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Title: Tripogon loliiformis tolerates rapid desiccation after metabolic and transcriptional priming during initial drying

Journal Article · · Scientific Reports

Abstract Crop plants and undomesticated resilient species employ different strategies to regulate their energy resources and growth. Most crop species are sensitive to stress and prioritise rapid growth to maximise yield or biomass production. In contrast, resilient plants grow slowly, are small, and allocate their resources for survival in challenging environments. One small group of plants, termed resurrection plants, survive desiccation of their vegetative tissue and regain full metabolic activity upon watering. However, the precise molecular mechanisms underlying this extreme tolerance remain unknown. In this study, we employed a transcriptomics and metabolomics approach, to investigate the mechanisms of desiccation tolerance in Tripogon loliiformis , a modified desiccation-tolerant plant, that survives gradual but not rapid drying. We show that T. loliiformis can survive rapid desiccation if it is gradually dried to 60% relative water content (RWC). Furthermore, the gene expression data showed that T. loliiformis is genetically predisposed for desiccation in the hydrated state, as evidenced by the accumulation of MYB, NAC, bZIP, WRKY transcription factors along with the phytohormones, abscisic acid, salicylic acid, amino acids (e.g., proline) and TCA cycle sugars during initial drying. Through network analysis of co-expressed genes, we observed differential responses to desiccation between T. loliiformis shoots and roots. Dehydrating shoots displayed global transcriptional changes across broad functional categories, although no enrichment was observed during drying. In contrast, dehydrating roots showed distinct network changes with the most significant differences occurring at 40% RWC. The cumulative effects of the early stress responses may indicate the minimum requirements of desiccation tolerance and enable T. loliiformis to survive rapid drying. These findings potentially hold promise for identifying biotechnological solutions aimed at developing drought-tolerant crops without growth and yield penalties.

Sponsoring Organization:
USDOE
Grant/Contract Number:
SC0014081
OSTI ID:
2217643
Alternate ID(s):
OSTI ID: 2281486
Journal Information:
Scientific Reports, Journal Name: Scientific Reports Journal Issue: 1 Vol. 13; ISSN 2045-2322
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (87)

Plant responses to water deficit journal February 1997
Jasmonates Induce Apoptosis and cell Cycle Arrest in Non-Small cell lung Cancer Lines journal January 2006
Photosynthesis in desiccation tolerant plants: Energy metabolism and antioxidative stress defense journal January 2012
Physiological and biochemical changes during drought and recovery periods at tillering and jointing stages in wheat (Triticum aestivum L.) journal March 2018
Desiccation Tolerance in the Resurrection Plant Craterostigma plantagineum . A Contribution to the Study of Drought Tolerance at the Molecular Level journal December 2001
Involvement of the Basic Helix-Loop-Helix Transcription Factor RERJ1 in Wounding and Drought Stress Responses in Rice Plants journal January 2005
ABI1 and PP2CA Phosphatases Are Negative Regulators of Snf1-Related Protein Kinase1 Signaling in Arabidopsis journal October 2013
Metabolic control and regulation of the tricarboxylic acid cycle in photosynthetic and heterotrophic plant tissues: TCA control and regulation in plant tissues journal June 2011
Methyl jasmonate and its potential in cancer therapy journal September 2015
Plant oxylipins: role of jasmonic acid during programmed cell death, defence and leaf senescence journal August 2009
Isolation and Identification of a Senescence-promoting Substance from Wormwood ( Artemisia absinthium L.) journal August 1980
Drought-stimulated genes correlated with desiccation tolerance of the resurrection grass Sporobolus stapfianus journal March 1998
The Biochemistry and the Physiological and Molecular Actions of Jasmonates journal June 1993
Sporobolus stapfianus: Insights into desiccation tolerance in the resurrection grasses from linking transcriptomics to metabolomics journal March 2017
MPLEx: a Robust and Universal Protocol for Single-Sample Integrative Proteomic, Metabolomic, and Lipidomic Analyses journal May 2016
Multilevel Regulation of Abiotic Stress Responses in Plants journal September 2017
Natural jasmonates of different structures suppress the growth of human neuroblastoma cell line SH-SY5Y and its mechanisms1 journal July 2008
Molecular cloning of abscisic acid-modulated genes which are induced during desiccation of the resurrection plant Craterostigma plantagineum journal April 1990
The Molecular Basis of Dehydration Tolerance in Plants journal June 1996
A comparison of mechanisms of desiccation tolerance among three angiosperm resurrection plant species journal November 2000
OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice journal February 2011
Mechanisms of plant desiccation tolerance journal September 2001
Desiccation Tolerance Studied in the Resurrection Plant Craterostigma plantagineum journal November 2005
A role for jasmonate in pathogen defense of Arabidopsis journal June 1998
The evolution of vegetative desiccation tolerance in land plants journal November 2000
Physiological Aspects of Desiccation Tolerance journal June 1979
Convergent energy and stress signaling journal September 2008
Potential Biotechnological Applications of Autophagy for Agriculture journal October 2021
Sugar signals and the control of plant growth and development journal January 2014
Photo- and antioxidative protection, and a role for salicylic acid during drought and recovery in field-grown Phillyrea angustifolia plants journal September 2003
Saving for a rainy day: Control of energy needs in resurrection plants journal June 2018
Centrality of BAGs in Plant PCD, Stress Responses, and Host Defense journal November 2020
Roots of the Resurrection Plant Tripogon loliiformis Survive Desiccation Without the Activation of Autophagy Pathways by Maintaining Energy Reserves journal April 2019
Plant stress hormones suppress the proliferation and induce apoptosis in human cancer cells journal April 2002
Desiccation tolerant vascular plants of southern Africa journal January 1977
The influence of alternative pathways of respiration that utilize branched-chain amino acids following water shortage in Arabidopsis : Influence of the ETF/ETFQO pathway under water stress journal March 2016
Nitric Oxide is Involved in Methyl Jasmonate-induced Defense Responses and Secondary Metabolism Activities of Taxus Cells journal June 2005
Silencing the Jasmonate Cascade: Induced Plant Defenses and Insect Populations journal July 2004
Capsaicin, a Spicy Component of Hot Pepper, Induces Apoptosis by Activation of the Peroxisome Proliferator-Activated Receptor γ in HT-29 Human Colon Cancer Cells journal September 2004
Abscisic acid Biosynthesis and Catabolism journal June 2005
Methyl jasmonate decreases membrane fluidity and induces apoptosis through tumor necrosis factor receptor 1 in breast cancer cells journal September 2008
Overexpression of the vascular brassinosteroid receptor BRL3 confers drought resistance without penalizing plant growth journal November 2018
A Regulatory Hierarchy of the Arabidopsis Branched-Chain Amino Acid Metabolic Network journal May 2017
A Re-Examination of the Relative Turgidity Technique for Estimating Water Deficits in Leaves journal January 1962
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks journal November 2003
Analysis of plant hormone profiles in response to moderate dehydration stress journal February 2017
Molecular responses to dehydration and desiccation in desiccation-tolerant angiosperm plants journal January 2018
Effect of Methyl Jasmonate on antioxidative enzyme activities and on the contents of ROS and H2O2 in Ricinus communis leaves journal January 2010
Methyl Jasmonate Induces Production of Reactive Oxygen Species and Alterations in Mitochondrial Dynamics that Precede Photosynthetic Dysfunction and Subsequent Cell Death journal June 2008
Core cellular and tissue‐specific mechanisms enable desiccation tolerance in Craterostigma journal March 2023
Methyl jasmonate stimulates the de novo biosynthesis of vitamin C in plant cell suspensions journal August 2005
Role of proline under changing environments: A review journal November 2012
Principal Transcriptional Programs Regulating Plant Amino Acid Metabolism in Response to Abiotic Stresses     journal March 2008
FiehnLib: Mass Spectral and Retention Index Libraries for Metabolomics Based on Quadrupole and Time-of-Flight Gas Chromatography/Mass Spectrometry journal December 2009
The Life and Death of a Plant Cell journal April 2017
Current and Future Perspectives on the Structural Identification of Small Molecules in Biological Systems journal December 2016
Water Deficit Enhances C Export to the Roots in Arabidopsis thaliana Plants with Contribution of Sucrose Transporters in Both Shoot and Roots journal January 2016
The unusual sugar composition in leaves of the resurrection plant Myrothamnus flabellifolia journal February 1993
AUTOPHAGY-RELATED11 Plays a Critical Role in General Autophagy- and Senescence-Induced Mitophagy in Arabidopsis journal February 2014
Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics journal March 2009
Phenylpropanoid Biosynthesis journal January 2010
POPP the question: what do LEA proteins do? journal January 2004
A footprint of desiccation tolerance in the genome of Xerophyta viscosa journal March 2017
ABA treatment increases both the desiccation tolerance of photosynthesis, and nonphotochemical quenching in the moss Atrichum undulatum journal November 2000
Understanding plant responses to drought — from genes to the whole plant journal January 2003
Overexpression of S-Adenosyl-l-Methionine Synthetase 2 from Sugar Beet M14 Increased Arabidopsis Tolerance to Salt and Oxidative Stress journal April 2017
An improved method for monitoring cell death in cell suspension and leaf disc assays using evans blue journal October 1994
Phytohormones and plant responses to salinity stress: a review journal December 2014
The evolution of desiccation tolerance in angiosperm plants: a rare yet common phenomenon journal January 2013
Carbon partitioning in A rabidopsis thaliana is a dynamic process controlled by the plants metabolic status and its circadian clock : Dynamic carbon partitioning in journal April 2015
Trehalose Accumulation Triggers Autophagy during Plant Desiccation journal December 2015
The effect of salicylic acid on barley response to water deficit journal September 2005
Linking drought‐resistance mechanisms to drought avoidance in upland rice using a QTL approach: progress and new opportunities to integrate stomatal and mesophyll responses journal May 2002
Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status journal February 2006
Tripogon loliiformis elicits a rapid physiological and structural response to dehydration for desiccation tolerance journal January 2016
The Biosynthetic Pathways for Shikimate and Aromatic Amino Acids in Arabidopsis thaliana journal January 2010
Transcriptome Analysis of Two Species of Jute in Response to Polyethylene Glycol (PEG)- induced Drought Stress journal November 2017
Contrapuntal role of ABA: Does it mediate stress tolerance or plant growth retardation under long-term drought stress? journal September 2012
Desiccation Tolerance: Avoiding Cellular Damage During Drying and Rehydration journal April 2020
Insights into the cellular mechanisms of desiccation tolerance among angiosperm resurrection plant species journal August 2004
Plant hormone interactions: innovative targets for crop breeding and management journal May 2012
SNF1/AMPK/SnRK1 kinases, global regulators at the heart of energy control? journal January 2007
Drying without senescence in resurrection plants journal January 2014
Abiotic Stresses: General Defenses of Land Plants and Chances for Engineering Multistress Tolerance journal December 2018
The metabolic response to drought journal February 2019
Desiccation Tolerance in Bryophytes: A Reflection of the Primitive Strategy for Plant Survival in Dehydrating Habitats? journal November 2005
Jasmonates: Novel Anticancer Agents Acting Directly and Selectively on Human Cancer Cell Mitochondria journal March 2005