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Light response, oxidative stress management and nucleic acid stability in closely related Linderniaceae species differing in desiccation tolerance

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Abstract

In the present study, three closely related Linderniaceae species which differ in their sensitivity to desiccation are compared in response to light and oxidative stress defence. Lindernia brevidens, a desiccation-tolerant plant, displayed intense purple pigmentation in leaves under long-day conditions in contrast to Craterostigma plantagineum (desiccation tolerant) and Lindernia subracemosa (desiccation sensitive). The intense pigmentation in leaves does not affect the desiccation tolerance behaviour but seems to be related to oxidative stress protection. Green leaves of short-day and purple leaves of long-day plants provided suitable material for comparing basic photosynthetic parameters. An increase in non-photochemical quenching in purple leaves appears to prevent photoinhibition. Treatment with methyl viologen decreased the photochemical activities in both long-day and short-day plants but long-day plants which accumulate anthocyanins maintained a higher non-photochemical quenching than short-day plants. No differences were seen in the expression of desiccation-induced proteins and proteins involved in carbohydrate metabolism in short-day and long-day grown plants, whereas differences were observed in the expression of transcripts encoding chloroplast-localised stress proteins and transcripts encoding antioxidant enzymes. While the expression of genes encoding antioxidant enzymes were either constitutive or up-regulated during desiccation in C. plantagineum, the expression was down-regulated in L. subracemosa. RNA expression analysis indicated degradation of mRNA during desiccation in L. subracemosa but not in desiccation tolerant species. These results indicate that a better oxidative stress management and mRNA stability are correlated with desiccation tolerance.

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Abbreviations

APX:

Ascorbate peroxidase

CAT:

Catalase

GR:

Glutathione reductase

MDAR:

Monodehydroascorbate reductase

ROS:

Reactive oxygen species

RT-PCR:

Reverse transcriptase polymerase chain reaction

RWC:

Relative water content

SOD:

Superoxide dismutase

References

  • Adams WW, Demmig-Adams B, Rosenstiel TN, Ebbert V (2001) Dependence of photosynthesis and energy dissipation activity upon growth form and light environment during the winter. Photosynth Res 67:51–62

    Article  PubMed  CAS  Google Scholar 

  • Albert NW, Lewis DH, Zhang H, Irving LJ, Jameson PE, Davies KM (2009) Light-induced vegetative anthocyanin pigmentation in Petunia. J Exp Bot 60:2191–2202

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Archetti M, Döring TF, Hagen SB, Hughes NM, Leather SR, Lee DW, Lev-Yadun S, Manetas Y, Ougham HJ, Schaberg PG, Thomas H (2009) Unravelling the evolution of autumn colours: an interdisciplinary approach. Trends Ecol Evol 24:166–173

    Article  PubMed  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  PubMed  CAS  Google Scholar 

  • Bartels D, Hussain SS (2011) Resurrection plants: physiology and molecular biology. In: Lüttge U, Beck E, Bartels D (eds) Plant desiccation tolerance. Ecological studies, vol 215. Heidelberg, Springer, pp 339–364

  • 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  Google Scholar 

  • Bartels D, Hanke C, Schneider K, Michel D, Salamini F (1992) A desiccation-related ELIP-like gene from the resurrection plant Craterostigma plantagineum is regulated by light and ABA. EMBO J 11:2771–2778

    PubMed  CAS  Google Scholar 

  • Bartels D, Ditzer A, Furini A (2006) What can we learn from resurrection plants? In: Ribaut JM (ed) Drought adaptation in cereals. Hayworth, New York, pp 599–622

    Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  PubMed  CAS  Google Scholar 

  • Becker B, Holtgrefe S, Jung S, Wunrau C, Kandlbinder A, Baier M, Dietz KJ, Backhausen JE, Scheibe R (2006) Influence of the photoperiod on redox regulation and stress responses in Arabidopsis thaliana L. (Henyh.) plants under long- and short-day conditions. Planta 224:380–393

    Article  PubMed  CAS  Google Scholar 

  • Bernacchia G, Schwall G, Lottspeich F, Salamini F, Bartels D (1995) The transketolase gene family of the resurrection plant Craterostigma plantagineum: differential expression during the rehydration phase. EMBO J 14:610–618

    PubMed  CAS  Google Scholar 

  • Bradford MM (1976) Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Chalker-Scott L (1999) Environmental significance of anthocyanins in plant stress responses. Photochem Photobiol 70:1–9

    Article  CAS  Google Scholar 

  • Cooper K, Farrant JM (2002) Recovery of the resurrection plant Craterostigma wilmsii from desiccation: protection versus repair. J Exp Bot 53:1805–1813

    Article  PubMed  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW III (1992) Photoprotection and other responses of plants to high light stress. Ann Rev Plant Physiol Plant Mol Biol 43:599–626

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097

    PubMed  CAS  Google Scholar 

  • Djilianov D, Ivanov S, Moyankova D, Miteva L, Kirova E, Alexieva V, Joudi M, Peshev D, Van den Ende W (2011) Sugar ratios, glutathione redox status and phenols in the resurrection species Haberlea rhodopensis and the closely related non-resurrection species Chirita eberhardtii. Plant Biol 13:767–776

    Article  PubMed  CAS  Google Scholar 

  • Ebbert V, Demmig-Adams B, Adams WWIII, Mueh KE, Staehelin LA (2001) Correlation between persistent forms of zeaxanthin-dependent energy dissipation and thylakoid protein phosphorylation. Photosynth Res 67:63–78

    Article  PubMed  CAS  Google Scholar 

  • Farrant JM (2000) Comparison of mechanisms of desiccation tolerance among three angiosperm resurrection plants. Plant Ecol 151:29–39

    Article  Google Scholar 

  • Farrant JM, Moore JP (2011) Programming desiccation-tolerance: from plants to seeds to resurrection plants. Curr Opin Plant Biol 14:340–345

    Article  PubMed  CAS  Google Scholar 

  • Farrant JM, Vander Willigen C, Loffell DA, Bartsch S, Whittaker A (2003) An investigation into the role of light during desiccation of three angiosperm resurrection plants. Plant Cell Environ 26:1275–1286

    Article  CAS  Google Scholar 

  • Fischer E (1992) Systematik der afrikanischen Lindernieae (Scrophulariaceae). Trop Subtrop Pflanzenwelt 81:1–365

    Google Scholar 

  • Franceschi VR, Grimes HD (1991) Induction of soybean vegetative storage proteins and anthocyanins by low-level atmospheric methyl jasmonate. Proc Nat Acad Sci USA 88:6745–6749

    Article  PubMed  CAS  Google Scholar 

  • Furini A, Koncz C, Salamini F, Bartels D (1997) High level transcription of a member of a repeated gene family confers dehydration tolerance to callus tissue of Craterostigma plantagineum. EMBO J 16:3599–3608

    Article  PubMed  CAS  Google Scholar 

  • Gaff DF (1977) Desiccation tolerant vascular plants of Southern Africa. Oecologia 31:95–109

    Article  Google Scholar 

  • Georgieva K, Lenk S, Buschmann C (2008) Responses of the resurrection plant Haberlea rhodopensis to high irradiance. Photosynthetica 46:208–215

    Article  Google Scholar 

  • Georgieva K, Sarvari E, Keresztes A (2010) Protection of thylakoids against combined light and drought by a luminal substance in the resurrection plant Haberlea rhodopensis. Ann Bot 105:117–126

    Article  PubMed  CAS  Google Scholar 

  • Gerlach WL, Bedbrook JR (1979) Cloning and characterization of ribosomal RNA genes from wheat and barley. Nucleic Acids Res 7:1869–1885

    Article  PubMed  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  PubMed  CAS  Google Scholar 

  • Gould KS, Dudle DA, Neufeld HS (2010) Why some stems are red: cauline anthocyanins shield photosystem II against high light stress. J Exp Bot 61:2701–2717

    Article  Google Scholar 

  • Grace SC, Logan BA (1996) Acclimation of foliar antioxidant systems to growth irradiance in three broad-leaved evergreen species. Plant Physiol 112:1631–1640

    PubMed  CAS  Google Scholar 

  • Harmer SL (2009) The circadian system in higher plants. Annu Rev Plant Biol 60:357–377

    Article  PubMed  CAS  Google Scholar 

  • Hoekstra FA, Golovina EA, Tetteroo FA, Wolkers WF (2001) Induction of desiccation tolerance in plant somatic embryos: how exclusive is the protective role of sugars? Cryobiology 43:140–150

    Article  PubMed  CAS  Google Scholar 

  • Hughes NM (2011) Winter leaf reddening in evergreen species. New Phytol 190:573–581

    Article  PubMed  Google Scholar 

  • Kleines M, Elster RC, Rodrigo MJ, Blervacq AS, Salamini F, Bartels D (1999) Isolation and expression analysis of two stress-responsive sucrose-synthase genes from the resurrection plant Craterostigma plantagineum (Hochst.). Planta 209:13–24

    Article  PubMed  CAS  Google Scholar 

  • Kranner I, Beckett RP, Wornik S, Zorn S, Pfeifhofer HW (2002) Revival of a resurrection plant correlates with its antioxidant status. Plant J 31:13–24

    Article  PubMed  CAS  Google Scholar 

  • Krol M, Gray GR, Hurry VM, Öquist G, Malek L, Huner NPA (1995) Low-temperature stress and photoperiod effect an increased tolerance to photoinhibition in Pinus banksiana seedlings. Can J Bot 73:1119–1127

    Article  CAS  Google Scholar 

  • Kyparissis A, Grammatikopoulos G, Manetas Y (2007) Leaf morphological and physiological adjustments to the spectrally selective shade imposed by anthocyanins in Prunus cerasifera. Tree Physiol 27:849–857

    Article  PubMed  CAS  Google Scholar 

  • Kytridis VP, Manetas Y (2006) Mesophyll versus epidermal anthocyanin as potential in vivo antioxidants: evidence linking the putative antioxidant role to the proximity of oxy-radical source. J Exp Bot 57:2203–2210

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Latowski D, Kuczyńska P, Strzałka K (2011) Xanthophyll cycle—a mechanism protecting plants against oxidative stress. Redox Rep 16:78–90

    Article  PubMed  CAS  Google Scholar 

  • Logan BA, Demmig-Adams B, Adams WWIII, Grace S (1998a) Antioxidants and xanthophyll cycle-dependant energy dissipation in Cucurbita pepo L. and Vinca major L. acclimated to four growth PPFDs in the field. J Exp Bot 49:1869–1879

    CAS  Google Scholar 

  • Logan BA, Grace SC, Adams WW III, Demmig-Adams B (1998b) Seasonal differences in xanthophyll cycle characteristics and antioxidant in Mahonia repens growing in different light environments. Oecologia 116:9–17

    Google Scholar 

  • Lücker J, Laszczak M, Smith D, Lund ST (2009) Generation of a predicted protein database from EST data and application to iTRAQ analyses in grape (Vitis vinifera cv. Cabernet Sauvignon) berries at ripening initiation. BMC Genomics 10:50

    Article  PubMed  Google Scholar 

  • Manetas Y (2006) Why some leaves are anthocyanic and why most anthocyanic leaves are red? Flora 201:163–177

    Article  Google Scholar 

  • Meesters C (2008) Expressionstudien für Gene des Zuckerstoffwechsels der austrocknungstoleranten Pflanze Craterostigma plantagineum. Diploma thesis, University of Bonn

  • 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  PubMed  CAS  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Moore JP, Le NT, Brandt WF, Driouich A, Farrant JM (2009) Towards a systems-based understanding of plant desiccation tolerance. Trends Plant Sci 14:110–117

    Article  PubMed  CAS  Google Scholar 

  • Mowla SB, Thomson JA, Farrant JM, Mundree SG (2002) A novel stress-inducible antioxidant enzyme identified from the resurrection plant Xerophyta viscosa Baker. Planta 215:716–726

    Article  PubMed  CAS  Google Scholar 

  • Neill SO, Gould KS, Kilmartin PA, Mitchell KA, Markham KR (2002) Antioxidant activities of red versus green leaves in Elatostema rugosum. Plant Cell Environ 25:539–547

    Article  CAS  Google Scholar 

  • Oliver MJ, Bewley JD (1997) Desiccation tolerance of plant tissues: a mechanistic overview. Hortic Rev 18:171–214

    Google Scholar 

  • Oliver MJ, Wood AJ, O’Mahony P (1998) To dryness and beyond- preparation for the dried state and rehydration in vegetative desiccation-tolerant plants. Plant Growth Regul 24:193–201

    Article  CAS  Google Scholar 

  • Phillips JR, Hilbricht T, Salamini F, Bartels D (2002) A novel abscisic acid- and dehydration-responsive gene family from the resurrection plant Craterostigma plantagineum encodes a plastid-targeted protein with DNA-binding activity. Planta 215:258–266

    Article  PubMed  CAS  Google Scholar 

  • Phillips JR, Fischer E, Baron M, van den Dries N, Facchinelli F, Kutzer M, Rahmanzadeh R, Remus D, Bartels D (2008) Lindernia brevidens: a novel desiccation-tolerant vascular plant, endemic to ancient tropical rainforests. Plant J 54:938–948

    Article  PubMed  CAS  Google Scholar 

  • Porembski S (2011) Evolution, diversity, and habitats of Poikilohydrous vascular plants. In: Lüttge U, Beck E, Bartels D (eds) Plant desiccation tolerance. Ecological studies, vol 215. Heidelberg, Springer, pp 139–154

  • Rahmanzadeh R, Müller K, Fischer E, Bartels D, Borsch T (2005) The Linderniaceae and Gratiolaceae are further lineages distinct from the Scrophulariaceae (Lamiales). Plant Biol 7:1–12

    Article  Google Scholar 

  • Rodriguez MCS, Edsgard D, Hussain SS, Alquezar D, Rasmussen M, Gilbert T, Nielsen BH, Bartels D, Mundy J (2010) Transcriptomes of the desiccation-tolerant resurrection plant Craterostigma plantagineum. Plant J 63:212–228

    Article  PubMed  CAS  Google Scholar 

  • Röhrig H, Colby T, Schmidt J, Harzen A, Facchinelli F, Bartels D (2008) Analysis of desiccation-induced candidate phosphoproteins from Craterostigma plantagineum isolated with a modified metal oxide affinity chromatography procedure. Proteomics 8:3548–3560

    Article  PubMed  Google Scholar 

  • Rucinska R, Waplak S, Gwozdz E (1999) Free radical formation and activity of antioxidant enzymes in lupin roots exposed to lead. Plant Physiol Biochem 37:187–194

    Article  CAS  Google Scholar 

  • Salin ML, Bridges SM (1981) Absence of iron-containing superoxide dismutase in mitochondria from mustard (Brassica campestris). Biochem J 195:229–233

    PubMed  CAS  Google Scholar 

  • Sankhalkar S, Sharma PK (2005) Photoinhibition of photosynthesis: role of abscisic acid and antioxidants. Physiol Mol Biol Plants 11:275–289

    CAS  Google Scholar 

  • Scheibe R, Beck E (2011) Drought, desiccation, and oxidative stress. In: Lüttge U, Beck E, Bartels D (eds) Plant desiccation tolerance. Ecological studies, vol 215. Heidelberg, Springer, pp 209–231

  • Schneider K, Wells B, Schmelzer E, Salamini F, Bartels D (1993) Desiccation leads to the rapid accumulation of both cytosolic and chloroplastic proteins in the resurrection plant Craterostigma plantagineum Hochst. Planta 189:120–131

    Article  CAS  Google Scholar 

  • Sherwin HW, Farrant JM (1998) Protection mechanism against excess light in the resurrection plants Craterostigma wilmsii and Xerophyta viscose. Plant Growth Regul 24:203–210

    Article  CAS  Google Scholar 

  • Smirnoff N (1993) Role of active oxygen in the response of plants to water deficits and desiccation. New Phytol 125:27–58

    Article  CAS  Google Scholar 

  • Stafford HA (1994) Anthocyanins and betalains: evolution of the mutually exclusive pathways. Plant Sci 10:91–98

    Article  Google Scholar 

  • Steyn WJ, Wand SJE, Holcroft DM, Jacobs G (2002) Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. New Phytol 155:349–361

    Article  CAS  Google Scholar 

  • Tanaka Y, Sasaki N, Ohmiya A (2008) Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J 54:733–749

    Article  PubMed  CAS  Google Scholar 

  • Valenzuela-Avendaño JP, Estrada IA, Lizama G, Souza R, Valenzuela-Soto EM, Zuniga-Aguilar JJ (2005) Use of a simple method to isolate intact RNA from partially hydrated Selaginella lepidophylla plants. Plant Mol Biol Rep 23:199a–199g

    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  Google Scholar 

  • Velez-Ramirez AI, van Leperen W, Vreugdenhil D, Millenaar FF (2011) Plants under continuous light. Trends Plant Sci 16:310–318

    Article  PubMed  CAS  Google Scholar 

  • Zeliou K, Manetas Y, Petropoulou Y (2009) Transient winter leaf reddening in Cistus creticus characterizes weak (stress-sensitive) individuals, yet anthocyanins cannot alleviate the adverse effects on photosynthesis. J Exp Bot 60:3031–3042

    Article  PubMed  CAS  Google Scholar 

  • Zhang KM, Yu HJ, Shi K, Zhou YH, Yu JQ, Xia XJ (2010) Photoprotective roles of anthocyanins in Begonia semperflorens. Plant Sci 179:202–208

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Katrin Hesse and Christiane Buchholz for technical support and providing plant material.

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Correspondence to Dorothea Bartels.

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Dinakar, C., Bartels, D. Light response, oxidative stress management and nucleic acid stability in closely related Linderniaceae species differing in desiccation tolerance. Planta 236, 541–555 (2012). https://doi.org/10.1007/s00425-012-1628-8

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