A systems‐biology approach identifies co‐expression modules in response to low phosphate supply in maize lines of different breeding history

Abstract

Plants cope with low phosphorus availability by adjusting growth and metabolism through transcriptomic and proteomic adaptations. We hypothesize that selected genotypes with distinct phosphorous (P) use efficiency covering the breeding history of European Flint heterotic pool provide a tool to reveal general and genotype-specific molecular responses to P limitation. We reconstructed protein and gene co-expression networks by weighted correlation network analysis and related these to phosphate deficiency-induced traits. In roots, low phosphate supply resulted in a decreasing abundance of proteins in the oxidative pentose phosphate pathway and a negative correlation with root and shoot phosphate content. We observed an increase in abundance and positive correlation with root and shoot phosphate content for proteins in sucrose biosynthesis, lipid metabolism, respiration and RNA processing. Purple acid phosphatases, superoxide dismutase and phenylalanine ammonia lyase were identified as being upregulated under low phosphate in all genotypes. Overall, correlations between protein and mRNA abundance changes were limited, with ribosomal proteins and the ubiquitin protein degradation pathway exclusively responding with protein abundance changes. Carbohydrate, phospho-and sulfo-lipid metabolism showed abundance changes at the protein and mRNA levels. These partially non-overlapping proteomic and transcriptomic adjustments to low phosphate suggest sugar and lipid metabolism as metabolic processes associated with improved P use efficiency specifically in Founder Flint lines. We identified a mitogen-activated protein kinase-kinase as a potential genotype-specific regulator of sucrose metabolism at low phosphate in Founder Flint line EP1. We conclude that, during breedingt of Elite Flint lines, regulation of primary metabolism has changed to result in a distinct low phosphate response in Founder lines.

Recent advances in research on phosphate starvation signaling in plants

“…In fact, so far, there have only been reported metabolomics and/or transcriptomic and ionomic studies focused on selected subsets of accessions/cultivars displaying high or low tolerance to limiting Pi growth conditions. In general, these studies identified some significant correlations between gene co-expression modules, metabolites, and/or elements with plant performance traits under low Pi growth conditions, which inform on metabolic pathways and transcriptional programs and potential TF regulators underlying low Pi tolerance, functional validation is still missing for most candidates (Hajheidari et al 2022;Han et al 2022;He et al 2022;Luo et al 2019). Only in one GWAS study in maize, the information on Pi starvation-responsive metabolites and the significant correlation between specific metabolites and plant performance traits has been used to identify potential candidate causal genes underlying QTLs for these traits.…”

Role of SiPHR1 in the Response to Low Phosphate in Foxtail Millet via Comparative Transcriptomic and Co-Expression Network Analyses

“…In maize, two prominent co-expression modules obtained by WGCNA, which included proteins and genes related to sucrose biosynthesis, lipid metabolism, respiration, and RNA processing, were found to be positively correlated with root and shoot traits in the maize phosphate-starvation response [ 48 ]. Based on WGCNA analysis, we found that two co-expression network modules, MEcoal2 and MEblue, were positively correlated with root and shoot traits under LP stress.…”

A high‐confidence Physcomitrium patens plasmodesmata proteome by iterative scoring and validation reveals diversification of cell wall proteins during evolution

“…Total protein was extracted in a urea thiourea environment (He et al ., 2021). Microsomal fraction isolation followed established protocols (Pertl et al ., 2001).…”