ., 38, 2171, 10.1111/pce.12545 Li, 2015, Spermine alleviates drought stress in white clover with different resistance by influencing carbohydrate metabolism and dehydrins synthesis, PLoS One, 10 Lu, 2009, Identification of OsbZIP72 as a positive regulator of ABA response and drought tolerance in rice, Planta, 229, 605, 10.1007/s00425-008-0857-3 Luo, 2020, Integrating multiple omics to identify common and specific molecular changes occurring in Arabidopsis under chronic nitrate and sulfate limitations, J. Exp. Bot., 71, 6471, 10.1093/jxb/eraa337 Maeda, 2010, RNAi suppression of Arogenate Dehydratase1 reveals that phenylalanine is synthesized predominantly via the arogenate pathway in petunia petals, Plant Cell, 22, 832, 10.1105/tpc.109.073247 Maere, 2005, BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks, Bioinformatics, 21, 3448, 10.1093/bioinformatics/bti551 Maruyama, 2014, Integrated analysis of the effects of cold and dehydration on rice metabolites, phytohormones, and gene transcripts, Plant Physiol., 164, 1759, 10.1104/pp.113.231720 Ma, 2016, Transcriptomic and metabolomic studies disclose key metabolism pathways contributing to well-maintained photosynthesis under the drought and the consequent drought-tolerance in rice, Front. Plant Sci., 7, 1886, 10.3389/fpls.2016.01886 McLoughlin, 2018, Maize multi-omics reveal roles for autophagic recycling in proteome remodelling and lipid turnover, Nat. Plants, 4, 1056, 10.1038/s41477-018-0299-2 McLoughlin, 2020, Autophagy plays prominent roles in amino acid, nucleotide, and carbohydrate metabolism during fixed-carbon starvation in maize, Plant Cell, 32, 2699, 10.1105/tpc.20.00226 Merico, 2010, Enrichment map: a network-based method for gene-set enrichment visualization and interpretation, PLoS One, 5, 10.1371/journal.pone.0013984 Mishra, 2018, Physiological characterization and allelic diversity of selected drought tolerant traditional rice (Oryza sativa L.) landraces of Koraput, India, Physiol. Mol. Biol. Plants, 24, 1035, 10.1007/s12298-018-0606-4 Mohammadi, 2012, Comparative proteome analysis of drought-sensitive and drought-tolerant rapeseed roots and their hybrid F1 line under drought stress, Amino Acids, 43, 2137, 10.1007/s00726-012-1299-6 Moumeni, 2011, Comparative analysis of root transcriptome profiles of two pairs of drought-tolerant and susceptible rice near-isogenic lines under different drought stress, BMC Plant Biol., 11, 174, 10.1186/1471-2229-11-174 Nelson, 2014, Climate change effects on agriculture: economic responses to biophysical shocks, Proc. Natl. Acad. Sci. U.S.A., 111, 3274, 10.1073/pnas.1222465110 Obata, 2015, Metabolite profiles of maize leaves in drought, heat, and combined stress field trials reveal the relationship between metabolism and grain yield, Plant Physiol., 169, 2665 Oliva, 2020, Enhanced production of aromatic amino acids in tobacco plants leads to increased phenylpropanoid metabolites and tolerance to stresses, Front. Plant Sci., 11 Paczkowska, 2020, Integrative pathway enrichment analysis of multivariate omics data, Nat. Commun., 11, 735, 10.1038/s41467-019-13983-9 Pareek, 2020, Mitigating the impact of climate change on plant productivity and ecosystem sustainability, J. Exp. Bot., 71, 451, 10.1093/jxb/erz518 Patel, 2012, NGS QC Toolkit: a toolkit for quality control of next generation sequencing data, PLoS One, 7, 10.1371/journal.pone.0030619 Paul, 2015, Dissecting root proteome of transgenic rice cultivars unravels metabolic alterations and accumulation of novel stress responsive proteins under drought stress, Plant Sci., 234, 133, 10.1016/j.plantsci.2015.02.006 Peleg, 2011, Hormone balance and abiotic stress tolerance in crop plants, Curr. Opin. Plant Biol., 14, 290, 10.1016/j.pbi.2011.02.001 Pillai, 2002, Molecular cloning, characterization, expression and chromosomal location of OsGAPDH, a submergence responsive gene in rice (Oryza sativa L.), Theor. Appl. Genet., 105, 34, 10.1007/s00122-001-0833-9 Poli, 2013, Characterization of a Nagina22 rice mutant for heat tolerance and mapping of yield traits, Rice, 6, 36, 10.1186/1939-8433-6-36 Quan, 2010, Overexpression of an ERF transcription factor TSRF1 improves rice drought tolerance, Plant Biotechnol. J., 8, 476, 10.1111/j.1467-7652.2009.00492.x Ramkumar, 2022, Identification of major candidate genes for multiple abiotic stress tolerance at seedling stage by network analysis and their validation by expression profiling in rice (Oryza sativa L.), 3 Biotech, 12, 127, 10.1007/s13205-022-03182-7 Ravikumar, 2014, Stress-inducible expression of AtDREB1A transcription factor greatly improves drought stress tolerance in transgenic indica rice, Transgenic Res., 23, 421, 10.1007/s11248-013-9776-6 Rezaul, 2019, Abscisic acid prevents pollen abortion under high-temperature stress by mediating sugar metabolism in rice spikelets, Physiol. Plantarum, 165, 644, 10.1111/ppl.12759 Robinson, 2010, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics, 26, 139, 10.1093/bioinformatics/btp616 Sailaja, 2015, Integrated physiological, biochemical, and molecular analysis identifies important traits and mechanisms associated with differential response of rice genotypes to elevated temperature, Front. Plant Sci., 6, 1044, 10.3389/fpls.2015.01044 Saleh, 2019, Brown rice versus white rice: nutritional quality, potential health benefits, development of food products, and preservation Technologies, Compr. Rev. Food Sci. Food Saf., 18, 1070, 10.1111/1541-4337.12449 Shankar, 2016, Transcriptome analysis in different rice cultivars provides novel insights into desiccation and salinity stress responses, Sci. Rep., 6, 10.1038/srep23719 Shao, 2015, NAC transcription factors in plant multiple abiotic stress responses: progress and prospects, Front. Plant Sci., 6, 902, 10.3389/fpls.2015.00902 Sharma, 2019, Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress, Molecules, 24, 2452, 10.3390/molecules24132452 Sharoni, 2011, Gene structures, classification and expression models of the AP2/EREBP transcription factor family in rice, Plant Cell Physiol., 52, 344, 10.1093/pcp/pcq196 Shu, 2011, Genetic, proteomic and metabolic analysis of the regulation of energy storage in rice seedlings in response to drought, Proteomics, 11, 4122, 10.1002/pmic.201000485 Siddiqui, 2021, Hydrogen sulfide (H2S) and potassium (K+) synergistically induce drought stress tolerance through regulation of H+-ATPase activity, sugar metabolism, and antioxidative defense in tomato seedlings, Plant Cell Rep., 40, 1543, 10.1007/s00299-021-02731-3 Singh, 2005, A comparison of proline, thiol levels and GAPDH activity in cyanobacteria of different origins facing temperature-stress, World J. Microbiol. Biotechnol., 21, 1, 10.1007/s11274-004-0872-x Singh, 2023, Unravelling the molecular mechanism underlying drought stress response in chickpea via integrated multi-omics analysis, Front. Plant Sci., 14, 10.3389/fpls.2023.1156606 Stekhoven, 2012, MissForest--non-parametric missing value imputation for mixed-type data, Bioinformatics, 28, 112, 10.1093/bioinformatics/btr597 Trapnell, 2010, Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation, Nat. Biotechnol., 28, 511, 10.1038/nbt.1621 Trenberth, 2014, Global warming and changes in drought, Nat. Clim., 4, 17, 10.1038/nclimate2067 Tyanova, 2016, The MaxQuant computational platform for mass spectrometry-based shotgun proteomics, Nat. Protoc., 11, 2301, 10.1038/nprot.2016.136 Vijayaraghavareddy, 2021, Metabolome profiling reveals impact of water limitation on grain filling in contrasting rice genotypes, Plant Physiol., Biochem. 162, 690 Wang, 2021, Physiological and proteomic responses of pitaya to PEG-induced drought stress, Collect. FAO Agric., 11, 632 Wang, 2017, Physiological and proteomic analysis of rice (Oryza sativa L.) in flag leaf during flowering stage and milk stage under drought stress, Plant Growth Regul., 82, 201, 10.1007/s10725-017-0252-9 Wei, 2019, Enhanced ROS scavenging and sugar accumulation contribute to drought tolerance of naturally occurring autotetraploids in Poncirus trifoliata, Plant Biotechnol. J., 17, 1394, 10.1111/pbi.13064 Xia, 2020, Temporal transcriptomic differences between tolerant and susceptible genotypes contribute to rice drought tolerance, BMC Genom., 21, 776, 10.1186/s12864-020-07193-7 Xie, 2011, KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases, Nucleic Acids Res., 39, W316, 10.1093/nar/gkr483 Xie, 2020, Aphid fecundity and defenses in wheat exposed to a combination of heat and drought stress, J. Exp. Bot., 71, 2713, 10.1093/jxb/eraa017 Xie, 2020, Integrated analysis of the transcriptome and metabolome revealed the molecular mechanisms underlying the enhanced salt tolerance of rice due to the application of exogenous melatonin, Front. Plant Sci., 11 Xiong, 2019, Comprehensive metabolomic and proteomic analysis in biochemical metabolic pathways of rice spikes under drought and submergence stress, Biochim. Biophys. Acta, Proteins Proteomics, 1867, 237, 10.1016/j.bbapap.2019.01.001 Yadav, 2022, Physiological and molecular signatures reveal differential response of rice genotypes to drought and drought combination with heat and salinity stress, Physiol. Mol. Biol. Plants, 28, 899, 10.1007/s12298-022-01162-y Yamakawa, 2010, Atlas of rice grain filling-related metabolism under high temperature: joint analysis of metabolome and transcriptome demonstrated inhibition of starch accumulation and induction of amino acid accumulation, Plant Cell Physiol., 51, 795, 10.1093/pcp/pcq034 Yang, 2020, Dynamic transcriptome and metabolome analyses of two types of rice during the seed germination and young seedling growth stages, BMC Genom., 21, 603, 10.1186/s12864-020-07024-9 Yang, 2016, Transcriptome profiling of watermelon root in response to short-term osmotic stress, PLoS One, 11 Yu, 2013, Arabidopsis enhanced drought tolerance1/HOMEODOMAIN GLABROUS11 confers drought tolerance in transgenic rice without yield penalty, Plant Physiol., 162, 1378, 10.1104/pp.113.217596 Zhang, 2018, Physiological and proteomic responses of contrasting alfalfa (Medicago sativa L.) varieties to PEG-induced osmotic stress, Front. Plant Sci., 9, 242, 10.3389/fpls.2018.00242 Zhang, 2016, Comparative transcriptome analysis highlights the crucial roles of photosynthetic system in drought stress adaptation in upland rice, Sci. Rep., 6 Zhao, 2018, Glycerol-3-phosphate dehydrogenase (GPDH) gene family in Zea mays L.: identification, subcellular localization, and transcriptional responses to abiotic stresses, PLoS One, 13 Zhou, 2022, Proteomic investigation of molecular mechanisms in response to PEG-induced drought stress in soybean roots, Plants, 11, 1173, 10.3390/plants11091173 Zhu, 2009, Glucose-induced delay of seed germination in rice is mediated by the suppression of ABA catabolism rather than an enhancement of ABA biosynthesis, Plant Cell Physiol, 50, 644, 10.1093/pcp/pcp022