Abstract

Organisms in the wild are subject to multiple, fluctuating environmental factors, and it is in complex natural environments that genetic regulatory networks actually function and evolve. We assessed genome-wide gene expression patterns in the wild in two natural accessions of the model plant Arabidopsis thaliana and examined the nature of transcriptional variation throughout its life cycle and gene expression correlations with natural environmental fluctuations. We grew plants in a natural field environment and measured genome-wide time-series gene expression from the plant shoot every three days, spanning the seedling to reproductive stages. We find that 15,352 genes were expressed in the A. thaliana shoot in the field, and accession and flowering status (vegetative versus flowering) were strong components of transcriptional variation in this plant. We identified between ∼110 and 190 time-varying gene expression clusters in the field, many of which were significantly overrepresented by genes regulated by abiotic and biotic environmental stresses. The two main principal components of vegetative shoot gene expression (PCveg) correlate to temperature and precipitation occurrence in the field. The largest PCveg axes included thermoregulatory genes while the second major PCveg was associated with precipitation and contained drought-responsive genes. By exposing A. thaliana to natural environments in an open field, we provide a framework for further understanding the genetic networks that are deployed in natural environments, and we connect plant molecular genetics in the laboratory to plant organismal ecology in the wild.

Highlights

  • Organisms in the real world are continuously exposed to multiple environmental signals and must respond appropriately to dynamic, fluctuating conditions found in nature [1]

  • Genes were designated as expressed if they were observed in all three replicates at a timepoint by the Affymetrix Microarray Suite 5 (MAS 5) algorithm [47], and we found that 47% to 58% of genes in Bay-0 and 45% to 61% in Sha were expressed at each timepoint

  • Using the same principal variance components analysis (PVCA) and mixed model analysis of variance (ANOVA) approach, we looked at global trends in gene expression observed within each of the two accessions by examining how variation in genomewide transcription levels is explained by various environmental factors

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Summary

Introduction

Organisms in the real world are continuously exposed to multiple environmental signals and must respond appropriately to dynamic, fluctuating conditions found in nature [1]. Temperature, water levels, biotic interactions and resource availability are just some key environmental conditions that cue organismal responses, and there have been significant advances in dissecting how these and other ecological signals are transduced by the organism to appropriate gene expression levels that may determine phenotypes [2,3,4,5,6,7,8,9]. The natural world, in contrast, is anything but controlled, and understanding how genes are regulated in natural ecological settings in the midst of fluctuating environmental signals remains a key objective of the new fields of ecological genomics and systems biology [6]

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