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Transgenic Research

, Volume 21, Issue 4, pp 785–795 | Cite as

Over-expression of OSRIP18 increases drought and salt tolerance in transgenic rice plants

  • Shu-Ye Jiang
  • Ritu Bhalla
  • Rengasamy Ramamoorthy
  • Hong-Fen Luan
  • Prasanna Nori Venkatesh
  • Minne Cai
  • Srinivasan RamachandranEmail author
Original Paper

Abstract

Both drought and high salinity stresses are major abiotic factors that limit the yield of agricultural crops. Transgenic techniques have been regarded as effective ways to improve crops in their tolerance to these abiotic stresses. Functional characterization of genes is the prerequisite to identify candidates for such improvement. Here, we have investigated the biological functions of an Oryza sativa Ribosome-inactivating protein gene 18 (OSRIP18) by ectopically expressing this gene under the control of CaMV 35S promoter in the rice genome. We have generated 11 independent transgenic rice plants and all of them showed significantly increased tolerance to drought and high salinity stresses. Global gene expression changes by Microarray analysis showed that more than 100 probe sets were detected with up-regulated expression abundance while signals from only three probe sets were down-regulated after over-expression of OSRIP18. Most of them were not regulated by drought or high salinity stresses. Our data suggested that the increased tolerance to these abiotic stresses in transgenic plants might be due to up-regulation of some stress-dependent/independent genes and OSRIP18 may be potentially useful in further improving plant tolerance to various abiotic stresses by over-expression.

Keywords

Drought stress Ectopic over-expression High salinity stress Ribosome-inactivating protein Rice 

Abbreviations

Mg

Megnaporthe grisea

PEG

Polyethylene glycol

qRT-PCR

Quantitative real-time RT-PCR

RACE

Rapid amplification of cDNA ends

RIP

Ribosome-inactivating proteins

WT

Wild type

Xoo

Xanthomonas oryzae pv oryzae

Supplementary material

11248_2011_9568_MOESM1_ESM.pdf (202 kb)
Supplementary material 1 (PDF 202 kb)

References

  1. Barnabas B, Jager K, Feher A (2008) The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ 31:11–38PubMedGoogle Scholar
  2. Bass HW, Krawetz JE, Obrian GR, Zinselmeier C, Habben JE, Boston RS (2004) Maize ribosome-inactivating proteins (RIPs) with distinct expression patterns have similar requirements for proenzyme activation. J Exp Bot 55:2219–2233PubMedCrossRefGoogle Scholar
  3. Bieri S, Potrykus I, Fütterer J (2000) Expression of active barley seed ribosome-inactivating protein in transgenic wheat. Theor Appl Genet 100:755–763CrossRefGoogle Scholar
  4. Bray EA, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stresses. In: Buchannan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. American Society of Plant Biologists, Rockville, pp 1158–1249Google Scholar
  5. Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: version 2. Plant Mol Biol Rep 1:19–22CrossRefGoogle Scholar
  6. Desmyter S, Vandenbussche F, Hao Q, Proost P, Peumans WJ, Van Damme EJ (2003) Type-1 ribosome-inactivating protein from iris bulbs: a useful agronomic tool to engineer virus resistance? Plant Mol Biol 51:567–576PubMedCrossRefGoogle Scholar
  7. Ding ZJ, Wu XH, Wang T (2002) The rice tapetum-specific gene RA39 encodes a type I ribosome-inactivating protein. Sex Plant Reprod 15:205–212CrossRefGoogle Scholar
  8. Dowd PF, Mehta AD, Boston RS (1998) Relative toxicity of the maize endosperm ribosome-inactivating protein to insects. J Agri Food Chem 46:3775–3779CrossRefGoogle Scholar
  9. Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875PubMedCrossRefGoogle Scholar
  10. Frohman KB, Dush M, Marlin G (1988) Rapid amplification of fulllength cDNAs from rare transcripts: amplification using a single-specific oligonucleotide primers. Proc Natl Acad Sci USA 85:8998–9002PubMedCrossRefGoogle Scholar
  11. Gatehouse A, Barbieri L, Stirpe F, Croy RRD (1990) Effects of ribosome inactivating proteins on insect development—differences between Lepidoptera and Coleoptera. Entomol Exp Appl 54:43–51CrossRefGoogle Scholar
  12. Girbes T, de Torre C, Iglesias R, Ferreras JM, Mendez E (1996) RIP for viruses. Nature 379:777–778CrossRefGoogle Scholar
  13. Girbes T, Ferreras JM, Arias FJ, Stripe F (2004) Description, distribution, activity and phylogenetic relationship of ribosome-inactivating proteins in plants, fungi and bacteria. MiniRev Med Chem 4:467–482Google Scholar
  14. Guo X, Ren Z, Zhao Y, Zhang H (2003) Over-expression of SOD2 increases salt tolerance of Arabidopsis. Plant Physiol 133:1873–1881CrossRefGoogle Scholar
  15. Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282Google Scholar
  16. Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103:12987–12992PubMedCrossRefGoogle Scholar
  17. Iglesias R, Perez Y, de Torre C, Ferreras JM, Antolin P, Jimenez P, Rojo MA, Mendez E, Girbes T (2005) Molecular characterization and systemic induction of single-chain ribosome-inactivating proteins (RIPs) in sugar beet (Beta vulgaris) leaves. J Exp Bot 56:1675–1684PubMedCrossRefGoogle Scholar
  18. Jach G, Gornhardt B, Mundy J, Logemann J, Pinsdorf E, Leah R, Schell J, Maas C (1995) Enhanced quantitative resistance against fungal disease by combinatorial expression of different barley antifungal proteins in transgenic tobacco. Plant J 8:97–109PubMedCrossRefGoogle Scholar
  19. Jiang SY, Ramachandran S (2010) Improving crop tolerance to abiotic stresses by plant biotechnology, chapter 15. In: Kumar A, Roy S (eds) Applications of plant biotechnology: in vitro propagation, plant transformations and secondary metabolite production. I.K. International Publishing House, New Delhi, pp 286–309Google Scholar
  20. Jiang SY, Bachmann D, La H, Ma Z, Venkatesh PN, Ramamoorthy R, Ramachandran S (2007) Ds insertion mutagenesis as an efficient tool to produce diverse variations for rice breeding. Plant Mol Biol 65:385–402PubMedCrossRefGoogle Scholar
  21. Jiang SY, Ramamoorthy R, Bhalla R, Luan HF, Venkatesh PN, Cai M, Ramachandran S (2008) Genome-wide survey of the RIP domain family in Oryza sativa and their expression profiles under various abiotic and biotic stresses. Plant Mol Biol 67:603–614PubMedCrossRefGoogle Scholar
  22. Kim JK, Duan X, Wu R, Seok SJ, Boston RS, Jang IC, Eun MY, Nahm BH (1999) Molecular and genetic analysis of transgenic rice plants expressing the ribosome inactivating protein b-32 gene and the herbicide resistance bar gene. Mol Breed 5:85–94CrossRefGoogle Scholar
  23. Koops P, Pelser S, Ignatz M, Klose C, Marrocco-Selden K, Kretsch T (2011) EDL3 is an F-box protein involved in the regulation of abscisic acid signalling in Arabidopsis thaliana. J Exp Bot. doi: 10.1093/jxb/err236
  24. Kumar MA, Timm DE, Neet KE, Owen WG, Peumans WJ, Rao AG (1993) Characterization of the lectin from the bulbs of Eranthis hyemalis (winter aconite) as an inhibitor of protein synthesis. J Biol Chem 268:25176–25183PubMedGoogle Scholar
  25. Lanceras JC, Pantuwan G, Jongdee B, Toojinda T (2004) Quantitative trait loci associated with drought tolerance at reproductive stage in rice. Plant Physiol 135:384–399PubMedCrossRefGoogle Scholar
  26. Lauchli A, Grattan SR (2007) Plant growth and development under salinity stress. In: Jenks MA, Hasegawa P, Jain SM (eds) Advances in molecular breeding toward drought and salt tolerant crops. Springer, Netherlands, pp 1–32CrossRefGoogle Scholar
  27. Lodge JK, Kaniewski WK, Tumer NE (1993) Broad-spectrum virus resistance in transgenic plants expressing pokeweed antiviral protein. Proc Natl Acad Sci USA 90:7089–7093PubMedCrossRefGoogle Scholar
  28. Logemann J, Jach G, Tommerup H, Mundy J, Schell J (1992) Expression of a barley ribosome-inactivating protein leads to increased fungal protection in transgenic tobacco plants. Nat Biotechnol 10:305–308CrossRefGoogle Scholar
  29. Maddaloni M, Forlani F, Balmas V, Donini G, Stasse L, Corazza L, Motto M (1997) Tolerance to the fungal pathogen Rhizoctonia solani AG4 of transgenic tobacco expressing the maize ribosome-inactivating protein b-32. Transgenic Res 6:393–402CrossRefGoogle Scholar
  30. Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158PubMedCrossRefGoogle Scholar
  31. Meskiene I, Bögre L, Glaser W, Balog J, Brandstötter M, Zwerger K, Ammerer G, Hirt H (1998) MP2C, a plant protein phosphatase 2C, functions as a negative regulator of mitogen-activated protein kinase pathways in yeast and plants. Proc Natl Acad Sci USA 95:1938–1943PubMedCrossRefGoogle Scholar
  32. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410PubMedCrossRefGoogle Scholar
  33. Narasimha Chary S, Bultema RL, Packard CE, Crowell DN (2002) Prenylcysteine alpha-carboxyl methyltransferase expression and function in Arabidopsis thaliana. Plant J 32:735–747PubMedCrossRefGoogle Scholar
  34. Perruc E, Charpenteau M, Ramirez BC, Jauneau A, Galaud JP, Ranjeva R, Ranty B (2004) A novel calmodulin-binding protein functions as a negative regulator of osmotic stress tolerance in Arabidopsis thaliana seedlings. Plant J 38:410–420PubMedCrossRefGoogle Scholar
  35. Reddy PR, Goss JA (1971) Effect of salinity on pollen I. Pollen viability as altered by increasing osmotic pressure with NaCl, MgCl2, and CaCl2. Am J Bot 58:721–725CrossRefGoogle Scholar
  36. Rippmann JF, Michalowski CB, Nelson DE, Bohnert HJ (1997) Induction of a ribosome-inactivating protein upon environmental stress. Plant Mol Biol 35:701–709PubMedCrossRefGoogle Scholar
  37. Rubio F, Gassmann W, Schroeder JI (1995) Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270:1660–1663PubMedCrossRefGoogle Scholar
  38. Saini HS (1997) Effects of water stress on male gametophyte development in plants. Sex Plant Reprod 10:67–73CrossRefGoogle Scholar
  39. Schaefer SC, Gasic K, Cammue B, Broekaert W, van Damme EJ, Peumans WJ, Korban SS (2005) Enhanced resistance to early blight in transgenic tomato lines expressing heterologous plant defense genes. Planta 222:858–866PubMedCrossRefGoogle Scholar
  40. Stirpe F, Battelli MG (2006) Ribosome-inactivating proteins: progress and problems. Cell Mol Life Sci 63:1850–1866PubMedCrossRefGoogle Scholar
  41. Stirpe F, Barbieri L, Gorini P, Valbonesi P, Bolognesi A, Polito L (1996) Activities associated with the presence of ribosome-inactivating proteins increase in senescent and stressed leaves. FEBS Lett 382:309–312PubMedCrossRefGoogle Scholar
  42. Vincent D, Lapierre C, Pollet B, Cornic G, Negroni L, Zivy M (2005) Water deficits affect caffeate O-methyltransferase, lignification, and related enzymes in maize leaves. A proteomic investigation. Plant Physiol 137:949–960PubMedCrossRefGoogle Scholar
  43. Vivanco JM, Savary BJ, Flores HE (1999) Characterization of two novel type I ribosome-inactivating proteins from the storage roots of the Andean crop Mirabilis expansa. Plant Physiol 119:1447–1456PubMedCrossRefGoogle Scholar
  44. Wei Q, Huang MX, Xu Y, Zhang XS, Chen F (2005) Expression of a ribosome inactivating protein (curcin 2) in Jatropha curcas is induced by stress. J Biosci 30:351–357CrossRefGoogle Scholar
  45. Xu J, Wang H, Fan J (2007) Expression of a ribosome-inactivating protein gene in bitter melon is induced by Sphaerotheca fuliginea and abiotic stimuli. Biotechnol Lett 29:1605–1610PubMedCrossRefGoogle Scholar
  46. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Ann Rev Plant Biol 57:781–803CrossRefGoogle Scholar
  47. Yuan H, Ming X, Wang L, Hu P, An C, Chen Z (2002) Expression of a gene encoding trichosanthin in transgenic rice plants enhances resistance to fungus blast disease. Plant Cell Rep 20:992–998CrossRefGoogle Scholar
  48. Zhang Y, Xu W, Li Z, Deng XW, Wu W, Xue Y (2008) F-box protein DOR functions as a novel inhibitory factor for abscisic acid-induced stomatal closure under drought stress in Arabidopsis. Plant Physiol 148:2121–2133PubMedCrossRefGoogle Scholar
  49. Zhou X, Li XD, Yuan JZ, Tang ZH, Liu WY (2000) Toxicity of cinnamomin—a new type II ribosome-inactivating protein to bollworm and mosquito. Insect Biochem Mol Biol 30:259–264PubMedCrossRefGoogle Scholar
  50. Zoubenko O, Uckun F, Hur Y, Chet I, Tumer N (1997) Plant resistance to fungal infection induced by nontoxic pokeweed antiviral protein mutants. Nat Biotechnol 15:992–996PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Shu-Ye Jiang
    • 1
  • Ritu Bhalla
    • 1
    • 2
  • Rengasamy Ramamoorthy
    • 1
  • Hong-Fen Luan
    • 1
  • Prasanna Nori Venkatesh
    • 1
  • Minne Cai
    • 1
  • Srinivasan Ramachandran
    • 1
    Email author
  1. 1.Rice Functional Genomics Group, Temasek Life Sciences Laboratory, 1 Research LinkThe National University of SingaporeSingaporeSingapore
  2. 2.Republic PolytechnicSingaporeSingapore

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