Co-silencing of ABA receptors (SlRCAR) reveals interactions between ABA and ethylene signaling during tomato fruit ripening

Jian Zou , Ning Li , Nan Hu , Ning Tang , Haohao Cao , Yudong Liu , Jing Chen , Wei Jian , Yanqiang Gao , Jun Yang , Zhengguo Li

Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) : uhac057

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Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) :uhac057 DOI: 10.1093/hr/uhac057
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Co-silencing of ABA receptors (SlRCAR) reveals interactions between ABA and ethylene signaling during tomato fruit ripening
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Abstract

The ripening of fleshy fruits is highly dependent on the regulation of endogenous hormones, including ethylene, abscisic acid (ABA) and other phytohormones. However, the regulatory mechanism of ABA signaling and its interaction with ethylene signaling in fruit ripening are still unclear. In this study, multi-gene interference (RNAi) was applied to silence the ABA receptor genes in tomato for screening the specific receptors that mediate ABA signaling during fruit ripening. The results indicated that the ABA receptors, including SlRCAR9, SlRCAR12, SlRCAR11, and SlRCAR13, participate in the regulation of tomato fruit ripening. Comparative analysis showed that SlRCAR11 and SlRCAR13 play more important roles in mediating ABA signaling during tomato fruit ripening. Co-silencing of the four genes encoding these receptors could weaken the ethylene biosynthesis and signaling pathway at the early stage of tomato fruit ripening, leading to delayed fruit ripening. Meanwhile, co-silencing enhanced fruit firmness, and altered the shelf-life and susceptibility to Botrytis cinerea of the transgenic fruits. Furthermore, blocking ABA signaling did not affect the ability of ethylene to induce fruit ripening, whereas the block may inhibit the effectiveness of ABA in promoting fruit ripening. These results suggested that ABA signaling may be located upstream of ethylene signaling in regulating fruit ripening. Our findings provide a new insight into the complex regulatory network of phytohormones in regulating fruit ripening in tomato.

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Jian Zou, Ning Li, Nan Hu, Ning Tang, Haohao Cao, Yudong Liu, Jing Chen, Wei Jian, Yanqiang Gao, Jun Yang, Zhengguo Li. Co-silencing of ABA receptors (SlRCAR) reveals interactions between ABA and ethylene signaling during tomato fruit ripening. Horticulture Research, 2022, 9 (1) : uhac057 DOI:10.1093/hr/uhac057

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References

[1]

Seymour GB, Taylor JE, Tucker GA . Biochemistry of fruit ripening. Chapman and Hall, London, pp 1-454.

[2]

Adams-Phillips L, Barry C, Giovannoni J . Signal transduction systems regulating fruit ripening. Trends Plant Sci. 2004; 9: 331-8.

[3]

Bapat VA, Trivedi PK, Ghosh A et al. Ripening of fleshy fruit: molecular insight and the role of ethylene. Biotechnol Adv. 2010; 28: 94-107.

[4]

Chervin C, El-Kereamy A, Roustan JP et al. Ethylene seems required for the berry development and ripening in grape, a non-climacteric fruit. Plant Sci. 2004; 167: 1301-5.

[5]

Seymour GB, Østergaard L, Chapman NH et al. Fruit development and ripening. Annu Rev Plant Biol. 2013; 64: 219-41.

[6]

Li JY, Tao X, Bu J et al. Global transcriptome profiling analysis of ethylene-auxin interaction during tomato fruit ripening. Postharvest Biol Technol. 2017; 130: 28-38.

[7]

Su L, Diretto G, Purgatto E et al. Carotenoid accumulation during tomato fruit ripening is modulated by the auxin-ethylene balance. BMC Plant Biol. 2015; 15: 114-25.

[8]

Jia HF, Chai YM, Li CL et al. Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiol. 2011; 157: 188-99.

[9]

Nicolas P, Lecourieux D, Kappel C et al. The bZIP transcription factor VvABF2 is an important transcriptional regulator of ABA-dependent grape berry ripening processes. Plant Physiol. 2013; 35: 523-5.

[10]

Sun L, Sun Y, Zhang M et al. Suppression of 9-cis-epoxycarotenoid dioxygenase, which encodes a key enzyme in abscisic acid biosynthesis, alters fruit texture in transgenic tomato. Plant Physiol. 2012; 158: 283-98.

[11]

Zhang M, Yuan B, Leng P . The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit. J Exp Bot. 2009; 60: 1579-88.

[12]

Mizrahi Y, Dostal HC, McGlasson W et al. Effects of abscisic acid and benzyladenine on fruits of normal and rin mutant tomatoes. Plant Physiol. 1975; 56: 544-6.

[13]

Galpaz N, Wang Q, Menda N et al. Abscisic acid deficiency in the tomato mutant high-pigment 3 leading to increased plastid number and higher fruit lycopene content. Plant J. 2008; 53: 717-30.

[14]

Nitsch L, Kohlen W, Oplaat C et al. ABA-deficiency results in reduced plant and fruit size in tomato. J Plant Physiol. 2012; 169: 878-83.

[15]

Sun L, Wang YP, Chen P et al. Transcriptional regulation of SlPYL, SlPP2C, and SlSnRK2 gene families encoding ABA signal core components during tomato fruit development and drought stress. J Exp Bot. 2011; 62: 5659-69.

[16]

Jiang Y, Joyce DC, Macnish AJ . Effect of abscisic acid on banana fruit ripening in relation to the role of ethylene. J Plant Growth Regul. 2000; 19: 106-11.

[17]

Zaharah SS, Singh Z, Symons GM et al. Mode of action of abscisic acid in triggering ethylene biosynthesis and softening during ripening in mango fruit. Postharvest Biol Technol. 2013; 75: 37-44.

[18]

Jiang Y, Joyce DC . ABA effects on ethylene production, PAL activity, anthocyanin and phenolic contents of strawberry fruit. Plant Growth Regul. 2003; 39: 171-4.

[19]

Mou W, Li D, Bu J et al. Comprehensive analysis of ABA effects on ethylene biosynthesis and signaling during tomato fruit ripening. PLoS One. 2016; 11: e0154072.

[20]

Park SY, Fung P, Nishimura N et al. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science. 2009; 324: 1068-71.

[21]

Umezawa T, Sugiyama N, Mizoguchi M et al. Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis . Proc Natl Acad Sci USA. 2009; 106: 17588-93.

[22]

Yoshida R, Umezawa T, Mizoguchi T et al. The regulatory domain of SRK2E/OST1/SnRK2.6 interacts with ABI1 and integrates abscisic acid (ABA) and osmotic stress signals controlling stomatal closure in Arabidopsis . J Biol Chem. 2006; 281: 5310-8.

[23]

Schweighofer A, Hirt H, Meskiene I . Plant PP2C phosphatases: emerging functions in stress signaling. Trends Plant Sci. 2004; 9: 236-43.

[24]

Gonzalez-Guzman M, Rodríguez L, Lorenzo-Orts L et al. Tomato PYR/PYL/RCAR abscisic acid receptors show high expression in root, differential sensitivity to the abscisic acid agonist quinabactin, and the capability to enhance plant drought resistance. J Exp Bot. 2014; 65: 4451-64.

[25]

Yan P, Shen W, Gao XZ et al. High-throughput construction of intron-containing hairpin RNA vectors for RNAi in plants. PLoS One. 2012; 7: e38186.

[26]

Curtis MD, Grossniklaus U . A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 2003; 133: 462-9.

[27]

Lee LY, Gelvin SB . T-DNA binary vectors and systems. Plant Physiol. 2008; 146: 325-32.

[28]

Fillatti JAJ, Kiser J, Rose R et al. Efficient transfer of a glyphosate tolerance gene into tomato using a binary agrobacterium tumefaciens vector. Nat Biotechnol. 1987; 5: 726-30.

[29]

Fan X, Blankenship SM, Mattheis JP . 1-Methylcyclopropene inhibits apple ripening. J Amer Soc Hort Sci. 1999; 124: 690-5.

[30]

Zou J, Chen J, Tang N et al. Transcriptome analysis of aroma volatile metabolism change in tomato (Solanum lycopersicum) fruit under different storage temperatures and 1-MCP treatment . Postharvest Biol Technol. 2018; 135: 57-67.

[31]

Zhang B, Yin XR, Li X et al. Lipoxygenase gene expression in ripening kiwifruit in relation to ethylene and aroma production. J Agric Food Chem. 2009; 57: 2875-81.

[32]

Yang L, Huang W, Xiong F et al. Silencing of SlPL, which encodes a pectate lyase in tomato, confers enhanced fruit firmness, prolonged shelf-life and reduced susceptibility to grey mould. Plant Biotechnol J. 2017; 15: 1544-55.

[33]

Nambeesan S, Datsenka T, Ferruzzi MG et al. Overexpression of yeast spermidine synthase impacts ripening, senescence and decay symptoms in tomato. Plant J. 2010; 63: 836-47.

[34]

Stefanato FL, Abou-Mansour E, Buchala A et al. The ABC transporter BcatrB from Botrytis cinerea exports camalexin and is a virulence factor on Arabidopsis thaliana . Plant J. 2009; 58: 499-510.

[35]

Zhang Y, Butelli E, De Stefano R et al. Anthocyanins double the shelf life of tomatoes by delaying overripening and reducing susceptibility to gray mold. Curr Biol. 2013; 23: 1094-100.

[36]

Williamson B, Tudzynski B, Tudzynski P et al. Botrytis cinerea: the cause of grey mould disease . Mol Plant Pathol. 2007; 8: 561-80.

[37]

Pilati S, Bagagli G, Sonego P et al. Abscisic acid is a major regulator of grape berry ripening onset: new insights into ABA signaling network. Front Plant Sci. 2017; 8: 1093.

[38]

Gupta MK, Lenka SK, Gupta S et al. Agonist, antagonist and signaling modulators of ABA receptor for agronomic and post-harvest management. Plant Physiol Biochem. 2020; 148: 10-25.

[39]

Hauser F, Waadt R, Schroeder J . Evolution of abscisic acid synthesis and signaling mechanisms. Curr Biol. 2011; 21: R346-55.

[40]

Vrebalov J, Lenka SK, Gupta S et al. A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science. 2002; 296: 343-6.

[41]

Bourquin V, Nishikubo N, Abe H et al. Xyloglucan endotransglycosylases have a function during the formation of secondary cell walls of vascular tissues. Plant Cell. 2002; 14: 3073-88.

[42]

Brummell DA, Harpster MH, Civello PM et al. Modification of expansin protein abundance in tomato fruit alters softening and cell wall polymer metabolism during ripening. Plant Cell. 1999; 11: 2203-16.

[43]

Rosli HG, Civello PM, Martinez GA . Changes in cell wall composition of three Fragaria x ananassa cultivars with different softening rate during ripening . Plant Physiol Biochem. 2004; 42: 823-31.

[44]

Saladié M, Rose JK, Cosgrove DJ et al. Characterization of a new xyloglucan endotransglucosylase/hydrolase (XTH) from ripening tomato fruit and implications for the diverse modes of enzymic action. Plant J. 2006; 47: 282-95.

[45]

Trainotti L, Ferrarese L, Vecchia FD et al. Two different endo- β-1,4-glucanases contribute to the softening of the strawberry fruits . J Plant Physiol. 1999; 154: 355-62.

[46]

Wang D, Yeats TH, Uluisik S et al. Fruit softening: revisiting the role of pectin. Trends Plant Sci. 2018; 23: 302-10.

[47]

Bennett AB, Labavitch JM . Ethylene and ripening-regulated expression and function of fruit cell wall modifying proteins. Plant Sci. 2008; 175: 130-6.

[48]

Villarreal NM, Marina M, Nardi CF et al. Novel insights of ethylene role in strawberry cell wall metabolism. Plant Sci. 2016; 252: 1-11.

[49]

Ketsa S . Effect of fruit size on weight loss and shelf life of tangerines. J Hortic Sci. 1990; 65: 485-8.

[50]

Cantu D, Vicente AR, Greve LC et al. The intersection between cell wall disassembly, ripening, and fruit susceptibility to Botrytis cinerea . Proc Natl Acad Sci USA. 2008; 105: 859-64.

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