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. 2024 Dec 11:15:1488553.
doi: 10.3389/fpls.2024.1488553. eCollection 2024.

Understanding the defense mechanism of Allium plants through the onion isoallicin-omics study

Heejung Cho  1 , Ji Yeon Park  1 , Duck Hyun Kim  2 , JiWon Han  3 , Karthi Natesan  1 , Min-Seon Choi  3 , Seon-Kyeong Lee  4 , Jiseon Kim  4 , Kun Cho  2 , Byoung Ohg Ahn  1
Affiliations

Understanding the defense mechanism of Allium plants through the onion isoallicin-omics study

Heejung Cho et al. Front Plant Sci. .

Abstract

Onion (Allium cepa L.) is an important seasoning vegetable worldwide. It belongs to the Allium genus, which produces distinctive flavor compounds, allicin/isoallicin. It has been known that allicin/isoallicin is produced upon cell damage by vacuole-localized alliinase releasing. Pungent isoallicin and lachrymaroty factor (LF) are unique features of onions. To understand the isoallicin system of onions, we identified and characterized the biosynthesis-related genes by displaying transcriptional profiles and analyzing the isoallicin contents of onion plants. The DHW30006 onion genome encoded 64 alliinase (ALL) and 29 LF synthase (LFS) proteins, which are the key enzymes for producing of isoallicin and LF. Interestingly, when we analyzed the N-terminal signal peptide sequences (SP) necessary for transport to the vacuole, we found that 14 ALLs contained the SP (SP-ALL) and 50 ALLs did not (non-SP-ALL). We hypothesized that non-SP-ALLs stayed in the cytosol of onion cells, reacted with isoalliin, and generated isoallicin without cell damage. Our transcriptome and LC-MS/MS analyses reveal that isoallicin levels vary significantly across onion tissues and growth stages, with substantial production occurring in intact cells through cytosolic alliinases and an increase through vacuolar alliinases upon tissue disruption. This novel observation suggests that the isoallicin system in onions functions as a dual-defense mechanism: cytosolic alliinases maintain a constant level of defense against biotic stress in undamaged tissues, while vacuolar alliinases enhance isoallicin production in response to tissue damage by herbivory and insects. Together, these coordinated mechanisms demonstrate an adaptable and dynamic defense strategy against biotic stresses in Allium plants.

Keywords: Allium cepa; DHW30006 onion; alliinase; defense mechanism; isoallicin; onion.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Chromosomal distribution of isoallicin biosynthetic pathway genes of DHW30006 onion genome. Dots indicate the signal peptide sequences (red) and the adh_short motif (dark yellow).
Figure 2
Figure 2
A simplified representation of the isoallicin biosynthetic pathway of onion and transcription profiles of the corresponding enzyme-encoding genes according to tissues and bulb growing stages (S1, S2, S3 and S4) of DHW30006 onion plants. The enzymes of each catalytic step are shown in red. Dots indicate the signal peptide (red) and the adh_short motif (dark yellow).
Figure 3
Figure 3
Integration of the genetic map, gene expression pattern and phylogenetic relationships of the onion ALL (A) and LFS (B) gene families. The phylogenetic tree was analyzed using the analogous protein sequences of each species, and the number of proteins is given in parentheses.
Figure 4
Figure 4
LC-MS/MS analysis of isoallicin in DHW30006 onion plants. (A) Isoallicin contents of field-grown onion plants according to tissues during bulb growing stages (S1, S2, S3 and S4). (B) Correlation of isoallicin contents and the expression (TPM) of putative isoalliin biosynthetic pathway (upper), ALL (middle) and LFS (lower) genes during bulb growing. S1 to S4 onion samples were extracted from lyophilized tissues by three replicates.
Figure 5
Figure 5
Isoallicin contents of onion tissues according to the extraction conditions. (No RXN) Direct extraction of onion tissues for vacuolar alliinase no-reaction and (30min RXN) 30 min incubation for vacuolar alliinase reaction. DHW30006 onion plants were grown in greenhouse for three months and samples were extracted from fresh tissues by four replicates.
Figure 6
Figure 6
Proposal of isoallicin defense mechanism of onion plants. (A) Isoallicin production mechanism in intact and burst cell states according to onion tissues. (B) Isoallicin defence system throughout onion plant lifetime.
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