Integrating transcriptomic network reconstruction and eQTL analyses reveals mechanistic connections between genomic architecture and Brassica rapa development

PLoS Genet. 2019 Sep 12;15(9):e1008367. doi: 10.1371/journal.pgen.1008367. eCollection 2019 Sep.

Abstract

Plant developmental dynamics can be heritable, genetically correlated with fitness and yield, and undergo selection. Therefore, characterizing the mechanistic connections between the genetic architecture governing plant development and the resulting ontogenetic dynamics of plants in field settings is critically important for agricultural production and evolutionary ecology. We use hierarchical Bayesian Function-Valued Trait (FVT) models to estimate Brassica rapa growth curves throughout ontogeny, across two treatments, and in two growing seasons. We find genetic variation for plasticity of growth rates and final sizes, but not the inflection point (transition from accelerating to decelerating growth) of growth curves. There are trade-offs between growth rate and duration, indicating that selection for maximum yields at early harvest dates may come at the expense of late harvest yields and vice versa. We generate eigengene modules and determine which are co-expressed with FVT traits using a Weighted Gene Co-expression Analysis. Independently, we seed a Mutual Rank co-expression network model with FVT traits to identify specific genes and gene networks related to FVT. GO-analyses of eigengene modules indicate roles for actin/cytoskeletal genes, herbivore resistance/wounding responses, and cell division, while MR networks demonstrate a close association between metabolic regulation and plant growth. We determine that combining FVT Quantitative Trait Loci (QTL) and MR genes/WGCNA eigengene expression profiles better characterizes phenotypic variation than any single data type (i.e. QTL, gene, or eigengene alone). Our network analysis allows us to employ a targeted eQTL analysis, which we use to identify regulatory hotspots for FVT. We examine cis vs. trans eQTL that mechanistically link FVT QTL with structural trait variation. Colocalization of FVT, gene, and eigengene eQTL provide strong evidence for candidate genes influencing plant height. The study is the first to explore eQTL for FVT, and specifically do so in agroecologically relevant field settings.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Bayes Theorem
  • Brassica rapa / genetics*
  • Brassica rapa / metabolism*
  • Gene Expression Profiling / methods
  • Gene Expression Regulation, Plant / genetics*
  • Gene Expression Regulation, Plant / physiology
  • Gene Regulatory Networks / genetics
  • Genomics / methods
  • Genotype
  • Phenotype
  • Quantitative Trait Loci / genetics
  • Transcriptome / genetics

Associated data

  • figshare/10.6084/m9.figshare.7661093

Grant support

This work is supported by National Science Foundation (https://nsf.gov) Grants IOS-1306574 to RLB and IOS-0923752 to CW, SW, and JNM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.