Skip to main content

Advertisement

Log in

Ectopic expression of a rice transcription factor, Mybleu, enhances tolerance of transgenic plants of Carrizo citrange to low oxygen stress

  • Original Paper
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

Oxygen deficit, which occurs in flooded or poorly drained soils, can limit plant growth and development. Low-oxygen environmental conditions also limit the distribution of many woody plants, such as citrus trees, which are considered flood-sensitive crops, although tolerance to this stress varies among genotypes and rootstocks. In this study, the rice transcription factor Mybleu was inserted into the pGA470 plant cloning vector and transferred into the epicotyl explants of the Carrizo citrange rootstock (Citrus sinensis × Poncirus trifoliata) using Agrobacterium tumefaciens-mediated transformation. The transgenic lines were confirmed for the presence and expression of the transgene, and physiological, biochemical and molecular parameters were evaluated for adaptation to hypoxic and anoxic stress conditions. The ectopic expression of Mybleu increased tolerance to oxygen deprivation in the transgenic lines, contributing to increased viability under this stress condition. This improved tolerance correlates with, and may depend on, the induction of genes and the activation of enzymes from various fermentation and carbohydrate metabolic pathways, antioxidant systems and nonsymbiotic haemoglobin-nitric oxide homeostasis mechanisms. Together, our data suggest a key role for Mybleu in coordinating the multifaceted plant response to low oxygen stress and the conservation of Mybleu-regulated pathways among species.

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

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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

Instant access to the full article PDF.

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

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Abbreviations

BA:

6-benzyladenine

CaMV:

Cauliflower mosaic virus

DTT:

Dithiothreitol

References

  • Agarwal S, Sairam RK, Srivastava GC, Meena RC (2005) Changes in antioxidant enzymes activity and oxidative stress by abscisic acid and salicylic acid in wheat genotypes. Biol Plantarum 49:541–550

    Article  CAS  Google Scholar 

  • Agarwal S, Kapoor A, Lakshmi OS, Grover A (2007) Production and phenotypic analysis of rice transgenics with altered levels of pyruvate decarboxylase and alcohol dehydrogenase proteins. Plant Physiol Biochem 45:637–646

    Article  CAS  PubMed  Google Scholar 

  • An G, Watson BD, Stachel S, Gordon MP, Nester EW (1985) New cloning vehicles for transformation of higher plants. EMBO J 4:277–284

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arbona V, Hossain Z, Lopez-Climent MF, Perez-Clemente RM, Gomez-Cadenas A (2008) Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus. Physiol Plant 132:452–466

    Article  CAS  PubMed  Google Scholar 

  • Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59:313–339

    Article  CAS  PubMed  Google Scholar 

  • Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179–194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bowler C, Van Montagu M, Inzé D (1992) Superoxide dismutase and stress tolerance. Ann Rev Plant Physiol Plant Mol Biol 43:83–116

    Article  CAS  Google Scholar 

  • Branco-Price C, Kawaguchi R, Ferreira RB, Bailey-Serres J (2005) Genome-wide analysis of transcript abundance and translation in Arabidopsis seedlings subjected to oxygen deprivation. Ann Bot 96:647–660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clough SJ (2005) Floral dip Agrobacterium-mediated germ line transformation. In: Peña L (ed) Methods in molecular biology. Transgenic plants: methods and protocols. Humana press Inc, Totowa, pp 91–101

    Google Scholar 

  • Crawford NM, Guo F-Q (2005) New insights into nitric oxide metabolism and regulatory functions. Trends Plant Sci 10:195–200

    Article  CAS  PubMed  Google Scholar 

  • Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795

    Article  CAS  PubMed  Google Scholar 

  • Du H, Zhang L, Liu L, Tang XF, Yang WJ, Wu YM, Huang YB, Tang YX (2009) Biochemical and molecular characterization of plant MYB transcription factor family. Biochemistry (Moscow) 74:1–11

    Article  CAS  Google Scholar 

  • Gao F, Xiong A, Peng R, Jin X, Xu J, Zhu B, Chen J, Yao Q (2010) OsNAC52, a rice NAC transcription factor, potentially responds to ABA and confers drought tolerance in transgenic plants. Plant Cell Tissue Organ Cult 100:255–262

    Article  CAS  Google Scholar 

  • Gibbs J, Greenway H (2003) Mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism. Funct Plant Biol 30:1–47

    Article  CAS  Google Scholar 

  • Gibbs J, Morrell S, Valdez A, Setter TL, Greenway H (2000) Regulation of alcoholic fermentation in coleoptiles of two rice cultivars differing in tolerance to anoxia. J Exp Bot 51:785–796

    Article  CAS  PubMed  Google Scholar 

  • Girhepuje PV, Shinde GB (2011) Transgenic tomato plants expressing a wheat endochitinase gene demonstrate enhanced resistance to Fusarium oxysporum f. sp.lycopersici. Plant Cell Tissue Organ Cult 105:243–251

    Article  CAS  Google Scholar 

  • Hake S, Kelley PM, Taylor WC, Freeling M (1985) Coordinate induction of alcohol dehydrogenase 1, aldolase, and other anaerobic RNAs in maize. J Biol Chem 260:5050–5054

    CAS  PubMed  Google Scholar 

  • Havir EA, McHale NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84:450–455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He C, Yang A, Zhang W, Gao Q, Zhang J (2010) Improved salt tolerance of transgenic wheat by introducing betA gene for glycine betaine synthesis. Plant Cell Tissue Organ Cult 101:65–78

    Article  CAS  Google Scholar 

  • Hood EE, Gelvin SB, Melchers LS, Hoekema A (1993) New agrobacterium helper plasmids for gene transfer to plants. Transgenic Res 2:208–218

    Article  CAS  Google Scholar 

  • Hossain Z, Lopez-Climent MF, Arbona V, Perez-Clemente RM, Gomez-Cadenas A (2009) Modulation of the antioxidant system in citrus under waterlogging and subsequent drainage. J Plant Physiol 166:1391–1404

    Article  CAS  PubMed  Google Scholar 

  • Igamberdiev AU, Baron K, Manac’h-Little N, Stoimenova M, Hill RD (2005) The haemoglobin/nitric oxide cycle: involvement in flooding stress and effects on hormone signalling. Ann Bot 96:557–564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ismond KP, Dolferus R, De Pauw M, Dennis ES, Good AG (2003) Enhanced low oxygen survival in Arabidopsis through increased metabolic flux in the fermentative pathway. Plant Physiol 132:1292–1302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin T, Chang Q, Li W, Yin D, Li Z, Wang D, Liu B, Liu L (2010) Stress-inducible expression of GmDREB1 conferred salt tolerance in transgenic alfalfa. Plant Cell Tissue Organ Cult 100:219–227

    Article  CAS  Google Scholar 

  • Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozakil K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nature Biotech 17:287–291

    Article  CAS  Google Scholar 

  • Kozlowski TT (1997) Responses of woody plants to flooding and salinity. Tree Physiology Monograph No. 1. Heron Publishing, Victoria, Canada http://www.heronpublishing.com/tp/monograph/kozlowski.pdf

  • Li C, Bai T, Ma F, Han M (2010) Hypoxia tolerance and adaptation of anaerobic respiration to hypoxia stress in two Malus species. Scientia Hort. 124:274–279

    Article  CAS  Google Scholar 

  • Liao C-T, Lin C-H (2001) Physiological adaptation of crop plants to flooding stress. Proc Natl Sci Counc 25:148–157

    CAS  Google Scholar 

  • Licausi F (2011) Regulation of the molecular response to oxygen limitations in plants. New Phytol 190:550–555

    Article  CAS  PubMed  Google Scholar 

  • Licausi F, van Dongen J, Giuntoli B, Novi G, Santaniello A, Geigenberger P, Perata P (2010) HRE1 and HRE2, two hypoxia-inducible ethylene response factors, affect anaerobic responses in Arabidopsis thaliana. Plant J 62:302–315

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Guo X, Naeem MS, Liu D, Xu L, Zhang W, Tang G, Zhou W (2011) Transgenic Brassica napus L. lines carrying a two gene construct demonstrate enhanced resistance against Plutella xylostella and Sclerotinia sclerotiorum. Plant Cell Tissue Organ Cult 106:143–151

    Article  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lo Piero AR, Puglisi I, Rapisarda P, Petrone G (2005) Anthocyanins accumulation and related gene expression in red orange fruit induced by low temperature storage. J Agric Food Chem 53:9083–9088

    Article  CAS  PubMed  Google Scholar 

  • Locatelli F, Bracale M, Magaraggia F, Faoro F, Manzocchi LA, Coraggio I (2000) The product of the rice myb7 unspliced mRNA dimerizes with the maize leucine zipper Opaque2 and stimulates its activity in a transient expression assay. J Biol Chem 275:17619–17625

    Article  CAS  PubMed  Google Scholar 

  • Luth D, Moore G (1999) Transgenic grapefruit plants obtained by Agrobacterium tumefaciens-mediated transformation. Plant Cell Tissue Organ Cult 57:219–222

    Article  CAS  Google Scholar 

  • Magaraggia F, Solinas G, Valle G, Giovinazzo G, Coraggio I (1997) Maturation and translation mechanisms involved in the expression of a myb gene of rice. Plant Mol Biol 35:1003–1008

    Article  CAS  PubMed  Google Scholar 

  • Mahe A, Grisvard J, Dron M (1992) Fungal and plant specific gene markers to follow the bean anthracnose infection process and normalize a bean chitinase mRNA induction. Mol Plant-Microbe Interact 5:242–248

    Article  CAS  Google Scholar 

  • Mattana M, Vannini C, Espen L, Bracale M, Genga A, Marsoni M, Iriti M, Bonazza V, Romagnoli F, Baldoni E, Coraggio I, Locatelli F (2007) The rice Mybleu transcription factor increases tolerance to oxygen deprivation in Arabidopsis plants. Physiol Plant 131:106–121

    Article  CAS  PubMed  Google Scholar 

  • McCord JM (1999) Analysis of superoxide dismutase activity. In: Wiley, online library Current protocols in toxicology: 7.3.1–7.3.9

  • McElfresh KC, Chourey PS (1988) Anaerobiosis induces transcription but not translation of sucrose synthase in maize. Plant Physiol 87:542–546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Menguzzato E, Valle G, Coraggio I (1995) A myb encoding cDNA (Accession No. X89605) expressed in anaerobic rice presents features suggesting post transcriptional regulation. Plant Physiol 109:1498

    Google Scholar 

  • Morrell S, Greenway H, Davies DD (1990) Regulation of pyruvate decarboxylase in vitro and in vivo. J Exp Bot 41:131–139

    Article  CAS  Google Scholar 

  • Peña L, Cervera M, Juárez J, Ortega C, Pina JA, Durán-Vila N, Navarro L (1995) High efficiency Agrobacterium-mediated transformation and regeneration of citrus. Plant Sci 104:183–191

    Article  Google Scholar 

  • Peña L, Cervera M, Fagoaga C, Pérez R, Romero J, Pina JA, Navarro L (2004a) Agrobacterium-mediated transformation of citrus. In: Curtis IS (ed) Transgenic crops of the world–essential protocols. Kluwer, Dordrecht, pp 145–157

    Chapter  Google Scholar 

  • Peña L, Pérez R, Cervera M, Juàrez JA, Navarro L (2004b) Early events in Agrobacterium-mediated transformation of citrus explants. Ann Bot 94:67–74

    Article  PubMed  PubMed Central  Google Scholar 

  • Prashanth SR, Sadhasivam V, Parida A (2008) Over expression of cytosolic copper/zinc superoxide dismutase from a mangrove plant Avicennia marina in indica Rice var Pusa Basmati-1 confers abiotic stress tolerance. Transgenic Res 17:281–291

    Article  CAS  PubMed  Google Scholar 

  • Rao MV, Paliyath G, Ormrod DP (1996) Ultraviolet-B- and ozone-induced biochemical changes in antioxidants enzymes of Arabidopsis thaliana. Plant Physiol 110:125–136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reforgiato Recupero G, Russo G, Recupero S, Zurru R, Deidda B, Mulas M (2009) Horticultural evaluation of new citrus latipes hybrids as rootstocks for citrus. HortScience 44:595–598

    Google Scholar 

  • Ricard B, Rivoal J, Spiteri A, Pradet A (1991) Anaerobic stress induces the transcription and translation of sucrose synthase in rice. Plant Physiol 95:669–674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rocha S (2007) Gene regulation under low oxygen: holding your breath for transcription. Trends Biochem Sci 32:389–397

    Article  CAS  PubMed  Google Scholar 

  • Rumpho ME, Kennedy RA (1981) Anaerobic metabolism in germinating seeds of Echinochloa crus-galli (barnyard grass). Plant Physiol 68:165–168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sairam RK, Kumutha D, Ezhilmathi K (2009) Waterlogging tolerance: non symbiotic haemoglobin-nitric oxyde homeostatis and antioxidants. Curr Sci 96:675–682

    Google Scholar 

  • Subramanyam K, Sailaja KV, Subramanyam K, Muralidhara Rao D, Lakshmidevi K (2011) Ectopic expression of an osmotin gene leads to enhanced salt tolerance in transgenic chilli pepper (Capsicum annum L.). Plant Cell Tissue Organ Cult 105:181–192

    Article  CAS  Google Scholar 

  • Syvertsen JP, Levy Y (2005) Salinity interactions with other abiotic and biotic stresses in citrus. HortTechnology 15:100–103

    Google Scholar 

  • Vannini C, Locatelli F, Bracale M, Magnani E, Marsoni M, Osnato M, Mattana M, Baldoni E, Coraggio I (2004) Overexpression of the rice Osmyb4 gene increases chilling and freezing tolerance of Arabidopsis thaliana plants. Plant J 37:115–127

    Article  CAS  PubMed  Google Scholar 

  • Wei Q, Guo YJ, Cao HM, Kuai BK (2011) Cloning and characterization of an AtNHX2-like Na+/H+ antiporter gene from Ammopiptanthus mongolicus (Leguminosae) and its ectopic expression enhanced drought and salt tolerance in Arabidopsis thaliana. Plant Cell Tissue Organ Cult 105:309–316

    Article  CAS  Google Scholar 

  • Xuan N, Jin Y, Zhang H, Xie Y, Liu Y, Wang G (2011) A putative maize zinc-finger protein gene, ZmAN13, participates in abiotic stress response. Plant Cell Tissue Organ Cult 107:101–112

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Dr. Concetta Licciardello and Dr. Franco Faoro for scientific support and critical suggestions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Franca Locatelli.

Additional information

Paola Caruso and Elena Baldoni contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Caruso, P., Baldoni, E., Mattana, M. et al. Ectopic expression of a rice transcription factor, Mybleu, enhances tolerance of transgenic plants of Carrizo citrange to low oxygen stress. Plant Cell Tiss Organ Cult 109, 327–339 (2012). https://doi.org/10.1007/s11240-011-0098-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-011-0098-1

Keywords

Profiles

  1. Elena Baldoni