Light Modulates Ethylene Synthesis, Signaling, and Downstream Transcriptional Networks to Control Plant Development

Abstract

The inhibition of hypocotyl elongation by ethylene in dark-grown seedlings was the basis of elegant screens that identified ethylene-insensitive Arabidopsis mutants, which remained tall even when treated with high concentrations of ethylene. This simple approach proved invaluable for identification and molecular characterization of major players in the ethylene signaling and response pathway, including receptors and downstream signaling proteins, as well as transcription factors that mediate the extensive transcriptional remodeling observed in response to elevated ethylene. However, the dark-adapted early developmental stage used in these experiments represents only a small segment of a plant's life cycle. After a seedling's emergence from the soil, light signaling pathways elicit a switch in developmental programming and the hormonal circuitry that controls it. Accordingly, ethylene levels and responses diverge under these different environmental conditions. In this review, we compare and contrast ethylene synthesis, perception, and response in light and dark contexts, including the molecular mechanisms linking light responses to ethylene biology. One powerful method to identify similarities and differences in these important regulatory processes is through comparison of transcriptomic datasets resulting from manipulation of ethylene levels or signaling under varying light conditions. We performed a meta-analysis of multiple transcriptomic datasets to uncover transcriptional responses to ethylene that are both light-dependent and light-independent. We identified a core set of 139 transcripts with robust and consistent responses to elevated ethylene across three root-specific datasets. This "gold standard" group of ethylene-regulated transcripts includes mRNAs encoding numerous proteins that function in ethylene signaling and synthesis, but also reveals a number of previously uncharacterized gene products that may contribute to ethylene response phenotypes. Understanding these light-dependent differences in ethylene signaling and synthesis will provide greater insight into the roles of ethylene in growth and development across the entire plant life cycle.

Keywords: ethylene; ethylene biosynthesis; ethylene response; hypocotyl; light; root; transcriptomic meta-analysis.

Figure 1

Ethylene and ACC inhibit hypocotyl elongation in the dark and increase elongation in the light. Wild-type seedlings were grown on media containing the indicated concentrations of ACC or on control media and treated with ethylene gas for 3 days in the dark or 5 days in light. The effects of (A) ACC or (B) ethylene on hypocotyl growth in dark and light conditions. Images generated by the Yoon lab (Seo and Yoon, 2019), recapitulating previous findings (Bleecker et al., 1988; Guzman and Ecker, 1990; Smalle et al., 1997; Le et al., 2005; Liang et al., 2012). Values shown are the average and SD of three replicates, each containing at least 20 seedlings.

Figure 2

Ethylene and shade regulate many of the same genes in Arabidopsis hypocotyls. A transcriptional dataset in which seedlings were grown in the light and then either treated with ethylene or moved to shade (Das et al., 2016) and were refiltered as described in Supplemental Datasheet 1 , revealing that many transcripts share both ethylene and shade regulation. (A) A heat map, generated using the Complex Heatmaps package in R (Gu et al., 2016), shows transcripts that had statistically significant responses to ethylene in at least one time point and how those transcripts responded to shade treatment. Most genes regulated by ethylene were also regulated by shade, with the majority changing in the same direction and a smaller subset changing in opposite directions, and with a limited number of transcripts showing no response to shade. (B) To better define the relationship between magnitude change in response to ethylene and light, the transcripts that showed significant changes in abundance with ethylene treatment in the 25.5 h sample (which showed most dramatic ethylene-induced abundance changes) were plotted as a function of their change in response to shading. Genes that were also regulated by shade in this dataset showed strong statistical correlations between ethylene logFC and shade logFC (positive for genes with the same direction of regulation (Pearson’s correlation, r = 0.89, p < 0.001), and negative for genes with the opposite direction of regulation (Pearson’s correlation, r = −0.87, p < 0.001).

Figure 3

Three root-specific ethylene response datasets show light-dependent and light-independent overlaps. Venn diagram represents number of overlapping and non-overlapping DE genes between three root-specific transcriptomic datasets: Stepanova et al. (2007), Harkey et al. (2018), and Feng et al. (2017). Differences in experimental conditions are summarized under each dataset name. Details of the analysis can be found in Supplemental Datasheet 1 . Once DE lists were generated for individual datasets, we compared the lists to find overlapping and non-overlapping genes. In the Venn diagram, the two light-grown datasets are represented in yellow, and the dark-grown dataset is represented in gray. The number of transcripts within each overlap are color coded, with the total in black, the number increasing in both or all three in red, the number decreasing in blue, and purple indicating transcripts that changed in different directions between datasets.