Chemical induction of leaf senescence and powdery mildew resistance involves ethylene-mediated chlorophyll degradation and ROS metabolism in cucumber

Dingyu Zhang , Shengdong Wu , Ning Li , Jiong Gao , Shihui Liu , Shuai Zhu , Zilin Li , Guodong Ren , Benke Kuai

Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) : uhac101

PDF (1801KB)
Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) :uhac101 DOI: 10.1093/hr/uhac101
Article
research-article
Chemical induction of leaf senescence and powdery mildew resistance involves ethylene-mediated chlorophyll degradation and ROS metabolism in cucumber
Author information +
History +
PDF (1801KB)

Abstract

Timely initiation of leaf senescence is an integral part of plant development and, importantly, an adaptive strategy by which plants cope with various stresses, e.g. to limit the spread of pathogens. Powdery mildew is a major cucumber disease that promotes the initiation/progression of leaf senescence and reduces leaf photosynthesis, resulting in severe losses of yield and quality. However, how powdery mildew induces leaf senescence and how cucumber plants respond to enhance their resistance remain unclear. Here, with established agrochemical induction and pathogen inoculation systems, we demonstrate that both probenazole (PBZ) and powdery mildew activate ethylene (ET) biosynthesis and signal transduction, consequently promoting leaf senescence and enhancing plant resistance to powdery mildew through CsEIN3 to directly upregulate the expression of CsCCGs and CsRBOHs. Our analysis convincingly suggests that the regulation of leaf senescence and powdery mildew resistance is interconnected and mediated mainly by ET in cucumber.

Cite this article

Download citation ▾
Dingyu Zhang, Shengdong Wu, Ning Li, Jiong Gao, Shihui Liu, Shuai Zhu, Zilin Li, Guodong Ren, Benke Kuai. Chemical induction of leaf senescence and powdery mildew resistance involves ethylene-mediated chlorophyll degradation and ROS metabolism in cucumber. Horticulture Research, 2022, 9 (1) : uhac101 DOI:10.1093/hr/uhac101

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Taylor L, Nunes-Nesi A, Parsley K et al. Cytosolic pyruvate, orthophosphate dikinase functions in nitrogen remobilization during leaf senescence and limits individual seed growth and nitrogen content. Plant J. 2010; 62: 641-52.

[2]

Woo HR, Kim HJ, Lim PO et al. Leaf Senescence: Systems and Dynamics Aspects. Annu Rev Plant Biol 2019; 70: 347-76.

[3]

Lim PO, Kim HJ, Nam HG . Leaf senescence. Annu Rev Plant Biol. 2007; 58: 115-36.

[4]

Kuai B, Chen J, Hortensteiner S . The biochemistry and molecular biology of chlorophyll breakdown. J Exp Bot. 2018; 69: 751-67.

[5]

Castro B, Citterico M, Kimura S et al. Stress-induced reactive oxygen species compartmentalization, perception and signalling. Nat Plants. 2021; 7: 403-12.

[6]

Yuan M, Jiang Z, Bi G et al. Pattern-recognition receptors are required for NLR-mediated plant immunity. Nature. 2021; 592: 105-9.

[7]

Miller G, Schlauch K, Tam R et al. The plant NADPH oxidase RBOHD mediates rapid systemic Signaling in response to diverse stimuli. Sci Signal. 2009; 2: ra45.

[8]

Peng YY, Liao LL, Liu S et al. Magnesium deficiency triggers SGR-mediated chlorophyll degradation for magnesium remobilization. Plant Physiol. 2019; 181: 262-75.

[9]

Li Z, Wu S, Chen J et al. NYEs/SGRs-mediated chlorophyll degradation is critical for detoxification during seed maturation in Arabidopsis. Plant J. 2017; 92: 650-61.

[10]

Zhang Y, Wang HL, Li Z et al. Genetic network between leaf senescence and plant immunity: crucial regulatory nodes and new insights. Plants-Basel. 2020; 9: 495.

[11]

Waszczak C, Carmody M, Kangasjarvi J . Reactive Oxygen Species. Plant Signaling in Annual Review of Plant Biology. 2018; 69: 209-36.

[12]

Zhang Y, Gao Y, Wang HL et al. Verticillium dahliae secretory effector PevD1 induces leaf senescence by promoting ORE1-mediated ethylene biosynthesis. Mol Plant. 2021; 14: 1901-17.

[13]

Wang Y, Tan J, Wu Z et al. STAYGREEN STAY HEALTHY: a loss-of-susceptibility mutation in the STAYGREEN gene provides durable, broad-spectrum disease resistances for over 50 years of US cucumber production. New Phytol. 2019; 221: 415-30.

[14]

Pan J, Tan J, Wang Y et al. STAYGREEN (CsSGR) is a candidate for the anthracnose (Colletotrichum orbiculare) resistance locus cla in Gy14 cucumber. Theor Appl Genet. 2018; 131: 1577-87.

[15]

Bektas Y, Eulgem T . Synthetic plant defense elicitors. Front Plant Sci. 2015; 5: 804.

[16]

Iwata M . Probenazole - a plant defence activator. Pesticide Outlook 10.1039/B100805F. 2001; 12: 28-31.

[17]

Yoshioka K, Nakashita H, Klessig DF et al. Probenazole induces systemic acquired resistance in Arabidopsis with a novel type of action. Plant J. 2001; 25: 149-57.

[18]

Yu J, Gao J, Wang XY et al. The pathway and regulation of salicylic acid biosynthesis in Probenazole-treated Arabidopsis. J Plant Biol. 2010; 53: 417-24.

[19]

Mejri S, Magnin-Robert M, Randoux B et al. Saccharin provides protection and activates Defense mechanisms in wheat against the Hemibiotrophic pathogen Zymoseptoria tritici. Plant Dis. 2021; 105: 780-6.

[20]

Wu Z, Wang G, Zhang B et al. Metabolic mechanism of plant Defense against Rice blast induced by Probenazole. Meta. 2021; 11: 246.

[21]

Zhu Z, Gao J, Yang JX et al. Synthetic promoters consisting of defined cis-acting elements link multiple signaling pathways to probenazole-inducible system. J Zhejiang Univ Sci B. 2015; 16: 253-63.

[22]

Chen Q, Yu G, Wang X et al. Genetics and resistance mechanism of the cucumber (Cucumis sativus L.) against powdery mildew. J Plant Growth Regul. 2021; 40: 147-53.

[23]

González Morejón N, Martínez Coca B, Infante Martínez D . Powdery mildew on cucurbits. Revista de Protección Vegetal. 2010; 25: 44-50.

[24]

Phuong LT, Zhao L, Fitrianti AN et al. The plant activator saccharin induces resistance to wheat powdery mildew by activating multiple defense-related genes. Nihon Shokubutsu Byori Gakkaiho. 2020; 86: 107-13.

[25]

Nakashita H, Yoshioka K, Yasuda M et al. Probenazole induces systemic acquired resistance in tobacco through salicylic acid accumulation. Physiol Mol Plant Pathol. 2002; 61: 197-203.

[26]

Yang KH, Huang CJ, Liu YH et al. Efficacy of probenazole for control of southern corn leaf blight. J Pestic Sci. 2011; 36: 235-9.

[27]

Zhang D, Zhu Z, Gao J et al. The NPR1-WRKY46-WRKY6 signaling cascade mediates probenazole/salicylic acid-elicited leaf senescence in Arabidopsis thaliana. J Integr Plant Biol. 2021; 63: 924-36.

[28]

Saijo Y, Loo EPI . Plant immunity in signal integration between biotic and abiotic stress responses. New Phytol. 2020; 225: 87-104.

[29]

Bostock RM . Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu Rev Phytopathol. 2005; 43: 545-80.

[30]

Berger S, Sinha AK, Roitsch T . Plant physiology meets phytopathology: plant primary metabolism and plant-pathogen interactions. J Exp Bot. 2007; 58: 4019-26.

[31]

Yang C, Lu X, Ma B et al. Ethylene Signaling in Rice and Arabidopsis: conserved and diverged aspects. Mol Plant. 2015; 8: 495-505.

[32]

van der Maaten L, Hinton G . Visualizing data using t-SNE. J Mach Learn Res. 2008; 9: 2579-605.

[33]

Dolgikh VA, Pukhovaya EM, Zemlyanskaya EV . Shaping ethylene response: the role of EIN3/EIL1 transcription factors. Front Plant Sci. 2019; 10: 1030.

[34]

Wang L, Qiao H . New insights in transcriptional regulation of the ethylene response in Arabidopsis. Front Plant Sci. 2019; 10: 790.

[35]

Chang KN, Zhong S, Weirauch MT et al. Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis. elife. 2013; 2: e00675.

[36]

Yang C, Li W, Cao J et al. Activation of ethylene signaling pathways enhances disease resistance by regulating ROS and phytoalexin production in rice. Plant J. 2017; 89: 338-53.

[37]

Li Q, Li H, Huang W et al. A chromosome-scale genome assembly of cucumber (Cucumis sativus L.). Gigascience. 2019; 8: giz072.

[38]

Mattila H, Khorobrykh S, Havurinne V et al. Reactive oxygen species: reactions and detection from photosynthetic tissues. Journal of Photochemistry and Photobiology B-Biology. 2015; 152: 176-214.

[39]

Van der Ent S, Pieterse CMJ . ETHYLENE: MULTI-TASKER IN PLANT-ATTACKER INTERACTIONS. In: McManus MT, ed. Plant Hormone Ethylene.New Jersey, USA: Wiley-Blackwell, Vol. 44. 2012, 343-77.

[40]

Xu XW, Liu X, Yan Y et al. Comparative proteomic analysis of cucumber powdery mildew resistance between a single-segment substitution line and its recurrent parent. Horticulture Research. 2019; 6: 115.

[41]

Chen H, Xue L, Chintamanani S et al. ETHYLENE INSENSITIVE3 and ETHYLENE INSENSITIVE3-LIKE1 repress SALICYLIC ACID INDUCTION DEFICIENT2 expression to negatively regulate plant innate immunity in Arabidopsis. Plant Cell. 2009; 21: 2527-40.

[42]

Peng J, Li Z, Wen X et al. Salt-induced stabilization of EIN3/EIL1 confers salinity tolerance by deterring ROS accumulation in Arabidopsis. PLoS Genet. 2014; 10: e1004664.

[43]

Qiu K, Li Z, Yang Z et al. EIN3 and ORE1 accelerate Degreening during ethylene-mediated leaf senescence by directly activating chlorophyll catabolic genes in Arabidopsis. PLoS Genet. 2015; 11: e1005399.

[44]

Shirasu K, Schulze-Lefert P . Regulators of cell death in disease resistance. Plant Mol Biol. 2000; 44: 371-85.

[45]

Yi X, Lu Y . Residues and dynamics of probenazole in rice field ecosystem. Chemosphere. 2006; 65: 639-43.

[46]

Guan R, Su J, Meng X et al. Multilayered regulation of ethylene induction plays a positive role in Arabidopsis resistance against pseudomonas syringae. Plant Physiol. 2015; 169: 299.

[47]

Glazebrook J . Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol. 2005; 43: 205-27.

[48]

Boatwright JL, Pajerowska-Mukhtar K . Salicylic acid: an old hormone up to new tricks. Mol Plant Pathol. 2013; 14: 623-34.

[49]

Zheng HY, Dong L, Han X et al. The TuMYB46L-TuACO3 module regulates ethylene biosynthesis in einkorn wheat defense to powdery mildew. New Phytol. 2020; 225: 2526-41.

[50]

Wang YH, VandenLangenberg K, Wen CL et al. QTL mapping of downy and powdery mildew resistances in PI 197088 cucumber with genotyping-by-sequencing in RIL population. Theor Appl Genet. 2018; 131: 597-611.

[51]

Ren GD, Zhou Q, Wu S et al. Reverse genetic identification of CRN1 and its distinctive role in chlorophyll degradation in Arabidopsis. J Integr Plant Biol. 2010; 52: 496-504.

[52]

Wu S, Li Z, Yang L et al. NON-YELLOWING2 (NYE2), a close Paralog of NYE1, plays a positive role in chlorophyll degradation in Arabidopsis. Mol Plant. 2016;9:624-7.

[53]

Iwai T, Seo S, Mitsuhara I et al. Probenazole-induced accumulation of salicylic acid confers resistance to Magnaporthe grisea in adult rice plants. Plant Cell Physiol. 2007; 48: 915-24.

[54]

Huang S, Li R, Li S et al. The genome of the cucumber, Cucumis sativus L. Nat Genet. 2009; 41: 1275-81.

[55]

Wang C, Huang J, Zhang J et al. The largest subunit of DNA Polymerase Delta is required for Normal formation of meiotic type I crossovers. Plant Physiol. 2019; 179: 446-59.

PDF (1801KB)

30

Accesses

0

Citation

Detail

Sections
Recommended

/