Transcriptome analysis reveals changes in whole gene expression, biological processes and molecular functions induced by nickel and copper ions in Jack Pine (Pinus banksiana)

Abstract

Understanding the genetic response of plants to nickel and copper stress is a necessary step to improving the utility of plants for environmental remediation and restoration. The objectives of this study were to: 1) Characterize the transcriptome of Jack Pine (Pinus banksiana) and 2) Analyze the gene expression profiles of genotypes exposed to nickel and copper ion toxicity. Pinus banksiana seedlings were treated with 1,600 mg/kg of nickel sulfate or 1,300 mg of copper sulfate and screened in a growth chamber. Overall, 25,552 transcripts were assigned gene ontology. Nickel resistant and water control genotypes were compared based on the gene expression of various gene ontology categories. The response to stress and to chemical terms comprised the highest proportion of upregulated gene expression whereas the biosynthetic process and carbohydrate metabolic process terms had the highest proportion of downregulated gene expression. The majority of upregulated genes were expressed in the extracellular region and the nucleus whereas most downregulated genes were expressed in the plasma membrane and extracellular region. For copper, there were 6,213 upregulated genes and 29038 downregulated genes expressed in the copper resistant genotype compared to the susceptible genotype at a high stringency. Among the top upregulated genes, the response to stress, the biosynthetic process and the response to chemical stimuli terms represented the highest proportion of gene expression for the biological processes. For the molecular function category, the majority of expressed genes were associated with nucleotide binding followed by transporter activity and kinase activity. For the cellular component category, the majority of upregulated genes were located in the plasma membrane. Half of the total downregulated genes were associated with the extracellular region. Two candidate genes associated with copper resistance were identified including genes encoding for heavy metal-associated isoprenylated plant proteins (AtHIP20 and AtHIP26) and a gene encoding the pleiotropic drug resistance protein 1 (NtPDR1). This study represents the first report of transcriptomic response of a conifer species to nickel and copper ions.