Cytokinins Are Abundant and Widespread among Insect Species

Abstract

Cytokinins (CKs) are a class of compounds that have long been thought to be exclusively plant growth regulators. Interestingly, some species of phytopathogenic bacteria and fungi have been shown to, and gall-inducing insects have been hypothesized to, produce CKs and use them to manipulate their host plants. We used high performance liquid chromatography-electrospray ionization tandem mass spectrometry (HPLC-MS/MS) to examine concentrations of a wide range of CKs in 17 species of phytophagous insects, including gall- and non-gall-inducing species from all six orders of Insecta that contain species known to induce galls: Thysanoptera, Hemiptera, Lepidoptera, Coleoptera, Diptera, and Hymenoptera. We found CKs in all six orders of insects, and they were not associated exclusively with gall-inducing species. We detected 24 different CK analytes, varying in their chemical structure and biological activity. Isoprenoid precursor nucleotide and riboside forms of trans-zeatin (tZ) and isopentenyladenine (iP) were most abundant and widespread across the surveyed insect species. Notably, the observed concentrations of CKs often markedly exceeded those reported in plants suggesting that insects are synthesizing CKs rather than obtaining them from the host plant via tissue consumption, compound sequestration, and bioaccumulation. These findings support insect-derived CKs as means for gall-inducing insects to manipulate their host plant to facilitate cell proliferation, and for both gall- and non-gall-inducing insects to modify nutrient flux and plant defenses during herbivory. Furthermore, wide distribution of CKs across phytophagous insects, including non-gall-inducing species, suggests that insect-borne CKs could be involved in manipulation of source-sink mechanisms of nutrient allocation to sustain the feeding site and altering plant defensive responses, rather than solely gall induction. Given the absence of any evidence for genes in the de novo CK biosynthesis pathway in insects, we postulate that the tRNA-ipt pathway is responsible for CK production. However, the unusually high concentrations of CKs in insects, and the tendency toward dominance of their CK profiles by tZ and iP suggest that the tRNA-ipt pathway functions differently and substantially more efficiently in insects than in plants.

The Origins and Roles of Methylthiolated Cytokinins: Evidence From Among Life Kingdoms

“…These types of inverse associations were also characteristic for the HPLC-MS/MS profiles of CKs reported from representatives of six orders of Insecta (Andreas et al, 2020). For example, larvae of two stem-boring beetle species, Mecinus janthinus and Mecinus janthiniformis, demonstrated highly elevated concentrations of nucleotide precursors of the classical CKs and only trace levels of 2MeS-CK derivatives.…”

“…The available studies of CKs in the kingdom of Animalia indicate the existence of an active tRNA pathway in insects and mammals. Cytokinin metabolites have been found in insects (e.g., Straka et al, 2010;Andreas et al, 2020); although, it has been postulated that CK presence in insects might be a result of the activity of bacterial symbionts (Giron et al, 2013). In silkworm (Bombyx mori), a candidate tRNA-IPT gene with three alternative splicing isoforms (BmIPT1-BmITP3) was recently identified (Chen et al, 2019).…”

The Evolution of Endophagy in Herbivorous Insects

“…Notably, plant manipulation is not only restricted to gall inducers and leaf miners, as commonly assumed, but is shared by other endophagous insects (Stone and Schönrogge, 2003;Gutzwiller et al, 2015;Giron et al, 2016), and perhaps even ectophagous species (Andreas et al, 2020). Because endophagous insects secure their nutrition (and shelter) via their feeding habit, they also must evolve feeding strategies allowing them to meet their energetic and nutrient requirements, face variation in food and nutrient composition, and counteract plant defensive mechanisms.…”

Comparative Transcriptome Analysis of Two Root-Feeding Grape Phylloxera (D. vitifoliae) Lineages Feeding on a Rootstock and V. vinifera

“…roots. However, other important factors play important roles for the fine-tuning of cellular processes resulting during root gall formation [ 98 , 99 , 100 , 101 ]. Thus, our study employing a defined bioassay exhibits part of the potential genes involved that determine host performance, in this case for biotype A and C.…”