Anastatica hierochuntica, an Arabidopsis Desert Relative, Is Tolerant to Multiple Abiotic Stresses and Exhibits Species-Specific and Common Stress Tolerance Strategies with Its Halophytic Relative, Eutrema (Thellungiella) salsugineum

The search for novel stress tolerance determinants has led to increasing interest in plants native to extreme environments – so called “extremophytes.” One successful strategy has been comparative studies between Arabidopsis thaliana and extremophyte Brassicaceae relatives such as the halophyte Eutrema salsugineum located in areas including cold, salty coastal regions of China. Here, we investigate stress tolerance in the desert species, Anastatica hierochuntica (True Rose of Jericho), a member of the poorly investigated lineage III Brassicaceae. We show that A. hierochuntica has a genome approximately 4.5-fold larger than Arabidopsis, divided into 22 diploid chromosomes, and demonstrate that A. hierochuntica exhibits tolerance to heat, low N and salt stresses that are characteristic of its habitat. Taking salt tolerance as a case study, we show that A. hierochuntica shares common salt tolerance mechanisms with E. salsugineum such as tight control of shoot Na+ accumulation and resilient photochemistry features. Furthermore, metabolic profiling of E. salsugineum and A. hierochuntica shoots demonstrates that the extremophytes exhibit both species-specific and common metabolic strategies to cope with salt stress including constitutive up-regulation (under control and salt stress conditions) of ascorbate and dehydroascorbate, two metabolites involved in ROS scavenging. Accordingly, A. hierochuntica displays tolerance to methyl viologen-induced oxidative stress suggesting that a highly active antioxidant system is essential to cope with multiple abiotic stresses. We suggest that A. hierochuntica presents an excellent extremophyte Arabidopsis relative model system for understanding plant survival in harsh desert conditions.

[1]  J. Mansbridge,et al.  Acclimation of the crucifer Eutrema salsugineum to phosphate limitation is associated with constitutively high expression of phosphate-starvation genes. , 2016, Plant, cell & environment.

[2]  A. Good,et al.  Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? , 2004, Trends in plant science.

[3]  R. Mittler,et al.  Abiotic stress, the field environment and stress combination. , 2006, Trends in plant science.

[4]  K. Shinozaki,et al.  Comparative genomic analysis of 1047 completely sequenced cDNAs from an Arabidopsis-related model halophyte, Thellungiella halophila , 2010, BMC Plant Biology.

[5]  H. Bohnert,et al.  Unraveling abiotic stress tolerance mechanisms--getting genomics going. , 2006, Current opinion in plant biology.

[6]  A. Amtmann Learning from evolution: Thellungiella generates new knowledge on essential and critical components of abiotic stress tolerance in plants. , 2009, Molecular plant.

[7]  E. Zaady Seasonal Change and Nitrogen Cycling in a Patchy Negev Desert: a Review , 2005 .

[8]  Nicholas J Provart,et al.  RNA-Seq effectively monitors gene expression in Eutrema salsugineum plants growing in an extreme natural habitat and in controlled growth cabinet conditions , 2013, BMC Genomics.

[9]  R. Hunt Basic Growth Analysis: Plant growth analysis for beginners , 1989 .

[10]  J. Boyer Plant Productivity and Environment , 1982, Science.

[11]  M. Stitt,et al.  Glycine decarboxylase controls photosynthesis and plant growth , 2012, FEBS letters.

[12]  P. Rey,et al.  Efficiency of biochemical protection against toxic effects of accumulated salt differentiates Thellungiella halophila from Arabidopsis thaliana. , 2007, Journal of plant physiology.

[13]  T. Lawson,et al.  C3 photosynthesis in the desert plant Rhazya stricta is fully functional at high temperatures and light intensities. , 2014, The New phytologist.

[14]  I. Al‐Shehbaz,et al.  Cabbage family affairs: the evolutionary history of Brassicaceae. , 2011, Trends in plant science.

[15]  F. Bakker,et al.  Molecular phylogenetics, temporal diversification, and principles of evolution in the mustard family (Brassicaceae). , 2010, Molecular biology and evolution.

[16]  C. Critchley,et al.  Rapid light curves: A new fluorescence method to assess the state of the photosynthetic apparatus , 2004, Photosynthesis Research.

[17]  D. Hincha,et al.  Comparison of freezing tolerance, compatible solutes and polyamines in geographically diverse collections of Thellungiella sp. and Arabidopsis thaliana accessions , 2012, BMC Plant Biology.

[18]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]/Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .

[19]  D. Lobell,et al.  Climate Trends and Global Crop Production Since 1980 , 2011, Science.

[20]  S. Barak,et al.  Evidence that differential gene expression between the halophyte, Thellungiella halophila, and Arabidopsis thaliana is responsible for higher levels of the compatible osmolyte proline and tight control of Na+ uptake in T. halophila. , 2006, Plant, cell & environment.

[21]  K. Anamthawat-Jónsson Preparation of chromosomes from plant leaf meristems for karyotype analysis and in situ hybridization. , 2003, Methods in cell science : an official journal of the Society for In Vitro Biology.

[22]  C. Foyer,et al.  Ascorbate and Glutathione: The Heart of the Redox Hub1 , 2011, Plant Physiology.

[23]  E. Waters,et al.  Boechera Species Exhibit Species-Specific Responses to Combined Heat and High Light Stress , 2015, PloS one.

[24]  A. Stamatakis,et al.  BrassiBase: introduction to a novel knowledge database on Brassicaceae evolution. , 2014, Plant & cell physiology.

[25]  K. Shinozaki,et al.  Effects of abiotic stress on plants: a systems biology perspective , 2011, BMC Plant Biology.

[26]  S. Shigeoka,et al.  Galactinol and Raffinose Constitute a Novel Function to Protect Plants from Oxidative Damage1[W][OA] , 2008, Plant Physiology.

[27]  M. Semenov,et al.  Heat tolerance around flowering in wheat identified as a key trait for increased yield potential in Europe under climate change , 2015, Journal of experimental botany.

[28]  Prof. Dr. Yitzchak Gutterman Survival Strategies of Annual Desert Plants , 2002, Adaptations of Desert Organisms.

[29]  F. Skoog,et al.  A revised medium for rapid growth and bio assays with tobacco tissue cultures , 1962 .

[30]  A. Liepman,et al.  Peroxisomal alanine : glyoxylate aminotransferase (AGT1) is a photorespiratory enzyme with multiple substrates in Arabidopsis thaliana. , 2001, The Plant journal : for cell and molecular biology.

[31]  E. Stackebrandt,et al.  Taxonomy and systematics. , 2005 .

[32]  N. Smirnoff,et al.  Hydroxyl radical scavenging activity of compatible solutes , 1989 .

[33]  M. Hagemann,et al.  Photorespiration and the potential to improve photosynthesis. , 2016, Current opinion in chemical biology.

[34]  N. Smirnoff THE FUNCTION AND METABOLISM OF ASCORBIC ACID IN PLANTS , 1996 .

[35]  F. Gao,et al.  Identification of a new 130 bp cis-acting element in the TsVP1 promoter involved in the salt stress response from Thellungiella halophila , 2010, BMC Plant Biology.

[36]  Simon Prochnik,et al.  The Reference Genome of the Halophytic Plant Eutrema salsugineum , 2013, Front. Plant Sci..

[37]  J. Friedman,et al.  Drought tolerance of germinating seeds and young seedlings of Anastatica hierochuntica L. , 2004, Oecologia.

[38]  M. Moshelion,et al.  The Arabidopsis-related halophyte Thellungiella halophila: boron tolerance via boron complexation with metabolites? , 2012, Plant, cell & environment.

[39]  A. Fernie,et al.  Gas chromatography mass spectrometry–based metabolite profiling in plants , 2006, Nature Protocols.

[40]  J. Cloudsley-Thompson Biology of Deserts , 1952, Nature.

[41]  J. Kopka,et al.  Metabolome and water homeostasis analysis of Thellungiella salsuginea suggests that dehydration tolerance is a key response to osmotic stress in this halophyte. , 2010, The Plant journal : for cell and molecular biology.

[42]  C. Abdelly,et al.  Physiological and Anatomical Adaptations Induced by Flooding in Cotula Coronopifolia , 2011, Acta biologica Hungarica.

[43]  M. Udvardi,et al.  Comparative ionomics and metabolomics in extremophile and glycophytic Lotus species under salt stress challenge the metabolic pre-adaptation hypothesis. , 2011, Plant, cell & environment.

[44]  I. Al‐Shehbaz,et al.  A generic and tribal synopsis of the Brassicaceae (Cruciferae) , 2012 .

[45]  Akhilesh Kumar,et al.  Pyroglutamic acid : throwing light on a lightly studied metabolite , 2012 .

[46]  Detlef Weigel,et al.  Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4 , 2008, Nature.

[47]  J. Palta,et al.  Responses to abiotic stresses. , 1998 .

[48]  G. Johnson,et al.  Contrasting Responses of Photosynthesis to Salt Stress in the Glycophyte Arabidopsis and the Halophyte Thellungiella: Role of the Plastid Terminal Oxidase as an Alternative Electron Sink1[C][OA] , 2008, Plant Physiology.

[49]  D. Galbraith,et al.  Salt Cress. A Halophyte and Cryophyte Arabidopsis Relative Model System and Its Applicability to Molecular Genetic Analyses of Growth and Development of Extremophiles1 , 2004, Plant Physiology.

[50]  J. Farrant,et al.  Desiccation tolerance in the vegetative tissues of the fern Mohria caffrorum is seasonally regulated. , 2009, The Plant journal : for cell and molecular biology.

[51]  D. Tilman,et al.  Global food demand and the sustainable intensification of agriculture , 2011, Proceedings of the National Academy of Sciences.

[52]  M. Kuntz,et al.  Plastid terminal oxidase (PTOX) has the potential to act as a safety valve for excess excitation energy in the alpine plant species Ranunculus glacialis L. , 2013, Plant, cell & environment.

[53]  J. Cheeseman The evolution of halophytes, glycophytes and crops, and its implications for food security under saline conditions. , 2015, The New phytologist.

[54]  K. Shinozaki,et al.  Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. , 2002, The Plant journal : for cell and molecular biology.

[55]  H. Lichtenthaler CHLOROPHYLL AND CAROTENOIDS: PIGMENTS OF PHOTOSYNTHETIC BIOMEMBRANES , 1987 .

[56]  D. Weigel,et al.  Beyond the thale: comparative genomics and genetics of Arabidopsis relatives , 2015, Nature Reviews Genetics.

[57]  F. Xiong,et al.  The Influence of Ultraviolet-B Radiation on Growth, Hydroxycinnamic Acids and Flavonoids of Deschampsia antarctica during Springtime Ozone Depletion in Antarctica† , 2005, Photochemistry and photobiology.

[58]  Nan Li,et al.  World Population Prospects, the 2010 Revision: Estimation and projection methodology , 2011 .

[59]  H. Bohnert,et al.  Shedding light on an extremophile lifestyle through transcriptomics. , 2009, The New phytologist.

[60]  Jun Wang,et al.  Insights into salt tolerance from the genome of Thellungiella salsuginea , 2012, Proceedings of the National Academy of Sciences.

[61]  B. Moffatt,et al.  Thellungiella: an Arabidopsis-related model plant adapted to cold temperatures. , 2007, Plant, cell & environment.

[62]  S. Rothstein,et al.  Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency. , 2011, Journal of experimental botany.

[63]  J. Ryals,et al.  Comparative metabolic profiling between desiccation-sensitive and desiccation-tolerant species of Selaginella reveals insights into the resurrection trait. , 2012, The Plant journal : for cell and molecular biology.

[64]  J. Nason,et al.  The influence of seed dispersal mechanisms on the genetic structure of tropical tree populations , 1993 .

[65]  H. Bohnert,et al.  A comparative study of salt tolerance parameters in 11 wild relatives of Arabidopsis thaliana , 2010, Journal of experimental botany.

[66]  I. Turkan,et al.  Changes in the alternative electron sinks and antioxidant defence in chloroplasts of the extreme halophyte Eutrema parvulum (Thellungiella parvula) under salinity. , 2015, Annals of botany.

[67]  A. Good,et al.  Engineering nitrogen use efficient crop plants: the current status. , 2012, Plant biotechnology journal.

[68]  G. Spangenberg,et al.  Xenogenomics: Genomic Bioprospecting in Indigenous and Exotic Plants Through EST Discovery, cDNA Microarray-Based Expression Profiling and Functional Genomics , 2005, Comparative and functional genomics.

[69]  Yang Zhong,et al.  Resolution of Brassicaceae Phylogeny Using Nuclear Genes Uncovers Nested Radiations and Supports Convergent Morphological Evolution , 2015, Molecular biology and evolution.

[70]  Kazuo Shinozaki,et al.  Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics. , 2009, The Plant journal : for cell and molecular biology.

[71]  David Niemeijer,et al.  Ecosystems and Human Well-Being: Desertification Synthesis , 2005 .

[72]  M. Koch,et al.  Taxonomy and systematics are key to biological information: Arabidopsis, Eutrema (Thellungiella), Noccaea and Schrenkiella (Brassicaceae) as examples , 2013, Front. Plant Sci..

[73]  M. Kuntz,et al.  Evidence for alternative electron sinks to photosynthetic carbon assimilation in the high mountain plant species Ranunculus glacialis , 2005 .

[74]  Kazuhito Inoue,et al.  The sites of electron donation of Photosystem I to methyl viologen , 1990 .

[75]  H. Bohnert,et al.  Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. , 2005, The Plant journal : for cell and molecular biology.

[76]  A. Hegazy,et al.  Anatomical significance of the hygrochastic movement in Anastatica hierochuntica. , 2006, Annals of botany.

[77]  R. Mittler,et al.  Genetic engineering for modern agriculture: challenges and perspectives. , 2010, Annual review of plant biology.

[78]  J. Malamy,et al.  Root System Architecture in Arabidopsis Grown in Culture Is Regulated by Sucrose Uptake in the Aerial Tissues[W] , 2008, The Plant Cell Online.

[79]  S. Barak,et al.  Low induction of non-photochemical quenching and high photochemical efficiency in the annual desert plant Anastatica hierochuntica. , 2014, Physiologia plantarum.

[80]  J. Friedman,et al.  Water response of the hygrochastic skeletons of the true rose of Jericho (Anastatica hierochuntica L.) , 2004, Oecologia.

[81]  R. Munns,et al.  Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. , 2015, Annals of botany.

[82]  L. D. Gottlieb Chromosome numbers. , 1980, Science.

[83]  A. Fehér,et al.  The effect of drought and heat stress on reproductive processes in cereals. , 2007, Plant, cell & environment.

[84]  S. Trevanion,et al.  How does photorespiration modulate leaf amino acid contents? A dual approach through modelling and metabolite analysis , 2002 .

[85]  Jian‐Kang Zhu The Next Top Models , 2015, Cell.

[86]  Paulo A. S. Nuin,et al.  Transcriptomic and metabolomic analysis of Yukon Thellungiella plants grown in cabinets and their natural habitat show phenotypic plasticity , 2012, BMC Plant Biology.

[87]  P. Binarová,et al.  Analysis of Nuclear DNA content in plant cells by Flow cytometry , 1989, Biologia Plantarum.

[88]  Naoko Ohkama-Ohtsu,et al.  A γ-Glutamyl Transpeptidase-Independent Pathway of Glutathione Catabolism to Glutamate via 5-Oxoproline in Arabidopsis1[W][OA] , 2008, Plant Physiology.

[89]  K. Shinozaki,et al.  HsfA1d, a protein identified via FOX hunting using Thellungiella salsuginea cDNAs improves heat tolerance by regulating heat-stress-responsive gene expression. , 2013, Molecular plant.

[90]  A. Amtmann,et al.  Thellungiella halophila, a salt‐tolerant relative of Arabidopsis thaliana, possesses effective mechanisms to discriminate between potassium and sodium , 2004 .

[91]  R. Vera-Estrella,et al.  Comparative 2D-DIGE analysis of salinity responsive microsomal proteins from leaves of salt-sensitive Arabidopsis thaliana and salt-tolerant Thellungiella salsuginea. , 2014, Journal of proteomics.

[92]  A. Fait,et al.  Growth Platform-Dependent and -Independent Phenotypic and Metabolic Responses of Arabidopsis and Its Halophytic Relative, Eutrema salsugineum, to Salt Stress1[W][OA] , 2013, Plant Physiology.

[93]  G. Edwards,et al.  Malate metabolism by NADP-malic enzyme in plant defense , 1999, Photosynthesis Research.

[94]  A. Amtmann,et al.  Low unidirectional sodium influx into root cells restricts net sodium accumulation in Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana. , 2006, Journal of experimental botany.

[95]  H. Bohnert,et al.  Life at the extreme: lessons from the genome , 2012, Genome Biology.

[96]  A. Fernie,et al.  Not just a circle: flux modes in the plant TCA cycle. , 2010, Trends in plant science.

[97]  H. Bohnert,et al.  Transcription strength and halophytic lifestyle. , 2011, Trends in plant science.

[98]  Hans J. Bohnert,et al.  Biotechnology for mechanisms that counteract salt stress in extremophile species: a genome-based view , 2012, Plant Biotechnology Reports.

[99]  F. Xiong,et al.  Effect of solar ultraviolet-B radiation during springtime ozone depletion on photosynthesis and biomass production of Antarctic vascular plants. , 2001, Plant physiology.

[100]  R. Munns Comparative physiology of salt and water stress. , 2002, Plant, cell & environment.

[101]  T. Sakurai,et al.  Comparative Genomics in Salt Tolerance between Arabidopsis and Arabidopsis-Related Halophyte Salt Cress Using Arabidopsis Microarray1 , 2004, Plant Physiology.

[102]  D. Guttman,et al.  Forward chemical genetic screens in Arabidopsis identify genes that influence sensitivity to the phytotoxic compound sulfamethoxazole , 2012, BMC Plant Biology.

[103]  J. Friedman,et al.  The influence of seed dispersal mechanisms on the dispersion of Anastatica hierochuntica (Cruciferae) in the Negev desert, Israel. , 1980 .

[104]  S. Rothstein,et al.  The Arabidopsis Halophytic Relative Thellungiella halophila Tolerates Nitrogen-Limiting Conditions by Maintaining Growth, Nitrogen Uptake, and Assimilation1[W][OA] , 2008, Plant Physiology.

[105]  D. Bartels,et al.  Molecular mechanisms of desiccation tolerance in resurrection plants , 2012, Cellular and Molecular Life Sciences.

[106]  S. Rothstein,et al.  The Genetics of Nitrogen Use Efficiency in Crop Plants. , 2015, Annual review of genetics.

[107]  A I Saeed,et al.  TM4: a free, open-source system for microarray data management and analysis. , 2003, BioTechniques.

[108]  R. Hunt Basic growth analysis. , 1990 .

[109]  N. Ramankutty,et al.  Influence of extreme weather disasters on global crop production , 2016, Nature.

[110]  Wolfgang Bilger,et al.  Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis , 1990, Photosynthesis Research.

[111]  Jorge Dinamarca,et al.  The role of photochemical quenching and antioxidants in photoprotection of Deschampsia antarctica. , 2004, Functional plant biology : FPB.

[112]  A. Amtmann,et al.  Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana, has specific root ion-channel features supporting K+/Na+ homeostasis under salinity stress. , 2006, The Plant journal : for cell and molecular biology.

[113]  T. Lawson,et al.  The temporal foliar transcriptome of the perennial C3 desert plant Rhazya stricta in its natural environment , 2014, BMC Plant Biology.

[114]  G. Edwards,et al.  Relationship between photosystem II activity and CO2 fixation in leaves , 1992 .

[115]  C. Babbs,et al.  Lethal hydroxyl radical production in paraquat-treated plants. , 1989, Plant physiology.

[116]  H. Bohnert,et al.  Genome Structures and Transcriptomes Signify Niche Adaptation for the Multiple-Ion-Tolerant Extremophyte Schrenkiella parvula1[C][W][OPEN] , 2014, Plant Physiology.

[117]  D. Galbraith,et al.  Genome Structures and Halophyte-Specific Gene Expression of the Extremophile Thellungiella parvula in Comparison with Thellungiella salsuginea (Thellungiella halophila) and Arabidopsis1[W] , 2010, Plant Physiology.

[118]  A. Fernie,et al.  The use of metabolomics to dissect plant responses to abiotic stresses , 2012, Cellular and Molecular Life Sciences.

[119]  William R. Raun,et al.  Improving Nitrogen Use Efficiency for Cereal Production , 1999 .

[120]  N. Grassly,et al.  United Nations Department of Economic and Social Affairs/population Division , 2022 .