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

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          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.

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          Most cited references64

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          Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2

          In comparative high-throughput sequencing assays, a fundamental task is the analysis of count data, such as read counts per gene in RNA-seq, for evidence of systematic changes across experimental conditions. Small replicate numbers, discreteness, large dynamic range and the presence of outliers require a suitable statistical approach. We present DESeq2, a method for differential analysis of count data, using shrinkage estimation for dispersions and fold changes to improve stability and interpretability of estimates. This enables a more quantitative analysis focused on the strength rather than the mere presence of differential expression. The DESeq2 package is available at http://www.bioconductor.org/packages/release/bioc/html/DESeq2.html. Electronic supplementary material The online version of this article (doi:10.1186/s13059-014-0550-8) contains supplementary material, which is available to authorized users.
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            Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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              STAR: ultrafast universal RNA-seq aligner.

              Accurate alignment of high-throughput RNA-seq data is a challenging and yet unsolved problem because of the non-contiguous transcript structure, relatively short read lengths and constantly increasing throughput of the sequencing technologies. Currently available RNA-seq aligners suffer from high mapping error rates, low mapping speed, read length limitation and mapping biases. To align our large (>80 billon reads) ENCODE Transcriptome RNA-seq dataset, we developed the Spliced Transcripts Alignment to a Reference (STAR) software based on a previously undescribed RNA-seq alignment algorithm that uses sequential maximum mappable seed search in uncompressed suffix arrays followed by seed clustering and stitching procedure. STAR outperforms other aligners by a factor of >50 in mapping speed, aligning to the human genome 550 million 2 × 76 bp paired-end reads per hour on a modest 12-core server, while at the same time improving alignment sensitivity and precision. In addition to unbiased de novo detection of canonical junctions, STAR can discover non-canonical splices and chimeric (fusion) transcripts, and is also capable of mapping full-length RNA sequences. Using Roche 454 sequencing of reverse transcription polymerase chain reaction amplicons, we experimentally validated 1960 novel intergenic splice junctions with an 80-90% success rate, corroborating the high precision of the STAR mapping strategy. STAR is implemented as a standalone C++ code. STAR is free open source software distributed under GPLv3 license and can be downloaded from http://code.google.com/p/rna-star/.
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                Author and article information

                Contributors
                URI : https://loop.frontiersin.org/people/645370Role: Role: Role: Role: Role: Role: Role: Role:
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                URI : https://loop.frontiersin.org/people/1374226Role: Role:
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                URI : https://loop.frontiersin.org/people/102458Role: Role:
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                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                11 December 2024
                2024
                : 15
                : 1488553
                Affiliations
                [1] 1 Genomics Division, National Institute of Agricultural Sciences, Rural Development Administration , Jeonju, Republic of Korea
                [2] 2 Digital Omics Research Center, Korea Basic Science Institute (KBSI) , Cheongju, Republic of Korea
                [3] 3 Allium Vegetable Research Center, National Institute of Horticultural and Herbal Science, Rural Development Administration , Muan, Republic of Korea
                [4] 4 Metabolic Engineering Division, National Institute of Agricultural Sciences, Rural Development Administration , Jeonju, Republic of Korea
                Author notes

                Edited by: Peng Wang, Jiangsu Province and Chinese Academy of Sciences, China

                Reviewed by: Qingping Hu, Shanxi Normal University, China

                Kalaiselvi Senthil, Avinashilingam Institute for Home Science and Higher Education for Women, India

                *Correspondence: Heejung Cho, chohj78@ 123456korea.kr
                Article
                10.3389/fpls.2024.1488553
                11668612
                39722878
                163ff38f-9ee2-4e40-bb6e-25943d7d83d6
                Copyright © 2024 Cho, Park, Kim, Han, Natesan, Choi, Lee, Kim, Cho and Ahn

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 30 August 2024
                : 18 November 2024
                Page count
                Figures: 6, Tables: 0, Equations: 0, References: 64, Pages: 12, Words: 5517
                Funding
                The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This research was supported by a grant from the National Institute of Agricultural Sciences (PJ015886), Rural Development Administration, Republic of Korea.
                Categories
                Plant Science
                Original Research
                Custom metadata
                Functional and Applied Plant Genomics

                Plant science & Botany
                allium cepa,onion,isoallicin,defense mechanism,dhw30006 onion,alliinase
                Plant science & Botany
                allium cepa, onion, isoallicin, defense mechanism, dhw30006 onion, alliinase

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