Induction of serotonin accumulation by feeding of rice striped stem borer in rice leaves

Abstract

Tryptophan (Trp)-related secondary metabolism has been implicated in the defense against pathogen infection and insect feeding in various gramineous species. Recently, we also reported that rice plant accumulated serotonin and tryptamine as well as their amide compounds coupled with phenolic acids in response to the infection by fungal pathogen. These compounds were likely to play an important role in the formation of physical barrier to the invading pathogens. To extend our study to elucidate the defensive role of Trp-derived secondary metabolism in gramineous plants, we examined in this study whether it is activated in response to herbivore attack as well. Third leaves of rice plant were fed on by third instar larvae of rice striped stem borer for 24 h or 48 h. The analysis of four Trp-derived metabolites including tryptamine, serotonin feruloyltryptamine (FerTry) and p-coumaroylserotonin (CouSer) by liquid chromatography coupled with tandem mass spectrometry revealed that their contents clearly increased in response to the larvae feeding. The respective amounts of tryptamine, serotonin, FerTry and CouSer in the larvae-fed leaves were 12-, 3.5-, 33-and 140-fold larger than those in control leaves 48 h after the start of feeding.Plants defend themselves from environmental stresses by utilizing secondary metabolism. One of major biological stresses that plants have to cope with is attack by herbivorous insects. In the interactions with herbivorous insects, various secondary metabolites that are derived from tryptophan (Trp) pathway have been shown to play defensive roles in plants including gramineous species. For example, benzoxazinone glucosides in wheat (Triticum aestivum), rye (Secale sereale) and maize (Zea mays) express toxic and antifeeding effects on herbivorous insects. 1,2 Benzoxazinones are biosynthesized from indole-3-glycerol phosphate, an intermediate of Trp synthesis. 3,4 Another example of those compounds is gramine in barley (Hordeum vulgare). Gramine is a Trp-rerived indole amine, 5 and has been received attention in the resistance mainly against aphids on the basis of its toxicity and deterrence. 6 We recently found that Trp-derived secondary metabolism is also involved in defense responses of rice (Oryza sativa) leaves to infection by brown spot fungus (Bipolaris oryzae). 7 The infection of the fungus activates Trp biosynthesis and accumulation of serotonin and of smaller amounts of tryptamine, feruloyltryptamine (FerTry) and p-coumaroylserotonin (CouSer). In addition, the enhancement of serotonin peroxidase activity and incorporation of serotonin in the cell walls were detected. Thus, it is very likely that that serotoninderived materials deposit in cell walls after oxidative polymerization to constitute a part of physical defense system of rice, which may be reminiscent of the wound sloughing in animals. These findings prompted us to investigate whether Trp-related secondary metabolism is also involved in the defense of rice plant against the attack by insects, as in the cases of other gram...

Arbuscular Mycorrhiza in Crop Improvement under Environmental Stress

“…Changes induced usually include: development of physical barriers, modifications in cell wall, and de novo synthesis of metabolites (Ishihara et al, 2008). Biotrophic fungi are effective in preventing fungal penetration because of their ability to terminate the development and functioning of the parasitic fungal intracellular hypha (haustorium), thereby restricting it from extracting nutrition from plant cells (Wen et al, 2011).…”

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

“…Rice plants that overexpress two putative TDC genes, TDC-1 and TDC-3, had increased serotonin levels, stunted growth and low fertility, indicating that serotonin overproduction may be deleterious to plants (Kanjanaphachoat et al 2012). In contrast, via its antioxidant properties and reinforcement of cell walls, serotonin confers protection against pathogens and herbivores and delays senescence (Ishihara et al 2008a, 2008b, Kang et al 2009). …”

“…An increasing number of reports have evidenced the critical role of serotonin in modulating plant growth and developmental processes, including germination, flowering, senescence, shoot branching, root architecture, adaptation to environmental stress and protection against pathogens (Csaba and Pal 1982, Odjakova and Hadjiivanova 1997, Murch et al 2001, Roshchina 2001, Ishihara et al 2008a, 2008b, Kang et al 2009, Pelagio-Flores et al 2011. Serotonin modulates root morphogenesis via auxin-dependent or -independent mechanisms (Csaba andPal 1982, Murch et al 2001).…”

Beyond a neurotransmitter: The role of serotonin in plants

“…It is well established that insects use serotonin as a neurotransmitter, and though the amount of serotonin present in plant tissues would be unlikely to have an effect on a larger herbivore, the levels of serotonin observed could have a potent effect on insects. In addition to the fact serotonin receptors are present in the insect gut [57] , serotonin has been found to accumulate at the site of insect feeding in response to the striped stem borer in rice [58] . Serotonin has been found to have effects on insect physiology including effects on: locomotion, circadian rhythms, reproduction, and feeding among others [59][60][61][62][63][64][65][66] .…”