Infection with phytopathogenic bacterium inhibits melatonin biosynthesis, decreases longevity of its vector, and suppresses the free radical‐defense

Abstract

Vector-borne phytopathogenic bacteria may alter the reproductive fitness, survival, behavior, and metabolism of their vectors. Candidatus Liberibacter asiaticus (CLas) is associated with the Huanglongbing (also known as citrus greening disease), one of the most destructive citrus diseases worldwide, and transmitted by Asian citrus psyllid, Diaphorina citri (Insecta, Hemiptera, Liviidae). The genome sequencing of CLas revealed that it does not have the ability to synthesize tryptophan, the precursor of melatonin, and it must acquire it from its host plant or insect vector to achieve its biologic processes, such as growth and multiplication. Herein, we aimed to develop a GC-MS-SIM-based method to detect the endogenous melatonin from small insects such as D. citri, and to explore the hidden relationship between melatonin content and D. citri-adult survival. Then, we studied the ability of exogenous melatonin supplementation to reverse the negative effects of CLas-infection. Our findings showed that CLas-infection reduced the levels of melatonin and its biosynthetic genes (DcTPHs, DcAAAD, DcSNAT, and DcASMT) of D. citri compared to uninfected insects. In addition, CLas decreased the longevity of its vector, D. citri via the suppression of the free radical-defense associated genes (SODs, GSTs, PODs, and PHGPXs). On the other hand, melatonin supplementation could reverse the negative effects of CLas-infection. Melatonin supplementation enhanced the endogenous melatonin content, melatonin biosynthetic genes, free radical-defense associated genes, and the longevity of both healthy and CLas-infected D. citri. Furthermore, melatonin supplementation decreased the CLas bacterial population within the D. citri psyllids. Based on these findings, we hypothesize that melatonin plays multi-layered defensive roles in D. citri. These roles include acting as a natural antioxidant or as an antibacterial compound.

Potential utility of melatonin in deadly infectious diseases related to the overreaction of innate immune response and destructive inflammation: focus on COVID-19

“…Some further examples are known from the botanical field and shall not be discussed here in detail. Both additional melatonin supply by an endophytic bacterium (155) and reduction of host melatonin synthesis by phytopathogenic bacteria (156) have been reported, as well as counteractions of exogenous melatonin (157).…”

Targeting Host Defense System and Rescuing Compromised Mitochondria to Increase Tolerance against Pathogens by Melatonin May Impact Outcome of Deadly Virus Infection Pertinent to COVID-19

“…It seems that targeting the melatonin biosynthesis to modify the host defense is a useful strategy for their rapid spreading inside of the host, e.g., when the bacteria Candidatus Liberibacter asiaticus infected insects Diaphorina citri . These bacteria attacked the host’s melatonin synthetic pathway by suppressing the gene expression of all melatonin synthetic enzymes including TPH, AAAD, SNAT , and ASMT and shut down melatonin production [ 147 ]. Another strategy taken by microbes including viruses is simply to deplete the precursor of melatonin synthesis, tryptophan, by activating indolamine 2,3-dioxygenase (IDO), which metabolizes tryptophan to kynurenine catabolites [ 148 ].…”

Melatonin and Its Protective Role against Biotic Stress Impacts on Plants

“…oryzicola [55,56]. Likewise, Nehela, et al [57] found that supplemented melatonin treatment could invert the negative disorders of Candidatus Liberibacter asiaticus (CLas) (the causal agent of citrus greening disease) on its insect vector by enhancement of melatonin content, extend the longevity of healthy and infected vectors, and reduce the CLas bacterial population within the vector psyllids. In another study, it was reported that direct transcriptional activators of melatonin biosynthesis genes in cassava crops, namely, MeRAV2 and MeRAV1 genes, are required to confer plant disease resistance against bacterial blight of cassava [58].…”