Skip to main content
SpringerLink
Log in

Transcriptional and metabolic changes in the desiccation tolerant plant Craterostigma plantagineum during recurrent exposures to dehydration

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Multiple dehydration/rehydration treatments improve the adaptation of Craterostigma plantagineum to desiccation by accumulating stress-inducible transcripts, proteins and metabolites. These molecules serve as stress imprints or memory and can lead to increased stress tolerance.

It has been reported that repeated exposure to dehydration may generate stronger reactions during a subsequent dehydration treatment in plants. This stimulated us to address the question whether the desiccation tolerant resurrection plant Craterostigma plantagineum has a stress memory. The expression of four representative stress-related genes gradually increased during four repeated dehydration/rehydration treatments in C. plantagineum. These genes reflect a transcriptional memory and are trainable genes. In contrast, abundance of chlorophyll synthesis/degradation-related transcripts did not change during dehydration and remained at a similar level as in the untreated tissues during the recovery phase. During the four dehydration/rehydration treatments the level of ROS pathway-related transcripts, superoxide dismutase (SOD) activity, proline, and sucrose increased, whereas H2O2 content and electrolyte leakage decreased. Malondialdehyde (MDA) content did not change during the dehydration, which indicates a gain of stress tolerance. At the protein level, increased expression of four representative stress-related proteins showed that the activated stress memory can persist over several days. The phenomenon described here could be a general feature of dehydration stress memory responses in resurrection plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

Abbreviations

ALAD:

5-Aminolevulinic acid dehydratase

APX:

Ascorbate peroxidase

BHT:

Butylated hydroxytoluene

CAT:

Catalase

CHLG:

Chlorophyll synthase

CHLM:

Mg-protoporphyrin IX methyltransferase

CPO:

Coprogen oxidase

Cu/Zn-SOD:

Copper/zinc superoxide dismutase

EDR1:

Early dehydration responsive 1

EF1a:

Elongation factor 1-alpha

GC/MS:

Gas chromatography/mass spectrometry

GSA:

Glutamate-1-semialdehyde aminotransferase

LEA:

Late embryogenesis abundant

MDA:

Malondialdehyde

Mn-SOD:

Manganese superoxide dismutase

NBT:

4-Nitro-blue tetrazolium chloride

NYE1:

Non-yellowing 1

OD:

Optical density

PaO:

Pheophorbide a oxygenase

PBGD:

Porphobilinogen deaminase

PPH:

Pheophytinase

RCCR:

Red chlorophyll catabolite reductase

ROS:

Reactive oxygen species

RWC:

Relative water content

SOD:

Superoxide dismutase

TBA:

Thiobarbituric acid

References

  • Alvarez-Venegas R, Abdallat AA, Guo M, Alfano JR, Avramova Z (2007) Epigenetic control of a transcription factor at the cross section of two antagonistic pathways. Epigenetics 2:106–113

    Article  PubMed  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Avramova Z (2015) Transcriptional ‘memory’ of a stress: transient chromatin and memory (epigenetic) marks at stress-response genes. Plant J 83:149–159

    Article  CAS  PubMed  Google Scholar 

  • Bartels D, Schneider K, Terstappen G, Piatkowski D, Salamini F (1990) Molecular cloning of abscisic acid-modulated genes which are induced during desiccation of the resurrection plant Craterostigma plantagineum. Planta 181:27–34

    Article  CAS  PubMed  Google Scholar 

  • Bianchi G, Gamba A, Murelli C, Salamini F, Bartels D (1991) Novel carbohydrate metabolism in the resurrection plant Craterostigma plantagineum. Plant J 1:355–359

    Article  PubMed  Google Scholar 

  • Blum A (2017) Osmotic adjustment is a prime drought stress adaptive engine in support of plant production. Plant, Cell Environ 40:4–10

    Article  CAS  Google Scholar 

  • Bruce TJ, Matthes MC, Napier JA, Pickett JA (2007) Stressful “memories” of plants: evidence and possible mechanisms. Plant Sci 173:603–608

    Article  CAS  Google Scholar 

  • Challabathula D, Djilianov D, Bartels D (2012) Photosynthesis in desiccation tolerant plants: energy metabolism and antioxidative stress defense. Plant Sci 182:29–41

    Article  CAS  Google Scholar 

  • Challabathula D, Zhang Q, Bartels D (2018) Protection of photosynthesis in desiccation-tolerant resurrection plants. J Plant Physiol 227:84–92

    Article  CAS  PubMed  Google Scholar 

  • Chen K, Arora R (2012) Priming memory invokes seed stress-tolerance. Environ Exp Bot 94:33–45

    Article  CAS  Google Scholar 

  • Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12:133–139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding Y, Fromm M, Avramova Z (2012) Multiple exposures to drought ‘train’ transcriptional responses in Arabidopsis. Nat Commun 3:740

    Article  CAS  PubMed  Google Scholar 

  • Ding Y, Liu N, Virlouvet L, Riethoven JJ, Fromm M, Avramova Z (2013) Four distinct types of dehydration stress memory genes in Arabidopsis thaliana. BMC Plant Biol 13:229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fleta-Soriano E, Munné-Bosch S (2016) Stress memory and the inevitable effects of drought: a physiological perspective. Front Plant Sci 7:143

    Article  PubMed  PubMed Central  Google Scholar 

  • Giarola V, Challabathula D, Bartels D (2015) Quantification of expression of dehydrin isoforms in the desiccation tolerant plant Craterostigma plantagineum using specifically designed reference genes. Plant Sci 236:103–115

    Article  CAS  PubMed  Google Scholar 

  • Goh CH, Nam HG, Park YS (2003) Stress memory in plants: a negative regulation of stomatal response and transient induction of rd22 gene to light in abscisic acid-entrained Arabidopsis plants. Plant J 36:240–255

    Article  CAS  PubMed  Google Scholar 

  • Hilker M, Schwachtje J, Baier M, Balazadeh S, Bäurle I, Geiselhardt S, Hincha DK, Kunze R, Mueller-Roeber B, Rillig MC, Rolff J (2016) Priming and memory of stress responses in organisms lacking a nervous system. Biol Rev 91:1118–1133

    Article  PubMed  Google Scholar 

  • Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611

    Article  CAS  Google Scholar 

  • Hu L, Wang Z, Du H, Huang B (2010) Differential accumulation of dehydrins in response to water stress for hybrid and common bermudagrass genotypes differing in drought tolerance. J Plant Physiol 167:103–109

    Article  CAS  PubMed  Google Scholar 

  • Hu L, Li H, Pang H, Fu J (2012) Responses of antioxidant gene, protein and enzymes to salinity stress in two genotypes of perennial ryegrass (Lolium perenne) differing in salt tolerance. J Plant Physiol 169:146–156

    Article  CAS  PubMed  Google Scholar 

  • Hu T, Jin Y, Li H, Amombo E, Fu J (2016) Stress memory induced transcriptional and metabolic changes of perennial ryegrass (Lolium perenne) in response to salt stress. Physiol Plant 156:54–69

    Article  CAS  PubMed  Google Scholar 

  • Kotchoni SO, Kuhns C, Ditzer A, Kirch HH, Bartels D, Kirch HH (2006) Over-expression of different aldehyde dehydrogenase genes in Arabidopsis thaliana confers tolerance to abiotic stress and protects plants against lipid peroxidation and oxidative stress. Plant Cell Environ 29:1033–1048

    Article  CAS  PubMed  Google Scholar 

  • Kozlowski TT, Pallardy SG (2002) Acclimation and adaptive responses of woody plants to environmental stresses. Bot Rev 68:270–334

    Article  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  PubMed  Google Scholar 

  • Li RH, Guo PG, Michael B, Stefania G, Salvatore C (2006) Evaluation of chlorophyll content and fluorescence parameters as indicators of drought tolerance in barley. Agric Sci China 5:751–757

    Article  CAS  Google Scholar 

  • Li X, Cai J, Liu F, Dai T, Cao W, Jiang D (2014) Cold priming drives the sub-cellular antioxidant systems to protect photosynthetic electron transport against subsequent low temperature stress in winter wheat. Plant Physiol Biochem 82:34–43

    Article  CAS  PubMed  Google Scholar 

  • Li X, Topbjerg HB, Jiang D, Liu F (2015) Drought priming at vegetative stage improves the antioxidant capacity and photosynthesis performance of wheat exposed to a short-term low temperature stress at jointing stage. Plant Soil 393:307–318

    Article  CAS  Google Scholar 

  • Liu X, Chan Z (2015) Application of potassium polyacrylate increases soil water status and improves growth of bermudagrass (Cynodon dactylon) under drought stress condition. Sci Hortic Amst 197:705–711

    Article  CAS  Google Scholar 

  • Liu N, Ding Y, Fromm M, Avramova Z (2014) Different gene-specific mechanisms determine the ‘revised-response’ memory transcription patterns of a subset of A. thaliana dehydration stress responding genes. Nucleic Acids Res 42:5556–5566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu N, Staswick PE, Avramova Z (2016) Memory responses of jasmonic acid-associated Arabidopsis genes to a repeated dehydration stress. Plant Cell Environ 39:2515–2529

    Article  CAS  PubMed  Google Scholar 

  • Lu S, Chen C, Wang Z, Guo Z, Li H (2009) Physiological responses of somaclonal variants of triploid bermudagrass (Cynodon transvaalensis × Cynodon dactylon) to drought stress. Plant Cell Rep 28:517–526

    Article  CAS  PubMed  Google Scholar 

  • Michel D, Furini A, Salamini F, Bartels D (1994) Structure and regulation of an ABA- and desiccation-responsive gene from the resurrection plant Craterostigma plantagineum. Plant Mol Biol 24:549–560

    Article  CAS  PubMed  Google Scholar 

  • Missihoun TD (2011) Characterisation of selected Arabidopsis aldehyde dehydrogenase genes: role in plant stress physiology and regulation of gene expression. Dissertation, University of Bonn

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  CAS  PubMed  Google Scholar 

  • Niinemets Ü, Kahru A, Mander Ü, Nõges P, Nõges T, Tuvikene A, Vasemägi A (2017) Interacting environmental and chemical stresses under global change in temperate aquatic ecosystems: stress responses, adaptation, and scaling. Reg Environ Change 17:2061–2077

    Article  Google Scholar 

  • Pintó-Marijuan M, Cotado A, Fleta-Soriano E, Munné-Bosch S (2017) Drought stress memory in the photosynthetic mechanisms of an invasive CAM species, Aptenia cordifolia. Photosynth Res 131:241–253

    Article  CAS  PubMed  Google Scholar 

  • Quan W, Liu X, Wang H, Chan Z (2016a) Comparative physiological and transcriptional analyses of two contrasting drought tolerant alfalfa varieties. Front Plant Sci 6:1256

    Article  PubMed  PubMed Central  Google Scholar 

  • Quan W, Liu X, Wang H, Chan Z (2016b) Physiological and transcriptional responses of contrasting alfalfa (Medicago sativa L.) varieties to salt stress. Plant Cell Tissue Org 126:105–115

    Article  CAS  Google Scholar 

  • Ramírez DA, Rolando JL, Yactayo W, Monneveux P, Mares V, Quiroz R (2015) Improving potato drought tolerance through the induction of long-term water stress memory. Plant Sci 238:26–32

    Article  CAS  PubMed  Google Scholar 

  • Savvides A, Ali S, Tester M, Fotopoulos V (2016) Chemical priming of plants against multiple abiotic stresses: mission possible? Trends Plant Sci 21:329–340

    Article  CAS  PubMed  Google Scholar 

  • Shi H, Wang Y, Cheng Z, Ye T, Chan Z (2012) Analysis of natural variation in bermudagrass (Cynodon dactylon) reveals physiological responses underlying drought tolerance. PLoS One 7:e53422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi H, Ye T, Chan Z (2014) Nitric oxide-activated hydrogen sulfide is essential for cadmium stress response in bermudagrass (Cynodon dactylon (L). Pers.). Plant Physiol Bioch 74:99–107

    Article  CAS  Google Scholar 

  • Sinclair BJ, Roberts SP (2005) Acclimation, shock and hardening in the cold. J Therm Biol 30:557–562

    Article  Google Scholar 

  • Sun RZ, Lin CT, Zhang XF, Duan LX, Qi XQ, Gong YH, Deng X (2018) Acclimation-induced metabolic reprogramming contributes to rapid desiccation tolerance acquisition in Boea hygrometrica. Environ Exp Bot 148:70–84

    Article  CAS  Google Scholar 

  • Todaka D, Zhao Y, Yoshida T, Kudo M, Kidokoro S, Mizoi J, Kodaira KS, Takebayashi Y, Kojima M, Sakakibara H, Toyooka K (2017) Temporal and spatial changes in gene expression, metabolite accumulation and phytohormone content in rice seedlings grown under drought stress conditions. Plant J 90:61–78

    Article  CAS  PubMed  Google Scholar 

  • Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valenzuela-Avendaño JP, Mota IA, Uc GL, Perera RS, Valenzuela-Soto EM, Aguilar JJ (2005) Use of a simple method to isolate intact RNA from partially hydrated Selaginella lepidophylla plants. Plant Mol Biol Rep 23:199–200

    Article  Google Scholar 

  • Van den Dries N, Facchinelli F, Giarola V, Phillips JR, Bartels D (2011) Comparative analysis of LEA-like 11-24 gene expression and regulation in related plant species within the Linderniaceae that differ in desiccation tolerance. New Phytol 190:75–88

    Article  CAS  PubMed  Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66

    Article  CAS  Google Scholar 

  • Virlouvet L, Fromm M (2015) Physiological and transcriptional memory in guard cells during repetitive dehydration stress. New Phytol 205:596–607

    Article  CAS  PubMed  Google Scholar 

  • Walter J, Nagy L, Hein R, Rascher U, Beierkuhnlein C, Willner E, Jentsch A (2011) Do plants remember drought? Hints towards a drought-memory in grasses. Environ Exp Bot 71:34–40

    Article  Google Scholar 

  • Wang X, Vignjevic M, Jiang D, Jacobsen S, Wollenweber B (2014) Improved tolerance to drought stress after anthesis due to priming before anthesis in wheat (Triticum aestivum L.) var. Vinjett. J Exp Bot 65:6441–6456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Vigjevic M, Liu F, Jacobsen S, Jiang D, Wollenweber B (2015) Drought priming at vegetative growth stages improves tolerance to drought and heat stresses during grain filling in spring wheat. Plant Growth Regul 75:677–687

    Article  CAS  Google Scholar 

  • Yoo CY, Pence HE, Jin JB, Miura K, Gosney MJ, Hasegawa PM, Mickelbart MV (2010) The Arabidopsis GTL1 transcription factor regulates water use efficiency and drought tolerance by modulating stomatal density via transrepression of SDD1. Plant Cell 22:4128–4141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Q, Linnemann TV, Schreiber L, Bartels D (2016) The role of transketolase and octulose in the resurrection plant Craterostigma plantagineum. J Exp Bot 67:3551–3559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Du H, Wang Z, Huang B (2011) Identification of proteins associated with water-deficit tolerance in C4 perennial grass species, Cynodon dactylon × Cynodon transvaalensis and Cynodon dactylon. Physiol Plant 141:40–55

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Missihoun TD, Bartels D (2017) The role of Arabidopsis aldehyde dehydrogenase genes in response to high temperature and stress combinations. J Exp Bot 68:4295–4308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Xun Liu is supported by the China Scholarship Council (2016-2020). Dinakar C acknowledges the support from the Indian National Science Academy (INSA-India) and Deutsche Forschungsgemeinschaft-GZ:BA712/19-1 (DFG, Germany). The authors would like to thank Christiane Buchholz for growing the plants and Prof. Dr. Lukas Schreiber and Dr. Viktoria Zeisler-Diehl (IZMB, University of Bonn) for supporting the measurements of sucrose and octulose.

Author information

Authors and Affiliations

  1. Institute of Molecular Physiology and Biotechnology of Plants (IMBIO), University of Bonn, Kirschallee 1, 53115, Bonn, Germany

    Xun Liu & Dorothea Bartels

  2. Department of Life Sciences, School of Basic and Applied Sciences, Central University of Tamil Nadu, Thiruvarur, India

    Dinakar Challabathula

  3. Key Laboratory for Quality Control of Characteristic Fruits and Vegetables of Hubei Province, College of Life Science and Technology, Hubei Engineering University, Xiaogan, 432000, Hubei, China

    Wenli Quan

Authors
  1. Xun Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dinakar Challabathula
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wenli Quan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dorothea Bartels
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dorothea Bartels.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

Thin layer chromatography of sugars extracted from C. plantagineum leaves

Fig. S2

(a) The chromatogram of sucrose (peak 3) and octulose (peak 2) extracted from C. plantagineum leaves, and the internal standard xylitol (peak 1). The fragmentation patterns of xylitol (b), octulose (c) and sucrose (d)

Supplementary material 3 (DOCX 18 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, X., Challabathula, D., Quan, W. et al. Transcriptional and metabolic changes in the desiccation tolerant plant Craterostigma plantagineum during recurrent exposures to dehydration. Planta 249, 1017–1035 (2019). https://doi.org/10.1007/s00425-018-3058-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-018-3058-8

Keywords

Search

Navigation