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Lipophilic signals lead to organ-specific gene expression changes in Arabidopsis seedlings.

ABSTRACT: In plants, N-acylethanolamines (NAEs) are most abundant in desiccated seeds and their levels decline during germination and early seedling establishment. However, endogenous NAE levels rise in seedlings when ABA or environmental stress is applied, and this results in an inhibition of further seedling development. When the most abundant, polyunsaturated NAEs of linoleic acid (18:2) and linolenic acid (18:3) were exogenously applied, seedling development was affected in an organ-specific manner. NAE 18:2 primarily affected primary root elongation and NAE 18:3 primarily affected cotyledon greening and expansion and overall seedling growth. The molecular components and signaling mechanisms involved in this pathway are not well understood. In addition, the bifurcating nature of this pathway provides a unique system in which to study the spatial aspects and interaction of these lipid-specific and organ-targeted signaling pathways. Using whole transcriptome sequencing (RNA-seq) and differential expression analysis, we identified early (1-3 hr) transcriptional changes induced by the exogenous treatment of NAE 18:2 and NAE 18:3 in cotyledons, roots, and seedlings. These two treatments led to a significant enrichment in ABA-response and chitin-response genes in organs where the treatments led to changes in development. In Arabidopsis seedlings, NAE 18:2 treatment led to the repression of genes involved in cell wall biogenesis and organization in roots and seedlings. In addition, cotyledons, roots, and seedlings treated with NAE 18:3 also showed a decrease in transcripts that encode proteins involved in growth processes. NAE 18:3 also led to changes in the abundance of transcripts involved in the modulation of chlorophyll biosynthesis and catabolism in cotyledons. Overall, NAE 18:2 and NAE 18:3 treatment led to lipid-type and organ-specific gene expression changes that include overlapping and non-overlapping gene sets. These data will provide future, rich opportunities to examine the genetic pathways involved in transducing early signals into downstream physiological changes in seedling growth.

SUBMITTER: Cannon AE

PROVIDER: S-EPMC7403840 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Lipophilic signals lead to organ-specific gene expression changes in <i>Arabidopsis</i> seedlings.

Cannon Ashley E AE Yan Chengshi C Burks David J DJ Rao Xiaolan X Azad Rajeev K RK Chapman Kent D KD

Plant direct 20200715 7

In plants, <i>N</i>-acylethanolamines (NAEs) are most abundant in desiccated seeds and their levels decline during germination and early seedling establishment. However, endogenous NAE levels rise in seedlings when ABA or environmental stress is applied, and this results in an inhibition of further seedling development. When the most abundant, polyunsaturated NAEs of linoleic acid (18:2) and linolenic acid (18:3) were exogenously applied, seedling development was affected in an organ-specific ma ...[more]

PMID: 32775951

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Project description:Purpose: Using RNA-seq and differential expression analysis, we examined the NAE-type and organ-specific genetic pathways involved in transducing ear;y signals into downstream physiological changes involved in Arabidopsis seedling growth. Methods: Intact seedlings and dissected cotyledon and root mRNA profiles of 3-day-old Arabidopsis seedlings treated with DMSO, 40 µM NAE 18:2 or 80 µM NAE 18:3 were generated by deep sequencing, in triplicate, using the Illumina Next-Seq 500 system. The sequence reads that passed quality filters were analyzed using STAR followed by DESeq2. qRT–PCR validation was performed using SYBR Green assays Results: Using RNA-seq and differential expression analysis, we identified early (1 h) transcriptional changes induced by the exogenous treatment of NAE 18:2 and NAE 18:3 in cotyledons, roots and intact seedlings. These two treatments led to a significant enrichment in ABA-response and chitin-response genes in organs where the treatments led to changes in development. In Arabidopsis seedlings, NAE 18:2 treatment led to the repression of genes involved in cell wall biogenesis and organization in roots and seedlings. In addition, cotyledons, roots, and seedlings treated with NAE 18:3 also showed a decrease in transcripts that encode proteins involved in growth processes. NAE 18:3 also led to changes in the abundance of transcripts involved in the modulation of chlorophyll biosynthesis and catabolism in cotyledons. Overall, NAE 18:2 and NAE 18:3 treatment led to lipid-type and organ-specific gene expression changes that include overlapping and non-overlapping gene sets. These data will provide future, rich opportunities to examine the genetic pathways involved in transducing early signals into downstream physiological changes in seedling growth. Conclusions: A detailed transcriptional analyses provided insight into the early organ-specific molecular responses to NAE 18:2 and NAE 18:3. Using this experimental and computational approach, we gained an unbiased view of the NAE 18:2- and NAE 18:3-modulated transcriptome changes that are activated and lead to downstream changes in seedling development. NAE 18:2 and NAE 18:3 induced the expression of several genes also induced by ABA or chitin treatment. The overlap with ABA-response genes corroborates previously work; however, this is the first time chitin-response genes have been identified as part of the NAE-modulation of seedling growth. Overall, the bioinformatic analyses presented here supports the hypothesis that NAE 18:2 and NAE 18:3 elicit organ-specific and signal- specific molecular changes that precede developmental changes in Arabidopsis seedlings. Further, these data provide novel insights into the genetic programs that are modulated by NAE 18:2 and NAE 18:3 at the organ-specific level in Arabidopsis seedlings, and will facilitate future studies of the corresponding signaling networks.

Dataset Information

Lipophilic signals lead to organ-specific gene expression changes in Arabidopsis seedlings.

Publications

Lipophilic signals lead to organ-specific gene expression changes in <i>Arabidopsis</i> seedlings.

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