Signalling mechanisms and agricultural applications of (Z)-3-hexenyl butyrate-mediated stomatal closure

Celia Payá, Borja Belda-Palazón, Francisco Vera-Sirera, Julia Pérez-Pérez, Lucía Jordá, Ismael Rodrigo, José María Bellés, María Pilar López-Gresa, Purificación Lisón

PDF
Horticulture Research ›› 2024, Vol. 11 ›› Issue (1) : 248. DOI: 10.1093/hr/uhad248
ARTICLES

Signalling mechanisms and agricultural applications of (Z)-3-hexenyl butyrate-mediated stomatal closure

Author information +
History +

Abstract

Biotic and abiotic stresses can severely limit crop productivity. In response to drought, plants close stomata to prevent water loss. Furthermore, stomata are the main entry point for several pathogens. Therefore, the development of natural products to control stomata closure can be considered a sustainable strategy to cope with stresses in agriculture. Plants respond to different stresses by releasing volatile organic compounds. Green leaf volatiles, which are commonly produced across different plant species after tissue damage, comprise an important group within volatile organic compounds. Among them, (Z)-3-hexenyl butyrate (HB) was described as a natural inducer of stomatal closure, playing an important role in stomatal immunity, although its mechanism of action is still unknown. Through different genetic, pharmacological, and biochemical approaches, we here uncover that HB perception initiates various defence signalling events, such as activation of Ca2+ permeable channels, mitogen-activated protein kinases, and production of Nicotinamide adenine dinucleotide phosphate (NADPH) oxidase-mediated reactive oxygen species. Furthermore, HB-mediated stomata closure was found to be independent of abscisic acid biosynthesis and signalling. Additionally, exogenous treatments with HB alleviate water stress and improve fruit productivity in tomato plants. The efficacy of HB was also tested under open field conditions, leading to enhanced resistance against Phytophthora spp. and Pseudomonas syringae infection in potato and tomato plants, respectively. Taken together, our results provide insights into the HB signalling transduction pathway, confirming its role in stomatal closure and plant immune system activation, and propose HB as a new phytoprotectant for the sustainable control of biotic and abiotic stresses in agriculture.

Cite this article

Download citation ▾
Celia Payá, Borja Belda-Palazón, Francisco Vera-Sirera, Julia Pérez-Pérez, Lucía Jordá, Ismael Rodrigo, José María Bellés, María Pilar López-Gresa, Purificación Lisón. Signalling mechanisms and agricultural applications of (Z)-3-hexenyl butyrate-mediated stomatal closure. Horticulture Research, 2024, 11(1): 248 https://doi.org/10.1093/hr/uhad248

References

[1.]
Jones JDG, Dangl JL. The plant immune system. Nature. 2006;444: 323-9
[2.]
Boutrot F, Zipfel C. Function, discovery, and exploitation of plant pattern recognition receptors for broad-spectrum disease resistance. Annu Rev Phytopathol. 2017;55:257-86
[3.]
Zhang J, Zhou JM. Plant immunity triggered by microbial molec-ular signatures. Mol Plant. 2010;3:783-93
[4.]
Bjornson M, Pimprikar P, Nürnberger T. et al. The transcriptional landscape of Arabidopsis thaliana pattern-triggered immunity. Nat plants. 2021;7:579-86
[5.]
Cui H, Tsuda K, Parker JE. Effector-triggered immunity: from pathogen perception to robust defense. Annu Rev Plant Biol. 2015;66:487-511
[6.]
Wang W, Feng B, Zhou JM. et al. Plant immune signaling: advanc-ing on two frontiers. J Integr Plant Biol. 2020;62:2-24
[7.]
Yuan M, Ngou BPM, Ding P. et al. PTI-ETI crosstalk: an integrative view of plant immunity. Curr Opin Plant Biol. 2021;62:102030
[8.]
Melotto M, Underwood W, Koczan J. et al. Plant stomata function in innate immunity against bacterial invasion. Cell. 2006;126: 969-80
[9.]
Kadota Y, Sklenar J, Derbyshire P. et al. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol Cell. 2014;54:43-55
[10.]
Arnaud D, Hwang I. A sophisticated network of signaling path-ways regulates stomatal defenses to bacterial pathogens. Mol Plant. 2015;8:566-81
[11.]
Bharath P, Gahir S, Raghavendra AS. Abscisic acid-induced stomatal closure: an important component of plant defense against abiotic and biotic stress. Front Plant Sci. 2021;12:1-18
[12.]
Su J, Zhang M, Zhang L. et al. Regulation of stomatal immunity by interdependent functions of a pathogen-responsive MPK3/MPK6 cascade and abscisic acid. Plant Cell. 2017;29:526-42
[13.]
Montillet JL, Leonhardt N, Mondy S. et al. An abscisic acid-independent oxylipin pathway controls stomatal closure and immune defense in Arabidopsis. PLoS Biol. 2013;11:13-5
[14.]
Heil M, Bueno JCS. Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci U S A. 2007;104:5467-72
[15.]
Baldwin IT, Halitschke R, Paschold A. et al. Volatile signaling in plant-plant interactions: ‘talking trees’ in the genomics era. Science. 2006;311:812-5
[16.]
Dudareva N, Klempien A, Muhlemann JK. et al. Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol. 2013;198:16-32
[17.]
Ameye M, Audenaert K, De Zutter N. et al. Priming of wheat with the green leaf volatile Z-3-hexenyl acetate enhances defense against Fusarium Graminearum but boosts deoxynivalenol pro-duction. Plant Physiol. 2015;167:1671-84
[18.]
Brilli F, Loreto F, Baccelli I. Exploiting plant volatile organic com-pounds (VOCS) in agriculture to improve sustainable defense strategies and productivity of crops. Front Plant Sci. 2019; 10:1-8
[19.]
Cofer TM, Engelberth M, Engelberth J. Green leaf volatiles protect maize (Zea mays) seedlings against damage from cold stress. Plant Cell Environ. 2018;41:1673-82
[20.]
Luna E. Using green vaccination to brighten the agronomic future. Pesticide outlook. 2016;27:136-40
[21.]
López-Gresa MP, Lisón P, Campos L. et al. A non-targeted metabolomics approach unravels the VOCs associated with the tomato immune response against Pseudomonas syringae. Front Plant Sci. 2017;8:1-15
[22.]
López-Gresa MP, Payá C, Ozáez M. et al. A new role for green leaf volatile esters in tomato stomatal defense against pseudomonas syringe pv. Tomato. Front Plant Sci. 2018;871:1-12
[23.]
Payá C, López-Gresa MP, Intrigliolo DS. et al. (Z)-3-hexenyl butyrate induces stomata closure and ripening in vitis vinifera. Agronomy. 2020;10, 1122.
[24.]
Tal M. Abnormal Stomatal behavior in Wilty mutants of tomato. Plant Physiol. 1966;41:1387-91
[25.]
Zhou J, Wang J, Zheng Z. et al. Characterization of the promoter and extended C-terminal domain of Arabidopsis WRKY33 and functional analysis of tomato WRKY33 homologues in plant stress responses. JExp Bot. 2015;66:4567-83
[26.]
Wang Y, Schuck S, Wu J. et al. A mpk3/6-wrky33-ald1-pipecolic acid regulatory loop contributes to systemic acquired resis-tance[open]. Plant Cell. 2018;30:2480-94
[27.]
Hahn A, Harter K. Mitogen-activated protein kinase cascades and ethylene: signaling, biosynthesis, or both? Plant Physiol. 2009;149:1207-10
[28.]
Kaur G, Asthir B. Proline: a key player in plant abiotic stress tolerance. Biol Plant. 2015;59:609-19
[29.]
Gonzalez-Guzmán M, Rodríguez PL, Lorenzo-Orts L. et al. Tomato PYR/PYL/RCAR abscisic acid receptors show high expression in root, differential sensitivity to the abscisic acid agonist quin-abactin, and the capability to enhance plant drought resistance. JExp Bot. 2014;65:4451-64
[30.]
Lisón P, López-Gresa MP, Rodrigo I., Bellés JM et al. Use of a compound for protecting plants by means of stomatal closure and Method for protecting plants by means of stomatal closure which Comprises applying said compound to the plants PCT/ES2018/070. WO 2018/206835. 05.01.2022
[31.]
Asai N, Nishioka T, Takabayashi J. et al. Plant volatiles regulate the activities of Ca2+-permeable channels and promote cyto-plasmic calcium transients in Arabidopsis leaf cells. Plant Signal Behav. 2009;4:294-300
[32.]
Mirabella R, Rauwerda H, Allmann S. et al. WRKY40 and WRKY6 act downstream of the green leaf volatile E-2-hexenal in Ara-bidopsis. Plant J. 2015;83:1082-96
[33.]
Engelberth J, Contreras CF, Dalvi C. et al. Early Transcriptome analyses of Z-3-Hexenol-treated Zea mays revealed distinct tran-scriptional networks and anti-herbivore defense potential of green leaf volatiles. PLoS One. 2013;8:e77465
[34.]
Duran-Flores D, Heil M. Sources of specificity in plant damaged-self recognition. Curr Opin Plant Biol. 2016;32:77-87
[35.]
Pirasteh-Anosheh H, Saed-Moucheshi A, Pakniyat H. et al. Stom-atal responses to drought stress. Water Stress Crop Plants. 2016; 24-40
[36.]
Ling H, Zeng X, Guo S. Functional insights into the late embryo-genesis abundant (LEA) protein family from Dendrobium offic-inale (Orchidaceae) using an Escherichia coli system. Sci Rep. 2016;6:39693
[37.]
Conrath U. Systemic acquired resistance. Plant Signal Behav. 2006;1:179-84
[38.]
Martínez-Aguilar K, Ramírez-Carrasco G, Hernández-Chávez JL. et al. Use of BABA and INA as activators of a primed state in the common bean (Phaseolus vulgaris L.). Front Plant Sci. 2016;7:1-17
[39.]
Aranega-Bou P, dela O Leyva M, Finiti I. et al. Priming of plant resistance by natural compounds. Hexanoic acid as a model. Front Plant Sci. 2014;5.
[40.]
Llorens E, Camañes G, Lapeña L. et al. Priming by hexanoic acid induce activation of mevalonic and linolenic pathways and promotes the emission of plant volatiles. Front Plant Sci. 2016;7: 1-12
[41.]
Cho L-H, Yoon J, An G. The control of flowering time by environ-mental factors. Plant J. 2017;90:708-19
[42.]
Taylor IB, Linforth R, Al-Naieb RJ. et al. The wilty tomato mutants flacca and sitiens are impaired in the oxidation of ABA-aldehyde to ABA. Plant Cell Environ. 1988;11:739-45
[43.]
Campos L, Lisón P, López-Gresa MP. et al. Trans-genic tomato plants overexpressing tyramine N-hydroxycinnamoyltransferase exhibit elevated hydrox-ycinnamic acid amide levels and enhanced resistance to Pseudomonas syringae. Mol Plant-Microbe Interact. 2014;27:1159-69
[44.]
Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015;12:357-60
[45.]
Pertea M, Pertea GM, Antonescu CM. et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol. 2015;33:290-5
[46.]
Pertea M, Kim D, Pertea GM. et al. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc. 2016;11:1650-67
[47.]
Raudvere U, Kolberg L, Kuzmin I. et al. G:profiler: a web server for functional enrichment analysis and conversions of gene lists (2019 update). Nucleic Acids Res. 2019;47:W191-8
[48.]
Mi H, Muruganujan A, Huang X. et al. Protocol update for large-scale genome and gene function analysis with the PANTHER classification system (v.14.0). Nat Protoc. 2019;14:703-21
[49.]
Abbott WS. A method of computing the effectiveness of an insecticide. J Econ Entomol. 1925;18:265-7
PDF

Accesses

Citations

Detail

Sections
Recommended

/