Plants exist a large number of secondary metabolites with complex structures, which constitute the unique taste of each plant species. Most of secondary plant metabolites have defensive effects on herbivorous insects. However, some specialist insects are not affected by these compounds, and even use them as token stimuli to recognize their host plants.

The cabbage butterfly Pieris rapae is an important agricultural pest in the world. The caterpillars of P. rapae prefer to feed on cruciferous vegetables such as cabbage, cauliflower, rapeseed, radish and so on, because they are addicted to glucosinolates, a specific group of secondary metabolites in cruciferous plants. These compounds trigger neural firing in larval maxillary sensilla and adult tarsal sensilla, and induce feeding and oviposition responses. Gustatory receptors (GRs) expressed in the gustatory receptor neurons (GRNs) in taste sensilla are involved in the recognition of different glucosinolates. For more than 100 years, scientists have done a lot of work to uncover the mystery of insect addiction to glucosinolates, but the GRs tuned to glucosinolates have been unknown.

On July 15, 2021, the team of Prof. Chen-Zhu Wang from Institute of Zoology, Chinese Academy of Sciences have published the research paper entitled “Identification of a gustatory receptor tuned to sinigrin in the cabbage butterfly Pieris rapae” in PLoS Genetics. This study uncovers that a bitter receptor in P. rapae is tuned to sinigrin, one of the most common and abundant glucosinolates in cruciferous plants.

Using a combination of behavioral, electrophysiological and molecular techniques and methods, the team investigated the molecular basis of glucosinolate detection of P. rapae at different levels. They found that five glucosinolates are the potent feeding stimulants for P. rapae larvae. Both larval maxilla and adult tarsi exist two types of taste sensilla responding to glucosinolates: one broadly responding to all tested glucosinolates, and another narrowly responding to the indolic and aromatic glucosinolates.

Figure 1. Larval maxillary sensilla and adult tarsal sensilla responding to glucosinolates in Pieris rapae (from Whiteman and Peláez, 2021).

Based on transcriptome sequencing and qRT-PCR analyses, they identified two highly expressed bitter receptors, PrapGr28 and PrapGr15 in female tarsi, and speculated that the two receptors might be involved in the chemoreception of glucosinolates. The subsequent functional analysis showed that the Xenopus oocytes only expressing PrapGr28 had specific responses to sinigrin by two-electrode voltage clamp. To further confirm the function of PrapGr28, they ectopically expressed PrapGr28 into Drosophila sweet GRNs by Gr5a-GAL4. PrapGr28 expressed in these neurons conferred sensitivity of the L-type sensilla to sinigrin. Finally, they used RNA interference experiments further showed that knockdown of PrapGr28 reduced the sensitivity of adult tarsal sensilla to sinigrin, confirming that the bitter receptor PrapGr28 is a gustatory receptor tuned to sinigrin in P. rapae.

Figure 2. Identification of a gustatory receptor tuned to sinigrin in Pieris rapae.

Dr. Jun Yang, a postdoc working with Prof. Chen-Zhu Wang is the first author of the paper. Hao Guo, Nan-Ji Jiang, Rui Tang, Guo-Cheng Li, Ling-Qiao Huang in the same laboratory, and Joop J. A. van Loon from Wageningen University and Research were involved in this research. The research was supported by the Strategic Priority Research Program of Chinese Academy of Sciences and the National Natural Science Foundation of China.

Meanwhile, Prof. Noah K. Whiteman and Julianne N. Peláez from University of California, Berkeley, USA wrote a perspective article for this study in the same issue of PLoS Genetics. They pointed out that the current work on the functional identification of bitter receptor tuned to glucosinolates is a major advance in the field of the neuroethology and sensory ecology of herbivorous insects, and takes a significant step towards revealing the molecular basis of the taste addiction to glucosinolates in the crucifer specialist insects, as well as the secrets of the complex taste system in herbivorous insects.

References:

Yang J, Guo H, Jiang NJ, Tang R, Li GC, Huang LQ, van Loon JJA, Wang CZ. (2021) Identification of a gustatory receptor tuned to sinigrin in the cabbage butterfly Pieris rapae. PLoS Genet. 17(7):e1009527. doi: 10.1371/journal.pgen.1009527.

Whiteman NK, Peláez JN. (2021) Taste-testing tarsi: Gustatory receptors for glucosinolates in cabbage butterflies. PLoS Genet. 17(7):e1009616. doi: 10.1371/journal.pgen.1009616.

(Contact: Chen-Zhu Wang, czwang@ioz.ac.cn)