Cytokinins are abundant and widespread among insect species

Citation

Andreas, P., Kisiala, A., Neil Emery, R.J., De Clerck-Floate, R., Tooker, J.F., Price, P.W., Miller, D.G., Chen, M.S., Connor, E.F. (2020). Cytokinins are abundant and widespread among insect species. Plants, [online] 9(2), http://dx.doi.org/10.3390/plants9020208

Plain language summary

Cytokinins (CKs) are a class of chemical compounds that have long been thought to be exclusively produced by plants in the control of their own growth (i.e. growth hormones). However, some species of bacteria and fungi that are parasitic on plants can manipulate their plant hosts for sustenance by producing and using their own CKs. It also is hypothesized that certain insects use CKs to induce the production of plant growths (galls) used for the sheltering and sustenance of their offspring. In this study, we used an analytical chemistry technique to separate, identify and examine concentrations of a wide range of CKs in 17 species of plant-feeding insects from all six major taxonomic groups that contain species known to produce galls; Thysanoptera (thrips), Hemiptera (aphids), Lepidoptera (moths), Coleoptera (beetles), Diptera (flies), and Hymenoptera (sawflies). The species chosen for analysis, however, included both gall– and non-gall-producing insects from each of the taxonomic groups. We found CKs in all six groups of insects, and they were not associated exclusively with gall-producing species. We detected 24 different types of CKs, varying in their chemical structure and their biological activities within plants. The observed concentrations of CKs often notably exceeded those reported as naturally occurring in plants, suggesting that insects are making their own CKs rather than obtaining and accumulating them from the host plant while feeding. These findings support the concept that gall-inducing insects are capable of producing their own CKs as a means of manipulating within-plant nutrient flow (also plant chemical defensive responses against herbivory) to their advantage. The wide occurrence of CKs across taxonomic groups of plant-feeding insects, including species that don’t produce galls, also suggests that the CKs insects produce serve a more general purpose of gaining greater access to the plant nutrients they need for sustenance. A potential chemical mechanism by which CKs may be created by insects also was identified, and suggests a substantially more efficient method than what is used by plants in the creation of their own CK growth hormones.

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.

Publication date

2020-02-01