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. 2024 Apr 29;27(6):109847.
doi: 10.1016/j.isci.2024.109847. eCollection 2024 Jun 21.

The mechanism of Andrena camellia in digesting toxic sugars

Zhen Li  1   2   3 , Shiqing Zhong  1   2 , Qiang Huang  1   2 , Yong Zhang  1   4 , Tianyu Xu  1   2 , Wenkai Shi  1   2 , Dongsheng Guo  3 , Zhijiang Zeng  1   2
Affiliations

The mechanism of Andrena camellia in digesting toxic sugars

Zhen Li et al. iScience. .

Abstract

Camellia oleifera is an economically and medicinally valuable oilseed crop. Honeybee, the most abundant pollinator, rarely visits C. oleifera because of the toxic sugars in the nectar and pollen. These toxic sugars cannot be fully digested by honeybees and inhibit the process of synthesizing trehalose in honeybees. C. oleifera exhibits self-incompatibility, and its pollination heavily depends on Andrena camellia. However, the mechanism by which A. camellia digests toxic sugars in C. oleifera nectar and pollen remains unknown. Consequently, we identified and validated four single-copy genes (α-N-acetyl galactosamine-like, galactokinase, galactose-1-phosphate uridyltransferase, and UDP-galactose-4'-epimerase, abbreviated as NAGA-like, GALK, GALT, and GALE) essential for detoxifying toxic sugars in vitro. Then, we cloned the four genes into Escherichia coli, and expressed enzyme successfully degraded the toxic sugars. The phylogeny suggests that the genes were conserved and functionally diverged among the evolution. These results provide novel insights into pollinator detoxification during co-evolution.

Keywords: Biotechnology; Evolutionary biology; Plant biology.

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Conflict of interest statement

The authors declare no conflicts of interests.

Figures

None
Graphical abstract
Figure 1
Figure 1
Chromosomal distribution of genes encoding GAL (ACW001516), GALK (ACW007457), GALT (ACW006345), and GALE (ACW003126) associated with oligosaccharide breakdown and galactose metabolism
Figure 2
Figure 2
The relative expression of NAGA-like, GALK, GALT, and GALE genes in the head and thorax of three honeybee species and GAL, GALK, GALT, and GALE enzymes in the gut of A. camellia, A. cerana, and A. mellifera, respectively (n=8) (A) Relative expression of NAGA-like genes in the head and thorax of A. camellia, A. cerana, and A. mellifera. (B) Relative expression of GALK genes in the head and thorax of A. camellia, A. cerana, and A. mellifera. (C) Relative expression of the GALT genes in the head and thorax of A. camellia, A. cerana, and A. mellifera. (D) Relative expression of GALE genes in the head and thorax of A. camellia, A. cerana, and A. mellifera. (E) GAL enzyme activity in the guts of A. camellia, A. cerana, and A. mellifera. (F) GALK enzyme activity in the guts of A. camellia, A. cerana, and A. mellifera. (G) GALT enzyme activity in the guts of A. camellia, A. cerana, and A. mellifera. (H) GALE enzyme activity in the guts of A. camellia, A. cerana, and A. mellifera. Note: The same lowercase letters in the same row indicate no significant differences (p > 0.05), and different lowercase letters indicate significant differences (p < 0.05).
Figure 3
Figure 3
Clustering relationship analysis of NAGA-like, GALK, GALT, and GALE in fifteen honeybee genomes, with Drosophila melanogaster as the outgroup (A) Clustering relationship analysis of NAGA-like gene in 16 species. (B) Clustering relationship analysis of GALK gene in 16 species. (C) Clustering relationship analysis of GALT gene in 16 species. (D) Clustering relationship analysis of GALE gene in 16 species.
Figure 4
Figure 4
Residual sugar levels after 48 h of continuous digestion of manninotriose, raffinose, and stachyose with the addition of GAL and GALK, GALT and GALE enzyme generate galactose 1-phosphate, UDP-galactose and UDP-glucose levels upon 48 h of continuous digestion of galactose in vitro (A) Manninotriose concentrations in the control and treatment groups. (B) Raffinose concentrations in the control and treatment groups. (C) Stachyose concentrations in control and treatment groups. (D) Galactose concentrations in the control and treatment groups. (E) Galactose 1-phosphate concentrations in the control and treatment groups. (F) UDP-galactose concentrations in the control and treatment groups. (G) UDP-glucose concentrations in control and treatment groups.
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