Abstract
Low temperature is one of the major abiotic stresses which severely affects the productivity and the geographical distribution of rice (Oryza sativa). Silicon is considered a broad spectrum alleviator to combat stress in rice plant. Rice root absorbs silicon by a silicon transporter, Low silicon gene 1 (Lsi1). To gain a better understanding of cold stress responses triggered by overexpression of Lsi1 in rice (Oryza sativa L.), we carried out physiological and molecular studies between Lsi1-overexpression Dular (Lsi1-D) and its wild type (WD). Two leaf stage rice seedlings of above mentioned both lines were treated at 15 °C/12 °C (day/night) for 7 days. WD seedling leaves were turned comparatively yellow as compared to Lsi1-D seedlings. Microscopic studies showed significantly more deposition of silicon bodies in epidermal cells of Lsi1-D leaf seedlings in comparison with WD leaves. Lsi1-D leaves comparatively, depicted more SOD, POD and CAT activity, chlorophyll a, b contents in consistency with more silicon concentration. Protein extraction was carried out from whole seedling of both lines and further analyzed by tandem mass tag quantitative proteomics approach with double replicates. Among 393 reproducible proteins, 63 were up-regulated and 39 proteins were down-regulated. The total cold responsive differential proteins were involved in several processes, i.e. photosynthesis, signal transduction, redox homeostasis, hormone metabolism, carbohydrate metabolism, cell wall organization, N-assimilation, protein processing and secondary metabolism. We confirmed up-regulation of key proteins involved in cold-responsive pathway at mRNA level through qPCR such as chlorophyll a–b binding protein 1, peroxidase 2, signaling G-proteins RIC1, aquaporin PIP1.2, 1, 4-alpha-glucan branching enzyme, germin-like protein subfamily 2 member 4 and germin-like protein subfamily 8 member 2. In conclusion, our study provides new insights into cold stress responses in rice seedlings triggered by Lsi1-overexpression defense pathway.
Similar content being viewed by others
Abbreviations
- Si:
-
Silicon
- WD:
-
Wild Dular
- TLS:
-
Two leaf stage
- Lsi1 :
-
Low silicon rice 1
- Lsi1-D:
-
Lsi1-overexpressed Dular
- NaOH:
-
Sodium hydroxide
- FAA:
-
Formaldehyde
- PBS:
-
Potassium phosphate buffer
- TCA:
-
Trichloroacetic acid
- TMT:
-
Tandem mass tags
- D/N:
-
Day/night
- SD:
-
Supplementary data
References
Agarie S et al (1996) Function of silica bodies in the epidermal system of rice (Oryza sativa L.): testing the window hypothesis. J Exp Bot 47(298):655–660
Allahverdiyeva Y et al (2005) Modulation of photosynthetic electron transport in the absence of terminal electron acceptors: characterization of the rbcL deletion mutant of tobacco. Biochimica et Biophysica Acta (BBA)-Bioenergetics 1709(1):69–83
Allakhverdiev SI, Murata N (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of Photosystem II in Synechocystis sp. PCC 6803. Biochimica et Biophysica Acta (BBA)-Bioenergetics 1657(1):23–32
Aroca R et al (2003) Involvement of abscisic acid in leaf and root of maize (Zea mays L.) in avoiding chilling-induced water stress. Plant Sci 165(3):671–679
Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Biol 50(1):601–639
Balakhnina TI et al (2015) The influence of Si-rich mineral zeolite on the growth processes and adaptive potential of barley plants under cadmium stress. Plant Growth Regul 75(2):557–565
Baruah AR et al (2009) Cold tolerance at the early growth stage in wild and cultivated rice. Euphytica 165(3):459–470
Benabdellah K et al (2009) Hydrogen peroxide effects on root hydraulic properties and plasma membrane aquaporin regulation in Phaseolus vulgaris. Plant Mol Biol 70(6):647–661
Bernier F, Berna A (2001) Germins and germin-like proteins: plant do all proteins. But what do they do exactly? Plant Physiol Biochem 39(7):545–554
Bloom A et al (2004) Water relations under root chilling in a sensitive and tolerant tomato species. Plant, Cell Environ 27(8):971–979
Board J et al (1980) Floret sterility in rice in a cool environment. Agron J 72(3):483–487
Cai H et al (2013) VennPlex—a novel Venn diagram program for comparing and visualizing datasets with differentially regulated datapoints. PLoS ONE 8(1):e53388
Casey W et al (2004) Aqueous silicate complexes in wheat, Triticum aestivum L. Plant, Cell Environ 27(1):51–54
da Silva Lobato AK et al (2013) Silicon: a benefic element to improve tolerance in plants exposed to water deficiency. INTECH Open Access Publisher
Dasso M (2002) The Ran GTPase: theme and variations. Curr Biol 12(14):R502–R508
Datnoff LE et al (2001) Silicon in agriculture, vol 8. Elsevier, Amsterdam
Davletova S et al (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17(1):268–281 (online)
Dingkuhn M et al (1995) Climatic determinants of irrigated rice performance in the Sahel-I. Photothermal and micro-climatic responses of flowering. Agric Syst 48(4):385–410
Dos Santos MG et al (2006) The role of inorganic phosphate on photosynthesis recovery of common bean after a mild water deficit. Plant Sci 170(3):659–664
Epstein E (1999) Silicon. Annu Rev Plant Biol 50(1):641–664
Epstein E (2009) Silicon: its manifold roles in plants. Ann Appl Biol 155(2):155–160
Fang C-X et al (2011) Suppression and overexpression of Lsi1 induce differential gene expression in rice under ultraviolet radiation. Plant Growth Regul 65(1):1–10
Galili G (2014) The aspartate-family pathway of plants. Plant Signal Behav 6(2):192–195
Gammulla CG et al (2011) Differential proteomic response of rice (Oryza sativa) leaves exposed to high- and low-temperature stress. Proteomics 11(14):2839–2850
Gandul-Rojas B et al (2004) Chlorophyll and carotenoid degradation mediated by thylakoid-associated peroxidative activity in olives (Olea europaea) cv. Hojiblanca. J Plant Physiol 161(5):499–507
Godfray HCJ et al (2010) Food security: the challenge of feeding 9 billion people. Science 327(5967):812–818
Godwin D et al (1994) Simulation of the effect of chilling injury and nitrogen supply on floret fertility and yield in rice. Anim Prod Sci 34(7):921–926
Greer D et al (1986) Photoinhibition of photosynthesis in intact bean leaves: role of light and temperature, and requirement for chloroplast-protein synthesis during recovery. Planta 168(2):253–260
Hoelz A, Blobel G (2004) Cell biology: popping out of the nucleus. Nature 432(7019):815–816
Hoshida H et al (2000) Enhanced tolerance to salt stress in transgenic rice that overexpresses chloroplast glutamine synthetase. Plant Mol Biol 43(1):103–111
Khush GS (1997) Origin, dispersal, cultivation and variation of rice. In: Sasaki T, Moore G (eds) Oryza: from molecule to plant. Springer, Amsterdam, pp 25–34
Lana R et al (2003) Effects of calcium silicate on the productivity and silicon accumulation in the tomato plant. Biosci J 19:15–20
Lee SH et al (2004) Rapid accumulation of hydrogen peroxide in cucumber roots due to exposure to low temperature appears to mediate decreases in water transport. J Exp Bot 55(403):1733–1741
Letourneur F et al (1994) Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum. Cell 79(7):1199–1207
Li X-B et al (2005) The cotton ACTIN1 gene is functionally expressed in fibers and participates in fiber elongation. Plant Cell 17(3):859–875
Liang Y et al (2007) Mechanisms of silicon-mediated alleviation of abiotic stresses in higher plants: a review. Environ Pollut 147(2):422–428
Liu P et al (2014) Aquaporin-mediated increase in root hydraulic conductance is involved in silicon-induced improved root water uptake under osmotic stress in Sorghum bicolor L. J Exp Bot 65(17):4747–4756
Locarno M et al (2011) Influence of silicate fertilization on chlorophylls of rose leaves. Cienc Agrotecnol 35(2):287–290
Lukacova Z et al (2013) Silicon mitigates the Cd toxicity in maize in relation to cadmium translocation, cell distribution, antioxidant enzymes stimulation and enhanced endodermal apoplasmic barrier development. Plant Growth Regul 70(1):89–103
Luu DT, Maurel C (2005) Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ 28(1):85–96
Ma JF (2004) Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses. Soil Sci Plant Nutr 50(1):11–18
Ma JF, Takahashi E (2002) Soil, fertilizer, and plant silicon research in Japan. Elsevier, Amsterdam
Ma JF, Yamaji N (2006) Silicon uptake and accumulation in higher plants. Trends Plant Sci 11:392–397
Ma JF, Yamaji N (2008) Functions and transport of silicon in plants. Cell Mol Life Sci CMLS 65(19):3049–3057
Ma J et al (2001) Silicon as a beneficial element for crop plants. Stud Plant Sci 8:17–39
Ma JF et al (2006) A silicon transporter in rice. Nature 440(7084):688–691
Ma JF et al (2007) An efflux transporter of silicon in rice. Nature 448(7150):209–212
Ma JF, Yamaji Naoki, Mitani-Ueno Namiki (2011) Transport of silicon from roots to panicles in plants. Proc Jpn Acad Ser B 87(7):377–385
Marwaha RS, Juliano BO (1976) Aspects of nitrogen metabolism in the rice seedling. Plant Physiol 57:923–927
Matsumoto T et al (2009) Role of the aquaporin PIP1 subfamily in the chilling tolerance of rice. Plant Cell Physiol 50(2):216–229
Maurel C et al (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624
Mitani N et al (2005) Identification of the silicon form in xylem sap of rice (Oryza sativa L.). Plant Cell Physiol 46(2):279–283
Mukhopadhyay A et al (2004) Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proc Natl Acad Sci USA 101(16):6309–6314
Muneer S, Jeong BR (2015) Proteomic analysis of salt-stress responsive proteins in roots of tomato (Lycopersicon esculentum L.) plants towards silicon efficiency. Plant Growth Regul. doi:10.1007/s10725-015-0045-y
Nishiyama Y et al (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochimica et Biophysica Acta (BBA)-Bioenergetics 1757(7):742–749
Ohyama N (1985) Amelioration of cold weather damage of rice by silicate fertilizer application. Agric Hort 60:1385–1389
Patnaik D, Khurana P (2001) Germins and germin like proteins: an overview. Indian J Exp Biol 39(3):191–200
Radmer RJ, Kok B (1976) Photoreduction of O2 primes and replaces CO2 assimilation. Plant Physiol 58(3):336–340
Raven PH (2014) GM crops, the environment and sustainable food production. Transgenic Res 23:915–921
Sacala E (2009) Role of silicon in plant resistance to water stress. J Elementol 14(3):619–630
Sakamoto T (2006) Phytohormones and rice crop yield: strategies and opportunities for genetic improvement. Transgenic Res 15(4):399–404
Savant NK et al (1997) Depletion of plant-available silicon in soils: a possible cause of declining rice yields 1. Commun Soil Sci Plant Anal 28(13–14):1245–1252
Shi G et al (2010) Silicon alleviates cadmium toxicity in peanut plants in relation to cadmium distribution and stimulation of antioxidative enzymes. Plant Growth Regul 61(1):45–52
Shimono H et al (2007) Low temperature-induced sterility in rice: evidence for the effects of temperature before panicle initiation. Field Crops Res 101(2):221–231
Simon McQueen-Mason DMD, Cosgrove Daniel J (1992) Two endogenous proteins that lnduce cell wall. Plant Cell 4:1425–1433
Singh RP, Brennan JP, Farrell T, Williams R, Reinke R, Lewin L, Mullen J (2005) Economic analysis of improving cold tolerance in rice in Australia. Australas Agribus Rev 1442–6951
Soundararajan P et al (2014) Influence of silicon supplementation on the growth and tolerance to high temperature in Salvia splendens. Hortic Environ Biotechnol 55(4):271–279
Thompson A et al (2003) Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal Chem 75(8):1895–1904
Watanabe S et al (2001) Effects of silicon nutrition on metabolism and translocation of nutrients in rice plants. In: Horst WJ, Schenk MK, Burkert A, Claassen N, Flessa H, Frommer WB, Goldbach H, Olfs H-W, Romheld V et al (eds) Plant nutrition. Springer, Netherlands, pp 174–175
Xu P, Cai W (2014) RAN1 is involved in plant cold resistance and development in rice (Oryza sativa). J Exp Bot 65(12):3277–3287
Yamaji N, Ma JF (2007) Spatial distribution and temporal variation of the rice silicon transporter Lsi1. Plant Physiol 143(3):1306–1313
Yan S-P et al (2006) Comparative proteomic analysis provides new insights into chilling stress responses in rice. Mol Cell Proteom 5(3):484–496
Yoshida S (1965) Chemical aspects of the role of silicon in physiology of the rice plant. Bull nat Inst agric Sci Jpn Ser B 15:1–58
Zhang X (1992) The measurement and mechanism of lipid peroxidation and SOD, POD and CAT activities in biological system. Research methodology of crop physiology. Agriculture Press, Beijing, pp 208–211
Zhang C et al (2013) Do lignification and silicification of the cell wall precede silicon deposition in the silica cell of the rice (Oryza sativa L.) leaf epidermis? Plant Soil 372(1–2):137–149
Acknowledgments
Thanks to Dr. Changxun Fang for providing Transgene rice line (Lsi1 overexpressed Dular) and for his continuous guidance to accomplish this research. This work was supported by the National Natural Science Foundation of China (Nos. 31271670, 31300336) and the National Research Foundation for the Doctoral Program of Higher Education of China (No. 20133515130001).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Azeem, S., Li, Z., Zheng, H. et al. Quantitative proteomics study on Lsi1 in regulation of rice (Oryza sativa L.) cold resistance. Plant Growth Regul 78, 307–323 (2016). https://doi.org/10.1007/s10725-015-0094-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-015-0094-2