Scientia Agricultura Sinica ›› 2013, Vol. 46 ›› Issue (24): 5188-5195.doi: 10.3864/j.issn.0578-1752.2013.24.013

• HORTICULTURE • Previous Articles     Next Articles

Study on the Metabolic Pathway of Trehalose in Pleurotus pulmonarius During Heat Stress Recovery

 LIU  Xiu-Ming, HUANG  Chen-Yang, CHEN  Qiang, WU  Xiang-Li, ZHANG  Jin-Xia   

  1. Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences/Key Laboratory of Microbial Resources, Ministry of Agriculture, Beijing 100081
  • Received:2013-05-08 Online:2013-12-16 Published:2013-05-31

Abstract: 【Objective】 The objective of this study is to explore the recovery mechanism after heat response stress of mushroom, in order to provide a theoretical basis for breeding. 【Method】 The responses of trehalose metabolism at the level of enzyme activity and gene relative expression quantity during heat stress recovery period in two strains of Pleurotus pulmonarius, including the heat sensitive strain CCMSSC 00494 and heat tolerant strain CCMSSC 00499 were investigated. 【Result】The results showed that the trehalose content of two strains rapidly decreased to the control level under heat stress recovery conditions, and the rate of decrease in heat sensitive strain CCMSSC 00494 was faster than that in CCMSSC 00499. During post-heat stress recovery period, trehalose-6-phosphate synthase (TPS) activity of CCMSSC 00494 increased with prolongation of treatment time, while it decreased slowly in CCMSSC 00499. And in both strains, trehalose phosphorylase (TP) activity in the direction of trehalose synthesis decreased suddenly, and TP activity in the direction of trehalose phosphorolysis and neutral trehalase (NTH) activity for trehalose hydrolysis were activated in the early and late period of recovery, respectively. In contrast with the case of tps and tp Genes, the increase of nth mRNA expression was not consistent with the elevation of neutral trehalase activity during heat stress in both strains. 【Conclusion】The main difference between heat sensitive and heat tolerant strains is that the activities and mRNA expression levels of TPS in heat sensitive strain was significantly higher during heat stress recovery period.

Key words: Pleurotus pulmonarius , trehalose , heat stress recovery , heat resistance

[1]Chang S T, Miles P G. Mushrooms: Cultivation, Nutritional Value, Medicinal Effect, and Environmental Impact. 2nd eds. Florida: CRC Press, 2004.

[2]Torrecillas A, Alarcón J J, Domingo R, Planes J, Sánchez-Blancoa M J. Strategies for drought resistance in leaves of two almond cultivars. Plant Science, 1996, 118(2): 135-143.

[3]Rouhi V, Samson R, Lemeur R, van Damme P. Photosynthetic gas exchange characteristics in three different almond species during drought stress and subsequent recovery. Environmental and Experimental Botany, 2007, 59(2): 117-129.

[4]Galani S, Wahid A, Arshad M. Tissue-specific expression and functional role of dehydrins in heat tolerance of sugarcane (Saccharum officinarum). Protoplasma, 2013, 250(2): 577-583.

[5]Hottiger T, Boiler T, Wiemken A. Rapid changes of heat and desiccation tolerance correlated with changes of trehalose content in Saccharomyces cerevisiae cells subjected to temperature shifts. FEBS Letters, 1981, 220(1): 113-115.

[6]Wiemken A. Trehalose in yeast, stress protectant rather than reserve carbohydrate. Antonie van Leeuwenhoek, 1990, 58(3): 209-217.

[7]Jorge J A, Polizeli M L T M, Thevelein J M, Terenzi H F. Trehalases and trehalose hydrolysis in fungi. FEMS Microbiology Letters, 1997, 154(2): 165-171.

[8]Sampedro J G, Cortés P, Muñoz-Clares R A, Fernándezc A, Uribe S. Thermal inactivation of the plasma membrane H+-ATPase from Kluyveromyces lactis protection by trehalose. Biochimica et Biophysica Acta, 2001, 154(2): 64-73.

[9]Kong W W, Huang C Y, Chen Q, Zou Y J, Zhao M R, Zhang J X. Nitric oxide is involved in the regulation of trehalose accumulation under heat stress in Pleurotus eryngii var. tuoliensis. Biotechnology Letters, 2012, 34(10): 1915-1919.

[10]Hottiger T, Schmutz P, Wiemken A. Heat-induced accumulation and futile cycling of trehalose in Saccharomyces cerevisiae. Journal of Bacteriology, 1987, 169(12): 5518-5522.

[11]Argüelles J C. Thermotolerance and trehalose accumulation induced by heat shock in yeast cells of Candida albicans. FEMS Microbiology Letters, 1997, 146(1): 65-71.

[12]D'Enfert C, Bonini B M, Zapella P D A, Fontaine T, da Silva A M, Terenzi H F. Neutral trehalases catalyse intracellular trehalose breakdown in the filamentous fungi Aspergillus nidulans and Neurospora crassa. Molecular Microbiology, 1999, 32(3): 471-484.

[13]Fillinger S, Chaveroche M K, van Dijck P, de Vries R, Ruijter G, Thevelein J, d’Enfert C. Trehalose is required for the acquisition of tolerance to a variety of stresses in the filamentous fungus Aspergillus nidulans. Microbiology, 2001, 147(7): 1851-1862.

[14]Ferreira A S, Tótola M R, Borges A C. Physiological implications of trehalose in the ectomycorrhizal fungus Pisolithus sp. under thermal stress. Journal of Thermal Biology, 2007, 32(1): 34-41.

[15]Uyar E O, Hamamci H, Türkel S. Effect of different stresses on trehalose levels in Rhizopus oryzae. Journal of Basic Microbiology, 2010, 50(4): 368-372.

[16]Al-Naama M, Ewaze J O, Green B J, Scott J A. Trehalose accumulation in Baudoinia compniacensis following abiotic stress. International Biodeterioration & Biodegradation, 2009, 63(6): 765-768.

[17]Wingler A, Fritzius T, Wiemken A, Boller T, Aeschbacher R A. Trehalose induces the ADP-glucose pyrophosphorylase gene, ApL3, and starch synthesis in Arabidopsis. Plant Physiology, 2000, 124(1): 105-114.

[18]Saito K, Kase T, Takahashi E, Horinouchi S. Purification and characterization of a trehalose synthase from the basidiomycete Grifola frondosa. Applied and Environmental Microbiology, 1998, 64(11): 4340-4345.

[19]San Miguel P F, Argüelles J C. Differential changes in the activity of cytosolic and vacuolar trehalases along the growth cycle of Saccharomyces cerevisiae. Biochimica et Biophysica Acta, 1994, 1200(2): 155-160.

[20]Kay R, Chan A M Y, Daly M, McPherson J. Duplication of CaMV 35S promoter sequences creates a strong enhancer for plant genes. Science, 1987, 236: 1299-1302.

[21]叶燕锐, 朱怡, 李莉莉, 林颖, 杜红丽, 韩双燕. 耐热酿酒酵母海藻糖代谢途径对热胁迫的响应. 华南理工大学学报, 2010, 38(5): 139-143.

Ye Y R, Zhu Y, Li L L, Lin Y, Du H L, Han S Y. Response of metabolic pathway of trrehalose in heat-resistant yeast Saccharomyces cerevisiae to heat stress. Journal of South China University of Technology, 2010, 38(5): 139-143. (in Chinese)

[22]Ocón A, Hampp R, Requena N. Trehalose turnover during abiotic atress in arbuscular mycorrhizal fungi. New Phytologist, 2007, 174(4): 879-891.

[23]Blázquez M A, Lagunas R, Gancedo C, Gancedo J M. Trehalose-6-phosphate, a new regulator of yeast glycolysis that inhibits hexokinases. FEBS Letters, 1993, 329(1-2): 51-54.

[24]Thevelein J M, Hohmann S. Trehalose synthase: guard to the gate of glycolysis in yeast? Trends in Biochemical Sciences, 1995, 20(1): 3-10.

[25]Voit E O. Biochemical and genomic regulation of the trehalose cycle in yeast: review of observations and canonical model analysis. Journal of Theoretical Biology, 2003, 223(1): 55-78.

[26]Kolbe A, Tiessen A, Schluepmann H, Paul M, Ulrich S, Geigenberger P. Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase. Proceedings of the National Academy Science of the USA, 2005, 102(31): 1118-1123.

[27]Fragoso S, Espíndola L, Páez-Valencia J, Gamboa A, Camacho Y, Martínez-Barajas E, Coello P. SnRK1 isoforms AKIN10 and AKIN11 are differentially regulated in Arabidopsis plants under phosphate starvation. Plant Physiology, 2009, 149(4): 1906-1916.

[28]Satoh-Nagasawa N, Nagasawa N, Malcomber S, Sakai H, Jackson D. A trehalose metabolic enzyme controls inflorescence architecture in maize. Nature, 2006, 441: 227-230.

[29]Zähringera H, Burgerta M, Holzera H, Nwaka S. Neutral trehalase Nth1p of Saccharomyces cerevisiae encoded by the NTH1 gene is a multiple stress responsive protein. FEBS Letters, 1997, 412(3): 615-620.

[30]Jepsen H F, Jensen B. Accumulation of trehalose in the thermophilic fungus Chaetomium thermophilum var. coprophilum in response to heat or salt stress. Soil Biology and Biochemistry, 2004, 36(10): 1669-1674.

[31]Kitamoto Y, Akashi H, Tanaka H, Mori N. α-Glucose-1-phosphate formation by a novel trehalose phosphorylase from Flammulina velutipes. FEMS Microbiology Letters, 1988, 55(2): 147-150.

[32]Schick I, Haltrich D, Kullbe K D. Trehalose phosphorylase from Pichia fermentans and its role in the metabolism of trehalose. Applied and Environmental Microbiology, 1995, 43(6): 1088-1095.

[33]Eis C, Watkins M, Prohaska T, Nidetzky B. Fungal trehalose phosphorylase: kinetic mechanism, pH-dependence of the reaction and some structural properties of the enzyme from Schizophyllum commune. Biochemical Journal, 2001, 356(Pt3): 757-767.

[34]Han S E, Kwon H B, Lee S B, Boller T, Herweijer M, Schoppink P, Vanderzee P, Wiemken A. Cloning and characterization of a gene encoding trehalose phosphorylase (TP) from Pleurotus sajor-caju. Protein Expression and Purification, 2003, 30(2): 194-202.

[35]Page-Sharp M, Behm C A, Smith G D. Involvement of the compatible solutes trehalose and sucrose in the response to salt stress of a cyanobacterial Scytonema species isolated from desert soils. Biochimica et Biophysica Acta, 1999, 1472(3): 519-528.

[36]Porchia A C, Fiol D f, Salerno G L. Differential synthesis of sucrose and trehalose in Euglena gracilis cells during growth and salt stress. Plant Science, 1999, 149(1): 43-49.

[37]Katoh H, Asthana R K, Ohmori M. Gene expression in the cyanobacterium Anabaena sp. PCC7120 under desiccation. Microbial Ecology, 2004, 47(2): 164-174.

[38]Higo A, Katoh H, Ohmori K, Ikeuchi M, Ohmori M. The role of a gene cluster for trehalose metabolism in dehyration tolerance of the filamentous cyanobacterium Anabaena sp. PCC7120. Microbiology, 2006, 152(4): 979-987.

[39]de Virgilio C, Bürckert N, Boller T, Wiemken A. A method to study the rapid phosphorylation-related modulation of neutral trehalase activity by temperature shifts in yeast. FEBS Letters, 1991, 291(2): 355-358.

[40]Gancedo C, Flores C L. The importance of a functional trehalose biosynthetic pathway for the life of yeasts and fungi. FEMS Yeast Research, 2004, 4(4-5): 351-359.

[41]Matthew P. Trehalose 6-phosphate. Current Opinion in Plant Biology, 2007, 10(3): 303-309.
[1] GE XinZhu,SHI YuXing,WANG ShaSha,LIU ZhiHui,CAI WenJie,ZHOU Min,WANG ShiGui,TANG Bin. Sequence Analysis of Harmonia axyridis Pyruvate Kinase Gene and Its Regulation of Trehalose Metabolism [J]. Scientia Agricultura Sinica, 2021, 54(23): 5021-5031.
[2] YU WeiDong,PAN BiYing,QIU LingYu,HUANG Zhen,ZHOU Tai,YE Lin,TANG Bin,WANG ShiGui. The Structure Characteristics and Biological Functions on Regulating Trehalose Metabolism of Two NlTret1s in Nilaparvata lugens [J]. Scientia Agricultura Sinica, 2020, 53(23): 4802-4812.
[3] DING YanJuan,LIU YongKang,LUO YuJia,DENG YingMei,XU HongXing,TANG Bin,XU CaiDi. Potential Functions of Nilaparvata lugens GSK-3 in Regulating Glycogen and Trehalose Metabolism [J]. Scientia Agricultura Sinica, 2019, 52(7): 1237-1246.
[4] TANG Bin,SHEN QiDa,ZENG BoPing,XIAO ZhongJiu,QIU LingYu,PAN BiYing,LI Kun,ZHANG DaoWei. Characteristics, Developmental Expression and RNAi Effect Analysis of a Novel Trehalose-6-Phosphate Synthase Gene in Nilaparvata lugens [J]. Scientia Agricultura Sinica, 2019, 52(3): 466-477.
[5] ZHANG DaoWei,YU YaYa,PAN BiYing,KANG Kui,ZENG BoPing,CHEN Jing,TANG Bin. Regulation Function of Trehalose-6-phosphate Synthase Genes on Chitin Synthesis in Sogatella furcifera [J]. Scientia Agricultura Sinica, 2019, 52(19): 3357-3366.
[6] TANG Bin, ZHANG Lu, XIONG XuPing, WANG HuiJuan, WANG ShiGui . Advances in Trehalose Metabolism and Its Regulation of Insect Chitin Synthesis [J]. Scientia Agricultura Sinica, 2018, 51(4): 697-707.
[7] JIANG Shan, LI Shuai, ZHANG Bin, LI Hong-gang, WAN Fang-hao, ZHENG Chang-ying. Effects of Extreme High Temperature on Survival Rate, Reproduction, Trehalose and Sorbitol of Frankliniella occidentalis [J]. Scientia Agricultura Sinica, 2016, 49(12): 2310-2321.
[8] . Comparative Study on Heat Resistance of Lily Hybrids and Their Parents
[J]. Scientia Agricultura Sinica, 2011, 44(6): 1201-1209 .
[9] ZHAO Yu, LI Hai-Lan, DU Jun, ZHAN Ji-Cheng. Effect of Trehalose in Resistance of Wine Yeast to Copper Stress [J]. Scientia Agricultura Sinica, 2011, 44(23): 4867-4873.
[10] GUO Xiao,LI Ke-bin,YIN Jiao,WANG Bing,CAO Ya-zhong . Effects of Wheat Varieties on Population Parameters of Macrosiphum avenae (Fabricius)
[J]. Scientia Agricultura Sinica, 2010, 43(10): 2056-2063 .
[11] Fang Lei,GuiFen Zhang,FangHao Wan,Jun Ma. Effects of Plant Species Switching on Contents and Dynamics of Trehalose and Trehalase Activity of Bemisia tabaci B-biotype and Trialeurodes vaporariorum [J]. Scientia Agricultura Sinica, 2006, 39(7): 1387-1394 .
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!