Comprehensive Transcriptome Analysis Reveals Genome-Wide Changes Associated with Endoplasmic Reticulum (ER) Stress in Potato (Solanum tuberosum L.)

Abstract

We treated potato (Solanum tuberosum L.) plantlets with TM and performed gene expression studies to identify genome-wide changes associated with endoplasmic reticulum (ER) stress and the unfolded protein response (UPR). An extensive network of responses was identified, including chromatin remodeling, transcriptional reprogramming, as well as changes in the structural components of the endomembrane network system. Limited genome-wide changes in alternative RNA splicing patterns of protein-coding transcripts were also discovered. Significant changes in RNA metabolism, components of the translation machinery, as well as factors involved in protein folding and maturation occurred, which included a broader set of genes than expected based on Arabidopsis research. Antioxidant defenses and oxygen metabolic enzymes are differentially regulated, which is expected of cells that may be experiencing oxidative stress or adapting to protect proteins from oxidation. Surges in protein kinase expression indicated early signal transduction events. This study shows early genomic responses including an array of differentially expressed genes that have not been reported in Arabidopsis. These data describe novel ER stress responses in a solanaceous host.

Keywords: RNA-seq; Solanum tuberosum; endoplasmic reticulum (ER) stress; potato genome; unfolded protein response (UPR).

Figure 1

Numbers of differentially expressed genes (DEGs). (A) In the volcano plots, the red dots represent the DEGs with the log2FC threshold of ±1.0 (p < 0.05). Gray, green, and blue indicate genes that are not significantly altered in expression at Log 2FC 1.0 cutoff. (B) A Venn diagram highlighting unique and common DEGs in TM-treated leaves at 2 and 5 h.

Figure 2

Level 3 Gene Ontology distribution of DEGs. Charts show the upregulated genes in TM-treated leaf tissues at (A) 2 and (B) 5 h.

Figure 3

Functional enrichment of the cellular component of upregulated genes. Upregulated genes at (A) 2 and (B) 5 h; p < 0.05 using Fisher’s exact test. Word Clouds present detailed cellular components at (C) 2 and (D) 5 h after the TM treatment.

Figure 4

Isoform enrichment analysis at 2 h. Selected isoforms and their differential expression. The coding potential, NMD sensitivity, and functional PFAM domains are indicated. *—p < 0.05, ***—p < 0.001, ns—not significant.

Figure 5

Isoform enrichment analysis at 5 h. Selected isoforms and their differential expression are shown. Coding potentials, NMD sensitivities, and functional PFAM domains are indicated. *—p < 0.05, ***—p < 0.001, ns—not significant.

Figure 6

UpSet plot displaying the comparative analysis between UPR-related DEGs in Arabidopsis and potato leaves in response to TM treatment. The UpSet plot shows potato DEGs (2 and 5 h) that were also represented in a published Arabidopsis UPR DEGs dataset obtained following induction by TM. S.t. x A.t. is shorthand for S. tuberosum by A. thaliana comparison of DEGs.