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Chitooligosaccharides enhance cold tolerance by repairing photodamaged PS II in rice

Published online by Cambridge University Press:  26 October 2018

Jiachun Zhou
Affiliation:
State Key Laboratory of Bioreactor Engineering, RandD Center of Separation and Extraction Technology in Fermentation Industry, East China University of Science and Technology, Shanghai 200237, China
Qiao Chen
Affiliation:
State Key Laboratory of Bioreactor Engineering, RandD Center of Separation and Extraction Technology in Fermentation Industry, East China University of Science and Technology, Shanghai 200237, China Shanghai Collaborative Innovation Center for Biomanufacturing Technology (SCIBT), Shanghai 200237, China
Yang Zhang
Affiliation:
State Key Laboratory of Bioreactor Engineering, RandD Center of Separation and Extraction Technology in Fermentation Industry, East China University of Science and Technology, Shanghai 200237, China Shanghai Collaborative Innovation Center for Biomanufacturing Technology (SCIBT), Shanghai 200237, China
Liqiang Fan*
Affiliation:
State Key Laboratory of Bioreactor Engineering, RandD Center of Separation and Extraction Technology in Fermentation Industry, East China University of Science and Technology, Shanghai 200237, China Shanghai Collaborative Innovation Center for Biomanufacturing Technology (SCIBT), Shanghai 200237, China
Zhen Qin
Affiliation:
State Key Laboratory of Bioreactor Engineering, RandD Center of Separation and Extraction Technology in Fermentation Industry, East China University of Science and Technology, Shanghai 200237, China
Qiming Chen
Affiliation:
State Key Laboratory of Bioreactor Engineering, RandD Center of Separation and Extraction Technology in Fermentation Industry, East China University of Science and Technology, Shanghai 200237, China
Yongjun Qiu
Affiliation:
State Key Laboratory of Bioreactor Engineering, RandD Center of Separation and Extraction Technology in Fermentation Industry, East China University of Science and Technology, Shanghai 200237, China Shanghai Collaborative Innovation Center for Biomanufacturing Technology (SCIBT), Shanghai 200237, China
Lihua Jiang
Affiliation:
State Key Laboratory of Bioreactor Engineering, RandD Center of Separation and Extraction Technology in Fermentation Industry, East China University of Science and Technology, Shanghai 200237, China
Liming Zhao*
Affiliation:
State Key Laboratory of Bioreactor Engineering, RandD Center of Separation and Extraction Technology in Fermentation Industry, East China University of Science and Technology, Shanghai 200237, China Shanghai Collaborative Innovation Center for Biomanufacturing Technology (SCIBT), Shanghai 200237, China
*
Author for correspondence: Liming Zhao and Liqiang Fan, E-mail: zhaoliming@ecust.edu.cn, fanglq@ecust.edu.cn
Author for correspondence: Liming Zhao and Liqiang Fan, E-mail: zhaoliming@ecust.edu.cn, fanglq@ecust.edu.cn

Abstract

Chitooligosaccharides (COS) are multi-functional foods and nutrients and environmentally friendly biological abiotic-resistance inducing agents for plants. In the current study, the effects and possible mechanisms of COS on improving the cold resistance of rice (II YOU 1259) seedlings were investigated. Compared with the control, a COS pre-soaking treatment enhanced photosynthesis, reduced oxidation damage and led to accumulation of more osmotic regulation substances under chilling treatment. In addition, a novel Deg/HtrA family serine endopeptidase (DegQ) gene, related to COS enhanced rice cold resistance, was identified. Quantitative real-time polymerase chain reaction (qRT-PCR) analysis revealed that transcription of DegQ and psbA (D1 protein encoding gene) were up-regulated in a time-dependent manner by COS treatment under cold stress. With increasing expression of the D1 protein, chlorophyll b content was enhanced correspondingly. The current results suggest that COS could enhance cold stress tolerance of rice by repairing the photodamaged photosystem II, altering osmotic regulation and reducing oxidation damage.

Type
Crops and Soils Research Paper
Copyright
Copyright © Cambridge University Press 2018 

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References

Allakhverdiev, SI, Nishiyama, Y, Miyairi, S, Yamamoto, H, Inagaki, N, Kanesaki, Y and Murata, N (2002) Salt stress inhibits the repair of photodamaged photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis. Plant Physiology 130, 14431453.Google Scholar
Allan, CR and Hadwiger, LA (1979) The fungicidal effect of chitosan on fungi of varying cell wall composition. Experimental Mycology 3, 285287.Google Scholar
Barker, M, de Vries, R, Nield, J, Komenda, J and Nixon, PJ (2006) The deg proteases protect Synechocystis sp. PCC 6803 during heat and light stresses but are not essential for removal of damaged D1 protein during the photosystem two repair cycle. Journal of Biological Chemistry 281, 3034730355.Google Scholar
Bates, LS, Waldren, RP and Teare, ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39, 205207.Google Scholar
Ben Ahmed, C, Ben Rouina, B, Sensoy, S, Boukhriss, M and Ben Abdullah, F (2010) Exogenous proline effects on photosynthetic performance and antioxidant defense system of young olive tree. Journal of Agricultural and Food Chemistry 58, 42164222.Google Scholar
Blum, A (2005) Drought resistance, water-use efficiency, and yield potential – are they compatible, dissonant, or mutually exclusive? Australian Journal of Agricultural Research 56, 11591168.Google Scholar
Boonlertnirun, S, Boonraung, C and Suvanasara, R (2008) Application of chitosan in rice production. Journal of Metals, Materials and Minerals 18, 4752.Google Scholar
Bradford, MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248254.Google Scholar
Cao, X, Zhong, C, Zhu, L, Zhang, J, Sajid, H, Wu, L and Jin, Q (2017) Glycine increases cold tolerance in rice via the regulation of N uptake, physiological characteristics and photosynthesis. Plant Physiology and Biochemistry 112, 251260.Google Scholar
Chan, Z and Shi, H (2015) Improved abiotic stress tolerance of bermudagrass by exogenous small molecules. Plant Signaling and Behavior 10, e991577.Google Scholar
Chaoui, A, Mazhoudi, S, Ghorbal, MH and El Ferjani, E (1997) Cadmium and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in bean (Phaseolus vulgaris L.). Plant Science 127, 139147.Google Scholar
Chen, AS, Taguchi, T, Sakai, K, Kikuchi, K, Wang, MW and Miwa, I (2003) Antioxidant activities of chitobiose and chitotriose. Biological and Pharmaceutical Bulletin 26, 13261330.Google Scholar
Chen, W, Guo, C, Hussain, S, Zhu, B, Deng, F, Xue, Y, Geng, M and Wu, L (2016) Role of xylo-oligosaccharides in protection against salinity-induced adversities in Chinese cabbage. Environmental Science and Pollution Research 23, 12541264.Google Scholar
Collard, BCY and Mackill, DJ (2009) Start Codon Targeted (SCoT) polymorphism: a simple, novel DNA marker technique for generating gene-targeted markers in plants. Plant Molecular Biology Reporter 27, 8693.Google Scholar
Datta, K and Datta, SK (2006) Indica rice (Oryza sativa, BR29 and IR64). Methods in Molecular Biology 343, 201212.Google Scholar
Ding, SJ, Shie, MY, Hoshiba, T, Kawazoe, N, Chen, G and Chang, HC (2010) Osteogenic differentiation and immune response of human bone-marrow derived mesenchymal stem cells on injectable calcium-silicate-based bone grafts. Tissue Engineering Part A 16, 23432354.Google Scholar
Dzung, NA, Khanh, VTP and Dzung, TT (2011) Research on impact of chitosan oligomers on biophysical characteristics, growth, development and drought resistance of coffee. Carbohydrate Polymers 84, 751755.Google Scholar
El Sayed, AI, Rafudeen, MS and Golldack, D (2014) Physiological aspects of raffinose family oligosaccharides in plants: protection against abiotic stress. Plant Biology 16, 18.Google Scholar
Fei, Y, Xue, Y, Du, P, Yang, S and Deng, X (2017) Expression analysis and promoter methylation under osmotic and salinity stress of TaGAPC1 in wheat (Triticum aestivum L). Protoplasma 254, 987996.Google Scholar
Foyer, CH and Noctor, G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant, Cell and Environment 28, 10561071.Google Scholar
Freguson, IB, Watkins, CB and Harman, JE (1983) Inhibition by calcium of senescence of detached cucumber cotyledons. Plant Physiology 71, 182186.Google Scholar
Fu, J, Sun, Y, Chu, X, Xu, Y and Hu, T (2014) Exogenous 5-aminolevulenic acid promotes seed germination in Elymus nutans against oxidative damage induced by cold stress. PLoS ONE 9, e107152.Google Scholar
Hamed, I, Özogul, F and Regenstein, JM (2016) Industrial applications of crustacean by-products (chitin, chitosan, and chitooligosaccharides): a review. Trends in Food Science and Technology 48, 4050.Google Scholar
Hart, KN, Kwon, IK, Lohakara, JD, Heo, S and Chae, BJ (2007) Chito-oligosaccharides as an alternative to antimicrobials in improving performance, digestibility and microbial ecology of the gut in weanling pigs. Asian Australasian Journal of Animal Sciences 20, 556562.Google Scholar
Haußühl, K, Andersson, B and Adamska, I (2001) A chloroplast DegP2 protease performs the primary cleavage of the photodamaged D1 protein in plant photosystem II. EMBO Journal 20, 713722.Google Scholar
Havaux, M and Tardy, F (1997) Thermostability and photostability of photosystem II in leaves of the Chlorina-f2 barley mutant deficient in light-harvesting chlorophyll a/b protein complexes. Plant Physiology 113, 913923.Google Scholar
Hirano, S and Nagao, N (1989) Effects of chitosan, pectic acid, lysozyme and chitinase on the growth of several phytopathogens. Agricultural and Biological Chemistry 53, 30653066.Google Scholar
Hu, M, Shi, Z, Zhang, Z, Zhang, Y and Li, H (2012) Effects of exogenous glucose on seed germination and antioxidant capacity in wheat seedlings under salt stress. Plant Growth Regulation 68, 177188.Google Scholar
Huesgen, PF, Schuhmann, H and Adamska, I (2009) Deg/HtrA proteases as components of a network for photosystem II quality control in chloroplasts and cyanobacteria. Research in Microbiology 160, 726732.Google Scholar
Jiang, FY, Li, Y and Weng, BQ (2002) Review on physiology of chilling stress and chilling resistance of plants. Fujian Journal of Agricultural Sciences 17, 190195.Google Scholar
Jing, P, Zou, J, Kong, L, Hu, S, Wang, B, Yang, J and Xie, G (2016) OsCCD1, a novel small calcium-binding protein with one EF-hand motif, positively regulates osmotic and salt tolerance in rice. Plant Science 247, 104114.Google Scholar
Jumaa, M, Furkert, FH and Müller, BW (2002) A new lipid emulsion formulation with high antimicrobial efficacy using chitosan. European Journal of Pharmaceutics and Biopharmaceutics 53, 115123.Google Scholar
Khan, MIR, Fatma, M, Per, TS, Anjum, NA and Khan, NA (2015 a) Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Frontiers in Plant Science 6, 462.Google Scholar
Khan, MS, Ahmad, D and Khan, MA (2015 b) Utilization of genes encoding osmoprotectants in transgenic plants for enhanced abiotic stress tolerance. Electronic Journal of Biotechnology 18, 257266.Google Scholar
Kiani, SP, Grieu, P, Maury, P, Hewezi, T, Gentzbittel, L and Sarrafi, A (2007) Genetic variability for physiological traits under drought conditions and differential expression of water stress-associated genes in sunflower (Helianthus annuus L.). Theoretical and Applied Genetics 114, 193207.Google Scholar
Kieselbach, T and Funk, C (2003) The family of Deg/HtrA proteases: from Escherichia coli to Arabidopsis. Physiologia Plantarum 119, 337346.Google Scholar
Korkmaz, A, Korkmaz, Y and Demirkıran, AR (2010) Enhancing chilling stress tolerance of pepper seedlings by exogenous application of 5-aminolevulinic acid. Environmental and Experimental Botany 67, 495501.Google Scholar
Kuang, YJ, Ye, GP and Qin, CQ (2009) Influence of oligochitosan on cold resistance of rice seedling. Hubei Agricultural Sciences 48, 15681571.Google Scholar
Kumar, V and Yadav, SK (2009) Proline and betaine provide protection to antioxidant and methylglyoxal detoxification systems during cold stress in Camellia sinensis (L.) O. Kuntze. Acta Physiologiae Plantarum 31, 261269.Google Scholar
Kumar, S, Kaur, G and Nayyar, H (2008) Exogenous application of abscisic acid improves cold tolerance in chickpea (Cicer arietinum L.). Journal of Agronomy and Crop Science 194, 449456.Google Scholar
Kumar, SG, Rahman, MA, Lee, SH, Hwang, HS, Kim, HA and Yun, JW (2009) Plasma proteome analysis for anti-obesity and anti-diabetic potentials of chitosan oligosaccharides in ob/ob mice. Protemics 9, 21492162.Google Scholar
Kurepin, LV, Ivanov, AG, Zaman, M, Pharis, RP, Hurry, V and Hüner, NPA (2017) Interaction of glycine betaine and plant hormones: protection of the photosynthetic apparatus during abiotic stress. In Hou, H, Najafpour, M, Moore, G and Allakhverdiev, S (eds), Photosynthesis: Structures, Mechanisms and Applications. Dordrecht, the Netherlands: Springer, Cham, pp. 185202.Google Scholar
Leborgne, N, Teulieres, C, Travert, S, Rols, MP, Teissie, J and Boudet, AM (1995) Introduction of specific carbohydrates into Eucalyptus gunnii cells increases their freezing tolerance. European Journal of Biochemistry 229, 710717.Google Scholar
Lei, P, Xu, Z, Liang, J, Luo, XH, Zhang, YX, Feng, XH and Xu, H (2016) Poly(γ-glutamic acid) enhanced tolerance to salt stress by promoting proline accumulation in Brassica napus L. Plant Growth Regulation 78, 233241.Google Scholar
Li, Y, Yin, H, Wang, Q, Zhao, XM, Du, YG and Li, FL (2009) Oligochitosan induced Brassica napus L. production of NO and H2O2 and their physiological function. Carbohydrate Polymers 75, 612617.Google Scholar
Lichtenthaler, HK and Buschmann, C (2001) Chlorophylls and carotenoids measurement and characterization by UV-VIS. In Wrolstad, RE, Acree, TE, An, H, Decker, EA, Penner, MH, Reid, DS, Schwartz, SJ, Shoemaker, CF and Sporns, P (eds), Current Protocols in Food Analytical Chemistry (CPFA). New York, USA: John Wiley, pp. F4.3.1F4.3.8.Google Scholar
Lin, ZF, Peng, CL, Lin, GZ, Ou, ZY, Yang, CW and Zhang, JL (2003) Photosynthetic characteristics of two new chlorophyll b-less rice mutants. Photosynthetica 41, 6167.Google Scholar
Lin, WL, Hu, XY, Zhang, WQ, Rogers, WJ and Cai, WM (2005) Hydrogen peroxide mediates defence responses induced by chitosans of different molecular weights in rice. Journal of Plant Physiology 162, 937944.Google Scholar
Liu, H, Zhang, YH, Yin, H, Wang, WX, Zhao, XM and Du, YG (2013) Alginate oligosaccharides enhanced Triticum aestivum l. tolerance to drought stress. Plant Physiology and Biochemistry 62, 3340.Google Scholar
Luo, C, He, XH, Chen, H, Ou, SJ and Gao, MP (2010) Analysis of diversity and relationships among mango cultivars using Start Codon Targeted (SCoT) markers. Biochemical Systematics and Ecology 38, 11761184.Google Scholar
Marco, F, Bitrián, M, Carrasco, P, Rajam, MV, Alcázar, R and Tiburcio, AF (2015) Genetic engineering strategies for abiotic stress tolerance in plants. In Bahadur, B, Venkat Rajam, M, Sahijram, L and Krishnamurthy, K (eds), Plant Biology and Biotechnology. New Delhi, India: Springer, pp. 579609.Google Scholar
Marta, B, Szafrańska, K and Posmyk, MM (2016) Exogenous melatonin improves antioxidant defense in cucumber seeds (Cucumis sativus L.) germinated under chilling stress. Frontiers in Plant Science 7, 575,.Google Scholar
Mendis, E, Kim, MM, Rajapakse, N and Kim, SK (2007) An in vitro cellular analysis of the radical scavenging efficacy of chitooligosaccharides. Life Sciences 80, 21182127.Google Scholar
Minorsky, PV (2003) Raffinose oligosaccharides. Plant Physiology 131, 11591160.Google Scholar
Mir, BA, Mir, SA, Khazir, J, Tonfack, LB, Cowan, DA, Vyas, D and Koul, S (2015) Cold stress affects antioxidative response and accumulation of medicinally important with anolides in Withania somnifera (L.) Dunal. Industrial Crops and Products 74, 10081016.Google Scholar
Mutlu, S, Atıcı, Ö, Nalbantoğlu, B and Mete, E (2016) Exogenous salicylic acid alleviates cold damage by regulating antioxidative system in two barley (Hordeum vulgare L.) cultivars. Frontiers in Life Science 9, 99109.Google Scholar
Nahar, K, Hasanuzzaman, M, Alam, MM and Fujita, M (2015) Exogenous glutathione confers high temperature stress tolerance in mung bean (Vigna radiata L.) by modulating antioxidant defense and methylglyoxal detoxification system. Environmental and Experimental Botany 112, 4454.Google Scholar
Nazar, R, Umar, S and Khan, NA (2015) Exogenous salicylic acid improves photosynthesis and growth through increase in ascorbate-glutathione metabolism and S assimilation in mustard under salt stress. Plant Signaling and Behavior 10, e1003751.Google Scholar
Nishiyama, Y, Allakhverdiev, SI, Yamamoto, H, Hayashi, H and Murata, N (2004) Singlet oxygen inhibits the repair of photosystem II by suppressing translation elongation of the D1 protein in Synechocystis sp. PCC 6803. Biochemistry 43, 1132111330.Google Scholar
Pallen, MJ and Wren, BW (1997) The HtrA family of serine proteases. Molecular Microbiology 26, 209221.Google Scholar
Park, EJ, Jeknic, Z and Chen, TH (2006) Exogenous application of glycinebetaine increases chilling tolerance in tomato plants. Plant and Cell Physiology 47, 706714.Google Scholar
Prasil, O, Adir, N and Ohad, I (1992) Dynamics of photosystem II: mechanism of photoinhibition and recovery in vivo. In Barber, J (ed.), Topics in Photosynthesis, Vol. 11, Amsterdam, the Netherlands: Elsevier Biomedical Press, pp. 295348.Google Scholar
Qian, H, Li, J, Sun, L, Chen, W, Sheng, GD, Liu, W and Fu, Z (2009) Combined effect of copper and cadmium on Chlorella vulgaris growth and photosynthesis-related gene transcription. Aquatic Toxicology 94, 5661.Google Scholar
Qiang, XJ, Yu, GH, Jiang, LL, Sun, LL, Zhang, SH, Wei, LI and Cheng, XG (2015) Thellungiella halophila ThPIP1 gene enhances the tolerance of the transgenic rice to salt stress. Journal of Integrative Agriculture 14, 19111922.Google Scholar
Rathinasabapathi, B (2000) Metabolic engineering for stress tolerance: installing osmoprotectant synthesis pathways. Annals of Botany 86, 709716.Google Scholar
Sakamoto, A and Murata, N (2002) The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant, Cell and Environment 25, 163171.Google Scholar
Sami, F, Yusuf, M, Faizan, M, Faraz, A and Hayat, S (2016) Role of sugars under abiotic stress. Plant Physiology and Biochemistry 109, 5461.Google Scholar
Sen, G, Eryilmaz, IE and Ozakca, D (2014) The effect of aluminium-stress and exogenous spermidine on chlorophyll degradation, glutathione reductase activity and the photosystem II D1 protein gene (psbA) transcript level in lichen Xanthoria parietina. Phytochemistry 98, 5459.Google Scholar
Shen, KT, Chen, MH, Chan, HY, Jeng, JH and Wang, YJ (2009) Inhibitory effects of chitooligosaccharides on tumor growth and metastasis. Food and Chemical Toxicology 47, 18641871.Google Scholar
Soliman, MH, Alayafi, AA, El Kelish, AA and Abu-Elsaoud, AM (2018) Acetylsalicylic acid enhance tolerance of Phaseolus vulgaris L. to chilling stress, improving photosynthesis, antioxidants and expression of cold stress responsive genes. Botanical Studies 59, 6.Google Scholar
Sun, Z, Qi, X, Wang, Z, Li, P, Wu, C, Zhang, H and Zhao, Y (2013) Overexpression of TsGOLS2, a galactinol synthase, in Arabidopsis thaliana enhances tolerance to high salinity and osmotic stresses. Plant Physiology and Biochemistry 69, 8289.Google Scholar
Thomashow, MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annual Review of Plant Physiology and Plant Molecular Biology 50, 571599.Google Scholar
Walsh, NP, Alba, BM, Bose, B, Gross, CA and Sauer, RT (2003) OMP peptide signals initiate the envelope-stress response by activating DegS protease via relief of inhibition mediated by its PDZ domain. Cell 113, 6171.Google Scholar
Wang, M, Chen, Y, Zhang, R, Wang, W, Zhao, X, Du, Y and Yin, H (2015) Effects of chitosan oligosaccharides on the yield components and production quality of different wheat cultivars (Triticum aestivum L.) in Northwest China. Field Crops Research 172, 1120.Google Scholar
Wang, F, Liu, J, Chen, M, Zhou, L, Li, Z, Zhao, Q, Pan, G, Zaidi, SHR and Cheng, F (2016) Involvement of abscisic acid in PSII photodamage and D1 protein turnover for light-induced premature senescence of rice flag leaves. PLoS ONE 11, e0161203.Google Scholar
Wilken, C, Kitzing, K, Kurzbauer, R, Ehrmann, M and Clausen, T (2004) Crystal structure of the DegS stress sensor: how a PDZ domain recognizes misfolded protein and activates a protease. Cell 117, 483494.Google Scholar
Wright, GC and Smith, RCG (1983) Differences between two grain sorghum genotypes in adaptation to drought stress. II. Root water uptake and water use. Australian Journal of Agricultural Research 34, 627636.Google Scholar
Yin, H, Li, Y, Zhang, HY, Wang, WX, Lu, H, Grevsen, K, Zhao, XM and Du, YG (2013) Chitosan oligosaccharides-triggered innate immunity contributes to oilseed rape resistance against Sclerotinia sclerotiorum. International Journal of Plant Sciences 174, 722732.Google Scholar
Yin, H, Du, Y and Dong, Z (2016) Chitin oligosaccharide and chitosan oligosaccharide: two similar but different plant elicitors. Frontiers in Plant Science 7, 522.Google Scholar
Yoon, HJ, Moon, ME, Park, HS, Kim, HW, Im, SY, Lee, JH and Kim, YH (2008) Effects of chitosan oligosaccharide (COS) on the glycerol-induced acute renal failure in vitro and in vivo. Food and Chemical Toxicology 46, 710716.Google Scholar
Zhang, HY, Zhao, XM, Yang, JL, Yin, H, Wang, WX, Lu, H and Du, YG (2011) Nitric oxide production and its functional link with OIPK in tobacco defense response elicited by chitooligosaccharide. Plant Cell Reports 30, 11531162.Google Scholar
Zhang, X, Li, K, Liu, S, Zou, P, Xing, R, Yu, H, Chen, X, Qin, Y and Li, P (2017) Relationship between the degree of polymerization of chitooligomers and their activity affecting the growth of wheat seedlings under salt stress. Journal of Agricultural and Food Chemistry 65, 501509.Google Scholar
Zhao, XM, She, XP, Du, YG and Liang, XM (2007) Induction of antiviral resistance and stimulary effect by oligochitosan in tobacco. Pesticide Biochemistry and Physiology 87, 7884.Google Scholar
Zheng, K, Zhao, J, Lin, D, Chen, J, Xu, J, Zhou, H, Teng, S and Dong, Y (2016) The rice TCM5 gene encoding a novel Deg protease protein is essential for chloroplast development under high temperatures. Rice 9, 13.Google Scholar
Zong, H, Li, K, Liu, S, Song, L, Xing, R, Chen, X and Li, P (2017) Improvement in cadmium tolerance of edible rape (Brassica rapa L.) with exogenous application of chitooligosaccharide. Chemosphere 181, 92100.Google Scholar
Zou, P, Li, K, Liu, S, Xing, R, Qin, Y, Yu, H, Zhou, M and Li, P (2015) Effect of chitooligosaccharides with different degrees of acetylation on wheat seedlings under salt stress. Carbohydrate Polymers 126, 6269.Google Scholar
Zou, P, Li, K, Liu, S, He, X, Zhang, X, Xing, R and Li, P (2016) Effect of sulfated chitooligosaccharides on wheat seedlings (Triticum aestivum L.) under salt stress. Journal of Agricultural and Food Chemistry 64, 28152821.Google Scholar
Zou, P, Tian, X, Dong, B and Zhang, C (2017) Size effects of chitooligomers with certain degrees of polymerization on the chilling tolerance of wheat seedlings. Carbohydrate Polymers 160, 194202.Google Scholar