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Journal of Integrative Agriculture  2022, Vol. 21 Issue (3): 697-709    DOI: 10.1016/S2095-3119(21)63630-4
Special Issue: 园艺-分子生物合辑Horticulture — Genetics · Breeding
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Tomato SlPti5 plays a regulative role in the plant immune response against Botrytis cinerea through modulation of ROS system and hormone pathways
TANG Qiong1, ZHENG Xiao-dong1, GUO Jun2, YU Ting1
1 College of Biosystems Engineering and Food Science, National Engineering Laboratory of Intelligent Food Technology and Equipment, Key Laboratory for Agro-Products Postharvest Handling of Ministry of Agriculture, Zhejiang Key Laboratory for Agro-Food Processing, Zhejiang University, Hangzhou 310058, China
2 State Key Laboratory of Food Nutrition and Safety, Key Laboratory of Food Nutrition and Safety, Ministry of Education of China, Tianjin Key Laboratory of Food Nutrition and Safety, Tianjin University of Science and Technology, Tianjin 300457, China
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摘要  

虽然SlPti5基因在茄属植物和拟南芥病原体感染中已表现出对相关拮抗基因的关键调控作用,但是关于其对番茄植株生长和抗病过程中ROS系统和激素途径的调控响应机制的研究尚不全面。本研究利用基于病毒诱导的基因沉默(VIGS)系统研究了SlPti5基因在番茄对灰霉防御反应中的作用。表达谱分析表明,SlPti5基因在灰霉病感染后被显著诱导,在番茄叶片和果实中表达量较高。沉默抑制了番茄植株的早期生长,减弱了植株的抗病性,促进了活性氧(ROS)的爆发,影响了参与活性氧清除系统相关基因的表达以及降低了乙烯/茉莉酸信号和茉莉酸介导的信号通路以及调控一些关键的PR蛋白基因的表达来刺激番茄植株对灰霉感染的免疫应答。




Abstract  While SlPti5 has been shown to play a crucial role in the regulation of antagonistic genes in Solanum lycopersicum and Arabidopsis against pathogen infection, there have been no comprehensive studies on the effects of SlPti5 on the regulatory response mechanism of reactive oxygen species (ROS) system and hormone pathways during growth and disease resistance of tomato plants.  Here, we investigated the function of SlPti5 in the defense response of tomato against Botrytis cinerea utilizing a virus-induced gene silencing (VIGS)-based system.  Expression profile analysis showed that SlPti5 was significantly induced upon B. cinerea infection, with high expression levels in the leaves and fruit of tomato.  VIGS-based silencing of SlPti5 inhibited early vegetative growth, increased the plant’s susceptibility to infection, promoted the development of ROS, affected the expression of genes involved in the ROS scavenging system, and attenuated the expression of genes associated with pathogenesis and the ethylene/jasmonic acid signaling pathways.  In sum, our data demonstrated that SlPti5 stimulates the immune response of tomato plant to Botrytis cinerea infection by involving the ethylene (ET)- and jasmonic acid (JA)-mediated pathways and modulating the expression of some key pathogenesis-related (PR) genes.
Keywords:  Tomato (Solanum lycopersicum)        Botrytis cinerea        SlPti5        Immune response        ET - and JA - mediated signaling pathways        Pathogenesis-related proteins  
Received: 06 August 2020   Accepted: 15 January 2021
Fund: This research was supported by the National Key Technology R&D Program of China (2016YFD0401201), the National Natural Science Foundation of China (31801602 and 31571897), the Project of Tianjin Education Commission Scientific Research Plan, China (2018KJ094) and the National Science and Technology Major Project of China (2018ZX10101003-002-004).
Corresponding Authors:  TANG Qiong, E-mail: tangqiong1104@zju.edu.cn;    
About author:  TANG Qiong, E-mail: tangqiong1104@zju.edu.cn; Correspondence YU Ting, Tel/Fax: +86-571-88982191, E-mail: yuting@zju.edu.cn; GUO Jun, Tel/Fax: +022-60912486, E-mail: guojun@tust.edu.cn;

Cite this article: 

TANG Qiong, ZHENG Xiao-dong, GUO Jun, YU Ting. 2022. Tomato SlPti5 plays a regulative role in the plant immune response against Botrytis cinerea through modulation of ROS system and hormone pathways. Journal of Integrative Agriculture, 21(3): 697-709.

AkagiI A, Dandekar A M, Stotz H U. 2011. Resistance of Malus domestica fruit to Botrytis cinerea depends on endogenous ethylene biosynthesis. Phytopathology, 101, 1311–1321.
Alazem M, Lin N S. 2015. Roles of plant hormones in the regulation of host–virus interactions. Molecular Plant Pathology, 16, 529–540.
Alves M S, Dadalto S P, Gonalves A B, Souza G, Barros V A, Fietto L G. 2013. Plant bZIP transcription factors responsive to pathogens: A review. International Journal of Molecular Sciences, 14, 7815–7828.
Bernoux M, Ellis J G, Dodds P N. 2011. New insights in plant immunity signaling activation. Current Opinion in Plant Biology, 14, 512–518.
Buscaill P, Rivas S. 2014. Transcriptional control of plant defence responses. Current Opinion in Plant Biology, 20, 35–46.
Dangl J L, Jones J D G. 2001. Plant pathogens and integrated defence responses to infection. Nature, 411, 826–833.
Doke N. 1983. Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of phytophthora-infestans and to the hyphal wall components. Physiological Plant Pathology, 23, 345–357.
Dong X N. 1998. SA, JA, ethylene, and disease resistance in plants. Current Opinion in Plant Biology, 1, 316–323.
Genty B, Biantais J M, Baker N R. 1989. The relationship between the quantum yield of photosynthetic electron-transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta, 990, 87–92.
Gonorazky G, Guzzo M C, Abd-El-Haliem A M, Joosten M H A J, Laxalt A M. 2016. Silencing of the tomato phosphatidylinositol-phospholipase C2 (SlPLC2) reduces plant susceptibility to Botrytis cinerea. Molecular Plant Pathology, 17, 1354–1363.
Gu Y Q, Wildermuth M C, Chakravarthy S, Loh Y T, Yang C M, He X H, Han Y, Martin G B. 2002. Tomato transcription factors Pti4, Pti5, and Pti6 activate defense responses when expressed in Arabidopsis. Plant Cell, 14, 817–831.
Harel Y M, Mehari Z H, Rav-David D, Elad Y. 2014. Systemic resistance to gray mold induced in tomato by benzothiadiazole and Trichoderma harzianum T39. Phytopathology, 104, 150–157.
He P, Warren R F, Shan L B, Zhao T H, Zhou J M. 2001. Overexpression of Pti5 in tomato potentiates pathogen-induced defense gene expression and enhances disease resistance to Pseudomonas syringae pv. tomato. Molecular Plant–Microbe Interactions, 14, 1453–1457.
Hu Y, Wu Q Y, Peng Z, Sprague S A, Wang W, Park J, Akhunov E, Jagadish K, Nakata P A, Cheng N. 2017. Silencing of OsGRXS17 in rice improves drought stress tolerance by modulating ROS accumulation and stomatal closure. Scientific Reports, 7, 15950.
Hu Z J, Shao S J, Zheng C F, Sun Z, Shi J, Qi Z, Shi K. 2018. Induction of systemic resistance in tomato against Botrytis cinerea by N-decanoyl-homoserine lactone via jasmonic acid signaling. Planta, 247, 1217–1227.
Lai J, Cao X, Yu T, Wang Q, Zhang Y, Zheng X, Lu H. 2018. Effect of Cryptococcus laurentii on inducing disease resistance in cherry tomato fruit with focus on the expression of defense-related genes. Food Chemistry, 254, 208–216.
Li X H, Huang L, Zhang Y F, Ouyang Z, Hong Y, Zhang H, Li D, Song F. 2014. Tomato SR/CAMTA transcription factors SlSR1 and SlSR3L negatively regulate disease resistance response and SlSR1L positively modulates drought stress tolerance. BMC Plant Biology, 14, 286.
Liu M C, Gomes B L, Mila I, Purgatto E, Peres L E P, Frasse P, Maza E, Zouine M, Roustan J P, Bouzayen M. 2016. Comprehensive profiling of ethylene response factor expression identifies ripening-associated ERF genes and their link to key regulators of fruit ripening in tomato. Plant Physiology, 170, 1732–1744.
Liu M C, Pirrello J, Kesari R, Mila I, Regad F. 2013. A dominant repressor version of the tomato SI-ERF.B3 gene confers ethylene hypersensitivity via feedback regulation of ethylene signaling and response components. Plant Journal, 76, 406–419.
Liu Y L, Schiff M, Dinesh-Kumar S P. 2002. Virus-induced gene silencing in tomato. Plant Journal, 31, 777–786.
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real time quantitive PCR and the 2–ΔΔCT method. Methods, 25, 402–408.
Mata C I, Van De Poel B, Hertog M L, Tran D, Nicolaia B M. 2018. Transcription analysis of the ethylene receptor and CTR genes in tomato: The effects of on and off-vine ripening and 1-MCP. Postharvest Biology and Technology, 140, 67–75.
Mengiste T. 2012. Plant immunity to necrotrophs. Annual Review of Phytopathology, 50, 267–294.
Min D, Li F, Zhang X, Pan S, Cui X, Dong L, Ren C, Meng D, Jian L. 2018. Effect of methyl salicylate in combination with 1-methylcyclopropene on postharvest quality and decay caused by Botrytis cinerea in tomato fruit. Journal of the Science and Food and Agriculture, 98, 3815–3822.
Mohamed E O, Taha A E R, Luciano, Abdelbasset E H, María C R, Fouad D, Adrian V, Kamal B. 2011. Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato. Plant Cell, 23, 2405–2421.
Nie P, Xia L, Wang S, Guo J, Zhao H, Niu D. 2017. Induced systemic resistance against Botrytis cinerea by Bacillus cereus AR156 through a JA/ET- and NPR1-dependent signaling pathway and activates PAMP-triggered immunity in Arabidopsis. Frontiers in Plant Science, 8, 238.
Ohmetakagi M, Shinshi H. 1995. Ethylene-inducible DNA-binding proteins that interact with an ethylene-responsive element. Plant Cell, 7, 173–182.
Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran L S P. 2013. Sensing the environment: Key roles of membrane-localized kinases in plant perception and response to abiotic stress. Journal of Experimental Botany, 64, 445–458.
Ouyang Z, Liu S, Huang L, Hong Y, Li X, Huang L, Zhang Y, Zhang H, Li D, Song F. 2016. Tomato SlERF.A1, SlERF.B4, SlERF.C3 and SlERF.A3, members of B3 group of ERF family, are required for resistance to Botrytis cinerea. Frontiers in Plant Science, 7, 1964.
Pieterse C M J, Leon-Reyes A, Van der Ent S, Van Wees S C M. 2009. Networking by small-molecule hormones in plant immunity. Nature Chemical Biology, 5, 308–316.
Pietrowska E, Malolepsza U, Rozalska S, Nawrocka J, Kazmierczak A. 2015. Reactive oxygen and nitrogen (ROS and RNS) species generation and cell death in tomato suspension cultures–Botrytis cinerea interaction. Protoplasma, 252, 307–319.
Segarra G, Santpere G, Elena G, Trillas I. 2013. Enhanced Botrytis cinerea resistance of Arabidopsis plants grown in compost may be explained by increased expression of defense-related genes, as revealed by microarray analysis. PLoS ONE, 8, e56075.
Shigenaga A M, Argueso C T. 2016. No hormone to rule them all: Interactions of plant hormones during the responses of plants to pathogens. Seminars Cell & Developmental Biology, 56, 174–189.
Souza T P, Dias R O, Silva-Filho M C. 2017. Defense-related proteins involved in sugarcane responses to biotic stress. Genetics and Molecular Biology, 40, 360–372.
Tang Q, Zhu F H, Cao X, Zheng X D, Yu T, Lu L F. 2019. Cryptococcus laurentii controls gray mold of cherry tomato fruit via modulation of ethylene-associated immune responses. Food Chemistry, 278, 240–247.
Thara V K, Tang X, Gu Y Q, Martin G B, Zhou J. 1999. Pseudomonas syringae pv tomato induces the expression of tomato EREBP-like genes Pti4 and Pti5 independent of ethylene, salicylate and jasmonate. Plant Journal, 20, 475–483.
Thordal C H, Zhang Z G, Wei Y D, Collinge D B. 1997. Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley–powdery mildew interaction. Plant Journal, 11, 1187–1194.
Townsend A J, Saccon F, Giovagnetti V, Wilson S, Ungerer P, Ruban A V. 2018. The causes of altered chlorophyll fluorescence quenching induction in the Arabidopsis mutant lacking all minor antenna complexes. Biochimica et Biophysica Acta-Bioenergetics, 1859, 666–675.
Wang Y, Bao Y, Shen D, Feng W, Xiao D Z. 2008. Biocontrol of Alternaria alternata on cherry tomato fruit by use of marine yeast Rhodosporidium paludigenum Fell & Tallman. International Journal of Food Microbiology, 123, 234–239.
Wu C J, Avila C A, Goggin F L. 2015. The ethylene response factor Pti5 contributes to potato aphid resistance in tomato independent of ethylene signalling. Journal of Experimental Botany, 66, 559–570.
Yang H H, Shen F Y, Wang H X, Zhao T T, Li J F. 2020. Functional analysis of the SlERF01 gene in disease resistance to S. lycopersici. BMC Plant Biology, 20, 376–387.
Zhang H, Hu Z, Lei C, Zheng C, Wang J, Shao S, Li X, Xia X, Cai X, Zhou J. 2018. A plant phytosulfokine peptide initiates auxin-dependent immunity through cytosolic Ca2+ signaling in tomato. Plant Cell, 30, 652–667.
Zhang H J, Huang L, Dai Y, Liu S X, Hong Y B, Tian L M, Huang L H, Cao Z Y, Li D Y, Song F M. 2015. Arabidopsis AtERF15 positively regulates immunity against Pseudomonas syringae pv. tomato DC3000 and Botrytis cinerea. Frontiers in Plant Science, 6, 686–698. 
Zhang L M, Leng C Y, Luo H, Wu X Y, Liu Z Q, Zhang Y M, Zhang H, Xia Y, Shang L, Cai H W, Jing H C. 2018. Sweet sorghum originated through selection of dry, a plant-specific NAC transcription factor gene. Plant Cell, 30, 2286–2307.
Zhang Q M, Yong D J, Zhang Y, Shi X P, Li B H, Li G F, Liang W X, Wang C X. 2016. Streptomyces rochei A-1 induces resistance and defense-related responses against Botryosphaeria dothidea in apple fruit during storage. Postharvest Biology and Technology, 115, 30–37.
Zhang S, Li X, Sun Z H, Shao S J, Hu L F, Ye M, Zhou Y H, Xia X J, Yu J Q, Shi K. 2015. Antagonism between phytohormone signalling underlies the variation in disease susceptibility of tomato plants under elevated CO2. Journal of Experimental Botany, 66, 1951–1963.
Zhang Y F, Li D Y, Zhang H J, Hong Y B, Huang L, Liu S X, Li X H, Ouyang Z G, Song F M. 2015. Tomato histone H2B monoubiquitination enzymes SlHUB1 and SlHUB2 contribute to disease resistance against Botrytis cinerea through modulating the balance between SA- and JA/ET-mediated signaling pathways. BMC Plant Biology, 15, 1–20.
Zhou J M, Tang X Y, Martin G B. 1997. The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes. EMBO Journal, 16, 3207–3218.


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