Serotonin modulates Arabidopsis root growth via changes in reactive oxygen species and jasmonic acid–ethylene signaling

Abstract

Serotonin (5-hydroxytryptamine) is a bioactive indoleamine with neurotransmitter function in vertebrates, which represents an emerging signaling molecule in plants, playing key roles in the development and defense. In this study, the role of reactive oxygen species (ROS) and jasmonic acid (JA)-ethylene (Et) signaling in root developmental alterations induced by serotonin was investigated. An Arabidopsis thaliana mutant defective at the RADICAL-INDUCED CELL DEATH1 (RCD1) locus was resistant to paraquat-induced ROS accumulation in primary roots and showed decreased inhibition or root growth in response to serotonin. A suite of JA- and Et-related mutants including coronatine insensitive1, jasmonic acid resistant1 (jar1), etr1, ein2 and ein3 showed tolerance to serotonin in the inhibition of primary root growth and ROS redistribution within the root tip when compared with wild-type (WT) seedlings. Competence assays between serotonin and AgNO3 , a well-known blocker of Et action, showed that primary root growth in medium supplemented with serotonin was normalized by AgNO3 , whereas roots of eto3, an Et overproducer mutant, were oversensitive to serotonin. Comparison of ROS levels in WT, etr1, jar1 and rcd1 primary root tips using the ROS-specific probe 2',7'-dichlorofluorescein diacetate and confocal imaging showed that serotonin inhibition of primary root growth likely occurs independently of its conversion into melatonin. Our results provide compelling evidence that serotonin affects ROS distribution in roots, involving RCD1 and components of the JA-Et signaling pathways.

Melatonin and serotonin: Mediators in the symphony of plant morphogenesis

“…The current research into the metabolism and mechanisms of action of MEL has characterized biosynthetic pathways and morphological responses in a few model species such as rice, Arabidopsis, and tomato, but many aspects remain undiscovered. Investigation of regeneration systems has included St. John's wort, Echinacea, coffee, Arabidopsis , lupin, blueberry, sweet cherry, pomegranate, Withania somnifera, and mimosa . In general, MEL and 5HT appear to enhance shoot organogenesis from root cultures at least in part via modification of phytohormone networks .…”

Comparative physiological responses and transcriptome analysis reveal the roles of melatonin and serotonin in regulating growth and metabolism in Arabidopsis

“…Melatonin (N-acetyl-5-methoxytryptamine) and its precursor serotonin (5-hydroxytryptamine) are two highly conserved molecules that mediate a series of physiological activities in humans, animals, and plants [1–5]. Under normal conditions, the melatonin content is relatively low; however, biotic and abiotic stresses, such as pathogen infection, low temperature, salt, drought, iron deficiency, and heavy metal toxicity, markedly induce melatonin accumulation in plants [6–12].…”

NO and ROS implications in the organization of root system architecture

“…In this case, pyocyanin modulation of the primary root growth required the gaseous hormone ethylene for signaling. Not only bacterial toxins modulate ROS levels in roots but Pelagio‐Flores et al () also have found that the neurotransmitter serotonin acts as a plant signaling molecule, while the ethylene inhibitor AgNO 3 antagonized its effects on Arabidopsis primary roots. Thus, ethylene and ROS are mediators in transducing serotonin and pyocyanin bioactivity.…”