Dissecting nutrient-related co-expression networks in phosphate starved poplars

PLoS One. 2017 Feb 21;12(2):e0171958. doi: 10.1371/journal.pone.0171958. eCollection 2017.

Abstract

Phosphorus (P) is an essential plant nutrient, but its availability is often limited in soil. Here, we studied changes in the transcriptome and in nutrient element concentrations in leaves and roots of poplars (Populus × canescens) in response to P deficiency. P starvation resulted in decreased concentrations of S and major cations (K, Mg, Ca), in increased concentrations of N, Zn and Al, while C, Fe and Mn were only little affected. In roots and leaves >4,000 and >9,000 genes were differently expressed upon P starvation. These genes clustered in eleven co-expression modules of which seven were correlated with distinct elements in the plant tissues. One module (4.7% of all differentially expressed genes) was strongly correlated with changes in the P concentration in the plant. In this module the GO term "response to P starvation" was enriched with phosphoenolpyruvate carboxylase kinases, phosphatases and pyrophosphatases as well as regulatory domains such as SPX, but no phosphate transporters. The P-related module was also enriched in genes of the functional category "galactolipid synthesis". Galactolipids substitute phospholipids in membranes under P limitation. Two modules, one correlated with C and N and the other with biomass, S and Mg, were connected with the P-related module by co-expression. In these modules GO terms indicating "DNA modification" and "cell division" as well as "defense" and "RNA modification" and "signaling" were enriched; they contained phosphate transporters. Bark storage proteins were among the most strongly upregulated genes in the growth-related module suggesting that N, which could not be used for growth, accumulated in typical storage compounds. In conclusion, weighted gene coexpression network analysis revealed a hierarchical structure of gene clusters, which separated phosphate starvation responses correlated with P tissue concentrations from other gene modules, which most likely represented transcriptional adjustments related to down-stream nutritional changes and stress.

MeSH terms

  • Aluminum / analysis
  • Calcium / analysis
  • Gene Expression Regulation, Plant
  • Iron / analysis
  • Magnesium / analysis
  • Manganese / analysis
  • Metabolic Networks and Pathways
  • Nitrogen / analysis
  • Oligonucleotide Array Sequence Analysis
  • Phosphates / deficiency*
  • Phosphorus / analysis
  • Populus / chemistry
  • Populus / metabolism*
  • Potassium / analysis
  • Sulfur / analysis
  • Zinc / analysis

Substances

  • Phosphates
  • Phosphorus
  • Manganese
  • Sulfur
  • Aluminum
  • Iron
  • Magnesium
  • Zinc
  • Nitrogen
  • Potassium
  • Calcium

Grants and funding

The Georg-August University of Göttingen (http://www.uni-goettingen.de/de/1.html) funded the PhD position of MJK. The Deutsche Forschungsgemeinschaft (DFG, http://www.dfg.de/foerderung/programme/listen/projektdetails/index.jsp?id=220238996), Priority Program SPP 1685 “Ecosystem Nutrition” provided financial support for this research Project under grant number Po362/22-2. The publication fund of the University of Göttingen and the Deutsche Forschungsgemeinschaft supported open access publication of this article. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.