Pheromone receptor of the globally invasive quarantine pest of the palm tree, the red palm weevil (Rhynchophorus ferrugineus)

Abstract

Palm trees are of immense economic, sociocultural, touristic and patrimonial significance all over the world, and date palm-related knowledge, traditions and practices are now included in UNESCO’s list of the Intangible Cultural Heritage of Humanity. Of all the pests that infest these trees, the red palm weevil (RPW), Rhynchophorus ferrugineus (Olivier) is its primary enemy. The RPW is a category-1 quarantine insect pest that causes enormous economic losses in the cultivation of palm trees worldwide. The RPW synchronizes mass gathering on the palm tree for feeding and mating, regulated by a male-produced pheromone composed of two methyl-branched compounds, (4RS,5RS)-4-methylnonan-5-ol (ferrugineol) and 4(RS)-methylnonan-5-one (ferrugineone). Despite the importance of odorant detection in long-range orientation towards palm trees, palm colonization and mating, nothing regarding the molecular mechanisms of pheromone detection in this species is known. In this study, we report the identification and characterization of the first RPW pheromone receptor, RferOR1. Using gene silencing and functional expression in Drosophila olfactory receptor neurons, we demonstrate that RferOR1 is tuned to both ferrugineol and ferrugineone and binds five other structurally related molecules. We reveal the lifetime expression of RferOR1, which correlates with adult mating success irrespective of age, a factor that could explain the wide distribution and spread of this pest. As palm weevils are challenging to control based on conventional methods, elucidation of the mechanisms of pheromone detection opens new routes for mating disruption and the early detection of this pest via the development of pheromone receptor-based biosensors.

Antennal Transcriptome Analysis and Identification of Candidate Chemosensory Genes of the Harlequin Ladybird Beetle, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae)

“…Possibly, high expression of one OR, HaxyOR5, in males may suggest a role in the detection of one sex pheromone molecule. In support of this latter hypothesis is that HaxyOR5 clustered in the clade 7 of the Coleoptera OR phylogeny, in which pheromone receptors from other Cucujiformia ( R. ferrugineus and I. typographus ) have been characterized [ 68 , 69 ]. Together with the fact that Coleoptera ORs exhibit high sequence divergence, this makes it difficult to predict HaxyOR functions.…”

“…Functionally characterized odorant receptors from the beetles Megacyllene caryae (Gahan. ), Ips typographus L., and Rhyncophorus ferrugineus (Olivier) were included [ 66 , 67 , 68 , 69 ] as well as gustatory receptors from D. melanogaster [ 13 ]. Similarly, sequences of functionally characterized odorant- and pheromone-binding proteins were considered from beetles, i.e., Anomala cuprea (Hope) and Anomala octiescostata Burmeister [ 70 ], Agrilus mali Matsumura [ 71 ], Cyrtotrachelus buqueti Guérin-Méneville [ 72 ], Holotrichia oblita Faldermannor [ 73 , 74 ], Holotrichia parallela (Motschulsky) [ 75 ], Phyllopertha diversa Waterhouse [ 76 ], Popillia japonica Newman [ 77 ], R. ferrugineus [ 78 ], and from the aphid Acyrthosiphon pisum (Harris) [ 79 ].…”

Putative ligand binding sites of two functionally characterized bark beetle odorant receptors

“…Functional characterization of insect ORs has been biased towards moths [34][35][36], flies, and mosquitos [37,38]. In contrast, Coleoptera-arguably the largest order of the Metazoa-remains an understudied group with only five characterized ORs from a few species: the cerambycid Megacyllene caryae [39], the scarab Holotrichia parallela [40], and the curculionid Rhynchophorus ferrugineus [41]. The paucity of functional data is a bottleneck that severely limits our understanding of the molecular evolution of olfaction in this diverse taxon [42].…”

Non-palm Plant Volatile α-Pinene Is Detected by Antenna-Biased Expressed Odorant Receptor 6 in the Rhynchophorus ferrugineus (Olivier) (Coleoptera: Curculionidae)

“…The air was filtered through activated charcoal, and the entry flow to the olfactometer was 1.2 L/min controlled by using a vacuum pump. RPW was starved overnight, and the experiment was carried out during daytime between 9:00 and 17:00 h at a temperature of 27°C ± 1°C and a humidity of 75 ± 5% ( Antony et al, 2021 ). During the experiment, the Y-tube olfactometer was washed with ethanol and heated every time, and the compound position was changed when every 10 adults were tested.…”