Hydrogen sulfide inhibits ethylene-induced petiole abscission in tomato (Solanum lycopersicum L.)

Abstract

Abscission is a dynamic physiological process that is ubiquitous in plants and can also be an essential agronomic trait in crops, thus attracting attention from plant growers and breeders. In general, the process of plant organ abscission can be divided into four steps, among which the step to obtain the competence to respond to abscission signals (step 2) is the most complex; however, the molecular mechanism underlying this process remains unclear. In this study, we found that hydrogen sulfide (H 2 S) inhibited the abscission of the tomato petiole in a dose-dependent manner, and the abscission of the petiole was accelerated when an H 2 S scavenger was applied. Further enzymatic activity and gene expression analyses showed that H 2 S suppressed the activity of enzymes capable of modifying the cell wall by inhibiting the usual upregulation of the transcription of the corresponding genes during the abscission process but not by affecting the activities of these enzymes by direct posttranslational modification. H 2 S treatment upregulated the expression levels of SlIAA3 and SlIAA4 but downregulated the transcription of ILR-L3 and ILR-L4 in the earlier stages of the abscission process, indicating that H 2 S probably functioned in the second step of the abscission process by preventing the abscission zone cells from obtaining the competence to respond to abscission signals by modulating the content of the bioactive-free auxin in these cells. Moreover, similar H 2 S inhibitory effects were also demonstrated in the process of floral organ abscission and anther dehiscence in other plant species, suggesting a ubiquitous role for H 2 S in cell separation processes.

Hydrogen Sulfide Signaling Protects Chlamydomonas reinhardtii Against Allelopathic Damage From Cyanobacterial Toxin Microcystin-LR

“…For qRT-PCR analysis, C. reinhardtii samples were collected after different treatments to extract total RNA using the Trizol reagent (Invitrogen, Carlsbad, CA, USA). First-strand cDNA synthesis and qRT-PCR analysis were performed as described previously ( Liu et al., 2020 ). The primers used for qRT-PCR are listed in Supplemental Table 1 .…”

Crosstalk between Hydrogen Sulfide and Other Signal Molecules Regulates Plant Growth and Development

“…Furthermore, ET is associated with INFLORESCENCE DEFICIENT IN ABSCISSION (IDA)-mediated floral organ abscission through regulation of the transcription of DNA binding with one finger 4.7 (AtDOF4.7), which can directly impair the expression of the abscission-related gene ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE 2 (ADPG2) in Arabidopsis [ 79 ]. Liu et al (2020) demonstrated that H 2 S also participates in ET-induced petiole abscission of tomato [ 18 ]. The research showed that H 2 S treatment could delay abscission of the tomato petiole, but the situation was reversed when the plants were exposed to an H 2 S scavenger.…”

“…Moreover, H 2 S treatment reduced the enzymatic activities that modify the cell wall. Along with the expression levels of IAA/AUX family genes ( SlIAA3 and SlIAA4 ), the transcription of genes in the IAA-amino acid conjugate hydrolase (ILR) family ( ILR-L3 and ILR-L4 ) were found to be up-regulated and down-regulated, respectively, in the abscission process, suggesting that H 2 S prevented ET-induced petiole abscission by increasing the content of auxin in abscission zone tissues [ 18 ]. Additionally, Hideo et al (2019) reported that D-Cys, as a physiologically relevant substrate, participates in the process of root abscission and that exogenous application of H 2 S chemical donors or polysulfides can positively induce abscission to cope with environmental stimuli in the water fern Azolla [ 80 ].…”

“…In addition to fruit ripening, ET positively regulates organ abscission. Liu et al (2020) recently showed through H 2 S-ET co-treatment that H 2 S inhibited the up-regulation of ET synthesis and signal transduction genes, including ACS6 , ACO1 , ACO4 , ERF1 , and ETR4 , eventually resulting in the suppression of ET-induced petiole abscission in tomato [ 18 ]. Together, these experiments show that, during fruits ripening, senescence and organ abscission, H 2 S antagonizes the effects of ET by reducing oxidative stress and reducing the expression of ET-related genes and ET synthesis, thereby suppressing the ET signaling.…”

“…In Arabidopsis, mutation of des1 leads to premature senescence of leaves [ 15 ]. In many fruits and vegetables, H 2 S treatment delays premature leaf senescence and the decay of fruits after harvest via reducing the accumulation of reactive oxygen species (ROS) [ 16 , 17 ] and inhibits the abscission of plant organs via increasing the content of auxin in abscission zone tissues [ 18 ]. A recent report has shown that there is a significant increase in the S-sulfhydration level of the actin proteins in an H 2 S-overproducing line, created by the over-expression of LCD in the Arabidopsis O-acetylserine(thiol)lyase isoform a1 ( oasa1 ) mutant ( OE LCD-5 / oas-a1 ).…”